Next Article in Journal
Recovery of Phosphorus from Waste Water Profiting from Biological Nitrogen Treatment: Upstream, Concomitant or Downstream Precipitation Alternatives
Previous Article in Journal
Temporal Responses to Direct and Induced Iron Deficiency in Parietaria judaica
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:

State and Progress of Andean Lupin Cultivation in Europe: A Review

Laboratory of Plant Breeding and Biometry, Department of Crop Science, Agricultural University of Athens, 11855 Athens, Greece
Department of Plant Breeding, Institute of Sustainable Agriculture, 14080 Córdoba, Spain
HBLFA Raumberg-Gumpenstein, 8952 Irdning-Donnersbachtal, Austria
Department of Agriculture, University of the Peloponnese, 24100 Kalamata, Greece
Lusosem S.A., 1495-137 Lisbon, Portugal
Centre of Applied Research Biobased Economy, Hanze University of Applied Sciences, 9747 AS Groningen, The Netherlands
Soil Conservation Service of Iceland (SCSI), Gunnarsholt, 851 Hella, Iceland
Instituto Superior de Agronomia, Universidade de Lisboa, 1349-017 Lisbon, Portugal
Department of Breeding & Innovative production chains, Louis Bolk Institute, 3981 AJ Bunnik, The Netherlands
Department of Plant Sciences, University of Agricultural Sciences and Veterinary Medicine Iaşi, 700490 Iaşi, Romania
LEAF, Linking Landscape, Environment, Agriculture and Food, Instituto Superior de Agronomia, Universidade de Lisboa, 1349-017 Lisbon, Portugal
Author to whom correspondence should be addressed.
Agronomy 2020, 10(7), 1038;
Submission received: 28 May 2020 / Revised: 10 July 2020 / Accepted: 13 July 2020 / Published: 18 July 2020


Lupinus mutabilis is an important source of protein in different Andean countries, and its use in diets, particularly those of less wealthy individuals, has been observed for thousands of years. There is an increasing demand for protein crops suitable for Europe and this species is a potential candidate. Assessment of Lupinus mutabilis genetic material in European conditions started more than 40 years ago, with the characterization of a vast number of accessions from the Andean region. In this review, abiotic and biotic constraints to L. mutabilis cultivation in European soil and climatic conditions are discussed, and cultivation management practices are suggested. The beneficial interaction of L. mutabilis with Bradyrhizobium strains in the soil and various pollinator species is also discussed, and the effect of abiotic stresses on these interactions is highlighted. Prospects of alternative uses of L. mutabilis biomass in Northern Europe and opportunities for breeding strategies are discussed. In conclusion, the different approach to crop modeling for Southern and Northern European climatic conditions is highlighted.

1. Introduction

Lupins are legumes that belong to a large and diverse genus, Lupinus, comprising approximately 280 species [1,2,3,4,5]. Lupins are divided into two major groups according to their geographical origin: (1) the “New World” species, originating in Western North America (ca. 100 species) and the Andean region (ca. 85 species) [1,6,7] and (2) thirteen “Old World” species, with origins in the Mediterranean region [1,7,8]. Among them, only four lupin species present high agricultural importance. Three belong to the “Old World” group, namely L. albus L. (white lupin), L. angustifolius L. (blue or narrow-leaved lupin) and L. luteus L. (yellow lupin) [2,9]. The fourth is the only representative from the 185 species of the “New World” group named L. mutabilis (Andean lupin, pearl lupin), called either tarwi or chocho bean, in regard to the tall species with long branches and the short plant growth type with few branches [10]. Three other lupins worth mentioning, although only of regional agricultural importance, are L. pilosus L., an Old World lupin used as a coffee substitute (Altreier Kaffee) in Northern Italy [11], L. nootkatensis D. ex S. (Nootka lupin), used for land reclamation [12,13,14] and L. polyphyllus Lindl. (Washington lupin), used as an ornamental in many European countries including Germany, Poland, Russia, Spain, Sweden, Ukraine and the United Kingdom. The latter, however, has also been studied for its use as a low alkaloid forage [15] and land rehabilitation species in Central Europe [16,17].
It is suggested that L. mutabilis domestication took place in the Cajamarca region, located between Southern Peru and Northern Bolivia. Remains of seeds are present in the tombs of the pre-Inca Nazca culture (about 500 AD) in the Peruvian coastal desert, and the plant is represented in stylized paintings on large pots from the Tiahuanaco culture (500 to 1,000 AD) of the Andean highlands [8,18,19,20,21,22,23]. Lupinus mutabilis was used by the American Indians as food, after the removal of alkaloids, by soaking the seeds in running water for several days; however, new biological, chemical or aqueous methods for the removal of alkaloids are now available [24]. Andean lupins were also used for green manure and as medicine for cardiac diseases, internal parasite infections, rheumatism and malaria [19]. However, following the European invasion, the culinary habits of the locals changed due to the displacement of Andean lupin by new species such as quinoa [25,26,27]. Nowadays, L. mutabilis is mainly cultivated throughout the Andean region, in countries like Peru, Ecuador and Bolivia, and less so in other South American countries.
The adaptation of L. mutabilis to European and European–Russian soil and climate conditions has been a subject of research since the 1930s [28,29], and in the last few decades, L. mutabilis has been cultivated for agricultural purposes, although it is not yet commercially available [2,20,22,27,30,31,32]. The spread of L. mutabilis in Europe has increased more recently as lupin species have gained the interest of the European Commission due to their high protein and oil content, low starch content and the roles that they could play in reducing soya imports and as biorefinery crops [19,30]. The main interest in Andean lupin cultivation in Europe is based on its higher protein (41–51%) and oil content (14–24%) [27] in comparison to white, blue and yellow lupin species and on its pharmaceutical and cosmetic potential [24,33,34].
Europe is considered one of the main continents where white, blue and yellow lupin are cultivated, with a total production reaching up to 341,970 tons in 2018 [35]. Despite the great interest, Andean lupin is not yet considered commercial because its introduction is facing considerable challenges, such as a low and unstable yield production, the long cropping cycle and difficulties of incorporation into the local cultivation systems, mainly due to various abiotic stresses [22,23]. Various pests and diseases have also been found to be responsible for lower yields of L. mutabilis in Europe [8,36,37]. Considering Andean lupin’s potential in Europe, this paper summarizes L. mutabilis genetic material as tested under European edaphoclimatic conditions and the abiotic and biotic factors that prevail in the area affecting its cultivation, as well as the cropping practices and techniques applied for their management. Its symbiosis with other living organisms, i.e., rhizobacteria and effective pollinator species that predominate in the area, is also assessed. Finally, future alternative uses in the context of adaptation and commercialization in European soil and climatic conditions and the research prospects of the crop are mentioned.

2. Andean Lupin Genetic Material Tested under European Conditions

The evaluation of Lupinus mutabilis genetic material started in European edaphoclimatic conditions in the mid-1930s in Germany [29], the mid-1970s in France and the United Kingdom (UK) [38,39,40] and later in 1983 in Germany and Poland [26,41,42], aiming to define genotypes of early maturity and determinate or semi-determinate growth habit that were considered promising for cultivation and commercial production in Europe. A genotype named KW, with a determinate growth habit, was developed in Poland using mutation breeding [26,42], and Olczak et al. [41] found a fragment in the genetic material of L. mutabilis (KW mutant) that could be used as a molecular marker for a determinate growth habit [41].
In the 1990s, the European Agrimed research project “Lupinus mutabilis: Its adaptation and production under European pedoclimatic conditions” took place. In this project, 149 different lines and selected sub-lines of L. mutabilis populations collected in Peru were evaluated in Southern European conditions, in Portugal, for two consecutive years [43]. During 1993–1996, another European project (AIR20865) followed, “Adaptation of L. mutabilis to European soil and climate conditions”, that aimed to evaluate sixteen different Andean lupin genotypes in Northern (Germany, UK and Poland) and Southern (Southern France and Portugal) Europe.
Since then, many of these Andean lupin genotypes were further evaluated regarding their response and susceptibility to various biotic factors prevailing in Europe, such as cucumber mosaic virus (CMV) [44] and thrips [45]. Intercropping with other temperate legume species for forage production was also assessed, in a two-year experiment with promising results [46]. Recently, many mutant lines were studied in Poland [34], while an interspecific L. mutabilis (LM-13) × L. albus hybrid was developed and its adaptation to European conditions was evaluated [47]. In the context of the previously mentioned projects, and others, in Europe, 167 different L. mutabilis accessions have been tested in the soil and climatic conditions of Portugal, 44 in Poland, 28 in the UK, 26 in Germany and 24 in France, while only one has been tested in Serbia. These accessions were populations, sub-populations, lines, mutant lines, epigonal lines, epigonal mutant lines and landraces [26,39,41,42,43,46,48,49,50,51,52,53,54,55].
In the European LIBBIO project (No 720726, Horizon 2020) titled “Lupinus mutabilis for Increased Biomass from marginal lands and value for BIOrefineries” (, we aim to evaluate the suitability of Andean lupins to different marginal lands in Europe. In this framework, the social and environmental impacts of Andean lupin cultivation in Europe are being evaluated, as well as its techno-economic viability in different European countries. Genotypes are evaluated in field experiments in seven European countries, under Mediterranean conditions (Greece, Portugal, Spain) and in North-Central European (Austria, Iceland, the Netherlands, Romania) conditions, including L. mutabilis genotypes, genetic material from Instituto Superior de Agronomia (ISA, Lisbon, Portugal) and Vandinter Semo (VDS, Scheemda, The Netherlands). In this context, Guilengue et al. [56] and Lazaridi et al. [57] assessed the phenotypic and genetic diversity of Andean lupin for defining appropriate genotypes for cultivation under Mediterranean climatic conditions and the N-fixing potential of LIBBIO breeding lines in alkaline soils [58].

3. Abiotic Restrictive Factors and Cropping Practices

3.1. High and Low Temperature Effects

Temperature is considered one of the most important abiotic factors affecting Andean lupin cropping in Europe [52,59]. Especially in Southern European countries where autumn-winter sowing is practiced and cultivation lasts until summer, the crop is subjected both to low air temperature during the vegetative phase and to high temperatures during the flowering and pod filling stages. Low seed yield production is often recorded under cultivation in Southern European climatic conditions, as a result of flowering abortion at temperatures around and above 27 °C [59] that are common in countries such as Spain, Portugal and Greece. The pod and seed filling stages of lupin species have also been reported to be inhibited by high temperatures (38 °C) [60].
In Northern European countries, Andean lupin seedlings are often exposed to low spring temperatures, and in Southern Europe, to winter frosts, which can be detrimental to plant growth. Even though L. mutabilis has been found to be resistant to frost during the seed filling stage, it is very susceptible to low temperatures during the vegetative stage. Exposure to low temperatures can lead to severe plant losses [61], inhibited plant growth [52] and result in longer periods of vegetative growth [62]. Studies in the 1930s revealed that susceptibility to low temperatures differs among lupin species, in the order of increasing sensitivity, namely L. angustifolius, L. luteus, L. albus and L. mutabilis [29,63].
The screening and selection of genotypes for indeterminate growth, tolerance to frosty conditions at the vegetative stage, and high temperatures at the flowering and podding stages, are therefore considered to be of primary importance in Southern European countries. In Northern Europe, short-cycle genotypes with determinate growth and tolerance to low temperatures are preferred [22]. Defining the appropriate sowing date for each region is also critical for seed yield production [64].
The response of Lupinus spp. to vernalization effect varies among species and even among cultivars [65]. Dominant gene presence or absence, like the Flowering locus T (FT) gene and Bo, Ku and Jul loci, have been reported to remove or reduce the vernalization response in L. cosentini and L. angustifolius, respectively [5,66,67]. However, these genes have not been reported in other lupin species [65]. Książkiewicz et al. [68] found that the genetic control of vernalization differs among lupin species. In areas where lupins are grown as spring-sown and autumn-sown, when winters are mild, the requirements of vernalization can be a restrictive factor. While Jacobsen and Mujica [27] reported that L. mutabilis is neutral to vernalization, Hardy et al. [52] and later Adhikari et al. [65] observed that when late flowering genotypes were subjected to vernalization, they flowered two weeks earlier.

3.2. Impact of Day Length on Growth and Production

Long days are considered to favor the production of flowers in Lupinus spp. [65]. No effect of photoperiod within the range 12.5–14.5 h on the number of days to first flowering were found by Keatinge et al. [59], suggesting that flowering of Andean lupin is insensitive to photoperiod. However, according to Jacobsen and Mujica [27], short days accelerate grain filling, while Hackbarth [69] reported increased oil content in the seeds developed under short days. The response to the photoperiod varies in regard to genotype (early or late flowering); in this context, late flowering genotypes are not favored in Southern Europe, because grain filling occurs on long days at the end of spring and, as mentioned above, seed oil content and yield are reduced.

3.3. Effects of Water Logging and Water Deficit on Growth and Seed Quality

Lupin plants grown under water deficit have a smaller leaf area and fewer lateral shoots, and they tend to mature earlier [70,71]. Water deficit can also cause significant decreases in leaf water potential, stomatal conductance and gas exchange [71]. According to Carvalho et al. [72], water deficit does not affect pod production but it causes a slight decrease in the dry weight of pod husks and a slight increase in the dry weight of seeds. In addition, water deficit does not affect seed protein content levels but reduces the oil content of the seeds (on dry weight basis), increases seed sugar content (on dry weight basis) and changes the composition of carbohydrates, e.g., increased sucrose/alpha-galactoside ratio [72]. Among several L. mutabilis accessions from USDA (United States Department of Agriculture) that were tested for drought resistance, only one was found to be tolerant to water stress [73].
Genetic diversity has been identified among L. mutabilis accessions for tolerance to water logging. Within the genus, the level of water logging tolerance in L. mutabilis is comparable to that of L. angustifolius, higher than in L. albus and lower than in L. luteus [74]. Water deficit in Andean lupin cropping can be prevented by sowing early in Southern European countries to exploit autumn precipitation. In addition, in both Southern and Northern European countries in regions that are prone to waterlogging incidents, cropping in heavy soils should be avoided or otherwise the soil should be tilled well.

3.4. Alkaline, Calcareous Soils and Their Effects on L. mutabilis as a Crop

Lupins are calcifuge species [75]. A significant variation in tolerance to the lime content of soil among Lupinus species has been observed [29,76,77]. Calcium carbonate (CaCO3) in combination with alkaline soils can be catastrophic for the cultivation of Andean lupin. Andean lupin plants grown on soils with a high calcium carbonate content usually exhibit chlorosis symptoms (Figure 1), although different levels of susceptibility have been observed among different genotypes [78]. In alkaline soils, calcium carbonate inhibits iron uptake [79] and has a negative effect on plant photosynthesis, inhibiting the shoot growth rate and seed yield [80]. Although, L. mutabilis is more tolerant than L. luteus and L. angustifolius, it presents similar sensitivity to calcium carbonate in the soil as L. albus [61].

4. Biotic Constraints in Europe for Lupinus mutabilis

Several biotic factors can cause significant problems and limit the production of Andean lupin crops, including mainly fungal and virus pathogens that act similarly on all cultivated lupin species [81].

4.1. Fungal and Bacterial Diseases

Anthracnose caused by Colletotrichum lupini (Bondar) Damm, P.F. Cannon & Crous [81,82] is the most important fungal disease that severely affects Andean lupin in Ecuador, but it has also spread in the last few decades throughout all lupin growing regions [37]. In regard to European regions, anthracnose was responsible for a rapid decrease in L. albus cultivation in Germany and other Central European countries (Austria, France, Poland, Ukraine and Russia) [37,83]. The most obvious symptoms of anthracnose are bending of the main axis, circular or elongated lesions on stems and pods and infected seeds [10,84] with a reduced oil content [85], but a severe infection can cause serious to complete yield losses. In comparison to other cultivated lupins, no resistance is available yet for L. mutabilis [37], which has been proven to be less resistant than L. luteus and L. angustifolius [6,86].
Therefore, other control methods, like seed disinfection and seed hygiene, are generally implemented for anthracnose (Table 1). Some screening efforts have been made [87], revealing that less susceptible genotypes are mainly characterized by a central stem dominance, belonging to the chocho type, while tarwi type genotypes are semi-tolerant [6,88] or present anthocyanin pigmentation in their stems [84]. However, the vulnerability of each developmental stage seems to differ, with the stages after flowering being defined as more susceptible [89,90].
Fusarium wilt and root rot (Fusarium spp.) are also considered one of the main lupin seed-borne fungal diseases, and many Fusarium species have been recorded to infest Andean lupin in Europe, such as in Poland [42] and in Russia [75]. Among cultivated lupins, L. mutabilis is considered the least susceptible to Fusarium spp. [101]. In contrast to anthracnose, genotypes that are resistant to this fungus are available [86] (Table 1).
Another disease to which L. mutabilis is less sensitive than the other lupin species [8,102] is pleiochaeta root rot and brown (leaf) spot induced by Pleiochaeta setosa (Kirchner) S.J. Hughes (Table 1). The disease causes typical symptoms on the roots of the plants [103], leading to a dramatic reduction in crop yield. The transmission of the pathogen seems to be enhanced particularly in low rainfall areas [97]. Until now, no resistance has been found in Andean lupin or in the Old World species [8,86,104,105], although some variability has been observed regarding its resistance [97]. Only in Australia, some active substances (i.e., iprodione and procymidone) are registered and can be applied to seeds for partial control of this disease [106]. In Europe, specific cultivation management techniques have been implemented based on worldwide guidelines (Table 1). Root rot symptoms in L. mutabilis, caused by Phytophthora sojae Kaufm. & Gerd. [107] and Rhizoctonia solani J.G. Kuhn have also been previously reported [92]. The common existence of these fungal diseases around the world and their ability to affect other lupin species [8,108,109] is a serious threat to the spreading of L. mutabilis cultivation in European countries. As there are no available fungicides to suppress the disease in L. mutabilis, various management techniques have been proposed (Table 1).
Recently, a method has been patented for preventing or inhibiting infection in various plant species, including lupins, by fungal pathogens like Fusarium, Rhizoctonia and Botrytis cinerea Pers. [110]. The method is based on the prevention of microorganisms from degrading α-1,3-glucan on cell walls by α-1,3-glucanase, avoiding host immune recognition by pathogens. Another patented product [111], a solution consisting of an ethylhexyl sulfate or salt, an alkylbenzenesulfonic acid and a carrier is also available for inhibiting grey mold and powdery mildew in lupins and is applicable to L. mutabilis. Plant growth promoting rhizobacteria could also help the production of lupin metabolites against fungi, like in many other plant species [112], within the aspects of biocontrol.
Other common fungal diseases have also been reported, causing some less frequent symptoms in Andean Lupin [2,6,85,92,113]. However, no occurrences have been reported yet in L. mutabilis in the European continent. Bacteria-induced diseases by Pseudomonas lupini and P. xanthochlora have also been reported to affect lupins [36,114]. Among these bacterial and fungal pathogens of L. mutabilis, resistance has been reported for a few of them [115], while for others, proper cultivation practices are suggested or no control is needed due to their minor importance.

4.2. Virus Diseases and Carriers

Lupinus mutabilis, like other cultivated lupins, is also susceptible to bean yellow mosaic virus (BYMV) and, compared to other lupin species, it shows high susceptibility [8]. The virus is transmitted by aphids [97,116]. Affected plants present symptoms like vein clearing and leaf mottling, mosaic and leaf deformation, depending on the strain and the infected genotype [36,117,118]. BYMV symptoms have already been recorded in Andean lupin across Europe [118,119,120]. Using certified seed is considered the principal control method [101,121]. In Australia, early sowing, high seeding rates and crop rotation are recommended [122]. Similar practices should probably also be implemented in Europe, since the application of insecticides has not been proven to adequately prevent BYMV transmission [123].
Cucumber mosaic virus (CMV) can also cause a very destructive disease, resulting in up to 60% yield losses in Mediterranean climate [124]. The virus can also be transmitted to L. mutabilis in a non-persistent way by aphids [35,124]. Symptoms recorded in plants of L. mutabilis include vein clearing of young leaves, leaf deformation, mottling and size reduction, pallor and stunting [44]. To prevent transmission of the virus, cultivation management practices (as used to prevent BYVM) are recommended in Australia, as well as the use of resistant varieties [101]. Regarding L. mutabilis, after testing multiple lines, only one showed resistance to CMV [125,126]. The same line has also shown resistance to pea seed-borne mosaic virus (PsbMV) [127].
Lupinus mutabilis also presents immunity to various viruses, commonly found in lupins, such as lupin mosaic virus (LuMV) [128] and alfalfa mosaic virus (AMV) [123]. The main carriers of lupin viruses are aphids [129], which feed on lupin plants, resulting in significant yield losses [130,131,132]. Ferguson [133] reported a late season infestation in plants of L. mutabilis in Great Britain by Macrosiphum albifrons Essig, which is able to transmit cucumber mosaic virus (CMV). Μany reports suggest that aphids are expanding throughout Europe [134,135,136,137,138]. In Poland, thrips Frankliniella intonsa and Thrips tabaci, known as virus carriers [139], were reported to feed on L. mutabilis plants at the flowering stage [45]; however, this did not have a high impact on lupin production. Tomato black ring virus (TBRV), a lupin nematode-transmitted virus, was reported to affect L. mutabilis and to cause leaf deformation and dwarfing after inoculation, although not limiting yield [117].

4.3. Main Insect Pests of L. mutabilis in Europe

Among pests, Agromyza spp. is the most destructive to Andean lupin in Europe. Its larvae feeds on leaves and stems [6]. Weevil (Sitona spp.) or lupin-root weevil, Sitona gressorius and S. griseus are considered major lupin pests across Europe that can strongly reduce lupin grain yield [140], either due to larvae feeding on root nodules or due to adults feeding on the leaves of sweet plants [36,141]. In terms of weevil preference, Ferguson [133] recorded higher weevil percentages in L. albus and L. luteus plants than in L. mutabilis, indicating the lowest preference for L. mutabilis. Macrosiphum albifrons is another aphid that can cause serious damage to lupins [142]. These aphids prefer alkaloids, which they use as a weapon against predators [142,143].
Many flower and pollen-feeding polyphagous beetles (Coleoptera, Astylus spp.) were found to prefer Andean lupin flowers over vegetative parts of the plant [133], causing flower and pod abscission. Three Coleoptera species were recorded recently in L. mutabilis in Greece, in two experimental locations, feeding on flowers, namely Tropinota hirta Poda, T. squalida Scopoli and Oxythyrea funesta Poda [78,144]. These findings enhance the statement of Ferguson [133], who suggested that Astylus spp. beetles preferred the flowers because of different alkaloid levels in pollen and flowers and in the vegetative parts of the plant. Additionally, the timing of sowing had an impact on beetle feeding, as sowing later led to the delayed flowering of many accessions and therefore beetle immigration was avoided [133]. Chemical control of these two beetles is nearly impossible; thus, using baited traps or cultivating very early or late flowering varieties could help in reducing their population density. Diabrotic cucumber beetles (Diabrotica trivittata Mannh.) and Liriomyza sp., found throughout Europe, have also been reported to feed on Andean lupin leaves and flowers in their center of origin [145].

4.4. Weed Species and Management in L. mutabilis Cultivation

Lupin crops are susceptible to weed infestation [146], which can reduce seed yield by up to 67% and also cause difficulties during harvesting [147,148]. Weed species were recorded in Andean lupin fields cultivated in two different regions in Greece (Table 2), namely in Athens (conventional field, no herbicides applied) and in Kalamata (bio cyclic), in two and one year respectively. In Athens, only Amaranthus spp. and Chenopodium spp. inhibited plant vegetative growth, while Calystegia sepium L. and Convolvulus arvensis L. could mix with the aerial biomass when harvest took place. In Kalamata, Capsella bursa-pastoris (L.) Medik., along with Fumaria officinalis L., was the most intense weed species. The spring weed species found in an Andean lupin field cultivated in an herbicide screening experiment in Santarém, Portugal are presented in Table 2 [149].
In this context, weed control seems to be essential for Andean lupin cultivation in Europe. Unfortunately, there are limited herbicides approved for lupins. Weed control in Andean lupin crops relies on pre-emergence chemical control, followed by mechanical methods such as harrowing or hoeing [150], as in other lupin species [151]. Increased sowing densities and strip cropping [147,148,151,152] have also been applied in many lupin species, reducing weed populations significantly.
Chemical weed control has been evaluated in L. mutabilis cropping in Southern Australia, where Sweetingham [74] states that L. mutabilis plants were tolerant to imazethapyr. Prins and van Haren [150] evaluated the effect of pendimethalin and florasulam on L. mutabilis and concluded that it can be safely used under European conditions.
In another experiment in Santarém, Portugal, the effects of seven herbicide treatments were tested in a L. mutabilis crop. Germination ratio evaluation showed that only treatment with metribuzin proved to be significantly different from the untreated plots, showing visible phytotoxicity symptoms. No negative effects on germination were observed in the other treatments (clomazone + pendimethalin, isoxaben, pendimethalin, propizamid, isoxaben + propizamid, s-metolachlor). Only treatments with clomazone + pendimethalin and s-metolachlor outperformed untreated plots when productivity was analyzed [150]. Articles in the literature regarding herbicide screening and weed control in L. mutabilis cropping are limited. Therefore, future studies in these fields are necessary for the commercialization of this crop.

5. Symbiosis with Other Species Abundant in Europe

5.1. Rhizobium–L. mutabilis Symbiosis and Nitrogen Fixation Potential

Rhizobium–legume symbiosis is a process that is characterized by high specificity [153]. Specificity has also been found for RhizobiumLupinus symbiosis. Although it is highly dependent on the geographical origin of the species, L. mutabilis is reported to be effectively nodulated worldwide, mainly by Bradyrhizobium strains [5,74,154,155,156,157]. Many strains of Bradyrhizobium sp. have therefore been isolated from L. mutabilis plants from different regions [155,157,158]. However, a strain named WSM1253, isolated from Ornithopus compressus and collected in Greece, has been found to be promising in nodulating L. mutabilis accession P28725 in Southern Australian soil and climatic conditions [74]. Effective nodulation was also observed recently in Andean lupin accessions by native rhizobia strains, in Greece [58]. European native Bradyrhizobium strains, as also mentioned by Stępkowski et al. [155], Bradyrhizobium canariense and Bradyrhizobium japonicum are therefore capable of nitrogen fixation in Andean lupin plants and could be even more promising than commercial strains nodulating other lupin species [159].
Lupins are able to fix higher amounts of nitrogen than many other leguminous species [160], with L. mutabilis reaching even up to 527 kg N × ha−1. A higher nitrogenase activity of L. mutabilis in comparison to other lupin species has also been reported by Kurlovich et al. [161]. However, the amount of nitrogen fixed by L. mutabilis varies greatly among experimental years [160]. Furthermore, the amount of fixed nitrogen by L. mutabilis under alkaline, calcareous and clay edaphic conditions is significantly lower than the amount fixed by native lupin species [58,162] and in relation to the values reported in Nepal [160]. The lower amounts of fixed nitrogen can be attributed to the specificity of Rhizobium strain–lupin species symbiosis [163] but also to the edaphoclimatic conditions, as alkaline and calcareous soils negatively affect nodule number and activity [8,61,164,165,166]. Nonetheless, there is an exception: L. mariae-josephae is successfully nodulated by Bradyrhizobium strain LmjC, and this symbiosis system prevails in alkaline soils [167,168].
LupinusBradyrhizobium symbiosis has been described as being relatively tolerant to abiotic stresses [169]. Many abiotic factors have been reported that interfere with the effectiveness of Bradyrhizobium - lupin symbiotic systems, like salinity [169,170], prolonged water logging [166,170] and increased nitrate soil content [171], which characterize many European fields. Also herbicides have been shown to negatively affect nodule structure and reduce nodule activity [172,173]. Bradyrhizobium strains often confer better tolerance to abiotic stresses such as herbicide and salinity tolerance than other Rhizobium–legume symbioses. The identification of such strains would greatly facilitate the introduction of L. mutabilis into sustainable crop cultivation systems in Europe.

5.2. Andean Lupin Interaction with Pollinator Species Abundant in Europe

The mating system of a species is of fundamental importance in determining the appropriate breeding strategies, the optimal genetic structure of improved varieties and the isolation requirements for seed production. Suso et al. [174] review the current knowledge of the patterns of mating systems in different Lupinus spp. According to the authors’ review, and citing Kazimierska and Kazimierski [175], the genus is composed of many species that, depending on genetic and environmental factors, present a range of pollination modes, from strictly self-pollination and self-pollination with facultative cross-pollination to prevailing cross-pollination. Even within each species, the outcrossing rates vary depending on the genotype, the location linked to the pollinator fauna species and population. Nevertheless, most cultivated lupin species are regarded as self-pollinated, although there is a degree of outcrossing [176].
By using ISSR markers in different germplasm accessions of L. mutabilis, Chirinos-Arias et al. [177] observed a relatively high genetic polymorphism for an autogamous species such as the Andean lupin. According to Chirinos-Arias et al. [177], the high degree of polymorphism observed might be the result of cross-pollination or in-situ gene flow. Caligari et al. [26] examined the rate of cross-pollination under top-cross experiments over two years, with low and high anthocyanin containing plants as markers. Outcrossing rates between 16.6% and 58.8% were obtained, which indicates that L. mutabilis is an entomogamous, partially allogamous crop that needs to be treated in breeding programs as a cross-pollinated crop.
Lupins are entomophilous species, attracting insects with multi-colored flowers, nutritious pollen and fragrance, which are visited by a great number of solitary and social bees. The presence of different species of pollinators can vary depending on the growing conditions and especially on the availability of bees [175]. Both self-pollination and cross-pollination can be facilitated by bees, which vary widely in behavior and frequency [175]. Bee pollinators play a key role in plant breeding, as they facilitate cross-fertilization, which is needed in order to achieve heterosis of agronomic trait exploitation. Empirical data (not published, in the frame of LIBBIO H2020 EU project) has shown that the most frequent positive floral visitors to lupins are bumblebees (Bombus terrestris) in Southern Spain, but solitary bees of the Eucera, Andrena and Anthophora genera are also visitors. Xylocopa was also noted as positively visiting, although at very low proportions. No negative visits, robbing nectar through holes bitten at the base of the flowers, were observed. Xylocopa bees were the most frequent pollinators observed on Andean lupin flowers in Athens, Greece, but Anthophora and Megachile bees, as well as Bombus sp., were also recorded [78,144]. Williams et al. [178] on the other hand mentioned that Apis mellifera, Bombus spp., Andrena ovulata, Andrena labialis and Eucera sp. have been observed to pollinate L. albus, L. luteus and L. mutabilis in France, although without identifying which pollinator species pollinates each lupin species separately. Studies on L. mutabilis pollinator species are still missing from the literature regarding Central and Northern Europe. Future pollinator studies could aim for the identification of the species responsible for the pollination of Andean lupin.

6. Future Uses and Investigation Prospects

Lupinus mutabilis is a legume with many uses (both as seed and biomass) that are mentioned with detail in the literature. On one hand, L. mutabilis has been used as a cover crop or green manure for improving soil quality [21,86,179]; on the other hand, seeds are commonly used as food for humans and animals in the Andean region [3], after debittering [180]. In addition, the seeds can also find applications in bread making [24], as cheese substitutes [181] and in other food products [24], medicine [177,182] and cosmetics [23,183,184]. A more thorough review of L. mutabilis uses can be found in the literature [3,21,23,24,86,177,179,180,181,182,183,184].

6.1. Prospects of Using L. mutabilis as Feed and Biomass for Bioenergy

Due to their high protein content, oil content and health-promoting secondary metabolites, lupin seeds form a great feed for ruminants, pigs, poultry and fish, improving their productivity when provided in the recommended amounts [185,186]. Until now, most research has focused on Old World lupins [185,186,187,188], while the use of L. mutabilis seeds has only been directly evaluated in experiments as feed for fish and shrimps [189,190]. In some Northern European countries, L. mutabilis grows continuously due to its indeterminate growth habit; in this context, the large mass of above ground biomass can be used as forage or for bioenergy. Gulisano et al. [23] propose the use of L. mutabilis as green fodder or silage, particularly for Northern Europe, where high biomass yields are achieved. Literature about L. mutabilis as forage or silage is limited. A lower fodder yield was observed from Mikić et al. [46] in L. mutabilis legume–legume intercrops, in comparison to L. albus relative intercrops. However, in the same study, among the intercrops and sole cropping, L. mutabilis yielded higher fodder when intercropped with pea. Until now, there have been no data about ensiling whole plants of Andean lupin, although there are some studies regarding white lupin and lupin–grass intercrops for silage. A study conducted in Northern Italy showed that whole crop lupin ensiling was successful only if it was inoculated with ensiling inoculants, due to the high moisture content after harvesting [191]. Carruthers et al. [192] found that intercropping white lupin with corn produced less biomass than soy–corn intercropping silage in Canada, with lupin biomass comprising only 0–6% of the whole intercrop harvest.
A new possibility for using Andean lupin biomass is to produce bioenergy from the whole plant. In Germany, the Julius Kühn-Institut and the University of Rostock tested the dry-matter yields of different Andean lupin accessions in comparison with white and blue lupins. Andean lupins had higher dry-matter yield than white or blue lupins, but not as high as silage maize [193]. In 2019, a new project was started by the Julius Kühn-Institut with a combined growing of Andean lupins and maize or white lupins and oats in the same field in order to optimize the cultivation and the adaptability for making silage.

6.2. Opportunities and Challenges for Breeding

The outcrossing rates obtained for L. mutabilis allow a high level of heterozygosity. The high degree of heterozygosity probably has repercussions on yield and resilience, mediated by heterosis. The variation in outcrossing rate among different cultivars, locations and years suggests that genetic and environmental conditions should be considered when selecting breeding approaches for this species. The importance of assessing cultivar-specific responses to insect pollination has been highlighted [194]. So far, breeders do not generally select for changing or even measuring traits related to pollinators [195,196].
It is therefore useful to reflect on the two basic philosophies that could be held by breeders to deal with the partial allogamy of L. mutabilis: (1) the development of uniform varieties/pure line cultivars through classical line-breeding methods, making crosses and selecting the most promising genotypes or (2) the development of hybrid cultivars and synthetic/open pollinated populations that demonstrate improved yield, mediated by heterosis. Synthetic varieties, produced by inter-crossing several parental lines on the basis of their general combining ability, make partial use of yield, yield stability and resistance to biotic and abiotic stresses mediated by heterosis. Based on the L. mutabilis partial allogamy, the development of synthetic varieties could be an objective in order to improve the sustainability of the crop by means of genetically heterogeneous cultivars. To develop synthetic varieties, breeders have to choose a method to maintain a high level of cross-pollination in the area where they have to work.
Lupinus mutabilis is a partially allogamous species, with estimates of allogamy as high as 58.8% [26], which allows the exploitation of heterosis, and F1 hybrids or synthetic populations could be used. High-yielding heterotic groups are one of the crucial determinants for the successful development of hybrid technology. Clements et al. [197], citing Hardy and Huyghe [53], reported a 46% heterosis yield increase for L. mutabilis.
Efforts to exploit heterosis in partially allogamous crops also require a cost-effective system for hybrid seed production as a result of an efficient pollen transfer mechanism. Stable male-sterile and female-fertile systems could be useful for increasing crossing efficiency. Male sterility is described in L. mutabilis by Clements et al. [197]. They identified and selected both naturally occurring and male-sterile induced plants. A naturally occurring male sterility was established to be cytoplasmic with the identification of restorer and maintainer genotypes. Once an appropriated male-sterility system is obtained, it is necessary to transfer the pollen from the male parent to the female parent. Similarly to other legumes, in L. mutabilis, manual cross-pollination to produce large quantities of hybrid seed for yield trials is difficult and time-consuming, and very poor rates of hybrid seed set are obtained [197]. With increasing interest in the potential of L. mutabilis to become a higher-value lupin grain, additional efforts to improve crossing and hybrid breeding technologies for this species are being carried out. Studies that are examining crossing methods to improve seed set without the use of sterility are underway.
Insect-aided technology and the efficient use of local pollinators as an agent of crossing for hybrid seed production has been recommended [198]. Pollinators forage non-randomly among plants by using floral cues to recognize the available options. Effective cross-pollination largely depends on the types of pollinators visiting flowers and the manipulation of their pollinator behavior by the plant’s reproductive characteristics [199]. The characteristics of flowers may lead to a substantial difference in outcrossing. The concept of this approach is to develop a crop with floral traits that influences pollinator behavior and pollination efficiency, which in turn is linked to plant mating patterns and thus to potentially increasing or decreasing the outcrossing rate. Therefore, both pollinator behavior and pollinator interactions with floral traits should be considered in the context of developing a hybrid seed technology.
To increase the level of outcrossing and simultaneously improve crops’ environmental functions (bee-pollinator conservation) in order to support better integration into a healthy agroecosystem, the crop design system (CDS) approach has been proposed. Detailed information on the CDS approach was published by Suso et al. [200]. In the CDS approach, breeders develop cultivars with enhanced heterozygosity as a result of appropriate functional floral traits (discovery, attraction and reward) within the crop for supporting the bee pollinator populations to be used as agents of crossings.
Flowers are the interface at which plants and pollinators interact, and their functional traits will influence how likely a pollinator is to visit the flower. Kazimierska and Kazimierski [175] review the biology of flowering in several Lupinus species. Lupin provides a rich foraging habitat for several beneficial insects, with mass flowering and substantial amounts of nutritious pollen. In addition to pollen, which provides nutritive rewards to bees, functional morphology modifies both attraction and handling efficiency [201]. Pollen transfer efficiency is mediated by the mechanical fit of pollinators to flower morphology. Lupinus mutabilis has a typical papilionated flower. The petals are modified into a standard, wings and keel, with the reproductive structures being enclosed by the keel. Due to the elaborate architecture of Papilionoideae flowers, the application and reception of pollen is achieved only through very specialized mechanisms [201]. The flower possesses three basic functional structures. The standard is for visual discovery and attraction. Besides its visual role as an advertisement, the standard has at least one other important role: the formation of a pollen guide. Lupinus mutabilis has a yellow spot that may help to highlight the design of the flower during the approach, making foraging more efficient. The wings facilitate the landing of the pollinator as well as the required active handling of the keel. The keel also has an essential function: it provides the structure that helps to release the hidden pollen and deposit it onto the visiting bee. Simple morphological mismatches appearing in the flowers could therefore be problematic (Figure 2). The manipulation of mechanisms that control various crop floral traits for the benefit of pollinators could represent a promising future direction for L. mutabilis crop improvement and hybrid breeding technology. This approach has been first proposed by Suso et al. [202] and Suso and Río [176], specifically for faba bean, and it has been advocated in several other crops by other researchers [192,203,204,205,206,207,208,209].

7. Crop Modeling for Yield Production Enhancement

Indirect introduction of a crop or a variety aiming to build up new industries, e.g., lupin oil, might be time consuming as the crop is not well adapted to the new environment. Andean lupin in its domestication area grows under the rainy season, from October to May, with annual average temperatures ranging from 11 to 18 °C [10]. In Europe, especially in southern countries, different edaphoclimatic conditions and cultivation practices are applied. Choosing appropriate genotypes, which are adapted to each region, is therefore essential [22]. In this context, plant traits like growth habit (indeterminate or determinate) and time interval between growth developmental stages were found to play a key role in the ability of L. mutabilis plants to grow and be productive [22]. A high genetic variability was also observed within the species [56] available for selection and breeding purposes.
After years of experimentation, determinate growth types were found to be more appropriate for Northern European countries, which are characterized by a shorter growth cycle and therefore are able to be productive under the short spring/summer period of cultivation, while indeterminate growth types were found to be more productive in Southern Europe [22,56,64]. In Southern European conditions, an early sowing from October to November [22,64] is also recommended, in parallel to appropriate genotype selection, since life cycle reduction and yield losses are observed due to the impact of high temperatures during the late crop season [64].
The number of days from sowing to flowering of an accession was recorded as varying among experimental years, and this was therefore not considered to be the most accurate method for predicting Andean lupin growth stages and production [64]. Regarding L. mutabilis, low temperatures during the vegetative phase do not seem to play an important role in the time of flowering [59], with the exception of late-maturing genotypes, where vernalization can decrease their flowering time by three weeks [65]. Furthermore, Andean lupin has been reported to be either neutral to photoperiod or affected and complete its biological cycle earlier during short days [27]. The number of days from sowing to the initiation of the different developmental stages of L. mutabilis has also been shown to vary among accessions, while day length and temperature effects were possibly responsible for this variation [64], as in other lupin species [210,211]. Determination of thermal and/or photoperiod requirements of selected L. mutabilis accessions would probably be a more helpful method in selecting Andean lupin accessions, as in other legume crops [212,213,214] and lupin species [61,70,215,216] under Mediterranean climate conditions.

8. Conclusions and Perspectives

Andean lupin is one of the “lost crops of the Incas” [217]. Worldwide, there has been an increased interest in this crop. This review demonstrates the possibilities of Andean lupin in the “Old World”. Andean lupin has many benefits for the farmer, the environment and processing industries, as well the consumer. Andean lupin is high in protein and oil, has beneficial effects on its environment and can serve as raw material for the development of added value products in the biobased economy. Since its first systematic research in Europe, Andean lupin is now becoming a promising new crop. Decades of breeding and agronomical research have eventually resulted in a few accessions which are (partly) adapted to European agro-ecological conditions. The EU funded project LIBBIO has created a few accessions and agronomical practices which provide perspectives for arable farming in Europe. As for every crop, Andean lupin needs to be improved and continuously adapted to the changing conditions imposed upon us by the consequences of climate change.
More research is necessary to further understand and improve the crop and its agronomical practices. Especially, the crop’s advantages relative to other crops, with respect to drought tolerance, pest and disease resistance and the effects of soil conditions like alkaline and calcareous soil on L. mutabilis growth and production, have not yet been studied extensively. Anthracnose is an important fungal disease and threat for lupin species worldwide. Breeding for anthracnose resistance and developing agronomical practices, e.g., seed disinfection, for reducing the probability of anthracnose infections is of the utmost importance. Anthracnose resistance appears to be available in gene bank collections and seems to be correlated with the anthocyanin pigmentation of L. mutabilis seeds. Cropping management practices for optimal weed control and the study of pollinators are other themes which need additional research. Future studies on L. mutabilis should aim to fill these knowledge gaps. Andean lupin, with its versatile applications, provided by valuable ingredients and its untapped genetic variability, is a promising crop and treasure that can fit into sustainable and resilient cropping systems and contribute to the biobased economy in Europe and the rest of the world.

Author Contributions

P.J.B. conceived the idea and was in charge of overall coordination and planning and prepared the final version of the manuscript. P.J.B., E.L., T.C., M.-J.S., W.H. and A.A.A. wrote the draft. P.J.B., E.L., T.C., M.-J.S., W.H., A.A.A., G.C., R.J.F.v.H., M.H.J., C.M., J.N.-M., U.P., F.S., D.P.S., P.T. and M.v.d.B. provided critical feedback and commented on the manuscript. All authors have read and agreed to the published version of the manuscript.


This research was funded by the Bio-based Industries Joint Undertaking under the European Union’s Horizon 2020 research and innovation programme, the LIBBIO project, under grant agreement No. 720726 and the APC was also funded under the framework of the LIBBIO project, under grant agreement No 720726.


We thank Francisco Javier Ortiz for helping with the bee and bumblebee studies.

Conflicts of Interest

The authors declare no conflict of interest.


  1. Eastwood, R.J.; Drummond, C.S.; Schifino-Wittmann, M.T.; Hughes, C.E. Diversity and Evolutionary History of Lupins—Insights from New Phylogenies. In Proceedings of the 12th International Lupin Conference—Lupins for Health and Wealth, Fremantle, Australia, 14–18 September 2008; pp. 346–354. [Google Scholar]
  2. Gresta, F.; Wink, M.; Prins, U.; Abberton, M.; Capraro, J.; Scarafoni, A.; Hill, G. Lupins in European cropping systems. Legum. Crop. Syst. 2017, 88–108. [Google Scholar] [CrossRef]
  3. Sherasia, P.L.; Garg, M.R.; Bhanderi, B.M. Pulses and Their By-Products As Animal Feed; Calles, T., Makkar, H.P.S., Eds.; FAO: Rome, Italy, 2018; ISBN 9789251099155. [Google Scholar]
  4. Mousavi-Derazmahalleh, M.; Nevado, B.; Bayer, P.E.; Filatov, D.A.; Hane, J.K.; Edwards, D.; Erskine, W.; Nelson, M.N. The western Mediterranean region provided the founder population of domesticated narrow-leafed lupin. Theor. Appl. Genet. 2018, 131, 2543–2554. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  5. Abraham, E.M.; Ganopoulos, I.; Madesis, P.; Mavromatis, A.; Mylona, P.; Nianiou-Obeidat, I.; Parissi, Z.; Polidoros, A.; Tani, E.; Vlachostergios, D. The use of lupin as a source of protein in animal feeding: Genomic tools and breeding approaches. Int. J. Mol. Sci. 2019, 20, 851. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  6. Cowling, W.; Buirchell, B.J.; Tapia, M.E. Lupin. Lupinus spp. In Plant Genetic Resources of Legumes in the Mediterranean; Maxted, N., Bennett, S.J., Eds.; Springer: Dordrecht, The Netherlands, 2001; pp. 191–206. [Google Scholar]
  7. Aïnouche, A.K.; Bayer, R.J. Phylogenetic relationships in Lupinus (Fabaceae: Papilionoideae) based on internal transcribed spacer sequences (ITS) of nuclear ribosomal DNA. Am. J. Bot. 1999, 86, 590–607. [Google Scholar] [CrossRef] [PubMed]
  8. Wolko, B.; Clements, J.C.; Naganowska, B.; Nelson, M.N.; Yang, H. Lupinus. In Wild Crop Relatives: Genomic and Breeding Resources: Legume Crops and Forages; Kole, C., Ed.; Springer: Berlin/Heidelberg, Germany, 2011; pp. 153–206. ISBN 978-3-642-14387-8. [Google Scholar]
  9. Finch, H.J.S.; Samuel, A.M.; Lane, G.P.F. Lockhart & Wiseman’s Crop Husbandry Including Grassland; Woodhead Publishing: Cambridge, UK, 2014; pp. 337–361. ISBN 978-1-78242-371-3. [Google Scholar]
  10. Falconí, C.E. Lupinus mutabilis in Ecuador with Special Emphasis on Anthracnose Resistance; Wageningen University: Wageningen, The Netherlands, 2012. [Google Scholar]
  11. Heistinger, A.; Pistrick, K. “Altreier Kaffee”: Lupinus pilosus L. cultivated as coffee substitute in Northern Italy (Alto Adige/Südtirol). Genet. Resour. Crop Evol. 2007, 54, 1623–1630. [Google Scholar] [CrossRef]
  12. Einarsson, S.; Gudmundsson, J.; Sverrisson, H.; Kristjansson, J.K.; Runolfsson, S. Production of Rhizobium inoculants for Lupinus nootkatensis on nutrient- supplemented pumice. Appl. Environ. Microbiol. 1993, 59, 3666–3668. [Google Scholar] [CrossRef] [Green Version]
  13. Björnsson, H. Fertilization of Notka lupin (Lupinus nootkatensis) for biomass production and carbon sequestration. Icel. Agric. Sci. 2007, 20, 81–92. [Google Scholar]
  14. Riege, D.A.; Sigurgeirsson, A. Facilitation of afforestation by Lupinus nootkatensis and by black plastic mulch in south-west Iceland. Scand. J. For. Res. 2009, 24, 384–393. [Google Scholar] [CrossRef]
  15. Aniszewski, T. Nutritive quality of the alkaloid-poor Washington lupin (Lupinus polyphyllus lindl var SF/TA) as a potential protein crop. J. Sci. Food Agric. 1993, 61, 409–421. [Google Scholar] [CrossRef]
  16. Douglas, G.B.; Foote, A.G. Establishment of perennial species useful for soil conservation and as forages. N. Z. J. Agric. Res. 1994, 37, 1–9. [Google Scholar] [CrossRef]
  17. Kurlovich, B.S.; Heinanen, J. Breeding of perennial fodder forms of multifoliate lupin (Lupinus polyphyllus Lindl.). In Proceedings of the Wild and Cultivated Lupins from the Tropics to the Poles, Laugarvatn, Iceland, 19–24 June 2002; Jónsdóttir, R.S., Ed.; International North Express: Laugarvatn, Iceland, 2002; pp. 67–69. [Google Scholar]
  18. Tello, F.T. Lupinus mutabilis sweet—A potent food source from the Andean region. Am. J. Clin. Nutr. 1976, 29, 933. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  19. Kurlovich, B.S.; Stankevich, A.K.; Stepanova, S.I. The history of lupin domestication. In Lupins (Geography, Classification, Genetic Resources and Breeding); Kurlovich, B.S., Ed.; OY International North Express: St. Petersburg, Russia, 2002; pp. 147–165. [Google Scholar]
  20. Eastwood, R.J.; Hughes, C.E. Origins of domestication o Lupinus mutabilis in the Andes. In Proceedings of the Lupins for Health and Wealth Proceedings 12th International Lupin Conference, Fremantle, Australia, 14–18 September 2008; pp. 14–18. [Google Scholar]
  21. Atchison, G.W.; Nevado, B.; Eastwood, R.J.; Contreras-Ortiz, N.; Reynel, C.; Madriñán, S.; Filatov, D.A.; Hughes, C.E. Lost crops of the incas: Origins of domestication of the Andean pulse crop Tarwi, Lupinus mutabilis. Am. J. Bot. 2016, 103, 1592–1606. [Google Scholar] [CrossRef] [PubMed]
  22. Neves Martins, J.M.; Talhinhas, P.; Bruno de Sousa, R. Yield and seed chemical composition of Lupinus mutabilis in Portugal. Rev. Ciências Agrárias 2016, 39, 518–525. [Google Scholar] [CrossRef] [Green Version]
  23. Gulisano, A.; Alves, S.; Martins, J.N.; Trindade, L.M. Genetics and Breeding of Lupinus mutabilis: An Emerging Protein Crop. Front. Plant Sci. 2019, 10, 1–13. [Google Scholar] [CrossRef] [PubMed]
  24. Carvajal-Larenas, F.E.; Linnemann, A.R.; Nout, M.J.R.; Koziol, M.; van Boekel, M.A.J.S. Lupinus mutabilis: Composition, Uses, Toxicology, and Debittering. Crit. Rev. Food Sci. Nutr. 2016, 56, 1454–1487. [Google Scholar] [CrossRef] [Green Version]
  25. Gross, R.; von Baer, E.; Koch, F.; Marquard, R.; Trugo, L.; Wink, M. Chemical composition of a new variety of the Andean lupin (Lupinus mutabilis cv. Inti) with low-alkaloid content. J. Food Compos. Anal. 1988, 1, 353–361. [Google Scholar] [CrossRef]
  26. Caligari, P.D.S.; Römer, P.; Rahim, M.A.; Huyghe, C.; Neves-Martins, J.; Sawicka-Sienkiewicz, E.J. The Potential of Lupinus mutabilis as a crop. In Linking Research and Marketing Opportunities for Pulses in the 21st Century: Proceedings of the Third International Food Legumes Research Conference; Knight, R., Ed.; Springer: Dordrecht, The Netherlands, 2000; pp. 569–573. ISBN 978-94-011-4385-1. [Google Scholar]
  27. Jacobsen, S.E.; Mujica, A. Geographical distribution of the Andean lupin (Lupinus mutabilis Sweet). Plant Genet. Resour. Newsl. 2008, 155, 1–8. [Google Scholar]
  28. Fischer, A.; Von Sengbusch, R. Geschichte des Lupinenanbaus und die Verbreitung der Lupinen in Deutschland, sowie die Möglichkeiten der Erweiterung des Lupinenbaus. Der Züchter (Zeitschrift für Theor. und Angew. Genet.) 1935, 7, 182–207. [Google Scholar]
  29. Raabe, A.; von Sengbusch, R. Züchterisch wichtige Beobachtungen an einigen Lupinenarten. Der Züchter 1935, 7, 244–248. [Google Scholar] [CrossRef]
  30. Lucas, M.M.; Stoddard, F.L.; Annicchiarico, P.; Frías, J.; Martínez-Villaluenga, C.; Sussmann, D.; Duranti, M.; Seger, A.; Zander, P.M.; Pueyo, J.J. The future of lupin as a protein crop in Europe. Front. Plant Sci. 2015, 6, 705. [Google Scholar] [CrossRef]
  31. Święcicki, W.; Kroc, M.; Kamel, K.A. Lupins. In Grain Legumes; De Ron, A.M., Ed.; Springer: New York, NY, USA, 2015; pp. 179–218. ISBN 978-1-4939-2797-5. [Google Scholar]
  32. van de Noort, M. Lupin: An Important Protein and Nutrient Source. In Sustainable Protein Sources; Nadathur, S.R., Wanasundara, J.P.D., Scanlin, L.B.T., Eds.; Academic Press: San Diego, CA, USA, 2017; pp. 165–183. ISBN 978-0-12-802778-3. [Google Scholar]
  33. Frick, K.M.; Kamphuis, L.G.; Siddique, K.H.M.; Singh, K.B.; Foley, R.C. Quinolizidine Alkaloid Biosynthesis in Lupins and Prospects for Grain Quality Improvement. Front. Plant Sci. 2017, 8, 87. [Google Scholar] [CrossRef] [PubMed]
  34. Galek, R.; Sawicka-Sienkiewicz, E.; Zalewski, D.; Stawiński, S.; Spychała, K. Searching for low alkaloid forms in the Andean lupin (Lupinus mutabilis) collection. Czech J. Genet. Plant Breed. 2017, 53, 55–62. [Google Scholar] [CrossRef] [Green Version]
  35. FAOSTAT Lupin Production in Tonnes in Europe. Available online: (accessed on 31 March 2020).
  36. Golubev, A.A.; Kurlovich, B.S. Diseases and pests. In Lupins (Geography, Classification, Genetic Resources and Breeding); Kurlovich, B.S., Ed.; OY International North Express: St. Petersburg, Russia, 2002; pp. 205–225. [Google Scholar]
  37. Talhinhas, P.; Baroncelli, R.; Le Floch, G. Anthracnose of lupins caused by Colletotrichum lupini: A recent disease and a successful worldwide pathogen. J. Plant Pathol. 2016, 98, 5–14. [Google Scholar] [CrossRef]
  38. Hill, G.D. The composition and nutritive value of lupin seed. Nutr. Abstr. Rev. Ser. B Livest. Feeds Feed. 1977, 47, 511–529. [Google Scholar]
  39. Horn, P.E.; Hill, G.D.; Porter, N.G. Yield and nutrient composition of seventeen Lupinus mutabilis lines. In Proceedings of the 8th Agronomy Society Conference; 1978; pp. 73–77. [Google Scholar]
  40. Adomas, B.; Galek, R.; Gas-Smereka, M.; Helios, W.; Hurej, M.; Kotecki, A.; Kozak, M.; Malarz, W.; Okorski, A.; Agnieszka, I.P.-C.; et al. Adaptation of the Andean lupin (Lupinus mutabilis Sweet) to Natural Conditions of South-Western Poland; Kotecki, A., Ed.; University of Life Sciences Publishing House in Wroclaw: Wrocław, Poland, 2015; ISBN 9788377172353. [Google Scholar]
  41. Olczak, T.; Rurek, M.; Janska, H.; Augustyniak, H.; Sawicka-Sienkiewicz, E. Screening of cytoplasmic DNA diversity between and within Lupinus mutabilis Sweet and Lupinus albus sensu lato by restriction fragment length polymorphism (RFLP). J. Appl. Genet. 2001, 42, 127–137. [Google Scholar]
  42. Pszczółkowska, A.; Okorski, A.; Kotecki, A.; Gas, M.; Kulik, T.; Reczek, A. Incidence of seed-borne fungi on Lupinus mutabilis depending on a plant morphotype, sowing date and plant density. J. Elem. 2016, 21, 501–512. [Google Scholar] [CrossRef] [Green Version]
  43. Neves-Martins, J.M.; Silva, P.M.R.; Sousa, R.F.X. Evaluation of Lupinus mutabilis accessions for protein and oil in Portugal. In Lupinus mutabilis: Its Adaptation and Production under European Pedoclimatic Conditions, Proceedings of a Workshop of the Agrimed Research Program, Cascais, Portugal, 26–27 April 1991; Commission of the European Communities: Cascais, Portugal, 1992; pp. 1–10. [Google Scholar]
  44. Jones, R.A.C.; Burchell, G.M. Resistance to Cucumber mosaic virus in Lupinus mutabilis (pearl lupin). Australas. Plant Pathol. 2004, 33, 591–593. [Google Scholar] [CrossRef]
  45. Hurej, M.; Kucharczyk, H.; Twardowski, J.P.; Kotecki, A. Thrips (Thysanoptera) associated with two morphological forms of Andean lupin (Lupinus mutabilis). Biologia (Bratisl) 2015, 70, 935–942. [Google Scholar] [CrossRef]
  46. Mikić, A.; Ćupina, B.; Mihailović, V.; Krstić, D.; Antanasović, S.; Zorić, L.; Dordević, V.; Perić, V.; Srebrić, M. Intercropping white (Lupinus albus) and Andean (Lupinus mutabilis) lupins with other annual cool season legumes for forage production. S. Afr. J. Bot. 2013, 89, 296–300. [Google Scholar] [CrossRef] [Green Version]
  47. Zoga, M.; Pawelec, A.; Galek, R.; Sawicka-Sienkiewicz, E. Morphological, cytological and molecular characteristics of parents and interspecific hybrid (Lupinus mutabilis LM-13 × Lupinus albus sensu lato). In Proceedings of the 12th International Lupin Conference, Fremantle, Australia, 14–18 September 2008; International Lupin Association: Canterbury, New Zealand, 2008; pp. 173–176. [Google Scholar]
  48. Galek, R.; Kozak, B.; Sawicka-Sienkiewicz, E.; Zalewski, D.; Nowosad, K. Searching for the most useful genotypes of Lupinus mutabilis sweet for breeding purpose. Electron. J. Pol. Agric. Univ. 2017, 20. [Google Scholar] [CrossRef]
  49. Masefield, G.B. A Preliminary Trial of the Pearl Lupin in England. Exp. Agric. 1975, 11, 113–118. [Google Scholar] [CrossRef]
  50. Masefield, G.B. Further Trials of Pearl Lupins in England. Exp. Agric. 1976, 12, 97–102. [Google Scholar] [CrossRef]
  51. Gnatowska, M.; Święcicki, W.K.; Wolko, B. Preliminary data on the outcrossing rate in sweet Lupinus mutabilis. In Lupin, an Ancient Crop for the New Millennium: Proceedings of the 9th International Lupin Conference, Klink/Müritz, Germany, 20–24 June 1999; International Lupin Association: Lima, Peru, 1999; pp. 167–168. [Google Scholar]
  52. Hardy, A.; Huyghe, C.; Rahim, M.A.; Roemer, P.; Neves-Martins, J.M.; Sawicka-Sienkiewicz, E.; Caligari, P.D.S. Effects of genotype and environment on architecture and flowering time of indeterminate Andean lupins (Lupinus mutabilis Sweet). Aust. J. Agric. Res. 1998, 49, 1241–1251. [Google Scholar] [CrossRef]
  53. Hardy, A.; Huyghe, C. Physiological bases of the poor adaptation of current Lupinus mutabilis genotypes to European conditions. Grain Legum. 1997, 15, 9–10. [Google Scholar]
  54. Lopez-Bellido, L.; Fuentes, M. Growth, Yield, and Yield Components of Lupin Cultivars. Agron. J. 1990, 82, 1050–1056. [Google Scholar] [CrossRef]
  55. Galek, R.A.; Kozak, B.; Biela, A.; Zalewski, D.; Sawicka-Sienkiewicz, E.; Spychała, K.; Stawiński, S. Seed coat thickness differentiation and genetic polymorphism for Lupinus mutabilis sweet breeding. Turk. J. Field Crops 2016, 21, 305–312. [Google Scholar] [CrossRef]
  56. Guilengue, N.; Alves, S.; Talhinhas, P.; Neves-Martins, J. Genetic and genomic diversity in a tarwi (Lupinus mutabilis sweet) germplasm collection and adaptability to mediterranean climate conditions. Agronomy 2020, 10, 21. [Google Scholar] [CrossRef] [Green Version]
  57. Lazaridi, E.; Sideris, E.; Tani, E.; Sotirakoglou, K.; Neves-Martins, J.; Bebeli, P.J. Assessing phenotypic diversity of lupin landraces (Lupinus mutabilis Sweet). In Proceedings of the 15th International Lupin Conference, Cochabamba, Bolivia, 18–21 March 2019; p. 130. [Google Scholar]
  58. Lazaridi, E.; Kapsi, E.; Papadopoulos, G.; Neves-Martins, J.; Bebeli, P.J. Lupinus mutabilis growth, seed yield and biological nitrogen fixation ability under different Rhizobia inoculation treatmentsin comparison to other lupin species. In Proceedings of the 15th International Lupin Conference, Cochabamba, Bolivia, 18–21 March 2019; p. 160. [Google Scholar]
  59. Keatinge, J.D.H.; Qi, A.; Wheeler, T.R.; Ellis, R.H.; Summerfield, R.J. Effects of temperature and photoperiod on phenology as a guide to the selection of annual legume cover and green manure crops for hillside farming systems. Field Crops Res. 1998, 57, 139–152. [Google Scholar] [CrossRef]
  60. Zou, L. Effects of Gradual and Sudden Heat Stress on Seed Quality of Andean Lupin, Lupinus mutabilis. Ph.D. Thesis, University of Helsinki, Helsinki, Finland, September 2009. [Google Scholar]
  61. López-Bellido, L. The potential of lupins in agriculture of the Iberian Peninsula. In Lupinus mutabilis: Its Adaptation and Production under European Pedoclimatic Conditions, Proceedings of a Workshop of the Agrimed Research Program, Cascais, Portugal, 26–27 April 1991; Commission of the European Communities: Cascais, Portugal, 1992; pp. 117–123. [Google Scholar]
  62. Sawicka-Sienkiewicz, E.J.; Augiewicz, J. Genetic studies of Andean lupin (Lupinus mutabilis Sweet). In Wild and Cultivated Lupins from the Tropics to the Poles, Proceedings of the 10th International Lupin Conference, Laugarvatn, Iceland, 19–24 June 2002; van Santen, E., Hill, H.D., Eds.; International Lupin Association: Canterbury, New Zealand, 2002; p. 136. [Google Scholar]
  63. Von Sengbusch, R.; Zimmermann, K. Die Auffindung der ersten gelben und blauen Lupinen (Lupinus luteus und Lupinus angustifolius) mit nichtplatzenden Hülsen und die damit zusammenhängenden Probleme, insbesondere die der Süßlupinenzüchtung. Der Züchter 1937, 9, 57–65. [Google Scholar] [CrossRef] [Green Version]
  64. Lazaridi, E.; Bebeli, P.J. Effect of sowing date on Andean lupin accessions performance under a Mediterranean climate. Manuscript under Preparation.
  65. Adhikari, K.N.; Buirchell, B.J.; Sweetingham, M.W. Length of vernalization period affects flowering time in three lupin species. Plant Breed. 2012, 131, 631–636. [Google Scholar] [CrossRef]
  66. Rahman, M.S.; Gladstones, J.S. Control of lupin flower initiation by vernalization, photoperiod and temperature under controlled environment. Aust. J. Exp. Agric. 1972, 12, 638–645. [Google Scholar] [CrossRef]
  67. Taylor, C.M.; Kamphuis, L.G.; Zhang, W.; Garg, G.; Berger, J.D.; Mousavi-Derazmahalleh, M.; Bayer, P.E.; Edwards, D.; Singh, K.B.; Cowling, W.A.; et al. INDEL variation in the regulatory region of the major flowering time gene LanFTc1 is associated with vernalization response and flowering time in narrow-leafed lupin (Lupinus angustifolius L.). Plant Cell Environ. 2019, 42, 174–187. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  68. Ksiazkiewicz, M.; Nazzicari, N.; Yang, H.; Nelson, M.N.; Renshaw, D.; Rychel, S.; Ferrari, B.; Carelli, M.; Tomaszewska, M.; Stawiński, S.; et al. A high-density consensus linkage map of white lupin highlights synteny with narrow-leafed lupin and provides markers tagging key agronomic traits. Sci. Rep. 2017, 7, 1–15. [Google Scholar] [CrossRef] [PubMed]
  69. Hackbarth, J. Die genzentren der Gattung Lupinus in der Neuen Welt und ihre Bedeutung für die Züchtung. Zeitschrift fur Pflanzenzuecht 1961, 63, 237–245. [Google Scholar]
  70. Huyghe, C. Possible ways to control the vegetative development in Lupinus mutabilis. Retrospects and Prospects. In Lupinus mutabilis: Its Adaptation and Production under European Pedoclimatic Conditions, Proceedings of a Workshop of the Agrimed Research Program; Commission of the European Communities: Cascais, Portugal, 1992; pp. 147–154. [Google Scholar]
  71. Carvalho, I.S.; Ricardo, C.P.; Chaves, M. Quality and distribution of assimilates within the whole plant of lupines (L. albus and L. mutabilis) influenced by water stress. J. Agron. Crop Sci. 2004, 190, 205–210. [Google Scholar] [CrossRef]
  72. Carvalho, I.S.; Chaves, M.; Pinto Ricardo, C. Influence of Water Stress on the Chemical Composition of Seeds of Two Lupins (Lupinus albus and Lupinus mutabilis). J. Agron. Crop Sci. 2005, 191, 95–98. [Google Scholar] [CrossRef]
  73. Lizarazo, C.; Stoddard, F.; Mäkelä, P.; Santanen, A. Genetic variability in the physiological responses of Andean lupin to drought stress. Suom. Maatal. Seuran Tied. NRO 2010, 1–5. [Google Scholar] [CrossRef]
  74. Sweetingham, M. The Potential of the Pearl Lupin (Lupinus mutabilis) for Southern Australia; Department of Agriculture and Food WA: Canberra, Australia, 2014.
  75. Peiter, E.; Yan, F.; Schubert, S. Lime-induced growth depression in Lupinus species: Are soil pH and bicarbonate involved? J. Plant Nutr. Soil Sci. 2001, 164, 165–172. [Google Scholar] [CrossRef]
  76. Annicchiarico, P.; Thami Alami, I. Enhancing white lupin (Lupinus albus L.) adaptation to calcareous soils through selection of lime-tolerant plant germplasm and Bradyrhizobium strains. Plant Soil 2012, 350, 131–144. [Google Scholar] [CrossRef]
  77. Ding, W.; Clode, P.L.; Clements, J.C.; Lambers, H. Sensitivity of different Lupinus species to calcium under a low phosphorus supply. Plant Cell Environ. 2018, 41, 1512–1523. [Google Scholar] [CrossRef]
  78. Barda, M. Characterization of Andean Lupin (L. mutabilis Sweet) Germplasm and Recording of Pollinators at Two Locations at Greece. Masters’s Thesis, Agricultural University of Athens, Athens, Greece, 5 March 2018. [Google Scholar]
  79. Tang, C.; Thomson, B.D. Effects of solution pH and bicarbonate on the growth and nodulation of a range of grain legume species. Plant Soil 1996, 186, 321–330. [Google Scholar] [CrossRef]
  80. Tang, C.; Robson, A.D.; Longnecker, N.E.; Buirchell, B.J. The growth of Lupinus species on alkaline soils. Aust. J. Agric. Res. 1995, 46, 255–268. [Google Scholar] [CrossRef]
  81. Yánez-Mendizábal, V.; Falconí, C.E. Efficacy of Bacillus spp. to biocontrol of anthracnose and enhance plant growth on Andean lupin seeds by lipopeptide production. Biol. Control 2018, 122, 67–75. [Google Scholar] [CrossRef]
  82. Falconí, C.E.; Yánez–Mendizábal, V. Dry heat treatment of Andean lupin seed to reduce anthracnose infection. Crop Prot. 2016, 89, 178–183. [Google Scholar] [CrossRef]
  83. Jacob, I.; Feuerstein, U.; Heinz, M.; Schott, M.; Urbatzka, P. Evaluation of new breeding lines of white lupin with improved resistance to anthracnose. Euphytica 2017, 213. [Google Scholar] [CrossRef]
  84. Guilengue, N.; Neves-Martins, J.; Talhinhas, P. Response to Anthracnose in a Tarwi (Lupinus mutabilis) Collection Is Influenced by Anthocyanin Pigmentation. Plants 2020, 9, 583. [Google Scholar] [CrossRef]
  85. Dewitte, K.; Landschoot, S.; Carrette, J.; Audenaert, K.; Haesaert, G. Exploration of essential oils as alternatives to conventional fungicides in lupin cultivation. Org. Agric. 2019, 9, 107–116. [Google Scholar] [CrossRef]
  86. Johnson, S.K.; Clements, J.; Villarino, C.B.J.; Coorey, R. Chapter 8—Lupins: Their Unique Nutritional and Health-Promoting Attributes. In Gluten-Free Ancient Grains: Cereals, Pseudocereals, and Legumes: Sustainable, Nutritious, and Health-Promoting Foods for the 21st Century; Taylor, J.R.N., Awika, Eds.; Elsevier: Amsterdam, The Netherlands, 2017; pp. 179–221. ISBN 978-0-08-100866-9. [Google Scholar]
  87. Guaytarilla, C.P.B.; Falconí, C.S. Seleccion por arquitectura de la planta y resistencia a la Antracnosis de 7 Genotipos de Chocho (Lupinus mutabilis). Congr. Cienc. Tecnol. 2014, 9, 63–70. [Google Scholar]
  88. Tapia, M.E. Cultivos Andinos Subexplotados y so Aporte a la Alimentacion, 2nd ed.; Oficina Regional de la FAO para América Latina y el Caribe: Santiago, Chile, 2000. [Google Scholar]
  89. von Bayer, E. Domestication of Andean Lupin (L. mutabilis). In Lupin Crops—An Opportunity for Today, a Promise for the Future, Proceedings of the 13th International Lupin Conference, Poznań, Poland, 6–10 June 2011; Naganowska, B., Kachlicki, P., Wolko, B., Eds.; International Lupin Association: Poznan, Poland, 2011; pp. 129–132. [Google Scholar]
  90. Falconi, C.E.; Visser, R.G.F.; van Heusden, S. Influence of plant growth stage on resistance to anthracnose in Andean lupin (Lupinus mutabilis). Crop Pasture Sci. 2015, 66, 729–734. [Google Scholar] [CrossRef] [Green Version]
  91. Falconí, C.E.; Visser, R.G.F.; van Heusden, A.W. Phenotypic, Molecular, and Pathological Characterization of Colletotrichum acutatum Associated with Andean Lupine and Tamarillo in the Ecuadorian Andes. Plant Dis. 2013, 97, 819–827. [Google Scholar] [CrossRef] [Green Version]
  92. Caicedo, C.V.; Peralta, E. El cultivo de chocho Lupinus mutabilis Sweet: Fitonutrición, Enfermedades y Plagas. INIAP Quito Equador 2001. [Google Scholar]
  93. Falconí, C.E.; Yánez-Mendizábal, V. Efficacy of UV-C radiation to reduce seedborne anthracnose (Colletotrichum acutatum) from Andean lupin (Lupinus mutabilis). Plant Pathol. 2018, 67, 831–838. [Google Scholar] [CrossRef]
  94. Lamichhane, J.R.; Dürr, C.; Schwanck, A.; Robin, M.-H.; Sarthou, J.-P.; Cellier, V.; Messean, A.; Aubertot, J.-N. Integrated management of damping-off diseases. A review. Agron. Sustain. Dev. 2017, 37, 1–25. [Google Scholar] [CrossRef]
  95. Singh, R.J.; Jauhar, P.P. Genetic Resources, Chromosome Engineering, and Crop Improvement. Vol 1: Grain Legumes; Taylor & Francis: Boca Raton, FL, USA, 2005; ISBN 0849314305. [Google Scholar]
  96. Sweetingham, M.W. Anthracnose workshop report. In Lupin, an Ancient Crop for the New Millennium, Proceedings of the 9th International Lupin Conference, Klink/Müritz, Germany, 20–24 June 1999; International Lupin Association: Klink/Muritz, Germany, 2000; pp. 63–69. [Google Scholar]
  97. Sweetingham, M.W.; Jones, R.A.C.; Brown, A.G.P. Diseases and Pests. In Lupin as Crop Plants. Biology, Production and Utilization; Gladstones, J., Atkins, C., Hamblin, J., Eds.; CAB International: Cambridge, UK, 1998; pp. 263–289. [Google Scholar]
  98. Thomas, G.; Jones, R.; Vanstone, V. Diseases of lupin. In Producing lupins; White, P., French, B., McLarty, A., Eds.; Department of Agriculture and Food: Perth, Australia, 2008; pp. 101–120. [Google Scholar]
  99. French, R.J. Lupin: Agronomy. In Encyclopedia of Food Grains, 2nd ed.; Wrigley, C., Corke, H., Seetharaman, K., Faubion, J., Eds.; Academic Press: Oxford, UK, 2016; pp. 231–239. ISBN 978-0-12-394786-4. [Google Scholar]
  100. Meng, Y.; Zhang, Q.; Ding, W.; Shan, W. Phytophthora parasitica: A model oomycete plant pathogen. Mycology 2014, 5, 43–51. [Google Scholar] [CrossRef]
  101. Duke, J. Handbook of Legumes of World Economic Importance, 1st ed.; Springer: New York, NY, USA, 1981. [Google Scholar]
  102. Sator, C. Lupins (Lupinus spp.) Legumes and Oilseed Crops I. In Biotechnology in Agriculture and Forestry; Bajaj, Y.P.S., Ed.; Springer: Berlin/Heidelberg, Germany, 1990; pp. 288–311. ISBN 978-3-642-74448-8. [Google Scholar]
  103. Landers, K.; Sutherland, S.; Sykes, J. Lupin, best practice management for sustainable production. In Lupin; NSW Agriculture: Orange, Australia, 2000; pp. 3–44. [Google Scholar]
  104. Wunderlich, N.; Ash, G.J.; Harper, J.D.I.; Cowley, R.B.; Luckett, D.J. Penetration and symptom development of Pleiochaeta root rot in susceptible and resistant Lupinus albus cultivars. Australas. Plant Pathol. 2008, 37, 387–391. [Google Scholar] [CrossRef]
  105. Wijayanto, T.; Barker, S.J.; Wylie, S.J.; Gilchrist, D.G.; Cowling, W.A. Significant reduction of fungal disease symptoms in transgenic lupin (Lupinus angustifolius) expressing the anti-apoptotic baculovirus gene p35. Plant Biotechnol. J. 2009, 7, 778–790. [Google Scholar] [CrossRef] [Green Version]
  106. Loughman, R.; Sweetingham, M.W. Control of Pleiochaeta setosa diseases of lupin using seed and fertiliser applied fungicides. Aust. J. Exp. Agric. 1991, 31, 493–498. [Google Scholar] [CrossRef]
  107. Chen, X.; Wang, Y. Phytophthora Sojae Biological Invasions and Its Management in China: Volume 2; Wan, F., Jiang, M., Zhan, A., Eds.; Springer: Singapore, 2017; pp. 199–223. ISBN 978-981-10-3427-5. [Google Scholar]
  108. Torrena, P.S. Phytophthora Parasitica and Lupin (Lupinus angustifolius) Interactions: Changes in Gene Expression during Infection and after Phosphate Treatment. Ph.D. Thesis, Australian National University, Canberra, Australia, 11 May 2017. [Google Scholar] [CrossRef]
  109. Blackman, L.M.; Cullerne, D.P.; Torreña, P.; Taylor, J.; Hardham, A.R. RNA-Seq Analysis of the Expression of Genes Encoding Cell Wall Degrading Enzymes during Infection of Lupin (Lupinus angustifolius) by Phytophthora parasitica. PLoS ONE 2015, 10. [Google Scholar] [CrossRef] [Green Version]
  110. Nishimura, M.; Nishizawa, Y.; Fujikawa, T.; Mitsuhara, I.; Minami, E.; Abe, K.; Tachiki, T.; Yano, S. Methods for Preventing or Inhibiting Microbial Infection of Plants and Plant Excibiting Resistance to Microbial Infection. U.S. Patent 002361.6, 26 January 2012. [Google Scholar]
  111. Curry, P.J.; Diehl, F.I. Antimicrobial Composition. U.S. Patent 0323,037 A1, 23 December 2010. [Google Scholar]
  112. Shaikh, S.; Wani, S.; Sayyed, R. Impact of Interactions between Rhizosphere and Rhizobacteria: A Review. J Bacteriol. Mycol. 2018, 5, 1058. [Google Scholar]
  113. Sato, T.; Tomioka, K.; Nakanishi, T.; Koganezawa, H. Charcoal rot of yacon (Smallanthus sonchifolius (Poepp. et Endl.) H. Robinson), Oca (Oxalis tuberosa Molina) and pearl lupin (Tarwi, Lupinus mutabilis Sweet) caused by Macrophomina phaseolina (Tassi) Goid. Bull. Shikoku Natl. Agric. Exp. Stn. 1999, 64, 1–8. [Google Scholar]
  114. Dankevych, L.; Leonova, N.; Dragovoz, I.; Patyka, V.; Kalinichenko, A.; Wlodarczyk, P.; Wlodarczyk, B. The synthesis of plant growth stimulators by phytopathogenic bacteria as factor of pathogenicity. Appl. Ecol. Environ. Res. 2018, 16, 1581–1593. [Google Scholar] [CrossRef]
  115. Gould, C.J.J. Diseases of Cultivated Lupines. Proc. Iowa Acad. Sci. 1939, 46, 119–125. [Google Scholar]
  116. DPIRD, G. My Crop. Lupins. Available online: (accessed on 31 October 2019).
  117. Jones, R.A.C.; McLean, G.D. Virus diseases of lupins. Ann. Appl. Biol. 1989, 114, 609–637. [Google Scholar] [CrossRef]
  118. Ferenc, B.; István, L.; János, K.G. Csillagfürtfajok Növény Védelme. Tecnológia 2008, 44, 279–296. [Google Scholar]
  119. Hull, R. Virus diseases of garden lupin in Great Britain. Ann. Appl. Biol. 1968, 61, 373–380. [Google Scholar] [CrossRef]
  120. Eppler, A.; Hinz, U.; Romer, P. Virus-diseases of Lupinus mutabilis Sweet in Germany. Meded. Fac. Landbou Wet. Rijksuniv. Gent 1986, 51, 817–826. [Google Scholar]
  121. Robertson, N.L.; Coyne, C.J. Evaluation of USDA Lupinus sp. collection for seed-borne potyviruses. Plant Genet. Resour. Characterisation Util. 2009, 7, 227–229. [Google Scholar] [CrossRef] [Green Version]
  122. Coutts, B. Diagnosing Bean Yellow Mosaic Virus—Early Symptoms in Narrow-Leafed Lupins. Available online: (accessed on 16 June 2020).
  123. Jones, R.; Coutts, B.; Burchell, G.; Wylie, S. Bean yellow mosaic virus in lupins: Strains, losses, epidemiology and control. In Lupins for Health and Wealth, Proceedings of the 12th International Lupin Conference, Fremantle, Australia, 14–18 September 2008; Palta, J.A., Berger, J.B., Eds.; International Lupin Association: Canterbury, New Zealand, 2008; pp. 420–424. [Google Scholar]
  124. Thackray, D.J.; Diggle, A.J.; Berlandier, F.A.; Jones, R.A.C. Forecasting aphid outbreaks and epidemics of Cucumber mosaic virus in lupin crops in a Mediterranean-type environment. Virus Res. 2004, 100, 67–82. [Google Scholar] [CrossRef]
  125. Jones, R.A.C.; Latham, L.J. Natural resistance to cucumber mosaic virus in lupin species. Ann. Appl. Biol. 1996, 129, 523–542. [Google Scholar] [CrossRef]
  126. Makkouk, K.M.; Kumari, S.G.; van Leur, J.A.G.; Jones, R.A.C. Control of Plant Virus Diseases in Cool-Season Grain Legume Crops, 1st ed.; Elsevier Inc.: Cambridge, MA, USA, 2014; Volume 90, ISBN 9780128012468. [Google Scholar]
  127. Coutts, B.A.; Prince, R.T.; Jones, R.A.C. Further studies on Pea seed-borne mosaic virus in cool-season crop legumes: Responses to infection and seed quality defects. Aust. J. Agric. Res. 2008, 59, 1130–1145. [Google Scholar] [CrossRef]
  128. Sarkisova, T.; Petrzik, K. Determination of the complete nucleotide sequence of a lupine potyvirus isolate from the Czech Republic reveals that it belongs to a new member of the genus Potyvirus. Arch. Virol. 2011, 156, 167–169. [Google Scholar] [CrossRef]
  129. Jones, R.A.C. Developing Integrated Disease Management Strategies Against Non-persistently Aphid-borne Viruses: A Model Programme. Integr. Pest Manag. Rev. 2001, 6, 15–46. [Google Scholar] [CrossRef]
  130. Berlandier, F.A.; Thackray, D.J.; Jones, R.A.C.; Latham, L.J.; Cartwright, L. Determining the relative roles of different aphid species as vectors of cucumber mosaic and bean yellow mosaic viruses in lupins. Ann. Appl. Biol. 1997, 131, 297–314. [Google Scholar] [CrossRef]
  131. Berlandier, F.A.; Sweetingham, M.W. Aphid feeding damage causes large losses in susceptible lupin cultivars. Aust. J. Exp. Agric. 2003, 43, 1357–1362. [Google Scholar] [CrossRef]
  132. Valenzuela, I.; Hoffmann, A.A. Effects of aphid feeding and associated virus injury on grain crops in Australia. Austral Entomol. 2015, 54, 292–305. [Google Scholar] [CrossRef]
  133. Ferguson, A.W. Pests and plant injury on lupins in the south of England. Crop Prot. 1994, 13, 201–210. [Google Scholar] [CrossRef]
  134. Stary, P.; Havelka, J. Macrosiphum albifrons Essig, an invasive lupin aphid and its natural- enemy complex in Czechoslovakia (Homoptera, Aphididae). Acta Entomol. Bohemoslov. 1991, 88, 111–120. [Google Scholar]
  135. Tsitsipis, J.A.; Katis, N.I.; Margaritopoulos, J.T.; Lykouressis, D.P.; Avgelis, A.D.; Gargalianou, I.; Zarpas, K.D.; Perdikis, D.C.; Papapanayotou, A. A contribution to the aphid fauna of Greece. Bull. Insectol. 2007, 60, 31–38. [Google Scholar]
  136. Vučetić, A.; Jovičić, I.; Petrović-Obradović, O. Several new and one invasive aphid species (Aphididae, Hemiptera) caught by yellow water traps in Serbia. Phytoparasitica 2014, 42, 247–257. [Google Scholar] [CrossRef]
  137. Havelka, J.; Tomanović, Ž.; Kos, K.; Kavallieratos, N.G.; Janeček, J.; Pons, X.; Rakhshani, E.; Starý, P. Mountain aphid and parasitoid guilds on Aconitum spp. in Europe. Bull. Insectol. 2014, 67, 57–62. [Google Scholar]
  138. Avtzis, D.N.; Coyle, D.R.; Christopoulos, V.; Roques, A. Biological invasions, national borders, and the current state of non-native insect species in Greece and the neighbouring Balkan countries. Bull. Insectol. 2017, 70, 161–169. [Google Scholar]
  139. Jones, D.R. Plant Viruses Transmitted by Thrips. Eur. J. Plant Pathol. 2005, 113, 119–157. [Google Scholar] [CrossRef]
  140. Ströcker, K.; Wendt, S.; Kirchner, W.H.; Struck, C. Feeding preferences of the weevils Sitona gressorius and Sitona griseus on different lupin genotypes and the role of alkaloids. Arthropod. Plant. Interact. 2013, 7, 579–589. [Google Scholar] [CrossRef]
  141. Cantot, P.; Papineau, J. Discrimination des lupins a basse teneur en alcaloides par les adultes de Sitona lineatus L. (Col., Curculionidae). Agron. Sci. Prod. Veg. L’environnement 1983, 3, 937–940. [Google Scholar] [CrossRef] [Green Version]
  142. Gruppe, A.; Roemer, P. The Lupin Aphid (Macrosiphum albifrons Essig, 1911) (Hom., Aphididae) in West Germany: Its occurrence, host plants and natural enemies. J. Appl. Entomol. 1988, 106, 135–143. [Google Scholar] [CrossRef]
  143. Wink, M.; Witte, L. Storage of Quinolizidine Alkaloids in Macrosiphum albifrons and Aphis genistae (Homoptera: Aphididae). Entomol. Gen. 1991, 15, 237–254. [Google Scholar] [CrossRef]
  144. Barda, M.; Bebeli, P.J. Recording of pollinators and studying the relationship plant-pollinator in lupin breeding. In Proceedings of the 17th Conference of the Hellenic Scientific Society of Plant Genetics and Breeding, Patras, Greece, 17–19 October 2018; pp. 86–87. [Google Scholar]
  145. Callohuari, Y.; Vergara, C.; Jiménez, J. Insect pests associated with Andean lupin (Lupinus mutabilis Sweet) and their parasitoids in Peruvian central coast – (Lima, La Molina). Peruv. J. Agron. 2018, 2, 27–33. [Google Scholar] [CrossRef]
  146. Ivany, J.A.; McCully, K.V. Evaluation of Herbicides for Sweet White Lupin (Lupinus albus). Weed Technol. 1994, 8, 819–823. [Google Scholar] [CrossRef]
  147. Herbert, S.J.; Lucas, R.J.; Pownall, D.B. Weed suppression in high density sowings of lupins. N. Z. J. Exp. Agric. 1978, 6, 299–303. [Google Scholar] [CrossRef] [Green Version]
  148. Cheriere, T. White lupin (Lupinus albus L.) Yield in Pays de la Loire and Its Nitrogen Provisioning Services. Master’s Thesis, Wageningen University & Research, Wageningen, The Netherlands & Ecole Supérieure d’Agricultures, Angers, France, 22 September 2016. [Google Scholar]
  149. Rodrigues-Alves, A.F. Herbicide Screening on Lupinus mutabilis Sweet. Licentiate Thesis, Instituto Politécnico de Santarém, Santarém, Portugal, 2019. [Google Scholar]
  150. Prins, U.; van Haren, R. Andean lupin (Lupinus mutabilis) Cropping and Its Opportunities for Europe; Hanzehogeschool Groningen: Groningen, The Netherlands, 2019. [Google Scholar]
  151. Glowacka, A. The influence of strip cropping and weed control methods on weed diversity in dent maize (Zea mays L.), narrow-leafed Lupin (Lupinus angustifolius L.) and oats (Avena sativa L.). Acta Agrobot. 2013, 66, 185–194. [Google Scholar] [CrossRef] [Green Version]
  152. Hashem, A.; Collins, R.M.; Bowran, D.G. Efficacy of Interrow Weed Control Techniques in Wide Row Narrow-Leaf Lupin. Weed Technol. 2011, 25, 135–140. [Google Scholar] [CrossRef]
  153. Duran, D.; Pacheco, A.; Ruiz-Argüeso, T.; Palacios, J.M.; Imperial, J.; De Rey, L. Centro Relevance of bacterial secretion systems Type III and Type VI in the Bradyrhizobium-Lupinus symbiosis. In Proceedings of the 14th International Lupin Conference, Milan, Italy, 21–26 June 2015; p. 48. [Google Scholar]
  154. Eckhardt, M.M.; Baldwin, I.L.; Fred, E.B. Studies of the Root-Nodule Organism of Lupinus. J. Bacteriol. 1931, 21, 273–285. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  155. Stȩpkowski, T.; Hughes, C.E.; Law, I.J.; Markiewicz, Ł.; Gurda, D.; Chlebicka, A.; Moulin, L. Diversification of lupine Bradyrhizobium strains: Evidence from nodulation gene trees. Appl. Environ. Microbiol. 2007, 73, 3254–3264. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  156. Andrews, M.; Andrews, M.E. Specificity in Legume-Rhizobia Symbioses. Int. J. Mol. Sci. 2017, 18, 705. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  157. Beligala, D.H.; Michaels, H.J.; Devries, M.; Phuntumart, V. Multilocus Sequence Analysis of Root Nodule Bacteria Associated with Lupinus spp. and Glycine max. Adv. Microbiol. 2017, 07, 790–812. [Google Scholar] [CrossRef] [Green Version]
  158. USDA Crop Germplasm Committees (CGC). Available online: (accessed on 31 October 2019).
  159. Reeve, W.; Terpolilli, J.; Melino, V.; Ardley, J.; Tian, R.; De Meyer, S.; Tiwari, R.; Yates, R.; O’Hara, G.; Howieson, J.; et al. Genome sequence of the lupin-nodulating Bradyrhizobium sp. strain WSM1417. Stand. Genomic Sci. 2013, 9, 273–282. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  160. Unkovich, M.J.; Pate, J.S. An appraisal of recent field measurements of symbiotic N2 fixation by annual legumes. Field Crops Res. 2000, 65, 211–228. [Google Scholar] [CrossRef]
  161. Kurlovich, B.S.; Kartuzova, L.T.; Cheremisov, B.M.; Emeljanenko, T.A.; Tikhonovich, I.A.; Kozhemyakov, A.P.; Tchetkova, S.A. Evaluation of the biological nitrogen-fixing ability. Plant Genet. Resour. Newsl. 2000, 123, 68–77. [Google Scholar]
  162. Tapia, M.E. El Tarwi, Lupino Andino, 1st ed.; Corporación Gráfica Universal SAC: Lima, Peru, 2015. [Google Scholar]
  163. Robinson, K.O.; Beyene, D.A.; Van Berkum, P.; Knight-Mason, R.; Bhardwaj, H.L. Variability in plant-microbe interaction between Lupinus lines and Bradyrhizobium strains. Plant Sci. 2000, 159, 257–264. [Google Scholar] [CrossRef]
  164. Howieson, J.G.; Fillery, I.R.P.; Legocki, A.B.; Sikorski, M.M.; Stepkowski, T.; Minchin, F.R.; Dilworth, M.J. Nodulation, nitrogen fixation and nitrogen balance. In Lupins As Crop Plants: Biology, Production and Utilization; Gladstones, J.S., Atkins, C., Hamblin, J., Eds.; CAB International: Oxon, UK, 1998; pp. 149–180. [Google Scholar]
  165. Papineau, J.; Huyghe, C. Le Lupin Doux Protéagineux; France Agricole: Paris, France, 2004. [Google Scholar]
  166. Walker, J.; Hertel, K.; Parker, P.; Edwards, J. Lupin Growth and Development; Edwards, J., Walker, J., McIntosh, G., Eds.; Industry & Investment NSW: New South Wales, Australia, 2011; ISBN 978 1 74256 059 5. [Google Scholar]
  167. Sánchez-Cañizares, C.; Rey, L.; Durán, D.; Temprano, F.; Sánchez-Jiménez, P.; Navarro, A.; Polajnar, M.; Imperial, J.; Ruiz-Argüeso, T. Endosymbiotic bacteria nodulating a new endemic lupine Lupinus mariae-josephi from alkaline soils in Eastern Spain represent a new lineage within the Bradyrhizobium genus. Syst. Appl. Microbiol. 2011, 34, 207–215. [Google Scholar] [CrossRef] [Green Version]
  168. Navarro, A.; Fos, S.; Laguna, E.; Durán, D.; Rey, L.; Rubio-Sanz, L.; Imperial, J.; Ruiz-Argüeso, T. Conservation of Endangered Lupinus mariae-josephae in Its Natural Habitat by Inoculation with Selected, Native Bradyrhizobium Strains. PLoS ONE 2014, 9. [Google Scholar] [CrossRef] [PubMed]
  169. Raza, S.; Jørnsgård, B.; Abou-Taleb, H.; Christiansen, J.L. Tolerance of Bradyrhizobium sp. (Lupini) strains to salinity, pH, CaCO3 and antibiotics. Lett. Appl. Microbiol. 2001, 32, 379–383. [Google Scholar] [CrossRef] [Green Version]
  170. Dracup, M.; Turner, N.; Tang, C.; Reader, M.; Palta, J.; Gladstones, J.; Atkins, C.; Hamblin, J. Responses to abiotic stresses. In Lupins As Crop Plants: Biology, Production and Utilization; Gladstones, J.S., Atkins, C.A., Hamblin, J., Eds.; CAB International: Wallingford, UK, 1998; pp. 227–262. [Google Scholar]
  171. Fernández-Pascual, M.; Pueyo, J.J.; de Felipe, M.R.; Golvano, M.P.; Lucas, M.M. Singular Features of the Bradyrhizobium-Lupinus Symbiosis. Dyn. Soil Dyn. Plant 2007, 1, 1–16. [Google Scholar]
  172. Fernández-Pascual, M.; De Lorenzo, C.; Pozuelo, J.M.; De Felipe, M.R. Alterations Induced by four Herbicides on Lupine Nodule Cortex Structure, Protein Metabolism and some Senescence-Related Enzymes. J. Plant Physiol. 1992, 140, 385–390. [Google Scholar] [CrossRef]
  173. De Felipe, M.R.; Fernandez-Pascual, M.; Pozuelo, J.M. Effects of the herbicides Lindex and Simazine on chloroplast and nodule development, nodule activity, and grain yield in Lupinus albus L. Plant Soil 1987, 101, 99–105. [Google Scholar] [CrossRef]
  174. Suso, M.J.; Bebeli, P.J.; Palmer, R.G. Reproductive Biology of Grain Legumes. In Grain Legumes; De Ron, A.M., Ed.; Springer: New York, NY, USA, 2015; pp. 365–399. ISBN 978-1-4939-2797-5. [Google Scholar]
  175. Kazimierska, E.M.; Kazimierski, T. Biology of flowering, embryological and caryological peculiarilies. In Lupins (Geography, Classification, Genetic Resources and Breeding); Kurlovich, B.S., Ed.; OY International North Express: St. Petersburg, Russia, 2002; pp. 205–239. [Google Scholar]
  176. Suso, M.J.; del Río, R. A crop–pollinator inter-play approach to assessing seed production patterns in faba bean under two pollination environments. Euphytica 2015, 201, 231–251. [Google Scholar] [CrossRef]
  177. Chirinos-Arias, M.C.; Jiménez, J.E.; Vilca-Machaca, L.S. Análisis de la Variabilidad Genética entre treinta accesiones de tarwi (Lupinus mutabilis Sweet) usando marcadores moleculares ISSR. Sci. Agropecu. 2015, 6, 17–30. [Google Scholar] [CrossRef] [Green Version]
  178. Williams, I.H. The Pollination of Lupins. Bee World 1987, 68, 10–16. [Google Scholar] [CrossRef]
  179. Roder, W.; Kharel, D.R.; Gurung, P.R.; Dukpa, P. Pearl Lupine (Lupinus mutabilis) as a Green Manure Crop in the Highlands of Bhutan. J. Sustain. Agric. 1993, 3, 9–20. [Google Scholar] [CrossRef]
  180. Hatzold, T.; Elmadfa, I.; Gross, R.; Wink, M.; Hartmann, T.; Witte, L. Quinolizidine alkaloids in seeds of Lupinus mutabilis. J. Agric. Food Chem. 1983, 31, 934–938. [Google Scholar] [CrossRef]
  181. Cortez, A.; Ruíz, H.; Torres, R. Substitution of Cow’s Milk for Milk of Lupinus mutabilis in the Production of Fresh Cheese. Int. J. Sci. Res. 2017, 6, 2156–2162. [Google Scholar] [CrossRef]
  182. Zambrana, S.; Lundqvist, C.E.L.; Mamani, O.; Catrina, S.-B.; Gonzales, E.; Östenson, C.-G. Lupinus mutabilis Extract Exerts an Anti-Diabetic Effect by Improving Insulin Release in Type 2 Diabetic Goto-Kakizaki Rats. Nutrients 2018, 10, 933. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  183. Msika, P.; Piccirilli, A.; Piccardi, N. Use of a Cosmetic of Pharmaceutical Composition, Comprising a Lupeol-Rich Extract As an Active Ingredient for Stimulating the Synthesis of Heat Shock Protens. U.S. Patent 8,747,815, 10 June 2014. [Google Scholar]
  184. van Haren, R.J.F.; Arnason, P. Lupinus Mutabilis for Increased Biomass from Marginal Lands and Value for BIOrefineries. Available online: (accessed on 14 February 2020).
  185. van Barneveld, R.J. Understanding the nutritional chemistry of lupin (Lupinus spp.) seed to improve livestock production efficiency. Nutr. Res. Rev. 1999, 12, 203–230. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  186. Sedláková, K.; Straková, E.; Suchý, P.; Krejcarová, J.; Herzig, I. Lupin as a perspective protein plant for animal and human nutrition—A review. Acta Vet. Brno 2016, 85, 165–175. [Google Scholar] [CrossRef] [Green Version]
  187. Jeroch, H.; Kozłowski, K.; Mikulski, D.; Jamroz, D.; Schöne, F.; Zduńczyk, Z. Lupinen (Lupinus spp.) als Eiweißfuttermittel für Geflügel. 2) Ergebnisse mit Lupinen in Fütterungsversuchen mit Geflügel und Empfehlungen für Geflügelalleinfutter. Eur. Poult. Sci. 2016, 80. [Google Scholar] [CrossRef]
  188. Jeroch, H.; Kozłowski, K.; Schöne, F.; Zduńczyk, Z. Lupinen (Lupinus spp.) als eiweißfuttermittel für geflügel. 1) sorten, zusammensetzung und nährwert für geflügel. Eur. Poult. Sci. 2016, 80, 1–14. [Google Scholar] [CrossRef]
  189. Glencross, B.; Sweetingham, M.; Hawkins, W. A digestibility assessment of pearl lupin (Lupinus mutabilis) meals and protein concentrates when fed to rainbow trout (Oncorhynchus mykiss). Aquaculture 2010, 303, 59–64. [Google Scholar] [CrossRef]
  190. Molina-Poveda, C.; Lucas, M.; Jover, M. Evaluation of the potential of Andean lupin meal (Lupinus mutabilis Sweet) as an alternative to fish meal in juvenile Litopenaeus vannamei diets. Aquaculture 2013, 410–411, 148–156. [Google Scholar] [CrossRef]
  191. Borreani, G.; Chion, A.R.; Colombini, S.; Odoardi, M.; Paoletti, R.; Tabacco, E. Fermentative profiles of field pea (Pisum sativum), faba bean (Vicia faba) and white lupin (Lupinus albus) silages as affected by wilting and inoculation. Anim. Feed Sci. Technol. 2009, 151, 316–323. [Google Scholar] [CrossRef]
  192. Carruthers, K.; Prithiviraj, B.; Fe, Q.; Cloutier, D.; Martin, R.C.; Smith, D.L. Intercropping corn with soybean, lupin and forages: Yield component responses. Eur. J. Agron. 2000, 12, 103–115. [Google Scholar] [CrossRef]
  193. Roux, S.R.; Höppner, F.; Wiedow, D.; Kanswohl, N. Züchterische Evaluierung der Andenlupine im Vergleich zur weißen und zur blauen Lupine für die Bioenergienutzung. In Proceedings of the Kongress “Mit Pflanzenzüchtung zum Erfolg”, Berlin, Germany, 3–4 April 2017; Gülzower Fachgespräche: Berlin, Germany, 2017. [Google Scholar]
  194. Klein, A.-M.; Vaissière, B.E.; Cane, J.H.; Steffan-Dewenter, I.; Cunningham, S.A.; Kremen, C.; Tscharntke, T. Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B Biol. Sci. 2007, 274, 303–313. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  195. Kobayashi, K.; Tsukamoto, S.; Tanaka, A.; Niikura, S.; Ohsawa, R. Selective flower visitation behavior by pollinators in a radish F1 seed production field. Breed. Sci. 2010, 60, 203–211. [Google Scholar] [CrossRef] [Green Version]
  196. Tester, M.; Langridge, P. Breeding Technologies to Increase Crop Production in a Changing World. Science 2010, 327, 818–822. [Google Scholar] [CrossRef] [PubMed]
  197. Clements, J.C.; Wilson, J.; Sweetingham, M.W.; Quealy, J.; Francis, G. Male Sterility in three crop Lupinus species. Plant Breed. 2012, 131, 155–163. [Google Scholar] [CrossRef]
  198. Palmer, R.G.; Perez, P.T.; Ortiz-Perez, E.; Maalouf, F.; Suso, M.J. The role of crop-pollinator relationships in breeding for pollinator-friendly legumes: From a breeding perspective. Euphytica 2009, 170, 35–52. [Google Scholar] [CrossRef] [Green Version]
  199. Harder, L.D.; Williams, N.M.; Jordan, C.Y.; Nelson, W.A. The effects of floral design and display on pollinator economics and pollen dispersal. In Cognitive Ecology of Pollination: Animal Behaviour and Floral Evolution; Thomson, J.D., Chittka, L., Eds.; Cambridge University Press: Cambridge, UK, 2001; pp. 297–317. ISBN 9780521781954. [Google Scholar]
  200. Suso, M.J.; Bebeli, P.J.; Christmann, S.; Mateus, C.; Negri, V.; Pinheiro de Carvalho, M.A.A.; Torricelli, R.; Veloso, M.M. Enhancing legume ecosystem services through an understanding of plant–pollinator interplay. Front. Plant Sci. 2016, 7, 1–18. [Google Scholar] [CrossRef] [Green Version]
  201. Westerkamp, C.; Weber, A. Keel flowers of the Polygalaceae and Fabaceae: A functional comparison. Bot. J. Linn. Soc. 1999, 129, 207–221. [Google Scholar] [CrossRef]
  202. Suso, M.J.; Harder, L.; Moreno, M.T.; Maalouf, F. New strategies for increasing heterozygosity in crops: Vicia faba mating system as a study case. Euphytica 2005, 143, 51–65. [Google Scholar] [CrossRef]
  203. Soto, V.C.; Maldonado, I.B.; Gil, R.A.; Peralta, I.E.; Silva, M.F.; Galmarini, C.R. Nectar and Flower Traits of Different Onion Male Sterile Lines Related to Pollination Efficiency and Seed Yield of F1 Hybrids. J. Econ. Entomol. 2013, 106, 1386–1394. [Google Scholar] [CrossRef]
  204. Mallinger, R.E.; Prasifka, J.R. Bee visitation rates to cultivated sunflowers increase with the amount and accessibility of nectar sugars. J. Appl. Entomol. 2017, 141, 561–573. [Google Scholar] [CrossRef]
  205. Bailes, E.J.; Pattrick, J.G.; Glover, B.J. An analysis of the energetic reward offered by field bean (Vicia faba) flowers: Nectar, pollen, and operative force. Ecol. Evol. 2018, 8, 3161–3171. [Google Scholar] [CrossRef] [PubMed]
  206. Portlas, Z.M.; Tetlie, J.R.; Prischmann-Voldseth, D.; Hulke, B.S.; Prasifka, J.R. Variation in floret size explains differences in wild bee visitation to cultivated sunflowers. Plant Genet. Resour. Characterisation Util. 2018, 16, 498–503. [Google Scholar] [CrossRef] [Green Version]
  207. Prasifka, J.R.; Mallinger, R.E.; Portlas, Z.M.; Hulke, B.S.; Fugate, K.K.; Paradis, T.; Hampton, M.E.; Carter, C.J. Using nectar-related traits to enhance crop-pollinator interactions. Front. Plant Sci. 2018, 9, 1–8. [Google Scholar] [CrossRef]
  208. Dey, S.S.; Bhatia, R.; Pramanik, A.; Sharma, K.; Parkash, C. A unique strategy to improve the floral traits and seed yield of Brassica oleracea cytoplasmic male sterile lines through honey bee-mediated selection. Euphytica 2019, 215, 111. [Google Scholar] [CrossRef]
  209. Shu, J.; Liu, Y.; Zhang, L.; Li, Z.; Fang, Z.; Yang, L.; Zhuang, M.; Zhang, Y.; Lv, H. Evaluation and selection of sources of cytoplasmic male sterility in broccoli. Euphytica 2019, 215, 1–16. [Google Scholar] [CrossRef]
  210. Keeve, R.; Loubser, H.L.; Krüger, G.H.J. Effects of temperature and photoperiod on days to flowering, yield and yield components of Lupinus albus (L.) under field conditions. J. Agron. Crop Sci. 2000, 184, 187–196. [Google Scholar] [CrossRef]
  211. Christiansen, J.L.; Jørnsgård, B. Influence of day length and temperature on number of main stem leaves and time to flowering in lupin. Ann. Appl. Biol. 2002, 140, 29–35. [Google Scholar] [CrossRef]
  212. Iannucci, A.; Terribile, M.R.; Martiniello, P. Effects of temperature and photoperiod on flowering time of forage legumes in a Mediterranean environment. Field Crops Res. 2008, 106, 156–162. [Google Scholar] [CrossRef]
  213. Papastylianou, P.T.; Bilalis, D. Flowering in sulla (Hedysarum coronarium L. cv. Carmen) and persian clover (Trifolium resupinatum L. cv. Laser) as affected by sowing date in a mediterranean environment. Aust. J. Crop Sci. 2011, 5, 1298–1304. [Google Scholar]
  214. Martos-Fuentes, M.; Fernández, J.A.; Ochoa, J.; Carvalho, M.; Carnide, V.; Rosa, E.; Pereira, G.; Barcelos, C.; Bebeli, P.J.; Egea-Gilabert, C. Genotype by environment interactions in cowpea (Vigna unguiculata L. Walp.) grown in the Iberian Peninsula. Crop Pasture Sci. 2017, 68, 924–931. [Google Scholar] [CrossRef]
  215. Dracup, M.; Thomson, R.J. Narrow-leafed lupins with restricted branching. Ann. Bot. 2000, 85, 29–35. [Google Scholar] [CrossRef] [Green Version]
  216. Karaguzel, O.; Baktir, I.; Cakmakci, S.; Ortacesme, V.; Aydinoglu, B.; Atik, M. Responses of native Lupinus varius (L.) to culture conditions: Effects of photoperiod and sowing time on growth and flowering characteristics. Sci. Hortic. (Amsterdam) 2005, 103, 339–349. [Google Scholar] [CrossRef]
  217. National Research Council. Lost Crops of the Incas: Little-Known Plants of the Andes with Promise for Worldwide Cultivation; The National Academies Press: Washington, DC, USA, 1989; ISBN 978-0-309-04264-2. [Google Scholar]
Figure 1. Chlorosis symptoms in L. mutabilis grown on soil with high calcium carbonate content (CaCO3—37.3%).
Figure 1. Chlorosis symptoms in L. mutabilis grown on soil with high calcium carbonate content (CaCO3—37.3%).
Agronomy 10 01038 g001
Figure 2. (a) Morphological match of a bee and a L. mutabilis flower; (b) Pollinator visit on a L. mutabilis flower, frontal view.
Figure 2. (a) Morphological match of a bee and a L. mutabilis flower; (b) Pollinator visit on a L. mutabilis flower, frontal view.
Agronomy 10 01038 g002
Table 1. Main fungal diseases affecting Andean lupin in Europe and control practices.
Table 1. Main fungal diseases affecting Andean lupin in Europe and control practices.
Fungal DiseasePathogenTransmissionControl Method
AnthracnoseColletotrichum lupiniInfested seed lots, crop stubble
Certified seed [92]
Seed disinfection, i.e., dry heat, UV-C 1 [82,93]
Fungicide application (e.g., azoxystrobin, chlorothalonil, mancozeb) [85]
Crop rotation [37]
Bacillus spp. strains [81]
Fusarium wilt and root rotFusarium spp.Infested seed lots, soilborne
Crop rotation [36]
Available resistance: ECU-688, ECU-5920, ECU-7293 breeding lines [92], K2135 [95], chocho type [96]
Pleiochaeta root rot and brown (leaf) spotPleiochaeta setosa (Ceratophorum setosum)Infested seed lots, plant residuals
Certified seed [98]
Minimum tillage application [98]
Deep dripping prior to the crop establishment [98]
Crop rotation with non-host plant species [98]
Deep sowing, up to 5 cm depth [99]
Root and hypocotyl rotPhytophthora sojae,
Rhizoctonia solani
Crop rotation with cereals [92]
Improvement of soil drainage or selection of well drained fields [92]
Deep dripping (25–30 cm) [98]
1 UV-C: Ultraviolet radiation with wavelengths from 100 to 280 nm
Table 2. Main weed species recorded in Andean lupin fields in Greece and Portugal.
Table 2. Main weed species recorded in Andean lupin fields in Greece and Portugal.
Weed SpeciesAthensKalamataSantarémLife Cycle
Abutilon theophrasti Medik. xA, Su
Ailanthus altissima (Mill.) Swinglex A, Su
Allium roseum L. x P, W
Amaranthus hybridus L.x A, Su
Amaranthus retroflexus L.x A, Su
Ammi majus L. xA, Su
Anthemis spp.xx A, W
Avena spp.xx A, W
Calendula arvensis L. xA, Su
Calystegia sepium (L.) R.Br.x P, Su
Capsella bursa-pastoris (L.) Medik.xx A, W
Chamaemelum fuscatum (Brot.) Vasc. xA, Sp
Chamomilla recutita L.xx A, Su
Chenopodium album L.x A, Su
Chenopodium murale (L.) S. Fuentes, Uotila and Borschx A, Su
Chrysanthemum coronarium (L.) Cass. ex Spachxx A, Su
Convolvulus arvensis L.x A, Su
Datura stramonium L.x xA, Su
Daucus carota L. x B, W
Euphorbia peplus L. x A, Su/W
Fumaria officinalis L.xx A, W
Fumaria parviflora Lam.xx A, W
Geranium spp. x A/B, W
Hordeum murinum L.x A, W
Lactuca serriola L.x A, Su
Lamium amplexicaule L.x A, W
Lavatera cretica L. xA/B, Su
Malva sylvestris L.x B, Su
Medicago arabica (L.) Huds. x A, W
Oryzopsis miliacea Michx. x P, Su
Oxalis pes-carpae L. x A, Su
Papaver rhoeas L.x A, W
Phalaris minor Retz.x A, W
Poa spp.xx A/B, W
Portulaca oleracea L. xA, Su
Rapistrum rugosum (L.) All. x A/B, W
Silybum marianum (L.) Gaertn.x A/B, W
Sinapis spp. x A, W
Sisymbrium irio L.xx A, W
Solanum eleagnifolium Cav.x A, Su
Sonchus oleraceus L.x A, W
Stellaria media (L.) Vill.x A, W
Taraxacum spp.x A, W
Trifolium spp. x A/B, W
Urtica dioica L.x A, Su
Urtica urens L.x A, Su
Veronica persica Poir.xx A.W
Xanthium strumarium L.x A, Su
A: Annual, B: Biennial, P: Perennial, W: Winter, Sp: Spring, Su: Summer.

Share and Cite

MDPI and ACS Style

Bebeli, P.J.; Lazaridi, E.; Chatzigeorgiou, T.; Suso, M.-J.; Hein, W.; Alexopoulos, A.A.; Canha, G.; van Haren, R.J.F.; Jóhannsson, M.H.; Mateos, C.; et al. State and Progress of Andean Lupin Cultivation in Europe: A Review. Agronomy 2020, 10, 1038.

AMA Style

Bebeli PJ, Lazaridi E, Chatzigeorgiou T, Suso M-J, Hein W, Alexopoulos AA, Canha G, van Haren RJF, Jóhannsson MH, Mateos C, et al. State and Progress of Andean Lupin Cultivation in Europe: A Review. Agronomy. 2020; 10(7):1038.

Chicago/Turabian Style

Bebeli, Penelope J., Efstathia Lazaridi, Tilemachos Chatzigeorgiou, Maria-José Suso, Waltraud Hein, Alexios A. Alexopoulos, Gonçalo Canha, Rob J.F. van Haren, Magnús H. Jóhannsson, Carmen Mateos, and et al. 2020. "State and Progress of Andean Lupin Cultivation in Europe: A Review" Agronomy 10, no. 7: 1038.

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop