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Review

Wild and Traditional Barley Genomic Resources as a Tool for Abiotic Stress Tolerance and Biotic Relations

by
Giorgia Capasso
†,
Giorgia Santini
†,
Mariagioia Petraretti
,
Sergio Esposito
* and
Simone Landi
Department of Biology, University of Naples “Federico II”, Via Cinthia, I-80126 Napoli, Italy
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work, so they should considered as co-first authors.
Agriculture 2021, 11(11), 1102; https://doi.org/10.3390/agriculture11111102
Submission received: 24 September 2021 / Revised: 25 October 2021 / Accepted: 3 November 2021 / Published: 5 November 2021
(This article belongs to the Topic Physiological and Molecular Characterization of Crop Tolerance to Abiotic Stresses)
Browse Figure
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Abstract

:
Barley (Hordeum vulgare L.) is one of the main crops cultivated all over the world. As for other cereals, throughout the centuries barley was subjected by human breeding to genetic erosion phenomena, which guaranteed improved yields in organized (and then mechanized) agriculture; on the other hand, this selection weakened the ability of barley to survive under adverse environments. Currently, it is clear that climate change requires an urgent availability of crop varieties able to grow under stress conditions, namely limited irrigation, salinity, high temperatures, and other stresses. In this context, an important role could be played by wild relatives and landraces selected by farmers, particularly in specific field areas and/or climatic conditions. In this review, we investigated the origin of barley and the potentialities of wild varieties and landraces in different contexts, and their resilience to abiotic stress. The data obtained from Next Generation Sequencing technologies were examined to highlight the critical aspects of barley evolution and the most important features for abiotic stress tolerance. Furthermore, the potential of appropriate mycorrhiza is discussed under the view of the essential role played by these symbioses in field crops. The abilities of specific barley wild varieties and landraces may represent novel opportunities and suggest innovative strategies for the improvement of abiotic tolerance in crops and particularly in barley.

1. Introduction

Environmental factors such as drought, salinity, nutrients starvation, and extreme temperatures are critical factors for agricultural production. Therefore, one of the most important challenge for plant researchers is the improvement of crops’ tolerance to stress conditions. [1]. In particular, drought has reduced the yields of most cultivated cereals, and specifically barley; as an example, European barley production has fallen by 3.8% due to temperature increase and rainfall trends in the decade 1989–2009 [2].
The Green Revolution (1940–1960) greatly enhanced agricultural productivity [3]. Crops were selected in order to increase the efficiency of fertilizers and irrigation, defining new strategies for controlling plant pathogens and parasites, thus guaranteeing better and higher yields [4]. On the other side, the massive changes introduced in agricultural techniques have also induced genetic erosion due to the loss of genomic variability [3]. Modern high-performance varieties currently cultivated have been selected for their improved yields under controlled growth conditions of fertilization, pesticides, supply, and irrigation. As consequence, this has caused a loss of genetic diversity with respect to landraces cultivated for centuries by farmers. Traditional landraces acquired a wide genetic diversity during domestication [3], when favorable alleles were selected and fixed [5].
Landraces are generally described as the traditional varieties selected by farmers throughout centuries; these have shown the ability to tolerate environmental changes, maintaining unaltered yields, thus highlighting specific characteristics that differentiate them from commercial, high-yield varieties selected by private companies and public research centers [3,6,7,8].
Among major crops, barley is the fourth most cultivated cereal, representing one of the main sources of carbohydrates in developing countries (FAOstat 2019—9), where it represents one of the main resources grown by small farmers in many arid areas [6,9,10,11,12].
As shown in Figure 1A, Russia was the major producer of barley in 2018 (almost 2.0 × 107 tons), followed by France, Germany, Australia, and Canada. A trend of the yield increases between 2010 and 2018 can be observed (Figure 1B).
Many studies have shown that, even if barley cultivars guarantee a higher yield performance under optimal growth conditions, traditional landraces can exceed selected genotypes yields up to 20% upon stress conditions [5]. These properties could be due to both their metabolic and biochemical flexibilities and molecular peculiarities [13,14,15]. It is worth pointing out that the identification of novel alleles, particularly from unexploited genotypes, is a central challenge for researchers, in order to improve crop productivity in vulnerable environments, thus possibly providing new tools to increase crop yields [16].
The focus of this review is to provide an analysis of traditional barley landraces, ecotypes, and wild relatives properties under abiotic stress. Genomic, transcriptomic, biochemical, and physiological resources will be investigated, also keeping in mind the geographical and evolutionary origin of genus Hordeum. Furthermore, the perspective of the use of appropriate mycorrhiza in order to improve yields and stress resilience will be examined.

2. Barley: Origin, Geographic Evolution, and Relation with Wild Relatives

Barley is one of the oldest domesticated cereals, possibly the first crop cultivated by humankind [17,18]. This cereal is cultivated from the Arctic Circle to equatorial latitudes; therefore, barley’s ability to grow in stressful environments will increase its importance in the coming years.
The history of barley domestication started in the Fertile Crescent, at least 10,000 years ago, selecting the current cultivated crop from a wild progenitor, Hordeum vulgare L. ssp. spontaneum [19,20].
The genus Hordeum comprises about 30 species both perennial and annual, distributed all over the world [21].
The genus is characterized by one-flowered spikelets, borne three together on each rachis. It should be noted that the two lateral spikelets are generally sterile in wild species; another property on Hordeum genus is the presence of a reduced glume on the dorsal side of spikelets.
Barley genome is about 5.1 Gb, showing abundance of repetitive elements [22]. Different authors reported genetic erosion processes, by comparing wild and domesticated barleys, thus highlighting a severe reduction (about 50%) of diversity [23,24]. Probably, this condition derived by reduced allelic re-assortment during meiosis and restricted recombination in the pericentromeric regions, possibly caused by an intensive and stringent selection by breeders [25].
A principal-components analysis (PCA) recently made partitioned 228 accessions into two distinct groups, representing 91 wild varieties (Hordeum vulgare ssp. spontaneum) and 137 landraces (Hordeum vulgare ssp. vulgare) [26]. Genome-wide analysis indicated that rare SNPs variants were more common in wild varieties, carrying on average over 5000 private alleles, while domesticated landraces showed less than 430 private alleles. Therefore, this large genetic variation observed in wild barley could represent a promising genetic pool to be studied and utilized for crop improvement in the next decades. Landraces, and possibly all cultivated, selected genotypes, exhibited a very low variation in private alleles, in order to obtain higher yields in farmer-assisted cultivated fields. On the other hand, domestication obviously resulted in a loss of diversity, as a consequence, further improvement of these varieties with respect to wild relatives is limited [26].
A number of barley varieties (both wild and selected) genomes have been recently sequenced. It is worth noting that a 4.28 Gb genome has been indicated for the wild barley WB1 (Hordeum vulgare ssp. spontaneum) [27], and a 3.89 Gb genome for the Tibetan barley “qingke” [28].
Hordeum vulgare ssp. spontaneum group exhibited a genetic diversity largely related to geographic distribution. This can be observed by ordering different samples along the Fertile Crescent and connecting these with accessions from Central Asia. The geographic correlation is more pronounced in Hordeum vulgare ssp. vulgare [26].
Barley landraces can be divided in two groups, distinguished by structure of inflorescence, containing two or six rows of grains, respectively. This feature has been recently used to define cultivated barley as two species, Hordeum distichum L. and Hordeum hexastichum L., obviously descending from H. vulgare ssp. spontaneum (originally presenting two-rows of grains). Interestingly, these changes occurred during—or soon after—domestication, when mutations arose in a single gene, SIX-ROWED SPIKE 1 (HvVRS1) [29].
The critical sweeps characterizing two key loci namely nonbrittle rachis 1 and 2 (Btr-1, Btr-2) have been analyzed and multiple novel candidate genes for domestication were identified [30]. Among these, interesting candidates are involved in light signaling regulation, circadian clock, and carbohydrate metabolism. It is worth noting that modifications in genes related to circadian clock are common during the breeding and selection of modern crops, thus suggesting a convergent evolution during domestication. Examples are EID1 (an F-box protein functioning as a negative regulator of phytochrome-A in tomato (Solanum lycopersicum)); or SUPPRESSOR of PHYTOCHROME A (SPA) and CUL4 in Arabidopsis thaliana, which are all components of the E3 ubiquitin ligase COP1-CUL4-SPA complex, the main regulator of photomorphogenesis in higher plants [30,31,32].
Genomic and geographic analyses delineated the occurrence of three different clusters in the genetic pool of wild barley: (i) Levant and Southern Turkey cluster, (ii) Southeastern Turkey cluster, and (iii) Eastern and Middle Asian cluster. Among these, the Levant cluster showed the highest diversity in wild Hordeum vulgare ssp. spontaneum gene pool [18]. Also, genomic analysis of wild barley accessions revealed the presence of 57.8 single nucleotide variants (SNVs) unique in these genotypes. This evidence suggested a huge loss of genetic diversity when comparing modern vs. wild barleys. These results also confirm that wild barley has a larger gene pool than cultivated varieties, thus indicating that many genetic resources for barley improvement are present and still unexploited [26,27]. Moreover, a genotyping approach on accessions from Anatolia identified further loci involved in the adaptation of barley to adverse environments: a calmodulin like protein (CML), a member of the heat shock protein 40 kDa (HSP40), an adenine nucleotide alpha hydrolases-like protein, and the transcriptional co-repressor SEUSS [20]. Beneficial effects by these alleles were proposed for flooding tolerance, leaf senescence, and scavenging of reactive oxygen species [20].
Possibly, modern barley originated in the Near East Fertile Crescent, which is commonly recognized as a major evolutionary center for this crop [19,33], but a theory for a mosaic origin of barley genome has been recently proposed [24]. Several authors recognized Tibet as a secondary but crucial center of diversification for the modern barley [24,34].
Particularly, the annual barley (Hordeum vulgare L.) of the Qinghai-Tibet plateau is considered one of the ancestors of cultivated barley [35]. It has been recently reported the transcript sequencing of 9 Hordeum vulgare ssp. vulgare and 12 H. Hordeum vulgare ssp. spontaneum genotypes, thus identifying 8177 and 7913 SNVs from Near East barleys and Tibetan barleys, respectively. The authors proposed a Fertile Crescent derivation for chromosomes 1 H, 2 H, and 3 H and a Tibet origin for chromosomes 4 H, 5 H, 6 H, and 7 H. This hypothesis was reinforced by the genomic characterization of the six-rowed wild barley Hordeum agriocrithon Åberg [36].
Zeng et al. [37] refused this hypothesis, by sequencing 177 barley genomes, prevalently from Tibet. They suggested a phylogenetic origin from eastern domesticated barley, refusing a parental role for Tibetan barley. To support their thesis, the authors analyzed five genes involved in key traits of domestication, namely btr1–2, sixrowed spike (vrs1 and int-c), and naked caryopsis (nud). Tibetan barley showed a sharing of these haplotypes with modern barley genotypes, thus sustaining the hypothesis that barley domestication has originally occurred in the Fertile Crescent [33,37]. Despite of a possible ambiguous relationship between cultivated and Tibetan barleys, genome sequencing clearly indicated a specific and useful adaptation to environmental stress by Eastern barleys. Particularly, these varieties have been predicted to show enhanced phenylpropanoid and flavonoid biosynthesis, essential for the accumulation of sunscreen molecules protecting against ultraviolet radiation, and for plant hormone signal transduction [28].
Therefore, peculiar characteristics from different geographic origins could be investigated and analyzed to identify particular genes and traits by conventional and specific -omics approaches.
Table 1 shows different genotypes, both landraces and wild relatives, described as tolerant to environmental perturbations, by physiological and/or molecular adaptations.

3. Omics Approach of Barley Genotypes Identified Peculiar Genes Involved in Abiotic Stress Tolerance

Traditional agricultural practices and modern breeding programs originated over 800 landraces and over than 100 QTLs associated with stress-sensitive traits [39,50,51,52]. These elite barley cultivars reported limited genetic variability when compared to wild progenitors, thus indicating the wild varieties and traditional landraces as a primary—and still unexplored—source of genes for genetic improvement [27,53,54].
Different wild barley genotypes exhibited interesting potential to improve drought tolerance [39,50,51]. Bedada et al. [39] identified genes expressed under drought conditions, studying two wild barley varieties from a collection of Hordeum vulgare ssp. spontaneum ecotypes [55]. In particular, B1K2 and B1K30 (from Negev Desert and Mediterranean area, respectively) showed 839 and 881 transcripts related to drought stress. The most abundant stress-related gene families were zinc-finger proteins (185 in B1K2; 241 in B1K30), ABC transporters (104 in B1K2; 93 in B1K30), and heat shock proteins (HSPs) (61 in B1K2; and 63 in B1K30).
In barley, changes in HSPs following growth and stress conditions, and the occurrence associated to different genotypes has been described over 30 years ago [56]. Accordingly, peculiar roles of HSP70 proteins have recently been analyzed in tolerant landraces, such as Batinì from MENA region, demonstrating a rapid up-regulation under drought stress and salinity [14].
The genomic resources from Tibetan barley varieties and other genotypes could represent a useful resource to design new breeding strategies to counteract environmental stress, increase tolerance against pathogens, and improve grain qualities. Recently, genes identified in Tibetan genotypes of Hordeum vulgare ssp. spontaneum have been used for biotechnology approaches. HsCBL8 (calcium-sensor calcineurin B-like) and HsCIPKs (CBL-interacting protein kinase) were overexpressed in rice, contributing to an improved tolerance to salinity [46].
Southern Asia represents one of the environments for barley diversification, producing a number of typical ecotypes in geographic areas such as China or Tibet [35,37]. Particularly, the Qinghai-Tibetan region offered the perfect background to develop landraces tolerant to different adverse conditions [43]. Accessions reported to be tolerant upon abiotic stress included XZ5, XZ147, XL, and Z772 for drought [43,45,48,49,57]; XZ166 for salinity [46]; X16 and XZ29 for aluminum [45,47]; and XZ149 for low nitrogen [44].
Tibetan varieties analyzed upon drought using -omics approaches were Z772, XL, XZ5, and Himalaya 10 [42,47,49,57]. These genotypes were analyzed using three different experimental strategies to induce stress: (i) dry dishes; (ii) hydroponic culture using PEG; (iii) irrigation deprivation in greenhouse. These studies identified comprehensive catalogues of candidate genes able to improve drought tolerance. Tibetan barley Z772 after 1 h and 5 h of dehydration stress, showed 5439 and 7203 up-regulated genes, respectively; the number of down-regulated genes was 1143 after 1 h and 1662 after 5 h. The XL genotype showed ≈550 up-regulated and about 350 down-regulated different abundant proteins (DAP) after both 4 and 8 h. In the cultivar Himalaya 10 the gene expression pattern of 853 potential drought-resistant-related genes clustered into nine clusters. Furthermore, Z772 was compared with the drought sensitive genotype Z013 [49]. Both showed among the best-expressed genes several LEA proteins (Late Embryogenesis Abundant) such as HVU0335383.1, HVU037049, HVU005858.3, HVU032486.1, and HVU037051. Moreover, common mechanisms in both drought-sensible and -tolerant genotypes were identified in phosphatidylinositol signaling and in the regulation of chlorophyll synthesis and photosynthetic antenna proteins; other up-regulated factors of drought stress response are threalose 6-phosphate synthase/phosphatase, delta-1-pyrroline-5-carboxylate synthase (P5CS), heat shock protein 70 kDA (HSP70), and protein phosphatase 2C (PP2C) [49].
Regulations of enzymes involved in the avoiding of water loss were also reported for Tibetan genotypes subjected to salinity and nitrogen starvation [58,59]. Particularly, wax biosynthesis was a major process regulated in Z772 after a short-term drought.
Cuticle wax and cell wall play an important role in the survival of plants, creating an interface between plants and biotic/abiotic environmental stress response [60,61]. CER1 (Very -long-chain aldehyde decarbonylase) and FAR (fatty acyl-CoA reductase) were quickly up regulated, thus highlighting the importance of an increased wax biosynthesis, in order to protect plant from an excessive water loss, particularly through non-stomatal processes. CER1 encodes for the major enzyme synthetizing long-chain alkanes; it plays a crucial role in wheat wax alkane biosynthesis under drought and other stresses [62]. Arabidopsis plants overexpressing CER1 showed a reduced cuticle permeability together with a minor water deficit susceptibility and an increased tolerance to osmotic stress [63]. Similarly, the expression of FAR genes is induced by drought, cold, and ABA treatments, increasing the cuticular wax accumulation in Brachypodium distachyon and wheat [61,64].
Different results have been obtained in XL genotypes where drought induced changes in the regulation of ethylene, salicylic acid, and abscisic acid [57]. Conversely, similar analysis in the drought-sensitive cultivar DQ showed an increase of osmotic stress sensors and leaf senescence-related genes. These differences could be caused by the different response of hormone-related genes, particularly for ethylene [57]. In addition, XL genotypes showed an efficient regulation of genes involved in ROS response. The expression of ascorbate peroxidase, glutathione peroxidase, and peroxyredoxins increased during the short-term drought response, suggesting an efficient detoxification mechanism in XL genotype [57].
Comparison between drought-tolerant and -sensitive genotypes were reported using the XZ5 and XZ54 genotypes [57]. This analysis identified 36 genes that were differentially up-regulated or unchanged in XZ5 and showing a decreased expression in XZ54 upon drought. These genes were related to cell wall modification, antioxidant process, and root hair development. In this regard, the authors identified a novel β-expansin gene (HvEXPB7), showing a critical role in root hair growth, conferring an increased drought stress tolerance [57].
Phenotyping and genotyping approaches on a collection of Mediterranean barley landraces identified QTLs able to contribute drought and heat stresses tolerance in these genotypes [65,66]. These landraces showed an efficient attenuation of leaf carbon metabolism under drought when compared with German genotypes [41,67]. Similarly, a sequencing approach on 135 barley landraces from Spain identified 9920 bi-allelic markers. These SNPs can be associated with agro-climatic parameters, thus identifying candidate genotypes adapted to cold-stress and water availability [67].
Furthermore, a comparison between Spanish barley landrace SBCC07 and German selected cultivar Scarlett (sensitive to water stress) identified genotypic and transcriptomic differences in different metabolic pathways in plants subjected to severe and prolonged water deficit, thus suggesting the evolution of different strategies to counteract environmental stresses in elite cultivar and landraces [41]. Particularly, SBCC07 showed the peculiar regulation of phenyalanine metabolism, glycine-betaine biosynthesis, ferulate, and sinapate biosynthetic pathways, while common drought-regulated mechanisms were observed, including starch phosphorylation, chorismate biosynthesis, ascorbate biosynthesis, and metabolism of spermidine [41].
Barley resistance to abiotic stress in different varieties, landraces, and wild relatives have important fallout on yields and quality of seed grains.
The most important utilization of barley harvested in Europe and North America is the utilization as substrate for malting process [68,69,70] and brewing, a thousand-years-old practice which has played a crucial role in human societies [71]. A metabolomic approach was made on cultivated genotypes and Tibetan barley accessions, in order to examine how the genomic differences and the drought response can affect malting quality [72]. Intriguingly, Tibetan accessions showed higher levels of sugars (e.g., fructose) and organic acids (e.g., malic acid) compared to cultivated genotypes, upon both control conditions and drought stress. Under water deprivation, the wild Tibetan barley showed an increased β-amylase expression and enzymatic activity.
Definitely, these results demonstrate the potential of barley landraces to improve malting quality in adverse environments.

4. Physiological Adaptation of Barleys upon Abiotic Stresses

Wild barley (Hordeum vulgare ssp. spontaneum L.) has a large geographical distribution, ranging from deserts to highlands [19]. This results in a wide environmental stress exposition, such as drought, high temperature, and soil salinity. The correlation between genetic and environmental variation vs. distribution suggests a local adaptation along micro- and macro-environmental gradients [39,73]. Among the traits characterizing the tolerance of barley to drought, leaf water content [74], osmotic potential, and full turgor [74,75], concentration of water-soluble carbohydrates [75] and chlorophyll parameters (e.g., fluorescence) [76] are the most evident. These characteristics are correlated with morphological characteristics such as germination, flowering time, plant height and tillering, root growth, and grain yield. Furthermore, differences between the ecotypes of desert and Mediterranean wild barleys were observed, suggesting the adaptation to specific environmental conditions [40,55,77].
High genomic variations were observed in five cultivated and wild barley cultivars from Barley1K collection, almost twice as much genetic variation in nature as cultivated barley [78]. This suggests that many untapped, and potentially useful, genetic variations are separated in wild barley [41,79]. Bedada et al. [39] have selected B1K2 and B1K30 from the B1K4 collection based on their response to drought. They observed perspiration, weight gain and weight loss, water efficiency (WUE), and relative leaf content (RWC) in greenhouse-grown plants, under natural light and semi-controlled humidity. Unexpectedly, the desert ecotype lost more water than the Mediterranean cultivar upon both well-watered conditions and drought (reduced volumetric water content to 30%). Despite its higher transpiration, the desert cultivar maintained a higher RWC than the Mediterranean ecotype in dry conditions. In addition, the ratio of cumulative weight gain on plant transpiration revealed that the desert ecotype has a higher WUE than the Mediterranean ecotype, with the WUE calculated as the ratio between RWC and transpiration rate [39].
Cantalapiedra et al. [41] determined—on two Scarlett cultivars and a Spanish landrace (SBCC073)—changes in physiological properties in both greenhouse and growth chamber, by imposing water stress after the beginning of stem lengthening. The authors analyzed parameters such as leaf water potential (LWP), stomatal conductance, and relative water content (RWC). LWP was proportional to different water regimes with drought-prone plants showing a higher LWP than those that were well irrigated. The highest absolute value corresponded to Scarlett’s plants upon drought, while SBCC073 plants were comparable to Scarlett exposed to heat and drought stress. RWC was lower in drought-stressed plants of both genotypes, but mild heat conditions showed similar values for SBCC073 control and treated plants, and drought-exposed Scarlett variety [41].
Rollins et al. [38] reported a case study for the Syrian landrace Arta and the Australian variety Keel upon drought, heat, and combined stresses. These treatments caused significantly stronger senescence of lower leaves in Arta than in Keel. Moreover, drought had a stronger effect on morphology than physiological traits. Water regime induced a 26% grain yield (GY) change, a 57% biomass increase, and 79% of the peak number variation (SN), while it caused only 18% of the relative water content (RWC) and less than 1% of the photosynthetic performance index (PI). In contrast, heat treatment had stronger effects than drought, thus explaining a 54% variation in water use effectiveness (WUE), 34% in RWC, and 74% in PI. In contrast, heat treatment had minor effects on plant growth, causing a slight 8% change in biomass and 2% in plant height [79].
More evident changes were observed under combined treatments, particularly a strong reduction in GY. GY was significantly lower in Keel than Arta under separate stress, while significant decreases in GY were not significantly different under either drought or heat [38].

5. Mycorrhizal Symbiosis in Cereals: Perspectives for Improving Barley Yields

Arbuscular mycorrhizal fungi (AMF) represent the most widespread form of symbiosis present in terrestrial environments, associated to the majority of land plants [80]. AMF strongly influence diversity and productivity of both forests and agricultural fields, playing a central role in nutrient cycles (e.g., phosphorus, K), and showing evident impacts on microbial populations, also protecting plants from pathogens’ attack, even affecting soil texture and composition [81,82]. Roughly 90% of plant species spontaneously associate with mycorrhizal fungi, and these symbioses are present in 79% of monocotyledons, including most cereal crops [80,83].
Endosymbiosis with mycorrhizal fungi requires hundreds of plant genes, involved in many signaling pathways, including stress response [84]. It has been suggested that land plant ancestors were pre-adapted to mycorrhizal symbioses: several components of signaling involved in symbiosis have been identified in the genome of green algae [85]. On the other hand, it has been recently proposed that fungal symbioses originated from the selective loss/shift of genes involved in the secretion of cell wall hydrolytic enzymes, in order to allow the access of microorganisms in the plant tissues [86].
In cereals, a genotype-dependent variation of mycorrhization levels has been reported, indicating that older wheat varieties (before 1950) show a higher root colonization degree when compared to varieties selected after 1950. Similarly, the oldest barley varieties (i.e., Nürnberg, 1831) present a deeper AM colonization with respect to more recent genotypes (i.e., Xanadu, 2003) [87].
Mycorrhizal symbioses in the roots of cereals have been thoroughly investigated and reviewed [88]. Furthermore, modern selected varieties lost part of those genes involved in symbioses with opportunistic AM strains, due to standard cultivation practices. This results in a loss of benefits deriving by mutualistic symbioses under not-controlled growth conditions, such as stress [89].
Many points are still obscure, e.g., the effects of phytohormones on the establishment of AM symbioses. It should be underlined that if the involvement of strigolactones/karrikins signaling during the establishment of AM is predictable [88], the effects of auxins [90] and gibberellins signaling and transduction on the type and degree of AM symbiosis requires further investigations [91]. These studies clearly connect the establishing of these symbioses with stress conditions, which could severely affect the colonization by specific mycorrhizal strains. Recently, wheat (Triticum aestivum ssp. vulgare) and spelt (Triticum aestivum var. spelta) have been studied under drought to establish changes in roots–fungi association [92]. It has been shown that changes occur in the composition of fungal communities in both endosphere and rhizosphere. Interestingly, it has been proven that over 117 fungal strains, representing 22 genera, are able to colonize T. aestivum ssp. spelta L. and T. aestivum ssp. vulgare L. [92].
Intriguingly, in wheat the composition of the mycobiome depends on root tissue and soil preparation, but it looks barely dependent on irrigation and/or drought [92]. In contrast, a recent study in Oryza sativa varieties demonstrates that drought tolerance is determinant for fungal colonization and endophytic mycobiota in rice [93]. Therefore, different parameters can influence the association and determine modifications in the growth and productivity of cereals.
The majority of fungal strains were detected in the rhizosphere (63 strains), while in the endosphere 54 strains were observed. It should be underlined an almost identical diversity among endophytic fungi; (25 vs. 27 strains). At the same time, one third of fungal species were detected in both endosphere and rhizosphere. Another point is that AM colonizing spelt are substantially identical to those known for wheat. This would suggest that the variability of fungal communities in different cereals would depend on soil composition more than specie-specific parameters. Particularly, Trichoderma strains exerted positive effects by ameliorating a number of physiologic and biochemical parameters and increasing the resistance vs. fungal pathogens, such as Botrytis cinerea, Fusarium spp., Pythium, and many others [93].
Thus, it could be argued that the age of the variety could affect AM protection against pathogens, and thus AMF colonization in plant roots causes bioprotective effects against soil fungal pathogens [94,95]. It has been reported that root colonization by AMF reduced root lesions caused by Gaeumannomyces graminis var. tritici in both wheat and barley [96].
Particularly, the protection in AM-colonized roots is more evident in some barley genotypes, but not in others. This protection against pathogens can be observed only over a critical level of AM root colonization. Furthermore, it looks like this protective effect varies between oldest and modern barley varieties [87].
Therefore, the use of mycorrhizal fungi in agricultural fields, and particularly in cereal crops, can reduce the use of agrochemicals, because AMF symbioses protect the roots against pathogens. In the long term, their use can reduce the cultivation charges both in developing and industrialized countries. In addition, mycorrhized plants are often more competitive and tolerant to environmental stress than not-mycorrhized plants [85].
A further important point is that the colonization of cereal roots by specific fungi is able to protect, or avoid, the infection from specific fungal pathogens, such as Gaeumannomyces graminis and different Fusarium species (F. avenaceum, F. culmorum, F. graminearum, F. oxysporum, and F. poae) [93].
As confirmed, the ancient barley landrace Nürnberg after AM root colonization showed a protective effect in lesioned roots, and an ameliorated fresh weight (FW), suggesting an enhanced bioprotection caused by AMF; in the modern variety Xanadu, only the root FW was positively affected by AM colonization [87].
Investigations of wild barley for reaction to different pests revealed extensive genetic variation as well in specie-specific as partial resistance. One exception is the mlo genes (Mildew Resistance Locus) in barley [97]. The Mlo resistance to powdery mildew (caused by the fungal pathogen Erysiphe graminis f. sp. hordei) derived from a spontaneously occurring mlo gene present in Ethiopian landrace barleys. MLO proteins have been identified as general mechanical-response proteins in plants [98,99]. Extensive studies on mutagen-induced Mlo resistance have paved the way for the present extensive use of Mlo resistance in barley breeding and production in Europe. It has been suggested that MLO1 gene was required for colonization by arbuscular mycorrhiza in cereals and other plants [100]. This hypothesis has been recently confirmed by demonstrating that orthologous of MLO1 are present only in those plants able to host vesicular arbuscular mycorrhiza (VAM) [84,99]. Correspondingly, MLO increase was observed during powdery mildew penetration [100] and the specificity of MLO1 in barley and wheat during plant–fungal interaction has been demonstrated [101].
In barley, the role of MLO1 gene was investigated using a polyphasic approach [101]; this study was based on phylogenetic analysis, mutant phenotypes, and gene expression revealing that MLO1 is required for well-timed and/or full-activation of early colonization by mycorrhiza, thus suggesting a conserved role for MLO1 in cereals, and particularly in barley. Moreover, MLOs act redundantly, with multiple MLOs playing different roles based on cell type and developmental stage. These results require further investigation about the role of MLO in mycorrhizal symbiotic interactions of land plants, in order to gain important information for sustainable agriculture [73,102].
These results underline the requirement of further studies on barley–fungi relationships, due to the evident influence that these associations can exert on growth, productivity and pathogen resistance.

6. Conclusions

The identification and integration of those traits responsible for significant improvements in abiotic stress tolerance, biotic association, and commercial application (e.g., malting) represent a significant challenge for barley. The results here reviewed suggest that valuable resources are yet to be explored to identify stress-responsive genes and proteins, highlighting the regulatory mechanisms of barley wild relatives and landraces from different regions of the world. A precious number of genes, physiological aspects, genotypes, and genomic traits has been released, thus providing new chances to understand the molecular basis of abiotic stress tolerance in barley, and possibly translate this knowledge to other cereal species as well. A further step of this research is the investigation of the interaction of landraces and varieties with specific strains of fungi able to establish AMF symbioses to reduce pathogen susceptibility of barley crops, decreasing the use of pesticides and increasing yields.
The data reviewed support the idea of landraces as a central—and still unexploited—resource to improve currently cultivated varieties through both conventional and unconventional approaches; at the same time, geographical and historical origin dissection of wild relatives and landraces could show the intrinsic and ancient ability of barley to tolerate adverse environments and complex stress conditions.
Finally, climatic change, and the possibility of more stressful environments, highlights the importance of further investigation about wild relatives, old genotypes, and local varieties, in order to improve barley quality and yields worldwide.

Author Contributions

Conceptualization, S.L.; Formal analysis, S.L., G.C., G.S. and M.P.; Resources, S.L.; Writing—original draft preparation, G.C. and G.S.; Writing—review and editing, S.E. and S.L.; Supervision, S.E. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Dwivedi, S.; Sahrawat, K.; Upadhyaya, H.; Ortiz, R. Food, Nutrition and Agrobiodiversity under Global Climate Change. Adv. Agron. 2013, 120, 1–128. [Google Scholar] [CrossRef] [Green Version]
  2. Moore, F.C.; Lobell, D. The fingerprint of climate trends on European crop yields. Proc. Natl. Acad. Sci. USA 2015, 112, 2670–2675. [Google Scholar] [CrossRef] [Green Version]
  3. Lopes, M.S.; El-Basyoni, I.; Baenziger, P.S.; Singh, S.; Royo, C.; Ozbek, K.; Aktas, H.; Ozer, E.; Ozdemir, F.; Manickavelu, A.; et al. Exploiting genetic diversity from landraces in wheat breeding for adaptation to climate change. J. Exp. Bot. 2015, 66, 3477–3486. [Google Scholar] [CrossRef]
  4. Van Oosten, M.J.; Costa, A.; Punzo, P.; Landi, S.; Ruggiero, A.; Batelli, G.; Grillo, S. Genetics of Drought Stress Tolerance in Crop Plants. In Drought Stress Tolerance in Plants; Springer: Berlin/Heidelberg, Germany, 2016; Volume 2. [Google Scholar] [CrossRef]
  5. Dwivedi, S.L.; Ceccarelli, S.; Blair, M.W.; Upadhyaya, H.D.; Are, A.K.; Ortiz, R. Landrace Germplasm for Improving Yield and Abiotic Stress Adaptation. Trends Plant Sci. 2016, 21, 31–42. [Google Scholar] [CrossRef] [PubMed]
  6. Hammami, Z.; Gauffreteau, A.; BelhajFraj, M.; Sahli, A.; Jeuffroy, M.-H.; Rezgui, S.; Bergaoui, K.; McDonnell, R.; Trifa, Y. Predicting yield reduction in improved barley (Hordeum vulgare L.) varieties and landraces under salinity using selected tolerance traits. Field Crop. Res. 2017, 211, 10–18. [Google Scholar] [CrossRef]
  7. Zeven, A. Landraces: A review of definitions and classifications. Euphytica 1998, 104, 127–139. [Google Scholar] [CrossRef]
  8. Tranchida-Lombardo, V.; Cigliano, R.A.; Anzar, I.; Landi, S.; Palombieri, S.; Colantuono, C.; Bostan, H.; Termolino, P.; Aversano, R.; Batelli, G.; et al. Whole-genome re-sequencing of two Italian tomato landraces reveals sequence variations in genes associated with stress tolerance, fruit quality and long shelf-life traits. DNA Res. 2018, 25, 149–160. [Google Scholar] [CrossRef] [Green Version]
  9. FAOSTAT, 2019. Available online: http://www.fao.org/faostat/en/#home (accessed on 1 November 2021).
  10. Shen, Q.; Fu, L.; Dai, F.; Jiang, L.; Zhang, G.; Wu, D. Multi-omics analysis reveals molecular mechanisms of shoot adaption to salt stress in Tibetan wild barley. BMC Genom. 2016, 17, 889. [Google Scholar] [CrossRef] [Green Version]
  11. Ben Azaiez, F.E.; Ayadi, S.; Capasso, G.; Landi, S.; Paradisone, V.; Jallouli, S.; Hammami, Z.; Chamekh, Z.; Zouari, I.; Trifa, Y.; et al. Salt Stress Induces Differentiated Nitrogen Uptake and Antioxidant Responses in Two Contrasting Barley Landraces from MENA Region. Agronomy 2020, 10, 1426. [Google Scholar] [CrossRef]
  12. Lee, S.; Lee, T.; Yang, S.; Lee, I. BarleyNet: A Network-Based Functional Omics Analysis Server for Cultivated Barley, Hordeum vulgare. Front. Plant Sci. 2020, 11, 98. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  13. Jallouli, S.; Ayadi, S.; Landi, S.; Capasso, G.; Santini, G.; Chamekh, Z.; Zouari, I.; Ben Azaiez, F.E.; Trifa, Y.; Esposito, S. Physiological and Molecular Osmotic Stress Responses in Three Durum Wheat (Triticum Turgidum ssp Durum) Genotypes. Agronomy 2019, 9, 550. [Google Scholar] [CrossRef] [Green Version]
  14. Landi, S.; Capasso, G.; Ben Azaiez, F.E.; Jallouli, S.; Ayadi, S.; Trifa, Y.; Esposito, S. Different Roles of Heat Shock Proteins (70 kDa) During Abiotic Stresses in Barley (Hordeum vulgare) Genotypes. Plants 2019, 8, 248. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  15. Ayadi, S.; Jallouli, S.; Landi, S.; Capasso, G.; Chamekh, Z.; Cardi, M.; Paradisone, V.; Lentini, M.; Karmous, C.; Trifa, Y.; et al. Nitrogen assimilation under different nitrate nutrition in Tunisian durum wheat landraces and improved genotypes. Plant Biosyst. Int. J. Deal. All Asp. Plant Biol. 2020, 154, 924–934. [Google Scholar] [CrossRef]
  16. Tuberosa, R. Phenotyping for drought tolerance of crops in the genomics era. Front. Physiol. 2012, 3, 347. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  17. Badr, A.; M, K.; Schäfer-Pregl, R.; El Rabey, H.; Effgen, S.; Ibrahim, H.H.; Pozzi, C.M.; Rohde, W.; Salamini, F. On the Origin and Domestication History of Barley (Hordeum vulgare). Mol. Biol. Evol. 2000, 17, 499–510. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  18. Jakob, S.S.; Rödder, D.; Engler, J.O.; Shaaf, S.; Özkan, H.; Blattner, F.R.; Kilian, B. Evolutionary history of wild barley (Hordeum vulgare subsp. spontaneum) analyzed using multilocus sequence data and paleodistribution modeling. Genome Biol. Evol. 2014, 6, 685–702. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  19. Harlan, J.R.; Zohary, D. Distribution of Wild Wheats and Barley. Science 1966, 153, 1074–1080. [Google Scholar] [CrossRef] [PubMed]
  20. Pournosrat, R.; Kaya, S.; Shaaf, S.; Kilian, B.; Ozkan, H. Geographical and environmental determinants of the genetic structure of wild barley in southeastern Anatolia. PLoS ONE 2018, 13, e0192386. [Google Scholar] [CrossRef] [Green Version]
  21. Von Bothmer, R. The wild species of Hordeum: Relationships and potential use for improvement of cultivated barley. In Barley: Genetics, Biochemistry, Molecular Biology and Biotechnology; Shewry, P.R., Ed.; CAB International: Oxon, UK, 1992; pp. 3–18. [Google Scholar]
  22. Mayer, K.F.; Waugh, R.; Brown, J.W.S.; Schulman, A.; Langridge, P.; Platzer, M.; Close, T.J.; Wise, R.P.; Graner, A.; Stein, N.; et al. International Barley Genome Sequencing Consortium: A physical, genetic and functional sequence assembly of the barley genome. Nature 2012, 491, 711–716. [Google Scholar] [PubMed]
  23. Kilian, B.; Özkan, H.; Kohl, J.; Von Haeseler, A.; Barale, F.; Deusch, O.; Brandolini, A.; Yucel, C.; Martin, W.F.; Salamini, F. Haplotype structure at seven barley genes: Relevance to gene pool bottlenecks, phylogeny of ear type and site of barley domestication. Mol. Genet. Genom. 2006, 276, 230–241. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  24. Dai, F.; Chen, Z.-H.; Wang, X.; Li, Z.; Jin, G.; Wu, D.; Cai, S.; Wang, N.; Wu, F.; Nevo, E.; et al. Transcriptome profiling reveals mosaic genomic origins of modern cultivated barley. Proc. Natl. Acad. Sci. USA 2014, 111, 13403–13408. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Mascher, M.; Gundlach, H.; Himmelbach, A.; Beier, S.; Twardziok, S.O.; Wicker, T.; Radchuk, V.; Dockter, C.; Hedley, P.; Russell, J.; et al. A chromosome conformation capture ordered sequence of the barley genome. Nature 2017, 544, 427–433. [Google Scholar] [CrossRef] [Green Version]
  26. Russell, J.; Mascher, M.; Dawson, I.; Kyriakidis, S.; Calixto, C.; Freund, F.; Bayer, M.; Milne, I.; Marshall-Griffiths, T.; Heinen, S.; et al. Exome sequencing of geographically diverse barley landraces and wild relatives gives insights into environmental adaptation. Nat. Genet. 2016, 48, 1024–1030. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  27. Liu, M.; Li, Y.; Ma, Y.; Zhao, Q.; Stiller, J.; Feng, Q.; Tian, Q.; Liu, D.; Han, B.; Liu, C. The draft genome of a wild barley genotype reveals its enrichment in genes related to biotic and abiotic stresses compared to cultivated barley. Plant Biotechnol. J. 2020, 18, 443–456. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  28. Zeng, X.; Long, H.; Wang, Z.; Zhao, S.; Tang, Y.; Huang, Z.; Wang, Y.; Xu, Q.; Mao, L.; Deng, G.; et al. The draft genome of Tibetan hulless barley reveals adaptive patterns to the high stressful Tibetan Plateau. Proc. Natl. Acad. Sci. USA 2015, 112, 1095–1100. [Google Scholar] [CrossRef] [Green Version]
  29. Komatsuda, T.; Pourkheirandish, M.; He, C.; Azhaguvel, P.; Kanamori, H.; Perovic, D.; Stein, N.; Graner, A.; Wicker, T.; Tagiri, A.; et al. Six-rowed barley originated from a mutation in a homeodomain-leucine zipper I-class homeobox gene. Proc. Natl. Acad. Sci. USA 2007, 104, 1424–1429. [Google Scholar] [CrossRef] [Green Version]
  30. Pankin, A.; Altmüller, J.; Becker, C.; von Korff, M. Targeted resequencing reveals genomic signatures of barley domestication. New Phytol. 2018, 2, 1247–1259. [Google Scholar] [CrossRef] [Green Version]
  31. Muller, N.A.; Wijnen, C.L.; Srinivasan, A.; Ryngajllo, M.; Ofner, I.; Lin, T.; Ranjan, A.; West, D.; Maloof, J.N.; Sinha, N.R. Domestication selected for deceleration of the circadian clock in cultivated tomato. Nat. Genet. 2016, 48, 89–93. [Google Scholar] [CrossRef]
  32. Zhu, L.; Bu, Q.; Xu, X.; Paik, I.; Huang, X.; Hoecker, U.; Deng, X.W.; Huq, E. CUL4 forms an E3 ligase with COP1 and SPA to promote light-induced degradation of PIF1. Nat. Commun. 2015, 6, 7245. [Google Scholar] [CrossRef] [Green Version]
  33. Nevo, E. Origin, evolution, population genetics and resources for breeding of wild barley, Hordeum spontaneum in the fertile crescent. In Barley: Genetics, Biochemistry, Molecular Biology and Biotechnology; Shewry, P.R., Ed.; CAB International: Oxon, UK, 1992; pp. 19–43. [Google Scholar]
  34. Ren, X.; Nevo, E.; Sun, D.; Sun, G. Tibet as a Potential Domestication Center of Cultivated Barley of China. PLoS ONE 2013, 8, e62700. [Google Scholar] [CrossRef] [Green Version]
  35. Dai, F.; Nevo, E.; Wu, D.; Comadran, J.; Zhou, M.; Qiu, L.; Chen, Z.; Beiles, A.; Chen, G.; Zhang, G. Tibet is one of the centers of domestication of cultivated barley. Proc. Natl. Acad. Sci. USA 2012, 109, 16969–16973. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  36. Pourkheirandish, M.; Kanamori, H.; Wu, J.; Sakuma, S.; Blattner, F.R.; Komatsuda, T. Elucidation of the origin of ‘ agriocrithon ’ based on domestication genes questions the hypothesis that Tibet is one of the centers of barley domestication. Plant J. 2018, 94, 525–534. [Google Scholar] [CrossRef] [Green Version]
  37. Zeng, X.; Guo, Y.; Xu, Q.; Mascher, M.; Guo, G.; Li, S.; Mao, L.; Liu, Q.; Xia, Z.; Zhou, J.; et al. Origin and evolution of qingke barley in Tibet. Nat. Commun. 2018, 9, 5433. [Google Scholar] [CrossRef] [PubMed]
  38. Rollins, J.; Habte, E.; Templer, S.E.; Colby, T.; Schmidt, J.; Von Korff, M. Leaf proteome alterations in the context of physiological and morphological responses to drought and heat stress in barley (Hordeum vulgare L.). J. Exp. Bot. 2013, 64, 3201–3212. [Google Scholar] [CrossRef] [Green Version]
  39. Bedada, G.; Westerbergh, A.; Müller, T.; Galkin, E.; Bdolach, E.; Moshelion, M.; Fridman, E.; Schmid, K.J. Transcriptome sequencing of two wild barley (Hordeum spontaneum L.) ecotypes differentially adapted to drought stress reveals ecotypespecific transcripts. BMC Genom. 2014, 15, 995. [Google Scholar] [CrossRef] [Green Version]
  40. Long, L.; Ma, X.; Ye, L.; Zeng, J.; Chen, G.; Zhang, G. Root plasticity and Pi recycling within plants contribute to low-P tolerance in Tibetan wild barley. BMC Plant Biol. 2019, 19, 341. [Google Scholar] [CrossRef] [Green Version]
  41. Cantalapiedra, C.P.; García-Pereira, M.J.; Gracia, M.P.; Igartua, E.; Casas, A.M.; Contreras-Moreira, B. Large Differences in Gene Expression Responses to Drought and Heat Stress between Elite Barley Cultivar Scarlett and a Spanish Landrace. Front. Plant Sci. 2017, 8, 647. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  42. Zeng, X.; Bai, L.; Wei, Z.; Yuan, H.; Wang, Y.; Xu, Q.; Tang, Y.; Nyima, T. Transcriptome analysis revealed the drought-responsive genes in Tibetan hulless barley. BMC Genom. 2016, 17, 386. [Google Scholar] [CrossRef] [Green Version]
  43. Zhao, J.; Sun, H.; Dai, H.; Zhang, G.; Wu, F. Difference in response to drought stress among Tibet wild barley genotypes. Euphytica 2010, 172, 395–403. [Google Scholar] [CrossRef]
  44. Quan, X.; Zeng, J.; Ye, L.; Chen, G.; Han, Z.; Shah, J.M.; Zhang, G. Transcriptome profiling analysis for two Tibetan wild barley genotypes in responses to low nitrogen. BMC Plant Biol. 2016, 16, 30. [Google Scholar] [CrossRef] [Green Version]
  45. Ahmed, I.M.; Cao, F.; Zhang, M.; Chen, X.; Zhang, G.; Wu, F. Difference in Yield and Physiological Features in Response to Drought and Salinity Combined Stress during Anthesis in Tibetan Wild and Cultivated Barleys. PLoS ONE 2013, 8, e77869. [Google Scholar] [CrossRef]
  46. Guo, W.; Chen, T.; Hussain, N.; Zhang, G.; Jiang, L. Characterization of Salinity Tolerance of Transgenic Rice Lines Harboring HsCBL8 of Wild Barley (Hordeum spontanum) Line from Qinghai-Tibet Plateau. Front. Plant Sci. 2016, 7, 1678. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  47. Ahmed, I.M.; Nadira, U.A.; Cao, F.; He, X.; Zhang, G.; Wu, F. Physiological and molecular analysis on root growth associated with the tolerance to aluminum and drought individual and combined in Tibetan wild and cultivated barley. Planta 2016, 243, 973–985. [Google Scholar] [CrossRef] [PubMed]
  48. He, X.; Zeng, J.; Cao, F.; Ahmed, I.M.; Zhang, G.; Vincze, E.; Wu, F. HvEXPB7, a novel β-expansin gene revealed by the root hair transcriptome of Tibetan wild barley, improves root hair growth under drought stress. J. Exp. Bot. 2015, 66, 7405–7419. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  49. Liang, J.; Chen, X.; Deng, G.; Pan, Z.; Zhang, H.; Li, Q.; Yang, K.; Long, H.; Yu, M. Dehydration induced transcriptomic responses in two Tibetan hulless barley (Hordeum vulgare var. nudum) accessions distinguished by drought tolerance. BMC Genom. 2017, 18, 775. [Google Scholar] [CrossRef] [Green Version]
  50. von Korff, M.; Grando, S.; Del Greco, A.; This, D.; Baum, M.; Ceccarelli, S. Quantitative trait loci associated with adaptation to Mediterranean dryland conditions in barley. Theor. Appl. Genet. 2008, 117, 653–669. [Google Scholar] [CrossRef] [PubMed]
  51. Poets, A.M.; Fang, Z.; Clegg, M.T.; Morrell, P.L. Barley landraces are characterized by geographically heterogeneous genomic origins. Genome Biol. 2015, 16, 173. [Google Scholar] [CrossRef] [Green Version]
  52. Fischbeck, G.; von Bothmer, T.; van Hintum, H.; Knüpffer; Sato, K. Diversification through breeding. In Diversity in Barley (Hordeum vulgare); Elsevier Science: Amsterdam, The Netherlands, 2003; pp. 29–52. [Google Scholar]
  53. Dawson, I.; Russell, J.; Powell, W.; Steffenson, B.; Thomas, W.T.B.; Waugh, R. Barley: A translational model for adaptation to climate change. New Phytol. 2015, 206, 913–931. [Google Scholar] [CrossRef] [PubMed]
  54. Varshney, R.K.; Langridge, P.; Graner, A. Application of Genomics to Molecular Breeding of Wheat and Barley. Adv. Genet. 2007, 58, 121–155. [Google Scholar] [CrossRef] [PubMed]
  55. Volis, S.; Mendlinger, S.; Ward, D. Adaptive traits of wild barley plants of Mediterranean and desert origin. Oecologia 2002, 133, 131–138. [Google Scholar] [CrossRef]
  56. Marmiroli, N.; Lorenzoni, C.; Cattivelli, L.; Stanca, A.M.; Terzi, V. Induction of heat shock proteins and acquisition of thermotol-erance in barley (Hordeum vulgare L.). Variations associated with growth habit and plant development. J. Plant Physiol. 1989, 135, 267–273, ISSN 0176-1617. [Google Scholar] [CrossRef]
  57. Wang, Y.; Sang, Z.; Xu, S.; Xu, Q.; Zeng, X.; Jabu, D.; Yuan, H. Comparative proteomics analysis of Tibetan hull-less barley under osmotic stress via data-independent acquisition mass spectrometry. GigaScience 2020, 9, 1–12. [Google Scholar] [CrossRef]
  58. Quan, X.; Zeng, J.; Chen, G.; Zhang, G. Transcriptomic analysis reveals adaptive strategies to chronic low nitrogen in Tibetan wild barley. BMC Plant Biol. 2019, 19, 68. [Google Scholar] [CrossRef] [Green Version]
  59. Landi, S.; Esposito, S. Nitrate Uptake Affects Cell Wall Synthesis and Modeling. Front. Plant Sci. 2017, 8, 1376. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  60. Chai, G.; Li, C.; Xu, F.; Li, Y.; Shi, X.; Wang, Y.; Wang, Z. Three endoplasmic reticulum-associated fatty acyl-coenzyme a reductases were involved in the production of primary alcohols in hexaploid wheat (Triticum aestivum L.). BMC Plant Biol. 2018, 18, 41. [Google Scholar] [CrossRef]
  61. Li, T.; Sun, Y.; Liu, T.; Wu, H.; An, P.; Shui, Z.; Wang, J.; Zhu, Y.; Li, C.; Wang, Y.; et al. TaCER1-1A is involved in cuticular wax alkane biosynthesis in hexaploid wheat and responds to plant abiotic stresses. Plant Cell Environ. 2019, 42, 3077–3091. [Google Scholar] [CrossRef]
  62. Bourdenx, B.; Bernard, A.; Domergue, F.; Pascal, S.; Léger, A.; Roby, D.; Pervent, M.; Vile, D.; Haslam, R.; Napier, J.; et al. Overexpression of Arabidopsis ECERIFERUM1 Promotes Wax Very-Long-Chain Alkane Biosynthesis and Influences Plant Response to Biotic and Abiotic Stresses. Plant Physiol. 2011, 156, 29–45. [Google Scholar] [CrossRef] [Green Version]
  63. Wang, Y.; Sun, Y.; You, Q.; Luo, W.; Wang, C.; Zhao, S.; Chai, G.; Li, T.; Shi, X.; Li, C.; et al. Three Fatty Acyl-Coenzyme A Reductases, BdFAR1, BdFAR2 and BdFAR3, are Involved in Cuticular Wax Primary Alcohol Biosynthesis in Brachypodium distachyon. Plant Cell Physiol. 2018, 59, 527–543. [Google Scholar] [CrossRef]
  64. Nevo, E. Genome evolution of wild cereal diversity and prospects for crop improvement. Plant Genet. Resour. 2006, 4, 36–46. [Google Scholar] [CrossRef]
  65. Ellis, R.P.; Forster, B.P.; Robinson, D.; Handley, L.L.; Gordon, D.C.; Russell, J.R.; Powell, W. Wild barley: A source of genes for crop improvement in the 21st century? J. Exp. Bot. 2000, 51, 9–17. [Google Scholar] [CrossRef]
  66. Templer, S.E.; Ammon, A.; Pscheidt, D.; Ciobotea, O.; Schuy, C.; Mccollum, C.; Sonnewald, U.; Hanemann, A.; Förster, J.; Ordon, F.; et al. Metabolite profiling of barley flag leaves under drought and combined heat and drought stress reveals metabolic QTLs for metabolites associated with antioxidant defense. J. Exp. Bot. 2017, 68, 1697–1713. [Google Scholar] [CrossRef] [Green Version]
  67. Contreras-Moreira, B.; Serrano-Notivoli, R.; Mohammed, N.E.; Cantalapiedra, C.P.; Beguería, S.; Casas, A.M.; Igartua, E. Genetic association with high-resolution climate data reveals selection footprints in the genomes of barley landraces across the Iberian Peninsula. Mol. Ecol. 2019, 28, 1994–2012. [Google Scholar] [CrossRef]
  68. Fox, G.P.; Panozzo, J.F.; Li, C.D.; Lance, R.C.M.; Inkerman, P.A.; Henry, R.J. Molecular basis of barley quality. Aust. J. Agric. Res. 2003, 54, 1081–1101. [Google Scholar] [CrossRef] [Green Version]
  69. Schmalenbach, I.; Pillen, K. Detection and verification of malting quality QTLs using wild barley introgression lines. Theor. Appl. Genet. 2009, 118, 1411–1427. [Google Scholar] [CrossRef] [Green Version]
  70. Laidig, F.; Piepho, H.-P.; Rentel, D.; Drobek, T.; Meyer, U. Breeding progress, genotypic and environmental variation and correlation of quality traits in malting barley in German official variety trials between 1983 and 2015. Theor. Appl. Genet. 2017, 130, 2411–2429. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  71. Hornsey, I.A. History of Beer and Brewing; Royal Society of Chemistry: Cambridge, UK, 2003; p. 720. [Google Scholar]
  72. Wu, X.; Cai, K.; Zhang, G.; Zeng, F. Metabolite Profiling of Barley Grains Subjected to Water Stress: To Explain the Genotypic Difference in Drought-Induced Impacts on Malting Quality. Front. Plant Sci. 2017, 8, 1547. [Google Scholar] [CrossRef]
  73. Hübner, S.; Günther, T.; Flavell, A.; Fridman, E.; Graner, A.; Korol, A.; Schmid, K.J. Islands and streams: Clusters and gene flow in wild barley populations from the Levant. Mol. Ecol. 2012, 21, 1115–1129. [Google Scholar] [CrossRef]
  74. Teulat, B.; Borries, C.; This, D. New QTLs identified for plant water status, water-soluble carbohydrate and osmotic adjustment in a barley population grown in a growth-chamber under two water regimes. Theor. Appl. Genet. 2001, 103, 161–170. [Google Scholar] [CrossRef]
  75. Diab, A.A.; This, D.; Ozturk, N.Z.; Benscher, D.; Sorrells, M.E. Identification of drought-inducible genes and differentially expressed sequence tags in barley. Theor. Appl. Genet. 2004, 109, 1417–1425. [Google Scholar] [CrossRef]
  76. Guo, P.; Baum, M.; Varshney, R.K.; Graner, A.; Grando, S.; Ceccarelli, S. QTLs for chlorophyll and chlorophyll fluorescence parameters in barley under post-flowering drought. Euphytica 2008, 163, 203–214. [Google Scholar] [CrossRef]
  77. Hübner, S.; Bdolach, E.; Ein-Gedy, S.; Schmid, K.J.; Korol, A.; Fridman, E. Phenotypic landscapes: Phenological patterns in wild and cultivated barley. J. Evol. Biol. 2013, 26, 163–174. [Google Scholar] [CrossRef]
  78. Hübner, S.; Höffken, M.; Oren, E.; Haseneyer, G.; Stein, N.; Graner, A.; Schmid, K.; Fridman, E. Strong correlation of wild barley (Hordeum spontaneum) population structure with temperature and precipitation variation. Mol. Ecol. 2009, 18, 1523–1536. [Google Scholar] [CrossRef]
  79. Mascher, M.; Richmond, T.A.; Gerhardt, D.J.; Himmelbach, A.; Clissold, L.; Sampath, D.; Ayling, S.; Steuernagel, B.; Pfeifer, M.; D’Ascenzo, M.; et al. Barley whole exome capture: A tool for genomic research in the genus Hordeum and beyond. Plant J. 2013, 76, 494–505. [Google Scholar] [CrossRef] [Green Version]
  80. Smith, S.E.; Read, D.J. Mycorrhizal symbiosis; Academic Press: Cambridge, UK, 2008. [Google Scholar]
  81. Wehner, J.; Antunes, P.M.; Powell, J.R.; Mazukatow, J.; Rillig, M.C. Plant pathogen protection by arbuscular mycorrhizas: A role for fungal diversity? Pedobiologia 2010, 53, 197–201. [Google Scholar] [CrossRef]
  82. Lenoir, I.; Fontaine, J.; Sahraoui, A.L.-H. Arbuscular mycorrhizal fungal responses to abiotic stresses: A review. Phytochemistry 2016, 123, 4–15. [Google Scholar] [CrossRef] [PubMed]
  83. Wilcox, H.E. Mycorrhizae. In Plant Roots—The Hidden Half; Waisel, Y., Eshel, A., Kafkafi, U., Eds.; Marcel Dekker: New York, NY, USA, 1991. [Google Scholar]
  84. Bravo, A.; York, T.; Pumplin, N.; Mueller, L.A.; Harrison, M.J. Genes conserved for arbuscular mycorrhizal symbiosis identified through phylogenomics. Nat. Plants 2016, 2, 15208. [Google Scholar] [CrossRef] [PubMed]
  85. Delaux, P.-M.; Radhakrishnan, G.; Jayaraman, D.; Cheema, J.; Malbreil, M.; Volkening, J.; Sekimoto, H.; Nishiyama, T.; Melkonian, M.; Pokorny, L.; et al. Algal ancestor of land plants was preadapted for symbiosis. Proc. Natl. Acad. Sci. USA 2015, 112, 13390–13395. [Google Scholar] [CrossRef] [Green Version]
  86. Miyauchi, S.; Kiss, E.; Kuo, A.; Drula, E.; Kohler, A.; Sánchez-García, M.; Morin, E.; Andreopoulos, B.; Barry, K.W.; Bonito, G.; et al. Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits. Nat. Commun. 2020, 11, 5125. [Google Scholar] [CrossRef]
  87. Castellanos-Morales, V.; Keiser, C.; Cárdenas-Navarro, R.; Grausgruber, H.; Glauninger, J.; García-Garrido, J.M.; Steinkellner, S.; Sampedro, I.; Hage-Ahmed, K.; Illana, A.; et al. The bioprotective effect of AM root colonization against the soil-borne fungal pathogen Gaeumannomyces graminis var. tritici in barley depends on the barley variety. Soil Biol. Biochem. 2011, 43, 831–834. [Google Scholar] [CrossRef]
  88. Besserer, A.; Puech-Pagès, V.; Kiefer, P.; Gomez-Roldan, V.; Jauneau, A.; Roy, S.; Portais, J.-C.; Roux, C.; Bécard, G.; Séjalon-Delmas, N. Strigolactones Stimulate Arbuscular Mycorrhizal Fungi by Activating Mitochondria. PLoS Biol. 2006, 4, e226. [Google Scholar] [CrossRef] [PubMed]
  89. Sawers, R.; Ramirez-Flores, M.R.; Olalde-Portugal, V.; Paszkowski, U. The impact of domestication and crop improvement on arbuscular mycorrhizal symbiosis in cereals: Insights from genetics and genomics. New Phytol. 2018, 220, 1135–1140. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  90. Etemadi, M.; Gutjahr, C.; Couzigou, J.-M.; Zouine, M.; Lauressergues, D.; Timmers, A.; Audran, C.; Bouzayen, M.; Bécard, G.; Combier, J.-P. Auxin perception is required for arbuscule development in arbuscular mycorrhizal symbiosis. Plant Physiol. 2014, 166, 281–292. [Google Scholar] [CrossRef] [Green Version]
  91. Floss, D.S.; Levy, J.G.; Levesque-Tremblay, V.; Pumplin, N.; Harrison, M.J. DELLA proteins regulate arbuscule formation in arbuscular mycorrhizal symbiosis. Proc. Natl. Acad. Sci. USA 2013, 110, E5025–E5034. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  92. Salamon, S.; Mikołajczak, K.; Błaszczyk, L.; Ratajczak, K.; Sulewska, H. Changes in root-associated fungal communities in Triticum aestivum ssp. spelta L. and Triticum aestivum ssp. vulgare L. under drought stress and in various soil processing. PLoS ONE 2020, 15, e0240037. [Google Scholar] [CrossRef] [PubMed]
  93. Jimenez, B.A.; Vandenkoornhuyse, P.; Van, A.L.; Heutinck, A.; Duhamel, M.; Kadam, N.; Jagadish, K.; Ruyter-Spira, C.; Bouwmeester, H. Plant host and drought shape the root associated fungal microbiota in rice. PeerJ 2019, 7, e7463. [Google Scholar] [CrossRef] [Green Version]
  94. St-Arnaud, M.; Vujanovic, V. Effect of the arbuscular mycorrhizal symbiosis on plant diseases and pests. In Mycorrhizae in Crop Production; Hamel, C., Plenchette, C., Eds.; Haworth Press: Binghampton, NY, USA, 2007; pp. 67–122. [Google Scholar]
  95. Vierheilig, H.; Steinkellner, S.; Khaosaad, T.; Garcia-Garrido, J.M. The biocontrol effect of mycorrhization on soil-borne fungal pathogens and the autoregulation of the AM symbiosis: One mechanism, two effects? In MYCORRHIZA: Genetics and Molecular Biology, Eco-Function, Biotechnology, Eco-Physiology, Structure and Systematics; Varma, A., Ed.; Springer: Heidelberg, Germany, 2008; pp. 307–320. [Google Scholar]
  96. Graham, J.H. Influence of Vesicular-Arbuscular Mycorrhizae and Soil Phosphorus on Take-All Disease of Wheat. Phytopathology 1982, 72, 95–98. [Google Scholar] [CrossRef]
  97. Jorgensen, J.H. Sources and genetics of resistance to fungal pathogens. In Barley: Genetics, Biochemistry, Molecular Biology and Biotechnology; Shewry, P.R., Ed.; CAB International: Oxon, UK, 1992; pp. 441–457. [Google Scholar]
  98. Ruiz-Lozano, J.M.; Roussel, H.; Gianinazzi, S.; Gianinazzi-Pearson, V. Defense Genes Are Differentially Induced by a Mycorrhizal Fungus and Rhizobium sp. in Wild-Type and Symbiosis-Defective Pea Genotypes. Mol. Plant Microbe Interact. 1999, 12, 976–984. [Google Scholar] [CrossRef] [Green Version]
  99. Hilbert, M.; Novero, M.; Rovenich, H.; Mari, S.; Grimm, C.; Bonfante, P.; Zuccaro, A. MLO Differentially Regulates Barley Root Colonization by Beneficial Endophytic and Mycorrhizal Fungi. Front. Plant Sci. 2019, 10, 1678. [Google Scholar] [CrossRef] [Green Version]
  100. Bhat, R.A.; Miklis, M.; Schmelzer, E.; Schulze-Lefert, P.; Panstruga, R. Recruitment and interaction dynamics of plant penetration resistance components in a plasma membrane microdomain. Proc. Natl. Acad. Sci. USA 2005, 102, 3135–3140. [Google Scholar] [CrossRef] [Green Version]
  101. Jacott, C.N.; Charpentier, M.; Murray, J.D.; Ridout, C.J. Mildew Locus O facilitates colonization by arbuscular mycorrhizal fungi in angiosperms. New Phytol. 2020, 227, 343–351. [Google Scholar] [CrossRef] [Green Version]
  102. Jennings, D.H.; Lysek, G. Fungal Biology: Understanding the Fungal Lifestyle; Bios Scientific Pub Ltd.: Oxfordshire, UK, 1996; ISBN 10: 1859961509/13: 9781859961506.
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Figure 1. (A) Barley production in different countries in 2018. (B) Evolution of barley production from 2003 to 2018 in different countries and macro-areas. The figure was obtained from data present in the FAO database [6] (http://www.fao.org/faostat/en/#home, accessed on 1 November 2021).
Figure 1. (A) Barley production in different countries in 2018. (B) Evolution of barley production from 2003 to 2018 in different countries and macro-areas. The figure was obtained from data present in the FAO database [6] (http://www.fao.org/faostat/en/#home, accessed on 1 November 2021).
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Table
Table 1. List of abiotic stress tolerant genotypes discussed in this review.
Table 1. List of abiotic stress tolerant genotypes discussed in this review.
Genotypes NameGermplams TypeGeographic OriginAbiotic Stress RelationPhysiological and/or Molecular PeculiarityReferences
ArtaLandraceSyriaDrought and Heat tolerantReduced impact of drought to photosynthesis; reduced proteomic effects upon drought; reduced effects of heat on plant growth[38]
B1K2Wild barley ecotypeIsraelDrought tolerantHigher RWC; improved WUE[39]
B1K30Wild barley ecotypeIsraelDrought tolerantReduced water loss and transpiration[39]
BatinìLandraceOmanAbiotic stress tolerantEnhanced protein folding regulation[15]
L118Double haploid lineTibetLow phosphorus tolerantIncreased shoot DW and root length upon low P condition[40]
L130Double haploid lineTibetLow phosphorus tolerantIncreased shoot DW and root length upon low P condition[40]
L138Double haploid lineTibetLow phosphorus tolerantIncreased shoot DW and root length upon low P condition[40]
SBCC073Landrace derived inbredSpainDrought and Heat tolerantImproved regulation of secondary metabolism[41]
Himalaya 10Inbred lineTibetDrought tolerantIncreased accumulation of hormones of ABA; efficient ROS detoxification[42]
XZ147Wild barley ecotypeTibetDrought tolerantImproved regulation of hormones and H2O2 homeostasis[43]
XZ149Wild barley ecotypeTibetLow nitrogen tolerantLess reduced shoot DW and increased root DW upon N deprivation; enhanced molecular regulation of N transporter and hormone biosynthesis-related genes[44]
XZ16Wild barley ecotypeTibetSalt and Aluminum tolerantImproved regulation of ions transport and location[45]
XZ166Wild barley ecotypeTibetSalt tolerantPresence of specific allele of HvCBL8 (calcium-sensor calcineurin B-like)[46]
XZ26Wild barley ecotypeTibetLow phosphorus tolerantIncreased plasticity of root system[40]
XZ29Wild barley ecotypeTibetAluminum tolerantIncreased accumulation of hormones (ABA, ethylene)[47]
XZ5Wild barley ecotypeTibetDrought and aluminum tolerantIncreased accumulation of hormones (ABA, ethylene); improved molecular regulation of cell wall modification, antioxidant process, and root hair development; increased shoot dry weight, photosynthesis rate, and WUE upon drought[45,47,48]
Z772AccessionTibetDrought tolerantEnhanced molecular regulation of protein folding complexes, photosynthetic complex, and wax biosynthesis[49]
Abbreviations: ABA = Abscissic acid; DW = Dry weight; RWC = Relative water content; SA = Salicylic acid; WUE = Water use efficiency.
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Capasso, G.; Santini, G.; Petraretti, M.; Esposito, S.; Landi, S. Wild and Traditional Barley Genomic Resources as a Tool for Abiotic Stress Tolerance and Biotic Relations. Agriculture 2021, 11, 1102. https://doi.org/10.3390/agriculture11111102

AMA Style

Capasso G, Santini G, Petraretti M, Esposito S, Landi S. Wild and Traditional Barley Genomic Resources as a Tool for Abiotic Stress Tolerance and Biotic Relations. Agriculture. 2021; 11(11):1102. https://doi.org/10.3390/agriculture11111102

Chicago/Turabian Style

Capasso, Giorgia, Giorgia Santini, Mariagioia Petraretti, Sergio Esposito, and Simone Landi. 2021. "Wild and Traditional Barley Genomic Resources as a Tool for Abiotic Stress Tolerance and Biotic Relations" Agriculture 11, no. 11: 1102. https://doi.org/10.3390/agriculture11111102

APA Style

Capasso, G., Santini, G., Petraretti, M., Esposito, S., & Landi, S. (2021). Wild and Traditional Barley Genomic Resources as a Tool for Abiotic Stress Tolerance and Biotic Relations. Agriculture, 11(11), 1102. https://doi.org/10.3390/agriculture11111102

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