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Agronomy 2017, 7(2), 28; doi:10.3390/agronomy7020028

Review
Opportunities for Napier Grass (Pennisetum purpureum) Improvement Using Molecular Genetics
1
Feed and Forage Development, International Livestock Research Institute, Box 5689, Addis Ababa, Ethiopia
2
School of Plant Science, College of Agriculture and Environmental Science, Haramaya University, Box 138, Dire Dawa, Ethiopia
*
Author to whom correspondence should be addressed.
Academic Editors: John W. Forster and Kevin F. Smith
Received: 28 February 2017 / Accepted: 4 April 2017 / Published: 13 April 2017

Abstract

:
Napier grass (Pennisetum purpureum Schumach.) is a fast-growing perennial grass native to Sub-Saharan Africa that is widely grown across the tropical and subtropical regions of the world. It is a multipurpose forage crop, primarily used to feed cattle in cut and carry feeding systems. Characterization and diversity studies on a small collection of Napier grasses have identified a moderate level of genetic variation and highlighted the availability of some good agronomic traits, particularly high biomass production, as a forage crop. However, very little information exists on precise phenotyping, genotyping and the application of molecular technologies to Napier grass improvement using modern genomic tools which have been applied in advancing the selection and breeding of important food crops. In this review paper, existing information on genetic resources, molecular diversity, yield and nutritional quality of Napier grass will be discussed. Recent findings on characterizing disease resistance and abiotic stress (drought) tolerance will also be highlighted. Finally, opportunities and future prospects for better conservation and use arising from the application of modern genomic tools in Napier grass phenotyping and genotyping will be discussed.
Keywords:
Napier grass; elephant grass; Uganda grass; Pennisetum purpureum; diversity analysis; characterization; phenotype; genotype

1. Introduction

Sustainable livestock production is highly dependent on the availability of quality feed and forage resources. Napier grass, also known as elephant or Uganda grass, is one of the most important tropical forage crops. It is widely used in cut and carry feeding systems [1,2,3] and is of growing importance in other agricultural systems. Napier grass possesses many desirable characteristics, including high yield per unit area, tolerance to intermittent drought and high water use efficiency [2], making it a forage of choice. It has the ability to withstand repeated cutting and will rapidly regenerate, producing palatable leafy shoots [4]. Consequently, enhancing the knowledge-based use and conservation of the available Napier grass resources promises to substantially benefit livestock value chains.

1.1. Origin, Propagation and Distribution

Napier grass is a monocotyledonous flowering plant belonging to the family Poaceae (the family of grasses) and the genus Pennisetum [5,6]. Pennisetum is a highly diverse genus consisting of a heterogeneous group of approximately 140 species [7,8,9] with different basic chromosome numbers of 5, 7, 8 or 9, a range of ploidy levels from diploid to octoploid, both sexual and apomictic reproductive behaviours and life cycles of an annual, biennial or perennial nature [10]. Napier grass is a perennial C4 grass species [11,12] native to Sub-Saharan Africa from where it is believed to have been distributed to other tropical and subtropical regions around the world. It has been reported to be adapted to grow across a wide range of soil conditions and agro-ecologies, from sea level to 2100 m, and it can withstand minor dry spells, although it grows best in areas where the annual rainfall is between 750 and 2500 mm [6]. Given its wide agro-ecological adaptation, Napier grass has been naturalized in areas of Central and South America, tropical parts of Asia, Australia, the Middle East and the Pacific islands [6,13]. As a result, today it is widely grown in tropical and subtropical regions of the world, for use predominantly as animal fodder (Figure 1). Napier grass can be more commonly distributed by vegetative cuttings and tillers [6], since the grass cannot produce many seeds and those that are produced are normally very small, light, of poor quality and the spikelets are prone to shattering [6,14]. Consequently, the seeds are considered inappropriate for propagation as they produce weak seedlings and, as Napier grass is an open pollinated crop, the seedlings are also highly heterozygous [6,14]. Therefore, propagation by stem cuttings is currently the dominant practice for the distribution of Napier grass propagules [6,15].

1.2. Economic Importance

A range of grass species are used as fodder crops by farmers in Africa, Asia and other tropical/subtropical regions of the world. Napier grass is one of the most important fodder crops, particularly in Eastern and Central African smallholder farming communities [1,2]. It is mainly used to feed livestock in cut and carry feeding systems [3,16,17]. It is a multipurpose forage crop that can be grazed directly, or made into silage or hay [18] and there have also been reports of using Napier grass as fish food, for example for feeding grass carp and tilapia in Nepal [19,20] and Bangladesh [21]. A recent report from Nigeria also indicated that young shoots of Napier grass were used as a cooked vegetable [22]. These varied uses provide an indication of the diversity of roles that Napier grass could contribute to the reduction of poverty and nutritional insecurity.
In addition to its value as a forage crop, Napier grass can also be used to make fences, as a windbreak, to demarcate boundaries among neighbouring farmers, and the dried material can be used as a fuel source [18]. In crop land management systems, it is used as a mulch to control weed infestation and soil erosion [2] and as a trap plant in the push–pull strategy, a pest management practice which uses repellent intercrop ‘push’ plants and attractant trap ‘pull’ plants [23] for insect pest control in Africa, particularly for the maize stem borer [24,25]. Plants are also used to scavenge pollutants, such as heavy metals, and Napier grass has been used in phytoremediation strategies, for example for the cleanup of cadmium-affected soil, reducing the concentration of cadmium to a depth of 15 cm in soil [17].
With growing global interest in reducing fossil fuel consumption and concerns about the impacts of climate change, the search for alternative biofuel sources has led to the promotion of large biomass plants as second- or next-generation biofuel crops. Napier grass, with its perennial nature and fast growing characteristics, has been reported to produce a dry matter (DM) yield of up to 78 tons/ha/annum (35–41 tons/ha average) [26]. Rengsirikul et al. [27] estimated a maximum ethanol production of 350–460 L/ton DM from Napier grass varieties grown in Thailand, and an estimated ethanol yield of 329 L/ton DM. Lima et al. [28] demonstrated that this potential was 6% and 15% higher than for the tropical forages Brachiaria brizantha and Panicum maximum, respectively, around 15% higher than Eucalyptus bark and 17% higher than for sugarcane. Consequently, the potential exists for the use of Napier grass for phytoremediation purposes, after which the large harvest could go into processing plants for biofuel production.

1.3. Genetic Resources, Molecular Diversity and Breeding

Napier grass is considered to be a socio-economically important tropical grass species and is therefore available across most of the tropical and subtropical regions of the world. As reviewed in Sanghu et al. [5], a number of genebanks (for example: the International Center for Tropical Agriculture (CIAT); the Commonwealth Scientific and Industrial Research Organisation (CSIRO); the International Livestock Research Institute (ILRI); and the National Bureau of Plant Genetic Resources (NBPGR)) are involved in conserving a substantial amount of tropical and sub-tropical forage genetic resources. Through early exploration, Napier grass germplasm has been collected from various geographical regions and is conserved by these different institutions [5,29,30]. Consequently, over 300 accessions of Napier grass are currently being maintained in different genebanks (Table 1). Genetic resources form an essential component of agriculture and livestock production value chains where in-depth knowledge of the existing resources is required. Accurate passport, characterization and evaluation data, together with an overall understanding of the diversity of the genetic resources, are considered the primary reasons for the conservation and use of available genetic resources [5]. For example, a broad array of Napier grass accessions are currently being maintained by the ILRI forage genebank in the field at Debre Zeit and Zwai, Ethiopia with considerable diversity in growth and form (Figure 2). However, germplasm available from genebanks has so far been largely underutilized [5].
Napier grass is a cross-pollinating allotetraploid species with a chromosome number of 2n = 4x = 28 (genome A’A’BB) [11,31,32]. Although there is no clear information on the genetic origin of allotetraploidy in Napier grass, the A’A’ genome has been reported to be homologous to the AA genome of pearl millet (Pennisetum glaucum (L.)) and the A’ chromosomes are larger than the B chromosomes, which contribute genes controlling the perennial growth habit [31]. To date, Napier grass ‘improvement’ has mainly been based on the evaluation and selection of existing accessions for traits of interest. For example, accessions were screened for resistance to diseases, and Napier grass head smut- and stunt-resistant lines were identified from the existing collections [33,34]. Plant breeding and selection in Napier grass has primarily been aimed at improving different agronomic traits such as disease resistance, yield, nutritional quality, growth habit (dwarfing), palatability and abiotic stress tolerance [6,11,35]. Napier grass is cross-compatible with the closely related species pearl millet (Pennisetum glaucum) (2n = 2x = 14, genome AA) [6,15]; the resultant hybrids are triploid and sterile [6] and can only be propagated by vegetative means which, although labour intensive, ensure a true-to-type variety [15]. A number of agronomically important traits, nutritional quality and palatability for example, have been introgressed into the genome of Napier grass from pearl millet through conventional plant breeding [29] and hybrids have become a crucial part of the forage crop value chain in Africa, Asia and South America [6,36].
Since the early 1990s there have been a number of reports characterizing the genetic diversity of Napier grass. Tcacenco and Lance [38] evaluated the usefulness of morphological characteristics for the characterization of Napier grass and were able to differentiate nine accessions based on leaf, stem and inflorescence characteristics. Van De Wouw et al. [39] also studied a collection of Napier grass using morphological and agronomic characters where the collection was clustered into six groups. Smith and co-workers [40] were the first group to develop and use molecular restriction fragment length polymorphism (RFLP) and random amplification of polymorphic DNA (RAPD), markers in Napier grass studies and they were able to link quantitative trait loci to several plant traits. A diversity analysis, based on RAPD molecular markers, revealed a moderate level of diversity with clear differentiation of Napier grass accessions from pearl millet and its hybrids, and the accessions were clustered into groups according to their geographical origin [4,41]. However, the difficulty of differentiating some of the accessions based on their RAPD profile was also acknowledged [4]. Bhandari and co-workers [42] were able to differentiate 64 accessions of Napier grass based on polymorphisms in isozymes and total proteins and reported the availability of a wide range of genetic diversity. They suggested that the markers could be used to efficiently complement the morphological traits for diversity assessment and varietal identification of Napier grass accessions.
Harris et al. [11] were able to study the genetic relationship among 89 nursery accessions using amplified fragment length polymorphism (AFLP) markers and the results revealed a moderate to high degree of genetic relatedness among the accessions. In addition, clustering of the accessions into five groups in line with geographical origin was observed, which was a similar result to that observed using RAPD markers [11]. However, in another study using AFLP markers, Napier grass accessions of different geographical background obtained from research centres in Botswana, Mozambique, Ghana, South Africa, and Ethiopia (ILRI forage genebank collection) came together into different groups, with no clear evidence of clustering according to geographical origin [43]. Recent studies using AFLP markers [44] provided an indication that there was little to moderate within population diversity and a clustering of two groups in the Napier grass collection held at the ILRI forage genebank together with some additional accessions collected from Kenya, Tanzania and Uganda. Interestingly, these results also did not reveal the clustering of different accessions according to their geographical origin, which was demonstrated by the previous morphological, agronomic and RAPD marker studies. Other types of molecular markers, such as inter-sequential simple repeat (ISSR) markers [41,45] and sequence-related amplified polymorphisms (SRAPs) [46] have also been used for the characterization and identification of Napier grass clones.
Finally, a number of microsatellite, or simple sequence repeat (SSR), markers from pearl millet genetic studies have been demonstrated to be transferable to Napier grass [47,48,49,50,51]. The transferrable markers were successfully used in diversity analyses and clone identification of Napier grass accessions [12,52]. Expressed sequence tag (EST)-based SSR markers have been successfully used to identify pearl millet-Napier grass hybrids (the majority of hybrid Napier grass varieties under cultivation have been developed using pearl millet as maternal parents and Napier grass as paternal parents) [53]. Napier grass collections from Kenya and Uganda [54], the United States Department of Agriculture-Agricultural Research Service (USDA-ARS, Tifton nursery) [12] and the ILRI forage genebank (unpublished data) have also been characterized using SSR markers. Results from the SSR analyses demonstrated the availability of a broad array of genetic diversity in Napier grass germplasm while some duplicates were also identified in the collections. Kawube and his colleagues [54] also reported the allelic uniqueness of Napier grass from Uganda when compared with some of the accessions from the ILRI forage genebank. This array of outcomes highlights the need for the integration of modern molecular tools (for example, genotyping by sequencing) for the establishment and management of core collections in order to better capture the available genetic diversity.

2. Current Status

Due to the fact that most smallholder livestock producers predominantly own small and fragmented pieces of land, grasses such as Napier grass offer a best-fit alternative to other feed options, as these are high yielding forages which require a minimum amount of inputs and acreage. Napier grass possesses a number of attributes including: high biomass yield [55,56]; rapid re-growth potential and ease of propagation [57]; attributes that help with the control of soil erosion [58]; resistance to a broad spectrum of pests and diseases [59]; and suitability for cellulosic biofuel production [60]. The growth rate and biomass production of Napier grass surpasses other tropical grasses including Johnson grass (Sorghum halepense), switchgrass (Panicum virgatum), maize (Zea mays) and sugarcane (Saccharum officinarum) [61]. In addition, by following best management practices (regular cutting between 60 to 90 days and keeping soil moisture level at an optimum level) and applying fertilizer when required, harvesting of Napier grass can be maintained for decades [39].
The aforementioned qualities of Napier grass make it an attractive option for livestock production systems. However, the adoption and utilization of Napier as an alternative forage crop has not been totally successful due to the limited amount of research and attention given to this crop [62]. At present, only a handful of molecular characterization studies have been reported and its genome is yet to be sequenced. Therefore, in order to increase the utility of Napier grass and advance its breeding initiatives, genotyping by sequencing (GBS) of the Napier grass collection held at ILRI is currently underway. This characterization will be of great importance to assess the available diversity within ILRI collections. Furthermore, GBS characterization will also help develop sufficient SNP markers for marker-assisted breeding of Napier grass.

2.1. Yield and Morphology

Napier grass cultivars have been reported to yield around 60 tonnes dry matter/ha/year, with some studies indicating significantly higher yields [26,27]. The yield of Napier grass mainly depends on the type of cultivar used which in turn is influenced by both the environment and management practices employed. Nevertheless, there are two major categories of Napier grass cultivars based on their morphology, the normal or tall (up to 4–7 m) varieties (for example ‘Australiano’, ‘Bana’ and ‘French Cameroon’) and the dwarf or semi-dwarf (<2 m) varieties (for example ‘Mott’) [27]. The normal varieties have been reported to produce up to twice as much yield as the dwarf ones [27,63]. However, dwarf varieties also have a number of positive attributes, including enhanced overwintering capacity in the border areas between subtropics and temperate zones, better nutritive value, and ease of management and harvesting [64,65]. Therefore, different cultivars of Napier grass can be adopted by farmers depending on their situation and ultimate use of the crop.
The performance and yield of Napier grass is heavily influenced by agro-ecology, climatic conditions, management practices and other edaphic factors [27,66]. According to Kebede et al. [67], the most significant factor affecting DM production of Napier grass is the environment, followed by genotype by environment interactions and then the genotype. However, the genotype is still important and the DM yield of Napier grass has been demonstrated to be superior to other tropical forages including Guinea grass (Megathysus maximus) and Rhodes grass (Chloris gayana) [68]. Table 2 provides a summary of the dry matter yield, and other important forage quality attributes, obtained in different studies conducted on Napier grass.

2.2. Nutritional Qualities

Significant variation in dry matter production (DM), crude protein (CP), neutral detergent fibre (NDF), acid detergent fibre (ADF) and other nutritional qualities have been reported across different studies and accessions of Napier grass (Table 2). Nutritional quality is strongly influenced by management practices and age at harvest but, on average, Napier grass is considered to contain 9% CP, 20% DM, 70% NDF, 50% ADF, 9% ash and 6% lignin in samples taken from 10–15 week old plants [74,75]. Apart from genetics, the nutritional qualities of forages are influenced by many factors including the climate [76], soil nutrition [77], season and grazing pressure [78], management [65,79,80] and fertilizer application [81]. Consequently, great care should be taken to determine the optimum time when planning to harvest or graze Napier grass in order to maximize both yield and nutritional qualities [82].
An important aspect for most forages is that cutting treatments and interval can have a significant impact on both yield and nutritional qualities [80,83]. For example, the CP content of Napier grass has been demonstrated to decrease significantly from 28.2% at a 40-day cutting interval to 8.8% at an 80-day interval [56,84]. In addition, the CP content of Napier grass has been shown to be negatively impacted over recurrent cuttings, although the possibility exists to increase both DM and protein content through increased fertilizer application [85]. On the other hand, DM production has been shown to increase significantly over consecutive cuttings from the first to the third [69]. Although cultivar and environment specific, Wanghchuck et al. [56] recommended a 60-day cutting interval in the optimum growing season to maintain a high yield without compromising nutrient composition too much.
Forages, when harvested during the early stages of their development, are considered to possess relatively higher crude protein content [76,86]. On the other hand, plant structural components (NDF, ADF and lignin) increase during later harvests, resulting in decreased dry matter digestibility [76,86]. Lignin, an integral component of the plant secondary cell wall [87], is the primary factor limiting organic matter digestibility and nutrient availability in forages [88,89] by interfering (as a physical barrier) with microbial enzymatic activity [88,90]. Despite many desirable characteristics, Napier grass is generally considered to be of inferior nutritional quality depending on management (particularly in terms of metabolisable energy, digestion kinetics and percentage crude protein) and palatability when compared to other forage crops [16,64,84]. Napier grass is reported to possess around 50% NDF, which is higher than the recommended NDF content for forage grasses [64]. Feeding experiments using Friesian cows revealed a loss of body weight and reduced milk yield when solely fed Napier grass varieties [71,74]. Lactating cows that were producing 10 kg/day milk yield, when fed on Rhodes grass (Chlolris gayana), produced only 6–8 kg/day, which was accompanied by a loss of body weight, when fed solely on Napier grass [74]. Therefore, when using Napier grass as a main forage supplement, it is recommended that a portion of the ration needs to be substituted with high energy/protein feed to prevent reduced rumen microbial activity and depressed digestibility [74]. On the other hand, dwarf and semi-dwarf Napier grass varieties have been shown to contain a higher CP content and lower ADF and hence are considered to be more suited as a forage for dairy farming applications [64]. In general, in areas where supplementary feed is scarce, intercropping Napier grass with legumes is considered to be a better option and such an approach could be the best alternative for smallholders who cannot supplement their milking cows with additional protein sources. In addition, using an increased amount of fertilizers can enhance organic matter content of Napier grass and subsequently enhance its nutritive quality as a feed [80].

2.3. Water Use Efficiency

A number of traits, including high dry matter production, ease of establishment and regeneration, persistence, and enhanced water use efficiency make Napier grass the primary forage of choice in the regions of Eastern and Central Africa where smallholder dairy farmers and pastoralists suffer from sporadic droughts and possess limited irrigation infrastructure [71]. Grasses which possess a C4 photosynthetic pathway are considered to have a competitive edge over C3 grass species when grown in tropical and subtropical regions [91]. Napier grass is a C4 grass species that also has the capacity to reduce shoot dry matter and maximize carbon assimilation during times of water stress, making it a desirable forage crop in areas subjected to intermittent droughts [92]. Napier grass undergoes changes in its morphology including leaf rolling, reduced stomatal conductance and enhanced water use efficiency when subjected to water stress conditions [93]. Since Napier grass is a perennial crop, it is expected to face rainfall fluctuations which would induce water stress at some point during the year and cultivars have been reported to lose as much as 20% of their yield potential when grown under water-deficient conditions in comparison to a control environment [93]. Hence, the development of cultivars that can withstand and produce during short periods of drought is considered to be useful for areas without irrigation, particularly as the effects of climate change are expected to impact on a growing number of regions.
Successful forage cultivation is influenced by the ability to minimize the trade-off between DM production and yield potential when grown under stress conditions such as drought. Biomass yield loss in Napier grass has been demonstrated to be less severe than in Guinea grass when grown under water stress conditions [93]. However, due to the fact that Napier grass has so far received little attention in terms of research investment, its advancement through breeding is considered to be minimal and lags behind other forages [62]. In addition, the lack of available genomic tools for Napier grass has hampered breeding initiatives. If an appropriate genomic toolbox is established and physiological responses to water stress are well understood, cultivars that can cope with intermittent drought should be able to be developed in the foreseeable future. The water use efficiency of a range of accessions from the ILRI forage genebank are currently being evaluated in irrigated and non-irrigated blocks, which will help further our understanding of their drought response mechanisms and provide the basis for the development of more drought tolerant Napier grass cultivars.

2.4. Pests and Diseases

Napier grass has been shown to be affected by many insects and other pests, bacteria, viruses, fungi and phytoplasmas, although most of them do not produce severe disease symptoms [3]. There have been numerous records of insect infestation on Napier grass. Farrell et al. [3] listed seventy-two different insects and mites that infect the species although for most of them, Napier grass acts as a reservoir in which the insect can survive between the growing seasons of other crops. To date, there has only been a single report of a bacterial infection (Xanthomonas albilineans), the causal agent of scald disease in sugarcane, in Napier grass and in this case the disease symptoms were unclear [94]. Potyviruses are considered to be the emerging problem for Napier grass but at the moment the two most significant threats to its productivity are the diseases smut and stunt which are caused by a fungus and a phytoplasma, respectively.

2.4.1. Viral Diseases

There have only been nine reported cases of viral infection of Napier grass worldwide. These viruses belong to the genera Mastrevirus, Potyvirus and Sobemovirus [3]. A geminivirus was the first virus reported to naturally infect Napier grass, described in Zimbabwe [94]. Subsequently, sugarcane mosaic virus [95], sugarcane chlorotic streak [96], maize mosaic (stripe disease) [97], die-back virus [98], maize streak geminivirus [99], elephant grass mosaic virus [100], a member of the potyviruses [101] and Johnson grass mosaic virus [3,95] have been reported. However, none of these were reported to produce serious disease symptoms or any significant productivity loss. The only report of symptoms was by Mih and Hanson [101], who reported that infection by one of the potyvirus isolates (Is16840), among three potyviruses isolated from the ILRI field genebank at Debre Zeit in Ethiopia in 1994–1996, produced severe mosaic and stunting symptoms in Napier grass that would cause productivity losses. Apart from this, an unclassified insect-borne virus was suggested to cause stunt disease in Napier grass in Uganda [102], that may also cause productivity loss.

2.4.2. Fungal Diseases

There have been as many as seventy-one different fungi reported to infect Napier grass [3]. Among them, only three diseases, namely eyespot, snow mould and head smut, have been addressed by researchers, mainly because the other fungi do not appear to have a significant effect on plant growth and productivity. The eyespot disease, caused by the fungus Helminthosporium spp., was first reported in the Caribbean in 1938 [96]. Although Burton [97] later reported that a Napier grass variety, ‘Merkeron’, was resistant to this disease (as the fungus did not cause a severe disease outbreak) there has been no significant effort to further any studies on this disease. The snow mould disease, also known as white mould disease, caused by the fungus Beniowskia sphaeroidea, was first reported to affect Napier grass in Kenya [98,99] and was later discovered in Malawi, Tanzania, Mauritius, Uganda and Zimbabwe [100,101]. The disease symptoms only appear during heavy rains and there is limited damage, restricted to during that season; it also does not appear to affect the vigour of the plants and livestock feeding on the diseased leaves do not appear to suffer any adverse effects. However, efforts have been made to introduce resistance to this disease and a resistant variety, ‘Clone 13’, was developed by conventional plant breeding in French Cameroon in the early 1970s [103].
The fungus responsible for head smut disease caused a severe disease outbreak with huge productivity losses of Napier grass in Kenya [18,95,102]. The causal agent of this disease is a fungus from the genus Ustilago, which was initially named as the species “kamerunensis” based on the place ‘Cameroon’ from where it was first isolated [104] and then later described as Ustilago kamerunensis” by Sydow and Sydow in 1911 [105]. The fungus appears to be slowly spreading from West Africa to the eastern parts of Africa as the disease was first reported in Cameroon [104], and subsequently in Uganda [106], Congo [107], Rwanda, Tanzania and then Kenya [108]. However, head smut occurs only in Africa as it has not been reported elsewhere outside the continent so far [95,109]. The mode of transmission of this disease is either by wind-borne spores or infected planting materials [110]. The spores of the smut-causing fungus are very light and have been reported to be able to spread by wind over large distances [111]. However, during a survey of the smut-infected districts of Kenya it was found that the disease spreads mainly by infected planting materials, as the farmers were completely unaware of this disease and the possible symptoms [110]. Although the smut disease of Napier grass has been recorded in many African countries, Kenya was the first country to be threatened by a potential epidemic. This could be because the strain identified in central Kenya causes the greatest yield losses when compared with the strains reported in other African countries [95,109,110]. The disease is widely spread across the central regions of Kenya and has been reported to cause 25–46% loss of biomass production [18,95,102]. The infected plants have thinner and shorter stems, a reduced numbers of leaves, and suffer from slower re-growth after cutting. The continual spread of the disease to other parts of the country, including the Rift valley and lower eastern region has also been recorded [1], which raises concerns about the possible future spread of this disease. Fungicide treatment is not currently an option to control the disease, especially for vegetatively propagated cuttings. Following diagnosis of infected planting material, destroying these materials by burning is currently the only option to control this disease. Efforts to select and breed resistant accessions or varieties have led to the identification of two resistant varieties, namely ‘Kakamega 1’ and ‘Kakamega 2’ [95,112] and the Muguga South branch of the Kenya Agricultural and Livestock Research Organization (KALRO) is promoting and distributing planting materials of these varieties to farmers in the affected regions in order to minimize the effect of this disease in the country. Co-evolutionary modification of some African accessions, particularly from Southern Africa, has also resulted in the development of resistance to the disease over time [113,114] and further focus is currently being placed on developing resistant plant material to manage the disease in the future. Many Napier grass clones have been collected from various sites across the world and are currently under trial in an attempt to discover whether they exhibit any selection bias related to their geographic origin which may have developed due to a co-evolutionary cycle of selection [109,112]. However, this co-evolutionary process in the induction of resistance may also lead to the selection of more virulent strains of the pathogen U. kamerunensis, in case of widespread use of selected resistant accessions [114]. Therefore, it is considered advisable to adopt a strategy which promotes the planting of varieties of mixed origin and resistance levels that could slow down the likely natural selection of the pathogen into a more virulent strain [33].

2.4.3. Phytoplasma (Stunt) Disease

Napier grass stunt disease is by far the most devastating disease of Napier grass as the infected plant material shows severe stunting symptoms, resulting in eventual death of the plant [115,116,117]. The disease was first observed in western Kenya in 1997 and has been reported to spread quickly, causing serious economic losses [118]. It has been demonstrated that the disease is associated with the 16SrXI phytoplasma (Candidatus (Ca.) Phytoplasma oryzae) group [118,119]. Subsequently, the disease has been reported to occur in Ethiopia [120], Uganda [116] and Tanzania and Rwanda [2]. The phytoplasma responsible for the stunt disease in Uganda was discovered to be similar to the Kenyan strain; however, in Ethiopia the strain was found to be a member of the 16SrIII group, ‘Ca. Phytoplasma pruni’ or X-disease [116,121], which caused symptoms similar to those observed for stunt disease in Uganda and Kenya but without the severe stunting [117]. The disease symptoms include yellowing of foliar material, smaller leaves, a proliferation of tillers, yellow to purple streaking and shortening of internodes to the extent that clumps appear severely stunted, resulting in a low biomass yield and eventual death of the plant, although this only occurs after cutting or grazing the grass [118]. However, the level of expression of the symptoms in phytoplasma-infected plants partly depends on the virulence of the strain, strain interference and phytoplasma concentration [122] and the abundance of insect vectors and phytoplasma-infested host plants [123]. The primary mode of transmission of the disease is by vegetative propagation of infected planting material or by phloem-feeding insects belonging to the families Cicadellidae (leafhoppers), Delphacidae (planthoppers) and some psyllids (Psylloidea) [124,125]. Obura et al. [126] identified Maiestas banda Kramer (Hemiptera:Cicadellidae) as a vector for Napier grass stunt disease phytoplasma in Kenya and Leptodelphax dymas and Exitianus spp. have been recorded in Ethiopia [127]. However, so far no vector has been identified in Uganda [126]. The vector–phytoplasma–host plant three-way interaction plays an important role in determining the spread of the disease [128]. There is the possible involvement of other phytoplasma susceptible food crops and grasses which could act as a reservoir, providing a source of inoculum for the spread of the disease [127] which would present a challenge to the development and implementation of management strategies for the disease. Two stunt-resistant varieties, ‘Ouma 2’ and ‘South Africa’, were selected by the International Centre of Insect Physiology and Ecology (icipe) in collaboration with KALRO and Rothamsted Research (UK) [129]. However, despite the efforts made to date to develop resistant varieties by national research organizations at various locations in western Kenya, many selected accessions have ultimately been found to be susceptible [130]. Consequently, the only guaranteed way to control the disease is through removal of the infected plants [131,132,133].

3. Future Prospects

Through years of effort, a number of cultivars have been selected and are currently in production in different regions of the world [6]. In addition, active breeding programs have been established to generate and capture greater diversity for both animal production and biofuel applications [134]. However, despite the efforts made so far, the production and use of Napier grass remains constrained by many factors. Nutritional quality, palatability, and propagation by seed or vegetative organs are currently the main limitations, and the diseases Napier grass stunt and head smut are significantly challenging its production in some regions of Africa. Moreover, enhancing the crop’s water use efficiency is another key area of research which will allow for production and use in areas with annual rainfall below its optimal range (<750 mm), and maintenance of current areas under the threat of climate change. In this review, we have compiled an extensive amount of evaluation and characterisation data which has been derived from various collections over the past few decades and demonstrated that significant diversity exists in these traits of interest which have the potential to be captured [39,44,54]. Consequently, by integrating modern molecular approaches into improvement strategies, some of the constraints in Napier grass production and use could now be efficiently addressed [44].
Opportunities to help capture the genetic diversity in crops for plant breeding and crop improvement have recently been revolutionized by the integration of advances in molecular genetics and genomics, plant biotechnology and next-generation sequencing. These advances have already been widely applied to crop improvement and offer the opportunity for new approaches to enhance quality and performance traits of feeds and forages at a relatively low cost. However orphan crops, which include tropical forages in general and Napier grass in particular, have not yet substantially benefited from these advances in molecular genetics and the associated modern tools that are available. There remain few reports on characterizing the genetic diversity of Napier grass through the application of molecular markers, and genetic maps and genome sequence information is largely lacking. As a result, there is little molecular information on Napier grass, which has implications for the knowledge-based use and conservation of available genetic resources for sustainable development. This, for example, has limited the ability to locate genomic regions controlling traits of interest and gene discovery. Consequently, the potential to use Napier grass as a ‘climate-smart’ forage crop, with traits such as enhanced water use efficiency, disease resistance and temperature tolerance stacked in new varieties which perform well in the face of climate change, has not been fully realised. Breeding efforts are also limited in Napier grass [6], which could be due to poor quality and limited seed production. The current distribution of planting materials to farmers is considered bulky, expensive [6] and carries the potential risk of disease distribution (for example, stunt disease) to new areas. In other vegetatively propagated crops such as potato, cassava and sugarcane, the use of diseased planting materials has been demonstrated to be the main source of inoculum for disease-causing agents [135]. Therefore, improving the seed production ability (both in terms of quantity and quality) of Napier grass potentially conveys a multitude of benefits including using seeds for distribution to farmers, creating genetic variation and new hybrid varieties through crossing and reducing the risk of disease spread related to distribution of vegetative propagules.
With respect to advances in nutritional quality of Napier grass, a number of opportunities exist to leverage the knowledge and advances seen in other fodder crops to the improvement of Napier grass and the benefit of livestock productivity. The plant cell wall provides the major source of dietary fibre and the nutritional availability of forage fibre to livestock is highly dependent on its composition and structure [136]. The plant cell wall is a complex biological structure, mainly composed of cellulose, hemicellulose, protein and lignin, which varies greatly depending on developmental stage, tissue type and plant species [137]. The bioavailability of cellulose, the major structural polymer of plants and the most abundant organic polymer on Earth [138] as an energy source is restricted by the β -glucosidic linkages, making it insoluble in water in its native form [139] and the lignin complex [140]. Lignin affects the digestion of cell-wall polysaccharides by interfering (as a physical barrier) with microbial enzymatic activity [88,90] and therefore, developing low-lignin Napier grass lines could substantially improve its digestibility and nutritional quality for enhanced livestock productivity. For example, it has been reported that a 1% increase in in vitro dry matter digestibility of forages leads to a 3.2% increase in daily weight gains of beef cattle [141]. Thus, the selection and/or development of low lignin varieties is another area of research where modern genomic tools could contribute substantially to improved feed quality in Napier grass. For example, the brown midrib mutants could offer an opportunity for selection in Napier grass. These mutants, which contain mutations in the lignin biosynthesis pathway and offer improved forage digestibility for livestock, have been selected in maize (Zea mays), sorghum (Sorghum bicolor) and pearl millet (Pennisetum glaucum) and a similar approach could be employed on Napier grass to improve its nutritional deficiency as a forage crop [142]. Transgenic approaches have also been used to enhance the nutritional quality of forages; for example, low-lignin alfalfa lines with enhanced digestibility have been developed [143] and similar technology can also be an option for Napier grass improvement. However, it is not only the reduction but the modification of lignin structure that can be important and the incorporation of p-coumaric acid instead of ferulic acid can improve cell wall digestibility in grasses by reducing cross linking [144].
In addition to enhancing nutritional quality, the improvement of other attributes of Napier grass, such as resistance to pests and diseases, also requires attention in order for this species to realise its full potential. Despite evidence demonstrating that insect vectors are responsible for transmitting diseases such as stunt and viruses, information on the impact of insects on feed yield and quality in Napier grass remains largely ambiguous. By employing modern molecular technologies and tapping into the genetic diversity available, we can develop a better understanding of the potential impacts and identify accessions which are tolerant to certain pests and diseases which could be used to introgress plant-derived resistance mechanisms into modern varieties. Two accessions, ‘Kakamega 1’ and ‘Kakamega 2’, have been identified and developed as varieties which provide resistance to the smut disease [95,112]. However, the mechanism of resistance is not fully understood and molecular approaches can play a role to augment and transfer the resistance genes in to commercial varieties. In addition, more severe strains of the pathogen may develop in the future through co-evolutionary mechanisms. Consequently, a more proactive effort is required, directed towards the discovery and development of new varieties with alternative resistance mechanisms to help address this threat in the future. The same applies for stunt disease, caused by the phytoplasmas, which results in severe productivity loss of Napier grass. To date there has been limited success achieved in the development of resistant varieties to combat this disease [133]. Therefore, the primary approach towards this disease would be screening the primary and secondary gene pool of Napier grass held in global collections that could lead to the identification of disease resistance genes with different modes of action against the phytoplasma.
The development of disease resistance in plants by introducing a gene, or a part thereof, from the pathogen is another approach which could be applied. For example, many viral diseases have been reported to infect Napier grass [3] which could have implications for both yield and quality, and the transgenic expression of viral coat proteins, replicases or other sequences from the virus genome could potentially be used to introduce resistance into the grass. Similarly, antifungal genes such as chitinases and glucanases could be introduced into the genome in order to confer resistance to fungal diseases such as the head smut disease reported to substantially affect household feed supply in Eastern and Central Africa. The use of antimicrobial genes to engineer the plant to produce antimicrobial proteins could also be considered to strengthen resistance mechanisms. Also, engineering with genes producing antibodies against a protein crucial for pathogenesis could result in a level of immunity or resistance to the pathogen. Alternatively, genetic modification or the recently developed technique of gene editing could be used in Napier grass to combat economically important insect pests. Accordingly, transgenic lines with resistance to different groups of insect pests can be generated using genes from various origins (Bt cry genes, the insect chitinase gene, RNA interference (RNAi) technology, plant-derived genes for proteinase inhibitors, and α-amylase inhibitors and lectins for example).
Good agricultural practices and management of diseases are currently the only option to protect against the spread of Napier grass diseases. The development and deployment of management practices to guard against any disease in a particular geographical area is guided by quantitative information on the existing levels of disease risk, definitive identification of the pathogen and a clear understanding of the factors that correlate strongly with disease/pathogen risk within a defined host population [145]. Although most of the viruses infecting Napier grass do not appear to cause any severe disease symptoms and productivity losses, there have been some reports on the effects of the potyvirus (Is 16840) identified in Ethiopia [146] and an insect-borne virus identified in Uganda [147] which need to be investigated more thoroughly, especially in terms of potential productivity loss, as they were reported to cause stunting in infected plants. There is limited information available on farmers’ knowledge and understanding of Napier grass diseases, in particular, and forages in general, which need to be addressed through extension packages. Similarly, in order to manage head smut disease of Napier grass, there is a need to educate farmers on the identification of disease symptoms and implementation of management strategies. Although burning of infected material is a good option to destroy the source of infection, the development of visible symptoms can take time, which allows the disease to spread further. Therefore, efficient diagnostic tools (serological or molecular) could offer a valuable asset for the early detection and diagnosis of the disease and to monitor its spread for improved management and containment. A number of studies have been undertaken towards the identification of the pathogen, possible vectors and disease severity for an outbreak of Napier grass stunt disease in Kenya [118,126,148]. However, further studies will be required to elucidate factors involved in the plant–host–vector three-way interaction related to the spread of stunt disease in Ethiopia and Uganda. There is also a need for further research to confirm whether Exitianus sp., L. dymas, or both species, act as a vector(s) of stunt disease. Further, for the disease outbreak in Uganda, there is a lack of information regarding the possible vectors involved in the transmission of the disease. Molecular studies would provide more information about the identity of the causal agent, vectors involved in disease transmission and the factors supporting the spread of the disease, which may help in the development of an effective management tool to control/minimize its spread. Seasonal monitoring of the insect vector populations could also provide information on the spread of the disease, and should facilitate the prediction of future Napier grass stunt disease outbreaks.
In a similar manner to the approaches reported for other crops, improvements in tolerance to abiotic stresses such as drought, salinity, soil pH and extreme temperatures in Napier grass could be achieved by employing a range of modern molecular tools. Despite the successful selection of a few accessions with resistance to the diseases head smut and stunt, the introgression of stress resistance into advanced breeding lines is yet to be effectively tackled in Napier grass. Moreover, genomic regions controlling desirable characteristics such as the dwarf growth habit, smooth (hairless) leaf, water use efficiency, etc. remain to be elucidated in Napier grass. Genetically Napier grass has two different sets of genomes: A’A’ and BB. The homologous nature of the A’A’ genome with the AA genome of pearl millet and the contribution of the B genome to perennial growth habit offers many other opportunities for future genomic studies in Napier grass.
It is expected that research in Napier grass characterization, phenotyping, genotyping and breeding will be aided by the application of modern tools in the near future. This will facilitate clone identification, the establishment, management and exploitation of core collections, generation of sequence information, development of genetic maps and identification of high throughput marker systems such as SSRs and single-nucleotide polymorphisms (SNPs) for the localization of genomic region(s) and discovery of genes controlling traits of interest in Napier grass. Once linkages between traits of interest and known genetic markers are well established, marker-assisted selection/breeding could facilitate the selection of new clones and/or varieties with improved agronomic traits. In general, modern molecular genetics should be quickly integrated into the current conservation, use and improvement strategies to address nutritional quality and palatability concerns, and biotic and abiotic stresses in Napier grass.

Acknowledgments

We acknowledge Michael Bolton for his analysis of the distribution of Napier grass accessions in genebanks and the generation of Table 1. We also acknowledge Michael Bolton for critical review of the manuscript. The authors were supported by the CGIAR Research Programs for Livestock and Fish and for Managing and Sustaining Crop Collections during the writing of this paper. ILRI fully supports the publication of open access articles.

Author Contributions

All authors contributed to writing the paper.

Conflicts of Interest

The authors declare no conflict of interest.

Abbreviations

The following abbreviations are used in this manuscript:
ADFAcid Detergent Fibre
AFLPAmplified Fragment Length Polymorphism
BtBacillus thuringiensis
CIATInternational Center for Tropical Agriculture
CPCrude Protein
CSIROCommonwealth Scientific and Industrial Research Organization
DMdry Matter
DRCDemocratic Republic of Congo
ESTExpressed Sequence Tag
GBSGenotyping by Sequencing
GRINGermplasm Resources Information Network
hahectare
icipeInternational Centre of Insect Physiology and Ecology
ILRIInternational Livestock Research Institute
ISSRInter-Sequential Simple Repeat
KALROKenya Agricultural and Livestock Research Organization
LLitre
NBPGRNational Bureau of Plant Genetic Resources, Delhi, India
NDFNeutral Detergent Fibre
RNAiRNA Interference
RAPDRandom Amplification of Polymorphic DNA
RFLPRestriction Fragment Length Polymorphism
RBGRoyal Botanic Gardens
SNPssingle-nucleotide polymorphisms
SRAPsSequence-Related Amplified Polymorphisms
SSRSimple Sequence Repeat
USDAUnited States Department of Agriculture

References

  1. Lukuyu, B.A.; Gachuiri, C.K.; Lukuyu, M.N.; Lusweti, C.; Mwendia, S. Feeding Dairy Cattle in East Africa; East Africa Dairy Development Project: Nairobi, Kenya, 2012. [Google Scholar]
  2. Kabirizi, J.; Muyekho, F.; Mulaa, M.; Msangi, R.; Pallangyo, B.; Kawube, G.; Zziwa, E.; Mugerwa, S.; Ajanga, S.; Lukwago, G.; et al. Napier Grass Feed Resource: Production, Constraints and Implications For Smallholder Farmers in Eastern and Central Africa; The Eastern African Agricultural Productivity Project: Naivasha, Kenya, 2015. [Google Scholar]
  3. Farrell, G.; Simons, S.; Hillocks, R. Pests, diseases and weeds of Napier grass, Pennisetum purpureum: A review. Int. J. Pest Manag. 2002, 48, 39–48. [Google Scholar] [CrossRef]
  4. Lowe, A.J.; Thorpe, W.; Teale, A.; Hanson, J. Characterisation of germplasm accessions of Napier grass (Pennisetum purpureum and P. purpureum× P. glaucum hybrids) and comparison with farm clones using RAPD. Genet. Resour. Crop Evol. 2003, 50, 121–132. [Google Scholar] [CrossRef]
  5. Sandhu, J.S.; Kumar, D.; Yadav, V.K.; Singh, T.; Sah, R.P.; Radhakrishna, A. Recent trends in breeding of tropical grass and forage species. In Proceedings of the 23rd International Grassland Congress, New Delhi, India, 20–24 November 2015; Vijay, D., Srivastava, M.K., Gupta, C.K., Malaviya, D.R., Roy, M.M., Mahanta, S.K., Singh, J.B., Maity, A., Ghosh, P.K., Eds.; Range Management Society of India: Jhansi, India, 2015; pp. 337–348. [Google Scholar]
  6. Singh, B.P.; Singh, H.P.; Obeng, E. Elephant grass. In Biofuel Crops: Production, Physiology and Genetics; Singh, B.P., Ed.; CAB International: Fort Valley State University, Fort Valley, GA, USA, 2013; pp. 271–291. [Google Scholar]
  7. Brunken, J.N. A systematic study of Pennisetum sect. Pennisetum (Gramineae). Am. J. Bot. 1977, 64, 161–176. [Google Scholar] [CrossRef]
  8. Donadío, S.; Giussani, L.M.; Kellogg, E.A.; Zuolaga, F.O.; Morrone, O. A preliminary molecular phylogeny of Pennisetum and Cenchrus (Poaceae-Paniceae) based on the trnL-F, rpl16 chloroplast markers. Taxon 2009, 58, 392–404. [Google Scholar]
  9. Dos Reis, G.B.; Mesquita, A.T.; Torres, G.A.; Andrade-Vieira, L.F.; Vander Pereira, A.; Davide, L.C. Genomic homeology between Pennisetum purpureum and Pennisetum glaucum (Poaceae). Comp. Cytogenet. 2014, 8, 199. [Google Scholar] [PubMed]
  10. Martel, E.; De Nay, D.; Siljak-Yakoviev, S.; Brown, S.; Sarr, A. Genome size variation and basic chromosome number in Pearl millet and fourteen related Pennisetum species. J. Hered. 1997, 88, 139–143. [Google Scholar] [CrossRef]
  11. Harris, K.; Anderson, W.; Malik, R. Genetic relationships among Napier grass (Pennisetum purpureum Schum.) nursery accessions using AFLP markers. Plant Genet. Resour. 2010, 8, 63–70. [Google Scholar] [CrossRef]
  12. Kandel, R.; Singh, H.P.; Singh, B.P.; Harris-Shultz, K.R.; Anderson, W.F. Assessment of genetic diversity in Napier Grass (Pennisetum purpureum Schum.) using microsatellite, single-nucleotide polymorphism and insertion-deletion markers from Pearl Millet (Pennisetum glaucum (L.) R. Br.). Plant Mol. Biol. Rep. 2016, 34, 265–272. [Google Scholar] [CrossRef]
  13. Cook, B.G.; Pengelly, B.C.; Brown, S.D.; Donnelly, J.L.; Eagles, D.A.; Franco, M.A.; Hanson, J.; Mullen, B.F.; Partridge, I.J.; Peters, M.; et al. Tropical Forages: An Interactive Selection Tool; [CD-ROM], CSIRO, DPI&F(Qld), CIAT and ILRI: Brisbane, Australia, 2005. [Google Scholar]
  14. Diz, D.A. Breeding Procedures and Seed Production Management in Pearl millet × Elephant grass Hexaploids Hybrids. Ph.D. Thesis, University of Florida, Gainesville, FL, USA, 1994. [Google Scholar]
  15. Cheng, Y. Forage breeding in Taiwan-Review. Asian Australas. J. Anim.Sci. 1991, 4, 203–209. [Google Scholar] [CrossRef]
  16. Heuzé, V.; Tran, G.; Giger-Reverdin, S.; Lebas, F. Elephant grass (Pennisetum purpureum). Available online: http://www.feedipedia.org/node/395 (accessed on 21 September 2016).
  17. Ishii, Y.; Hamano, K.; Kang, D.J.; Kannika, R.; Idota, S.; Fukuyama, K.; Nishiwaki, A. C4-Napier grass cultivation for cadmium phytoremediation activity and organic livestock farming in Kyushu, Japan. J. Agric. Sci. Technol. 2013, 3, 321. [Google Scholar]
  18. Orodho, A.B. The Role and Importance of Napier Grass in the Smallholder Dairy Industry in Kenya; Food and Agriculture Organization: Rome, Italy, 2006; p. 2011. [Google Scholar]
  19. Pandit, N.P.; Shrestha, M.K.; Yi, Y.; Diana, J.S.; Rampur, C. Polyculture of grass carp and Nile tilapia with Napier grass as the sole nutrient input in the subtropical climate of Nepal. In Proceedings of the 6th International Symposium on Tilapia in Aquaculture, Manila, Philippines, 12–16 September 2004; pp. 12–16. [Google Scholar]
  20. Shrestha, M.; Yadav, C. Feeding of Napier (Pennisetum purpureum) to grass carp in polyculture: A sustainable fish culture practice for small farmers. Asian Fish. Sci. 1998, 11, 287–294. [Google Scholar]
  21. Shaha, D.C.; Kundu, S.R.; Hasan, M.N. Production of organic grass carp (Ctenopharyngodon idella) and GIFT tilapia (Oreochromis niloticus) using Napier grass, Pennisetum purpureum. J. Fish. 2015, 3, 233–238. [Google Scholar] [CrossRef]
  22. Akah, N.; Onweluzo, J. Evaluation of water-soluble vitamins and optimum cooking time of fresh edible portions of Elephant Grass (Pennisetum purpureum L. Schumach) shoot. Niger. Food J. 2014, 32, 120–127. [Google Scholar] [CrossRef]
  23. Khan, Z.; Chiliswa, P.; Ampong-Nyarko, K.; Smart, L.; Polaszek, A.; Wandera, J.; Mulaa, M. Utilisation of wild gramineous plants for management of cereal stemborers in Africa. Int. J. Trop. Insect Sci. 1997, 17, 143–150. [Google Scholar] [CrossRef]
  24. Khan, Z.R.; Midega, C.A.; Hutter, N.J.; Wilkins, R.M.; Wadhams, L.J. Assessment of the potential of Napier grass (Pennisetum purpureum) varieties as trap plants for management of Chilo partellus. Entomol. Exp. Appl. 2006, 119, 15–22. [Google Scholar] [CrossRef]
  25. Khan, Z.R.; Midega, C.A.; Wadhams, L.J.; Pickett, J.A.; Mumuni, A. Evaluation of Napier grass (Pennisetum purpureum) varieties for use as trap plants for the management of African stemborer (Busseola fusca) in a push–pull strategy. Entomol. Exp. Appl. 2007, 124, 201–211. [Google Scholar] [CrossRef]
  26. Oliveira, M.L.F.; Daher, R.F.; Gravina, G.D.A.; da Silva, V.B.; Viana, A.P.; Rodrigues, E.V.; Shimoya, A.; Junior, A.T.D.A.; Menezes, B.R.D.S.; Rocha, A.D.S. Pre-breeding of Elephant grass for energy purposes and biomass analysis in Campos dos Goytacazes-RJ, Brazil. Afr. J. Agric. Res. 2014, 9, 2743–2758. [Google Scholar]
  27. Rengsirikul, K.; Ishii, Y.; Kangvansaichol, K.; Sripichitt, P.; Punsuvon, V.; Vaithanomsat, P.; Nakamanee, G.; Tudsri, S. Biomass yield, chemical composition and potential ethanol yields of eight cultivars of Napier grass (Pennisetum purpureum Schumach.) harvested 3-monthly in central Thailand. J. Sustain. Bioenergy Syst. 2013, 3, 107. [Google Scholar] [CrossRef]
  28. Lima, M.A.; Gomez, L.D.; Steele-King, C.G.; Simister, R.; Bernardinelli, O.D.; Carvalho, M.A.; Rezende, C.A.; Labate, C.A.; McQueen-Mason, S.J.; Polikarpov, I. Evaluating the composition and processing potential of novel sources of Brazilian biomass for sustainable biorenewables production. Biotechnol. Biofuels 2014, 7, 1. [Google Scholar] [CrossRef] [PubMed]
  29. Hanna, W.W.; Monson, W.G. Yield, quality, and breeding of Pearl millet × Napier grass interspecific hybrids. Agron. J. 1980, 72, 358–360. [Google Scholar] [CrossRef]
  30. Pitman, W.D.; Sotomayor-Rios, A. Tropical Forage Plants: Development and Use; CRC Press: Boca Raton, FL, USA, 2000. [Google Scholar]
  31. Anderson, W.F.; Casler, M.D.; Baldwin, B.S. Improvement of perennial forage species as feedstock for bioenergy. In Genetic Improvement of Bioenergy Crops; Vermerris, W., Ed.; Springer Science + Business Media LLC: New York, NY, USA, 2008; pp. 347–376. [Google Scholar]
  32. Paiva, E.A.; Bustamante, F.O.; Barbosa, S.; Pereira, A.V.; Davide, L.C. Meiotic behavior in early and recent duplicated hexaploid hybrids of Napier grass (Pennisetum purpureum) and Pearl millet (Pennisetum glaucum). Caryologia 2012, 65, 114–120. [Google Scholar] [CrossRef]
  33. Omayio, D.O.; Ajanga, S.I.; Muoma, J.V.; Muyekho, F.N.; Yamame, M.K.; Kariuki, I.M.S. Using Napier grass accessions’ origins, neighbour joining groups and their response to Ustilago kamerunensis to predict a probable co-evolutionary scenario. Int. J. Recent Sci. Res. 2015, 6, 2639–2645. [Google Scholar]
  34. Kawube, G.; Alicai, T.; Otim, M.; Mukwaya, A.; Kabirizi, J.; Talwana, H. Resistance of Napier grass clones to Napier grass stunt Disease. Afr. Crop Sci. J. 2014, 22, 229–236. [Google Scholar]
  35. Hanna, W.W.; Monson, W.G. Registration of dwarf Tift N75 Napier grass germplasm. Crop Sci. 1988, 28, 870–871. [Google Scholar] [CrossRef]
  36. Premaratne, S.; Premalal, G.G.C. Hybrid Napier (Pennisetum perpureum × Pennisetum americarnum) var. CO-3: A resourceful fodder grass for dairy development in Sri Lanka. J. Agric. Sci. 2006, 2. [Google Scholar] [CrossRef]
  37. Genesys. Available online: https://www.genesys-pgr.org/welcome (acessed on 30 November 2016).
  38. Tcacenco, F.A.; Lance, G.N. Selection of morphological traits for characterisation of Elephant grass accessions. Trop. Grassl. 1992, 26, 145–155. [Google Scholar]
  39. Van De Wouw, M.; Hanson, J.; Leuthi, S. Morphological and argonomic characterisation of a collection of Napier grass (Pennisetum purpureum) and P. purpureum × P. glaucum. Trop. Grassl. 1999, 33, 150–158. [Google Scholar]
  40. Smith, R.L.; Schweder, M.; Chowdhury, M.; Seib, J.; Schank, S. Development and application of RFLP and RAPD DNA markers in genetic improvement of Pennisetum for biomass and forage production. Biomass Bioenergy 1993, 5, 51–62. [Google Scholar] [CrossRef]
  41. Babu, C.; Sundaramoorthi, J.; Vijayakumar, G.; Ram, S.G. Analysis of genetic diversity in Napier grass (Pennisetum purpureum Schum) as detected by RAPD and ISSR markers. J. Plant Biochem. Biotechnol. 2009, 18, 181–187. [Google Scholar] [CrossRef]
  42. Bhandari, A.P.; Sukanya, D.; Ramesh, C. Application of isozyme data in fingerprinting Napier grass (Pennisetum purpureum Schum.) for germplasm management. Genet. Resour. Crop Evol. 2006, 53, 253–264. [Google Scholar] [CrossRef]
  43. Struwig, M.; Mienie, C.; Van Den Berg, J.; Mucina, L.; Buys, M. AFLPs are incompatible with RAPD and morphological data in Pennisetum purpureum (Napier grass). Biochem. Syst. Ecol. 2009, 37, 645–652. [Google Scholar] [CrossRef]
  44. Wanjala, B.W.; Obonyo, M.; Wachira, F.N.; Muchugi, A.; Mulaa, M.; Harvey, J.; Skilton, R.A.; Proud, J.; Hanson, J. Genetic diversity in Napier grass (Pennisetum purpureum) cultivars: Implications for breeding and conservation. AoB Plants 2013, 5, plt022. [Google Scholar] [CrossRef] [PubMed]
  45. De Lima, R.; Daher, R.; Goncalves, L.; Rossi, D.; do Amaral Júnior, A.; Pereira, M.; Lédo, F. RAPD and ISSR markers in the evaluation of genetic divergence among accessions of Elephant grass. Genet. Mol. Res. 2011, 10, 1304–1313. [Google Scholar] [CrossRef] [PubMed]
  46. Xie, X.-M.; Zhou, F.; Zhang, X.-Q.; Zhang, J.-M. Genetic variability and relationship between MT-1 Elephant grass and closely related cultivars assessed by SRAP markers. J. Genet. 2009, 88, 281–290. [Google Scholar] [CrossRef] [PubMed]
  47. Allouis, S.; Qi, X.; Lindup, S.; Gale, M.; Devos, K. Construction of a BAC library of pearl millet, Pennisetum glaucum. Theor. Appl. Genet. 2001, 102, 1200–1205. [Google Scholar] [CrossRef]
  48. Budak, H.; Pedraza, F.; Cregan, P.; Baenziger, P.; Dweikat, I. Development and utilization of SSRs to estimate the degree of genetic relationships in a collection of pearl millet germplasm. Crop Sci. 2003, 43, 2284–2290. [Google Scholar] [CrossRef]
  49. Mariac, C.; Luong, V.; Kapran, I.; Mamadou, A.; Sagnard, F.; Deu, M.; Chantereau, J.; Gerard, B.; Ndjeunga, J.; Bezançon, G. Diversity of wild and cultivated pearl millet accessions (Pennisetum glaucum (L.) R. Br.) in Niger assessed by microsatellite markers. Theor. Appl. Genet. 2006, 114, 49–58. [Google Scholar] [CrossRef] [PubMed]
  50. Qi, X.; Lindup, S.; Pittaway, T.; Allouis, S.; Gale, M.; Devos, K. Development of simple sequence repeat markers from bacterial artificial chromosomes without subcloning. Biotechniques 2001, 31, 358–362. [Google Scholar]
  51. Senthilvel, S.; Jayashree, B.; Mahalakshmi, V.; Kumar, P.S.; Nakka, S.; Nepolean, T.; Hash, C. Development and mapping of simple sequence repeat markers for pearl millet from data mining of expressed sequence tags. BMC Plant Biol. 2008, 8, 119. [Google Scholar] [CrossRef] [PubMed]
  52. Sousa Azevedo, A.L.; Costa, P.P.; Machado, J.C.; Machado, M.A.; Pereira, A.V.; José da Silva Lédo, F. Cross species amplification of microsatellite markers in and genetic diversity of Napier grass accessions. Crop Sci. 2012, 52, 1776–1785. [Google Scholar] [CrossRef]
  53. Dowling, C.D.; Burson, B.L.; Foster, J.L.; Tarpley, L.; Jessup, R.W. Confirmation of Pearl millet-Napier grass hybrids using EST-derived simple sequence repeat (SSR) markers. Am. J. Plant Sci. 2013, 4, 1004–1012. [Google Scholar] [CrossRef]
  54. Kawube, G.; Alicai, T.; Wanjala, B.; Njahira, M.; Awalla, J.; Skilton, R. Genetic diversity in Napier Grass (Pennisetum purpureum) assessed by SSR Markers. J. Agric. Sci. 2015, 7, 147. [Google Scholar] [CrossRef]
  55. Morais, R.F.D.; Souza, B.J.D.; Leite, J.M.; Soares, L.H.D.B.; Alves, B.J.R.; Boddey, R.M.; Urquiaga, S. Elephant grass genotypes for bioenergy production by direct biomass combustion. Pesqui. Agropecu. Bras. 2009, 44, 133–140. [Google Scholar] [CrossRef]
  56. Wangchuk, K.; Rai, K.; Nirola, H.; Dendup, C.; Mongar, D. Forage growth, yield and quality responses of Napier hybrid grass cultivars to three cutting intervals in the Himalayan foothills. Trop. Grassl. Forrajes Trop. 2015, 3, 142–150. [Google Scholar] [CrossRef]
  57. Lee, C.N.; Fukumoto, G.K.; Thorne, M.S.; Stevenson, M.H.; Nakahata, M.; Ogoshi, R.M. Bana Grass (Pennisetum purpureum): A Possible Forage for Ruminants in Hawai‘i; University of Hawai‘i: Honolulu, HI, USA, 2016. [Google Scholar]
  58. Magcale-Macandog, D.; Predo, C.; Menz, K.; Predo, A. Napier grass strips and livestock: A bioeconomic analysis. Agrofor. Syst. 1998, 40, 41–58. [Google Scholar] [CrossRef]
  59. Van den Berg, J.; Van Hamburg, H. Trap cropping with Napier grass, Pennisetum purpureum (Schumach), decreases damage by maize stem borers. Int. J. Pest Manag. 2015, 61, 73–79. [Google Scholar] [CrossRef]
  60. Tsai, W.-T.; Tsai, Y.-L. Thermochemical characterization of Napier grass as an energy source and its environmental and economic benefit analysis. Energy Sources Part B Econ. Plan. Policy 2016, 11, 130–136. [Google Scholar]
  61. Ra, K.; Shiotsu, F.; Abe, J.; Morita, S. Biomass yield and nitrogen use efficiency of cellulosic energy crops for ethanol production. Biomass Bioenergy 2012, 37, 330–334. [Google Scholar] [CrossRef]
  62. Mwendia, S.; Yunusa, I.; Whalley, R.; Sindel, B.; Kenney, D.; Kariuki, I. Use of plant water relations to assess forage quality and growth for two cultivars of Napier grass (Pennisetum purpureum) subjected to different levels of soil water supply and temperature regimes. Crop Pasture Sci. 2014, 64, 1008–1019. [Google Scholar]
  63. Williams, M.J.; Hanna, W.W. Performance and nutritive quality of dwarf and semi-dwarf Elephant grass genotypes in the south-eastern USA. Trop. Grassl. 1995, 29, 122–127. [Google Scholar]
  64. Halim, R.A.; Shampazuraini, S.; Idris, A.B. Yield and nutritive quality of nine Napier grass varieties in Malaysia. Malays. J. Anim. Sci. 2013, 16, 37–44. [Google Scholar]
  65. Mukhtar, M.; Ishii, Y.; Tudsri, S.; Idota, S.; Sonoda, T. Dry matter productivity and overwintering ability of the dwarf and normal Napier grasses as affected by the planting density and cutting frequency. Plant Prod. Sci. 2003, 6, 65–73. [Google Scholar] [CrossRef]
  66. Utamy, R.F.; Ishii, Y.; Idota, S.; Harada, N.; Fukuyama, K. Adaptability of dwarf Napier grass under cut and carry and grazing sysytems for smallholder beef farmers in southern Kyhushu, Japan. J. Warm Reg. Soc. Anim. Jpn. 2011, 54, 87–98. [Google Scholar]
  67. Kebede, G.; Feyissa, F.; Assefa, G.; Alemayehu, M.; Mengistu, A.; Kehaliew, A.; Melese, K.; Mengistu, S.; Tadesse, E.; Wolde, S. Chemical composition and in vitro organic matter digestibility of Napier Grass (Pennisetum purpureum (L.) Schumach) accessions in the mid and highland areas of Ethiopia. Int. J. Livest. Res. 2016, 6, 41–59. [Google Scholar] [CrossRef]
  68. Relwani, L.L.; Nakat, R.V.; Kandale, D.Y. Intercropping of four leuceana cultivars with three grasses. Leuceana Res. Rep. 1982, 3, 41. [Google Scholar]
  69. Amin, R.; Ali, N.R.S.M.Y.; Abul, H.M.; Khatun, M. Study on cutting intervals on biomass yield, nutritive value and their oxalate content of different high yielding Napier (P. purpureum) cultivars. Asian Australas. J. Biosci. Biotechnol. 2016, 1, 100–107. [Google Scholar]
  70. Zewdu, T. Variation in growth, yield, chemical composition and in vitro dry matter digestibility of Napier grass accessions (Pennisetum purpureum). Trop. Sci. 2005, 45, 67–73. [Google Scholar] [CrossRef]
  71. Nyambati, E.M.; Muyekho, F.N.; Onginjo, E.; Lusweti, C.M. Production, characterization and nutritional quality of Napier grass (Pennisetum purpureum (Schum.)) cultivars in Western Kenya. Afr. J. Plant Sci. 2010, 4, 496–502. [Google Scholar]
  72. Ortega-Gómez, R.; Castillo-Gallegos, E.; Jarillo-Rodríguez, J.; Escobar-Hernández, R.; Ocaña-Zavaleta, E.; de la Mora, B.V. Nutritive quality of ten grasses during the rainy season in a hot-humid climate and ultisol soil. Trop. Subtrop. Agroecosyst. 2011, 13, 481–491. [Google Scholar]
  73. Tavirimirwa, B.; Manzungu, E.; Ncube, S. The evaluation of dry season nutritive value of dominant and improved grasses in fallows in Chivi district, Zimbabwe. Online J. Anim. Feed Res. 2012, 2, 470–474. [Google Scholar]
  74. Gwayumba, W.; Christensen, D.; McKinnon, J.; Yu, P. Dry matter intake, digestibility and milk yield by Friesian cows fed two Napier grass varieties. Asian Australas. J. Anim. Sci. 2002, 15, 516–521. [Google Scholar] [CrossRef]
  75. Islam, M.; Saha, C.; Sarker, N.; Jalil, M.; Hasanuzzaman, M. Effect of variety on proportion of botanical fractions and nutritive value of different Napier grass (Pennisetum purpureum) and relationship between botanical fractions and nutritive Value. Asian Australas. J. Anim. Sci. 2003, 16, 837–842. [Google Scholar] [CrossRef]
  76. Keba, H.T.; Madakadze, I.C.; Angassa, A.; Hassen, A. Nutritive value of grasses in semi-arid rangelands of Ethiopia: Local experience based herbage preference evaluation versus laboratory analysis. Asian Australas. J. Anim. Sci. 2013, 26, 366. [Google Scholar] [CrossRef] [PubMed]
  77. Tessema, Z.K.; De Boer, W.F.; Baars, R.M.T.; Prins, H.H.T. Changes in soil nutrients, vegetation structure and herbaceous biomass in response to grazing in a semi-arid savanna of Ethiopia. J. Arid Environ. 2011, 75, 662–670. [Google Scholar] [CrossRef]
  78. Henkin, Z.; Ungar, E.D.; Dvash, L.; Perevolotsky, A.; Yehuda, Y.; Sternberg, M.; Voet, H.; Landau, S.Y. Effects of cattle grazing on herbage quality in a herbaceous Mediterranean rangeland. Grass Forage Sci. 2011, 66, 516–525. [Google Scholar] [CrossRef]
  79. Van der Westhuizen, H.; Snyman, H.; Fouché, H. A degradation gradient for the assessment of rangeland condition of a semi-arid sourveld in southern Africa. Afr. J. Range Forage Sci. 2005, 22, 47–58. [Google Scholar] [CrossRef]
  80. Okwori, A.I.; Magani, I.E. Influence of nitrogen sources and cutting interval on the digestibility of four grass species in the southern guinea savanna of Nigeria. Agric. Biol. J. N. Am. 2010, 1, 526–533. [Google Scholar]
  81. Hasyim, H.; Ishii, Y.; Ahmad, W.; Sachiko, I. Quality herbage production of dwarf Napier grass with Italian Ryegrass cropping under digested effluent application in Southern Kyushu, Japan. Am. J. Agric. Biol. Sci. 2015, 11, 35–44. [Google Scholar] [CrossRef]
  82. Na, C.I.; Fedenko, J.R.; Sollenberger, L.E.; Erickson, J.E. Harvest management affects biomass composition responses of C4 perennial bioenergy grasses in the humid subtropical USA. GCB Bioenergy 2016. [Google Scholar] [CrossRef]
  83. Butt, N.M.; Donart, G.B.; Southwara, M.G.; Pieper, R.D. Effect of defoliation on plant growth of Napier grass. Trop. Sci. Lond. 1993, 33, 111. [Google Scholar]
  84. Bayble, T.; Melaku, S.; Prasad, N. Effects of cutting dates on nutritive value of Napier (Pennisetum purpureum) grass planted sole and in association with Desmodium (Desmodium intortum) or Lablab (Lablab purpureus). Livest. Res. Rural Dev. 2007, 19, 120–136. [Google Scholar]
  85. Carvalho, C.A.B.D.; Menezes, J.B.D.O.X.D.; Cóser, A.C. Effect of fertilizer and cutting frequency on yield and nutritive value of Elephant grass. Cienc. Agrotecnol. 2000, 24, 233–241. [Google Scholar]
  86. Mirza, S.N.; Muhammad, N.; Qamar, I.A. Effect of growth stages on the yield and quality of forage grasses. Pak. J. Agric. Res. 2002, 17, 145–147. [Google Scholar]
  87. Boudet, A.M. Towards an understanding of the supramolecular organization of the lignified wall. Plant Cell Wall 2003, 8, 155–182. [Google Scholar]
  88. Jung, H.-J.G. Forage digestibility: The intersection of cell wall lignification and plant tissue anatomy. In Proceedings of the 23rd Annual Florida Ruminant Nutrition Symposium, Gainesville, FL, USA, 31 January–1 February 2012; University of Florida: Gainesville, FL, USA, 2012; pp. 162–174. [Google Scholar]
  89. Moore, K.J.; Jung, H.-J.G. Lignin and fiber digestion. J. Range Manag. 2001, 54, 420–430. [Google Scholar] [CrossRef]
  90. Agbor, V.B.; Cicek, N.; Sparling, R.; Berlin, A.; Levin, D.B. Biomass pretreatment: Fundamentals toward application. Biotechnol. Adv. 2011, 29, 675–685. [Google Scholar] [CrossRef] [PubMed]
  91. Taylor, S.; Ripley, B.; Woodward, F.; Osborne, C. Drought limitation of photosynthesis differs between C3 and C4 grass species in a comparative experiment. Plant Cell Environ. 2011, 34, 65–75. [Google Scholar] [CrossRef] [PubMed]
  92. Cardoso, J.A.; Pineda, M.; de la Cruz Jiménez, J.; Vergara, M.F.; Rao, I.M. Contrasting strategies to cope with drought conditions by two tropical forage C4 grasses. AoB Plants 2015, 7, plv107. [Google Scholar] [CrossRef] [PubMed]
  93. Purbajanti, E.; Anwar, S.; Wydiati, F.K. Drought stress effect on morphology characters, water use efficiency, growth and yield of guinea and napier grasses. Int. Res. J. Plant Sci. 2012, 3, 47. [Google Scholar]
  94. Rott, P.; Chatenet, M.; Granier, M.; Baudin, P. L’échaudure des feuilles de canne à sucre provoquée par Xanthomonas albilineans (Ashby) Dowson. II: Diagnostic et spectres d'hôtes de l'agent pathogène en Afrique tropicale. L'Agron. Trop. 1988, 43, 244–251. [Google Scholar]
  95. Farrell, G. Towards the Management of Ustilago kamerunensis H Sydow and Sydow, a Smut Pathogen of Napier Grass (Pennisetum purpureum Schum.) in Kenya. Ph.D. Thesis, University of Greenwich, London, UK, 1998. [Google Scholar]
  96. Paterson, D.D. Further experiments with cultivated tropical fodder crops. Emp. J. Exp. Agric. 1938, 6, 323–340. [Google Scholar]
  97. Burton, G.W. Registration of ‘Merkeron’ Napier grass. Crop Sci. 1989, 29, 1327. [Google Scholar] [CrossRef]
  98. Maher, C. Elephant grass (Pennisetum purpureum) as a cattle fodder in Kenya. East Afr. Agric. J. 1936, 1, 340–342. [Google Scholar] [CrossRef]
  99. Nattrass, R.M. Notes on plant diseases. East Afr. Agric. J. 1941, 7, 56. [Google Scholar]
  100. Lenné, J.M. A World List of Fungal Diseases of Tropical Pasture Species; CIAT: Wallingford, UK, 1990. [Google Scholar]
  101. Mtisi, E.; de Milliano, W. False mildew on Pearl millet and other hosts in Zimbabwe. East Afr. Agric. For. J. 1993, 59, 145–153. [Google Scholar]
  102. Farrell, G.; Simons, S.; Hillocks, R. A novel technique for measuring biomass loss in a diseased tussock grass. Trop. Grassl. 2000, 34, 118–124. [Google Scholar]
  103. Boonman, G. East Africa’s Grasses and Fodders: Their Ecology and Husbandry; Springer Science + Business Media, B.V.: Dordrecht, The Netherlands, 1993. [Google Scholar]
  104. Ledermann, C. Herbarium Record 162103, Systematic Botany and Mycology Laboratory, USDA, Maryland, USA. 1998. Available online: http://nt.ars-grin.gov/fungaldatabases/fungushost (accessed on 15 September 2016). [Google Scholar]
  105. Sydow, H.; Sydow, P. Fungi Africani novi. Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie/begr. Von A. Engler 1911, 45, 259–265. [Google Scholar]
  106. Snowden, J.D. Herbarium Record 162104, Systematic Botany and Mycology Laboratory, USDA, Maryland, USA. 1998. Available online: http://nt.ars-grin.gov/fungaldatabases/fungushost (accessed on 15 September 2016). [Google Scholar]
  107. Watson, A.J. Foreign Bacterial and Fungus Diseases of Food, Forage, and Fiber Crops: An Annotated List; Agricutural Research service, United States Department of Agrculture: Washington, DC, USA, 1971.
  108. Kung’u, J.N.; Waller, J.M. Occurrence of smut of Napier grass caused by Ustilago kamerunensis H Sydow and Sydow in Kenya. Int. J. Pest Manag. 2001. [Google Scholar] [CrossRef]
  109. Association of Strengthening Agricultural Research in East and Central Africa (ASARECA). Workshop on Mitigating the Impact of Napier Grass Smut and Stunt Diseases for the Smallholder Dairy Sector-Sharing Results: Final Report, June 1–3, 2010; ILRI: Addis Ababa Ethiopia, Ethiopia, 2010. [Google Scholar]
  110. Farrell, G.; Simons, S.; Hillocks, R. Ustilago kamerunensis on Napier grass in Kenya. Int. J. Pest Manag. 2002, 48, 25–28. [Google Scholar] [CrossRef]
  111. Simmonds, N.W. Some speculative calculations on the dispersal of sugarcane smut disease. Sugar Cane 1994, 1, 2–5. [Google Scholar]
  112. Mwendia, S.; Wanyoike, M.; Wahome, R.; Mwangi, D. Effect of napier head smut disease on Napier yields and the disease coping strategies in farming systems in central Kenya. Livest. Res. Rural Dev. 2007, 19. Available online: http://www.lrrd.org/lrrd19/8/mwen19109.htm (accessed on 11 November 2016). [Google Scholar]
  113. Friedman, A.R.; Baker, B.J. The evolution of resistance genes in multi-protein plant resistance systems. Curr. Opin. Genet. Dev. 2007, 17, 493–499. [Google Scholar] [CrossRef] [PubMed]
  114. Rausher, M.D. Co-evolution and plant resistance to natural enemies. Nature 2001, 411, 857–864. [Google Scholar] [CrossRef] [PubMed]
  115. Alicai, T.; Kabirizi, J.; Byenkya, S.; Kayiwa, S.; Ebong, C. Assessment of the Magnitude and Farmers' Management Practices of the Elephant Grass Stunting Disorder in Masaka District; Namulonge Agricultural and Animal Production Research Institute: Kampala, Uganda, 2004. [Google Scholar]
  116. Nielsen, S.L.; Ebong, C.; Kabirizi, J.; Nicolaisen, M. First report of a 16SrXI group phytoplasma (Candidatus phytoplasma oryzae) associated with Napier grass disease in Uganda. Plant Pathol. 2007, 56, 1039. [Google Scholar] [CrossRef]
  117. Rosete, Y.A.; Jones, P. Phytoplasma diseases of the Gramineae. In Phytoplasmas: Genomes, Plant Hosts and Vectors; Weintraub, P.G., Jones, P., Eds.; CAB International: Wallingford, UK, 2010; pp. 170–187. [Google Scholar]
  118. Jones, P.; Devonshire, B.; Holman, T.; Ajanga, S. Napier grass stunt: A new disease associated with a 16SrXI group phytoplasma in Kenya. Plant Pathol. 2004, 53, 519. [Google Scholar] [CrossRef]
  119. Jones, P.; Arocha, T.; Zerfy, J.; Proud, J.; Abebe, G.; Hanson, J. A stunting syndrome of Napier grass in Ethiopia is associated with a 16SrIII Group phytoplasma. New Dis. Rep. 2006, 10, 2006–2019. [Google Scholar] [CrossRef]
  120. Jones, P.; Arocha, Y.; Zerfy, T.; Proud, J.; Abebe, G.; Hanson, J. A stunting syndrome of Napier grass in Ethiopia is associated with a 16SrIII group phytoplasma. Plant Pathol. 2007, 56, 345. [Google Scholar] [CrossRef]
  121. Asudi, G.O.; Van den Berg, J.; Midega, C.A.; Schneider, B.; Seemüller, E.; Pickett, J.A.; Khan, Z.R. Detection, identification, and significance of Phytoplasmas in Wild Grasses in East Africa. Plant Dis. 2016, 100, 108–115. [Google Scholar] [CrossRef]
  122. Marcone, C. Movement of Phytoplasmas and the Development of Diseases in the Plant; CAB International: Wallingford, UK, 2010. [Google Scholar]
  123. Sharon, R.; Soroker, V.; Wesley, S.D.; Zahavi, T.; Harari, A.; Weintraub, P.G. Vitex agnus-castus is a preferred host plant for Hyalesthes obsoletus. J. Chem. Ecol. 2005, 31, 1051–1063. [Google Scholar] [CrossRef] [PubMed]
  124. Lee, I.-M.; Davis, R.E.; Gundersen-Rindal, D.E. Phytoplasma: Phytopathogenic Mollicutes. Annu. Rev. Microbiol. 2000, 54, 221–255. [Google Scholar] [CrossRef] [PubMed]
  125. Weintraub, P.G.; Beanland, L. Insect vectors of phytoplasmas. Annu. Rev. Entomol. 2006, 51, 91–111. [Google Scholar] [CrossRef] [PubMed]
  126. Obura, E.; Midega, C.A.; Masiga, D.; Pickett, J.A.; Hassan, M.; Koji, S.; Khan, Z.R. Recilia banda Kramer (Hemiptera: Cicadellidae), a vector of Napier stunt phytoplasma in Kenya. Naturwissenschaften 2009, 96, 1169–1176. [Google Scholar] [CrossRef] [PubMed]
  127. Arocha, Y.; Zerfy, T.; Abebe, G.; Proud, J.; Hanson, J.; Wilson, M.; Jones, P.; Lucas, J. Identification of potential vectors and alternative plant hosts for the phytoplasma associated with Napier grass stunt disease in Ethiopia. J. Phytopathol. 2009, 157, 126–132. [Google Scholar] [CrossRef]
  128. Lee, I.-M.; Martini, M.; Bottner, K.; Dane, R.; Black, M.; Troxclair, N. Ecological implications from a molecular analysis of phytoplasmas involved in an aster yellows epidemic in various crops in Texas. Phytopathology 2003, 93, 1368–1377. [Google Scholar] [CrossRef] [PubMed]
  129. International Centre of Insect Physiology and Ecology (ICIPE). Solving Napier Stunt Disease to Save the Smallholder Dairy Sector in East Africa—A Success Story; ICIPE: Nairobi, Kenya, 2014; Available online: http://www.push-pull.net/napier_stunt_brochure.pdf (accessed on 25 July 2016).
  130. Mulaa, M.; Awalla, B.; Hanson, J.; Proud, J.; Cherunya, A.; Wanyama, J.; Lusweti, C.; Muyekho, F. Stunting disease incidence and impact on Napier grass (Pennisetum purpureum Schumach) in western Kenya. In 12th Biennial Kenya Agricultural Research Institute (KARI) Conference: Transforming Agriculture for Improved Livelihoods through Agricultural Product Value Chains; Wasilwa, L.A., Ed.; Kenya Agricultural Research Institute: Nairobi, Kenya, 2010; pp. 936–943. [Google Scholar]
  131. Asudi, G.O.; van den Berg, J.; Midega, C.A.; Pittchar, J.; Pickett, J.A.; Khan, Z.R. Napier grass stunt disease in East Africa: Farmers’ perspectives on disease management. Crop Prot. 2015, 71, 116–124. [Google Scholar] [CrossRef]
  132. Kabirizi, J.; Nielsen, S.; Nicolaisen, M.; Byenkya, S.; Alacai, T. Napier stunt disease in Uganda: Farmers’ perceptions and impact on fodder production. In Proceedings of the 8th African Crop Science Society Conference Proceedings, El-Minia, Egypt, 27–31 Octber 2007; Ahmed, K.Z., Ed.; Volume 8, pp. 895–897. [Google Scholar]
  133. Khan, Z.R.; Midega, C.A.O.; Nyang’au, I.M.; Murage, A.; Pittchar, J.; Agutu, L.O.; Amudavi, D.M.; Pickett, J.A. Farmers’ knowledge and perceptions of the stunting disease of Napier grass in Western Kenya. Plant Pathol. 2014, 63, 1426–1435. [Google Scholar] [CrossRef]
  134. Faleiro, F.G.; Kannan, B.; Altpeter, F. Regeneration of fertile, hexaploid, interspecific hybrids of Elephant grass and pearl millet following treatment of embryogenic calli with antimitotic agents. Plant Cell Tissue Organ Cult. (PCTOC) 2016, 124, 57–67. [Google Scholar] [CrossRef]
  135. Sastry, K.S.; Zitter, T.A. Management of virus and viroid diseases of crops in the tropics. In Plant Virus and Viroid Diseases in the Tropics, volume 2: Epidemiology and management; Springer Netherlands: Dordrecht, The Netherlands, 2014; pp. 149–480. [Google Scholar]
  136. Buxton, D.R.; Redfearn, D.D. Plant limitations to fiber digestion and utilization. J. Nutr. 1997, 127, 814S–818S. [Google Scholar] [PubMed]
  137. Jung, H.; Allen, M. Characteristics of plant cell walls affecting intake and digestibility of forages by ruminants. J. Anima. Sci. 1995, 73, 2774–2790. [Google Scholar] [CrossRef]
  138. Berg, J.M.; Tymoczko, J.L.; Stryer, L. Biochemistry, 5th ed.; W H Freeman: New York, NY, USA, 2002. [Google Scholar]
  139. Bhatt, N.; Gupta, P.; Naithani, S. Preparation of cellulose sulfate from α-cellulose isolated from Lantana camara by the direct esterification method. J. Appl. Polym. Sci. 2008, 108, 2895–2901. [Google Scholar] [CrossRef]
  140. Klemm, D.; Heublein, B.; Fink, H.P.; Bohn, A. Cellulose: Fascinating biopolymer and sustainable raw material. Angew. Chem. Int. Ed. 2005, 44, 3358–3393. [Google Scholar] [CrossRef] [PubMed]
  141. Casler, M.D.; Vogel, K.P. Accomplishments and impact from breeding for increased forage nutritional value. Crop Sci. 1999, 39, 12–20. [Google Scholar] [CrossRef]
  142. Sattler, S.E.; Funnell-Harris, D.L.; Pedersen, J.F. Brown midrib mutations and their importance to the utilization of Maize, Sorghum, and Pearl millet lignocellulosic tissues. Plant Sci. 2010, 178, 229–238. [Google Scholar] [CrossRef]
  143. Guo, D.; Chen, F.; Wheeler, J.; Winder, J.; Selman, S.; Peterson, M.; Dixon, R.A. Improvement of in-rumen digestibility of alfalfa forage by genetic manipulation of lignin O-methyltransferases. Transgenic Res. 2001, 10, 457–464. [Google Scholar] [CrossRef] [PubMed]
  144. Hatfield, R.D.; Rancour, D.M.; Marita, J.M. Grass Cell Walls: A story of cross-Linking. Front. Plant Sci. 2017, 7, 2056. [Google Scholar] [CrossRef] [PubMed]
  145. Thébaud, G.; Yvon, M.; Alary, R.; Sauvion, N.; Labonne, G. Efficient transmission of ‘Candidatus phytoplasma Prunorum’ is delayed by eight months due to a long latency in its host-alternating vector. Phytopathology 2009, 99, 265–273. [Google Scholar] [CrossRef] [PubMed]
  146. Mih, A.M.; Hanson, J. Identification of potyviruses infecting forage grasses in Ethiopia. J. Cameroon Acad. Sci. 2004, 4, 205–210. [Google Scholar]
  147. Tiley, G.E.D. Elephant Grass. Kawanda Technical Communication No.23; Kawanda Research Station: Kawanda, Unganda, 1969. [Google Scholar]
  148. Mudavadi, P.O.; Otieno, K.; Wanambacha, J.W.; Odenya, J.O.; Odendo, M.; Njaro, O.K. Smallholder Dairy Production and Marketing in Western Kenya: A Review of Literature; ILRI: Nairobi, Kenya, 2001. [Google Scholar]
Figure 1. Regional distribution of Napier grass around the world (reproduced from [13]).
Figure 1. Regional distribution of Napier grass around the world (reproduced from [13]).
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Figure 2. Partial view of the Napier grass field genebank in Debre Zeit (Ethiopia).
Figure 2. Partial view of the Napier grass field genebank in Debre Zeit (Ethiopia).
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Table 1. Napier grass distribution and accessions in various genebanks around the world.
Table 1. Napier grass distribution and accessions in various genebanks around the world.
Native to *:Number of Accessions at **:
ILRIICRISATCIATEMBRAPA 1USDA GRIN 2RBG 3Total ***
Tanzania69 15
Uganda 1 1
Ethiopia1 12 c 13
Malawi1 214
Mozambique2 2
Zimbabwe115 8 24
Côte d’Ivoire 1 1
Nigeria1 135
Cameroon 81 9
Sub-total22221025474
Collected from
Australia 4 4
Brazil8 397 54
Burkina Faso 11
Burundi1 1
Central African R. 7 29
China 1 1
Colombia1 5 6
Costa Rica1 11 3
Cuba2 4 6
DRC (Zaire) 4 4
Ecuador 11
India28 32 15
Mexico 2 2
Namibia1 1
Panama 1 1
South Africa 12 12
Sudan 2 2
Swaziland6 3 9
USA16 a 16 23
Unknown14 b 22944 90
Sub-total5217283864244
Total74393831118318
a Breeding lines; b Includes 2 cultivars ‘Mott’ (=PI517947) and ‘Kizizi’. ILRI14983 may = PI667853; c 11 duplicates of ILRI accessions, not actually from Ethiopia, and none of the 12 are available; * Native distribution taken from [13]; ** Number of accessions from the forage registry, except for Brazil, United States Department of Agriculture (USDA) Germplasm Resources Information Network (GRIN), ICRISAT and RBG (Genesys [37]); *** Some of the accessions listed here are in fact duplicated between the collections (for example 20 of the ILRI collection are part of the Brazilian collection); 1 Brazilian Agricultural Research Corporation (EMBRAPA, Empresa Brasileira de Pesquisa Agropecuária); 2 Most USDA accessions not available; 3 Millennium Seedbank, Royal Botanic Gardens (RBG), Wakehurst Place, UK. ILRI: International Livestock Research Institute; CIAT: International Center for Tropical Agriculture.
Table 2. Yield and nutritional qualities of Napier grass accessions across different studies.
Table 2. Yield and nutritional qualities of Napier grass accessions across different studies.
CountryDM (t/ha/year)CP (%)NDF (%)ADF (%)No. of Accessions EvaluatedRef.
Bangladesh14.9–16.510.3–11.4NA29.9–45.94[69]
Brazil14.9–78NANANA85[26]
Ethiopia4.6–20.57.5–15.752–64.628.8–36.69[70]
Kenya12.1–19NANANA8[71]
Malaysia43.7–65.910–1260–7035–409[64]
MexicoNA9.2–9.965.2–69.742.2–44.73[72]
Thailand27.1–58.4NANANA8[27]
USA25.3–28.212.42–15.6862.7–66.837.2–39.62[57]
Zimbabwe90.25.3556.839.22[73]
DM: dry matter production; CP: crude protein; NDF: neutral detergent fibre; ADF: acid detergent fibre; NA: ‘Not available’ is given when that particular component was not measured in that study.
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