Sorghum: Improvement of Abiotic Stress Tolerance

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36 Sorghum: Improvement of Abiotic Stress Tolerance Monika Dalal, Karthikeyan Mayandi, and Viswanathan Chinnusamy Sorghum, the fifth most important cereal crop in the world, provides food, feed, fodder, fiber, and fuel. It is the second cereal crop and first C4 photosynthetic plant for which whole genome is sequenced. The importance of this crop will increase tremendously in future due to its better adaptability to abiotic stresses, which are expected to increase because of global climate change and diminishing fresh water supplies, coupled with increasing demand for food and bioenergy. The yield potential of sorghum is evident from the fact that production of sorghum has been maintained despite a steady decline in its area of cultivation over the past three decades. In fact, the true yield potential of sorghum has rarely been realized, as it is mainly grown in areas of low rainfall and resource-poor agronomic conditions. Owing to its ability to survive in water-limiting conditions, sorghum has majorly been studied for its drought resistance mechanism. The drought response in sorghum differs depending on the occurrence of stress during preflowering and postflowering. Postflowering response is associated with stay-green trait. Quantitative trait loci (QTL) for pre- and postflowering have been identified. However, the underlying genes that confer drought tolerance in sorghum have not been mapped. Moreover, other morphophysiological traits such as epicuticular wax content, osmotic adjustment, membrane stability, water use efficiency, or drought-related root traits that have been postulated to play a significant role in drought resistance in sorghum have been largely unexplored. Molecular genetic and physiological dissection of these traits will be of immense significance. Aluminum toxicity is a major problem in acidic soils. QTL and gene mapping approach led to the mapping of a Multidrug and Toxic Compound Extrusion (MATE) gene in sorghum. Later MATE family genes were identified as potential candidates that underlie aluminum tolerance QTL in maize. Since the rice, sorghum, and Brachypodium distachyon genome sequences are already available, and with impending maize genome sequence, there is an immense opportunity for comparative genetics and genomics to dissect abiotic stress tolerance mechanisms in cereals. This will accelerate the gene discovery among the cereal crops and will help improve other plant species as well. Thus, sorghum with its smaller genome, wide germplasm resource, well-studied genetics, C4 photosynthesis, and adaptability to

Improving Crop Resistance to Abiotic Stress, First Edition. Edited by Narendra Tuteja, Sarvajeet Singh Gill, Antonio F. Tiburcio, and Renu Tuteja Ó 2012 Wiley-VCH Verlag GmbH & Co. KGaA. Published 2012 by Wiley-VCH Verlag GmbH & Co. KGaA.

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harsh environments represents optimal amalgamation for omics approaches to decipher drought resistance mechanism.

36.1 Introduction

Sorghum (Sorghum bicolor (L.) Moench) is the fifth most important cereal crop in the world after wheat, rice, maize, and barley. Known for its ability to survive harsh environments with prolonged drought period, sorghum is grown in arid and semiarid areas of the world. It is a staple food in parts of Africa and Asia and a major feed crop in the United States, Mexico, Australia, and South Africa. It has extensive variability such as grain sorghum, forage sorghum, and sweet stalk sorghum that provides food, feed, fodder, fiber, and fuel. Sorghum is produced by about 104 countries in the world. In 2009, Sorghum was grown on 43.74 million ha of land worldwide with a yield of 14 198 Hg ha1 (http://Faostat.fao.org/; December 20, 2009). Average area under sorghum cultivation in Asia has declined from 26.19 million ha in the 1960s to 10.58 million ha in 2008. However, yield increased from 6935 Hg ha1 in the 1960s to 10 377 Hg ha1 in the late 2000s (http://Faostat.fao.org/ ; December 22, 2009). The yield potential of sorghum is evident from the fact that production of sorghum has been maintained despite a steady decline in its area of cultivation. In fact, the true yield potential of sorghum has rarely been realized, as it is grown mainly in areas of low rainfall and resource-poor agronomic conditions. Its ability to yield under such agronomic and adverse climate conditions is a proof of concept that sorghum is the crop of the future. In the changing global scenario, the world population is expected to rise from present 6.6 billion to 8.7–11.3 billion in 2050 [1]. The global demand for cereal production will also increase by 60% [2]. This task is challenging as the yield potential of cereal crops has reached its plateau, and there is reduction in cultivable land and availability of fresh water for irrigation. These problems are further exacerbated by global climate change-associated increase in the frequency of heat stress, droughts, and floods that negatively affect crop yields [3]. Ability of crops to adapt and yield under such harsh environment will be crucial in determining the sustainability of food production in days to come. This will require a combination of adaptive agricultural strategy that includes new management and agronomic practices and further improvement in the genetic potential of productivity and abiotic stress resistance of crops. This also implies that lessons need be learned from plants that show high adaptability and tolerance to abiotic stresses. Sorghum belonging to genus Poaceae and subfamily Panicoideae shares the tribe Andropogoneae with other major crops such as maize, sugarcane, and millets. The Andropogoneae species are native to tropical and subtropical climates, and are characterized by C4 photosynthesis, high rates of carbon fixation, high water and nutrient use efficiency, high biomass productivity, adaptation to diverse

36.2 Abiotic Stress Tolerance

environments, and have both annual and perennial life cycles. However, many of these species are polyploids with large complex genomes. Sorghum, besides having all the advantageous characteristics, has a diploid genome that is already sequenced [4]. Moreover, with its well-studied genetics, wide germplasm resource, lower level of gene duplication compared to other tropical cereals, and amicability for genetic transformation, sorghum can be an ideal system especially for grasses and plant genomics research as a whole.


Abiotic stresses limit the growth and productivity of crop plants to variable degrees depending on the time of onset, duration, and intensity of stress. It has been estimated that crops attain only about 25% of their potential yield because of the detrimental effects of environmental stresses [5]. During the second half of twentieth century, increase in crop productivity by plant breeding efforts kept in pace with the food demand of the increasing world population. This was achieved mainly by breeding programs aimed at increasing yield potential and disease resistance. However, the progress in breeding for abiotic stresses has been very slow as, first, the mechanism of abiotic stress tolerance was poorly understood and, second, the breeding in the past 50 years was more yield oriented [6]. Since the relative rate of yield increase for major crops such as rice and wheat is declining [7], there is a need to adopt and intensify the physiological trait-based molecular breeding approach for breeding abiotic stress-tolerant crops [8]. Physiological breeding, also known as analytical breeding, refers to selection for secondary traits that are associated with higher yield under optimal and/or abiotic stress environments [6]. On the basis of the physiological traits that contribute to yield in soil moisture-deficit environments, a general model for drought adaptation of wheat was proposed [8]. The model describes four main groups of traits relating to (i) preanthesis growth, rapid ground cover to shade the soil to prevent evaporation, and high assimilation capacity between jointing and lag phase, to permit accumulation of stem carbohydrates; (ii) high rooting depth and/or intensity to access water that would be expressed by a relatively cool canopy or favorable expression of water relation traits; (iii) water use efficiency (WUE), photosynthesis associated with refixation of respiratory CO2; and (iv) photoprotection including energy dissipation, antioxidant systems, and anatomic traits such as leaf wax [8]. Though these traits have been proposed for wheat per se, it may apply to any crop improvement program aimed at drought tolerance. Yet not all the crops will have the best amalgamation of these traits. Sorghum with its stay-green trait, deep rooting system, better WUE, C4 photosynthesis, and high epicuticular wax (EW) represents one good system to study physiological traits related to drought tolerance. However, genetic and molecular analyses of these traits are in its infancy. The chapter describes the progress in abiotic stress tolerance research and prospects for genetic improvement of sorghum. It includes the physiological trait-based studies conducted in

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sorghum in relation to drought, followed by cold, salt, and aluminum tolerance and the genetic and genomic resources for further progress in crop improvement in sorghum. 36.2.1 Drought Tolerance

Drought stress is one of the most critical stress affecting plants. Drought can be defined in multiple ways, be it meteorological, hydrological, or socioeconomical context. When drought is defined in relation to crops or agriculture, it refers to shortage of water in the root zone that reduces yield [9]. When a genotype yields higher than another genotype under severe drought, it is ranked relatively more drought tolerant. Plants deal with stress in three different ways, namely, escape, dehydration avoidance, and dehydration tolerance. Drought escape is defined as the ability of a plant to complete its life cycle before severe soil and plant water deficit develops. Escape mechanism involves rapid phenological development (early flowering and early maturity) and developmental plasticity (variation in duration of growth period depending on the extent of water deficit). Dehydration avoidance is defined as the ability of plants to sustain high plant water status or cellular hydration under drought conditions. Crop plants avoid dehydration by enhanced capture of soil moisture by efficient root system and osmotic adjustment (OA), by limited crop water loss from transpiration and other nonstomatal pathways such as through the plant cuticle, reduced absorption of radiation by radiation reflection, and leaf rolling/folding or drying. Dehydration tolerance is defined as the capacity to sustain or conserve plant function even in relatively low tissue water potential. Cellular water deficit stress tolerance in plants depends on modification of metabolism, production of organic compatible solutes (proline, sugars, polyols, betaine, etc.), and expression of genes involved in membrane integrity, cellular homeostasis (ionic-, osmotic-, and metabolic homeostasis), stress damage control, and repair. Traits associated with avoidance and tolerance can be constitutive (intrinsic traits that express constitutively) or adaptive (traits that express in response to stress). Depending on the occurrence of stress at vegetative or reproductive stage, sorghum exhibits preflowering and postflowering stress response, respectively. These two responses are apparently controlled by different genetic mechanisms [10]. Preflowering stress affects biomass, panicle size, grain number, and grain yield [11], while postanthesis drought leads to premature leaf and stem senescence, lodging, and reduced seed size [12]. Postanthesis drought also increases susceptibility of plants to biotic stresses such as charcoal rot (Macrophomina phaseolina (Tassi) Goidanich) and fusarium stalk rot (Fusarium moniliforme J. Sheld.) [12]. For preflowering drought tolerance, six distinct genomic regions were identified in sorghum recombinant inbred lines (RILs) derived from the cross between Tx 7078 (preflowering-tolerant, postflowering-susceptible) and B35 (preflowering-susceptible, postflowering-tolerant) genotypes [13]. These loci accounted for approximately 40% of the total phenotypic variation in yield under preflowering drought and were


detectable across a range of environments. Kebede et al. [14] identified four quantitative trait loci (QTL) associated with preflowering drought tolerance in sorghum from RILs derived from the cross, SC 56 Tx 7000. The major QTL influencing preflowering drought stress tolerance accounted for 15 and 37.7% of the phenotypic variance under two different environments, suggesting a strong G E interaction at this loci. 36.2.1.1 Stay Green Postflowering drought response is associated with stay-green trait in sorghum. Stay green is basically retention of green leaf area at maturity (GLAM). Maintenance of stay-green trait during grain-filling stage under soil moisture-deficit stress condition constitutes an important component of drought tolerance [15]. The stay-green phenotype has been classified into five types [16]. In type A stay green, the initiation of senescence is delayed, but proceeds at the same rate as the wild type. Type B stay green initiates senescence at the same time as the wild type, but senescence proceeds at slower rate. The above two types are regarded as functional stay green as retention of greenness is associated with extended photosynthetic activity during grain filling. On the other hand, type C or cosmetic stay green retains chlorophyll almost indefinitely; however, the photosynthetic rate declines. Type D stay green is the greenness retained after the leaf death by abrupt freezing or drying. Finally, type E stay green contains higher chlorophyll content to begin with, but follows senescence at normal time and rate. Functional stay green can be of immense importance as it has been correlated with higher grain filling and increased yield under postanthesis drought [12]. Moreover, there is no yield penalty associated with stay green under nondrought conditions [12]. Stay green has also been associated with higher leaf nitrogen content [17, 18], reduced lodging [12], lower susceptibility to charcoal rot [19], and higher levels of stem carbohydrates both during and after grain filling [12]. Thus, stay green contributes to various aspects of crop improvement and hence is a valuable trait for crops like sorghum where primary harvest can be grain, forage, juice, and/or fodder. In sorghum, different stay-green sources are available that include B35 (BTx 642), SC 56, E36-1, and KS19 [14, 20–22]. In breeding, B 35 and KS 19 are the two main sources used for stay green [20]. These two genotypes represent two different types of functional stay green: B 35-derived lines have a greater leaf area at flowering and a normal rate of leaf senescence, whereas KS 19-derived lines have a smaller leaf area at flowering and a slower rate of leaf senescence [12]. Although the ability of leaves to delay senescence has a genetic basis in sorghum, the expression of the character is strongly influenced by environmental factors [23]. The selection for trait depends upon the occurrence of a prolonged period of drought stress during the grain-filling period to accelerate normal leaf senescence. Genetic studies also showed that staygreen trait is governed by genes that act at varied levels of dominance or additive effects. For instance, the inheritance of the onset of senescence was additive, but a slow senescence rate was found to be dominant over a fast rate [23, 24]. Furthermore, the three components of stay-green trait, namely, green leaf area at flowering, time of

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Table 36.1 Summary of studies related to identification of QTL for stay-green trait in sorghum.

Stay-green parent

Nonstay-green parent

Experimental location

Population

Markers used

B35

Tx 7078

RIL

B35 B35 B35

Tx 430 Tx 7000 Tx 7000

Mexico USA USA USA USA

RIL RIL RIL

QL41

QL39

Australia

RIL

SC56 E36-1 E36-1

Tx 7000 IS9830 N13

USA India

RIL RIL

RAPD RFLP RFLP RFLP RAPD RFLP SSR RFLP SSR RFLP AFLP RAPD RFLPSSR

Reference

[25] [26] [27] [28]

[29] [14] [21]

onset of senescence, and subsequent rate of senescence also appear to be inherited independently [12, 23]. Several studies have mapped QTL contributing to the stay-green trait (Table 36.1). Most of these studies used B35 or derivatives of B35 as the stay-green source [25–29]. These studies led to identification of four major QTL, namely, Stg1, Stg2, Stg3, and Stg4. QTL Stg1 and Stg2 are located on LG-03, Stg3 on LG-02, and Stg4 on LG-05, and account for 20, 30, 16, and 10% of the phenotypic variance, respectively [11, 27]. Among these, Stg2 was found to be the most important QTL, followed by Stg1, Stg3, and Stg4 [27]. Stg2 was consistent in all the environments, in different genetic backgrounds, and explained the highest percentage of phenotypic variation (30%) in three different studies [26–28]. The near-isogenic lines (NILs) derived from the cross between B35 and RTx 7000 were evaluated under drought conditions at postflowering stage for their expression of stay-green phenotype. Physiological analysis of four NILs containing individual QTL, namely, Stg1, Stg2, Stg3, or Stg4, showed that B35 alleles in each of these loci could contribute to the stay-green phenotype. It was found that NILs having the genomic DNA of B35 spanning the region of the Stg2 were performing better than NILs having other QTL. NILs with Stg2 were showing higher GLAM and SPAD values and lesser rate of leaf senescence over others [30]. Stay-green expression is affected by the degree of stress during grain filling, and other factors such as flowering time and sink strength. It can be better manipulated using a marker-assisted breeding approach [31]. Therefore, efforts have also been initiated to transfer this trait through marker-assisted backcrossing (MABC) into elite cultivars and study their expression in different background [22, 31]. However, precision of marker-assisted breeding depends on how tightly the markers are linked to the genes or QTLs involved. Therefore, fine mapping of stay-green QTL still remains a prerequisite. Fine mapping of QTL can be achieved by increasing marker

36.2 Abiotic Stress Tolerance Table 36.2 List of selected genes in the corresponding Stg2 QTL region of BTx623 (http://www. phytozome.net).

Marker name

Position in chromosome 3 (bases)

Candidate genes

Predicted function

CSU58 RZ323

54 878 005 55 631 111

— Sb03g027940

— Similar to membrane-associated salt-inducible protein-like Similar to protein phosphatase 2C Similar to proline transport protein 2-like Similar to probable indole-3-acetic acid-amido synthetase GH3.5 Similar to heat shock factor RHSF13 Similar to carbonic anhydrase, chloroplast precursor Similar to malate dehydrogenase Similar to leaf senescence protein-like Similar to leaf senescence protein-like Similar to pyruvate kinase — —

Sb03g028070 Sb03g028210 Sb03g028240

UMC63

57 218 551

Xtxp002

57 539 612

WG889 Xtxp 114

58 956 759 60 794 047

Sb03g028470 Sb03g029190 Sb03g029570 Sb03g029740 Sb03g029760 Sb03g030110 — —

density within the chromosomal region of interest and/or increasing the number of segregating population for which phenotypic information can be obtained. With available genome sequence and genomics tools, increasing the marker density appears to be more straightforward approach. Many sequence-based markers (namely, SNPs) can be made. That will further help in fine-mapping the QTL. Simultaneously; integrated genomic approaches can be used for deciphering the staygreen trait in sorghum. For instance, location of Stg2 on available physical map of sorghum between markers RZ323 and WG889 [27, 28] in third chromosome of sorghum consists of more than 200 genes (Table 36.2). Some of these genes are predicted to function in important physiological processes such as photosynthesis, leaf senescence, and abiotic stress response (Table 36.2) that may contribute to the stay-green phenotype. Expression profile of these putative candidate genes can be correlated with the stay-green trait. This will narrow down the search for genes responsible for the trait. On the basis of in silico comparative genome analysis, a few markers have already been developed in Stg QTL of sorghum [32]. Moreover, QTL for stay-green trait in wheat and rice have also been identified [33, 34]. Hence, comparative studies can be used to expedite the process of identifying genes responsible for stay green not only in sorghum but also in other cereals. In addition to functional stay-green genotypes, stay-green mutants are also reported in many different species including rice [35], soybean [36], tomato [37], Phaseolus vulgaris [38], pepper [39], Festuca pratensis [40], and so on. The impetus on

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identifying gene responsible for stay-green phenotype in these mutants started with the finding of a single recessive nuclear gene, sgr (t), from a rice mutant [35]. Later, two research groups reported that sgr is a senescence-associated gene encoding a novel chloroplast protein. It was shown that the stay greenness of the sgr mutant was associated with a failure in the destabilization of the lightharvesting chlorophyll binding protein (LHCP) complexes of the thylakoid membranes, which is a prerequisite event for the degradation of chlorophyll and LHCPs during senescence [41, 42]. This was followed by identification of orthologous genes responsible for the stay-green character in other mutants that include Mendels green cotyledon mutant in pea, green-flesh (gf ) and chlorophyll retainer (cl) mutations of tomato and pepper, respectively [43, 44]. Though sgr has been associated with type C or cosmetic stay-green phenotype, yet it gives an insight into the mechanism of dismantling of photosynthetic chlorophyll–apoprotein complexes. It also implies that if found orthologous in nature, identification of functional stay-green genes in one species will speed up their elucidation in other cereal crops as well. 36.2.1.2 Epicuticular Wax Epicuticular wax forms an outer visible glaucous coating on many crop plants called as waxy bloom or bloom. The accumulation of wax varies greatly depending on species, organ, stage of development, and environmental conditions. EW is highly diverse in composition and structure. Its hydrophobic composition and distribution on many aerial organs of plants has been considered a potentially useful trait and has been associated with resistance to many diverse environmental stresses including drought, insect, and disease resistance [45–47]. Sorghum is distinct from other cereal crops due to its ability to produce profuse amount of epicuticular wax (EW or bloom) that is deposited on abaxial leaf blade and sheath and culms, especially during preflowering and at maturity stages. The wax composition of sorghum leaf sheath shows highest (96%) level of free fatty acids with chain length varying from 16 to 33 carbons, of which C28 and C30 represent 78 and 20% of the constituents, respectively [48]. Moreover, sorghum as a species has been reported to produce one of the highest amounts of leaf EW among cereal crops. Burow et al. [49] reported that on a per unit leaf area basis, sorghum produces an average of 1.9 mg dm1, while the reported value for rice (Oryza sativa L.) is 0.05 mg dm1 [50]. Similarly, on per unit weight basis, sorghum produces approximately 52.7 mg g1 wax, which is 3-fold higher than that of maize (17.0 mg g1) [51] and 1.5–2-fold higher than that of durum wheat (25–35.7 mg g1) [52]. The most common plant waxes are very long-chain aliphatic molecules, of mainly 16–34 carbons in length, that occur as free fatty acids, aldehydes, primary alcohols, alkanes, and esters [53]. However, there exists a difference in the biosynthetic pathway depending on the carbon length. Synthesis of fatty acids with 16 carbons or less, acyl chains is activated by a soluble plastidic acyl carrier protein (ACP) and elongated by a fatty acid synthase (FAS) complex that condenses acetyl groups from malonyl-ACP to growing acyl-ACP chains [54]. Acyl-CoA of 16C or 18C chain length is exported from plastid into endosplasmic reticulum for long-chain acyl-CoA


synthesis. Acyl chains that serve as direct wax precursors are activated by coenzyme A (CoA) and elongated by membrane-associated enzyme complexes called fatty acid elongases [55]. Elongases use malonyl-CoA as the two carbon donors instead of malonyl-ACP. Once synthesized, the very long acyl-CoA chains are catalyzed by other enzymatic reactions and form free acids, esters, aldehydes, and alkanes that constitute the EW [48]. Thus, being involved in early steps in the wax metabolic pathway, acyl-CoA elongases may serve as rate limiting and highly regulated reactions, and hence plays a pivotal role in overall plant cuticular wax biosynthesis [56]. Genetic analysis of Arabidopsis mutant led to the identification of two enzymes of FAE complex, namely, ECERIFERUM6 (CER6, b-ketoacyl-CoA synthase) and CER10 (enoyl-CoA reductase). CER4, fatty acyl-CoA reductase, synthesizes primary alcohol from very long-chain fatty acids. The WSD1, wax synthase/fatty acyl-CoA: fatty alcohol acyltransferase synthesizes wax esters. Most of this information on biosynthetic pathway of plant EW has been built on genetic analysis of Arabidopsis mutants [57]. Though a few genes have now been isolated and characterized in rice and maize [47, 58], none of the genes has been characterized at molecular level in sorghum. However, there have been some detailed genetic studies on chemically induced mutants in sorghum [48, 59, 60]. These mutants were designated bloomless (bm), which completely lacked visible waxes on sheath surfaces and sparse-bloom (h), those with reduced visible sheath waxes [59]. bm and h wax mutants produced significantly low wax load compared to wild type. It was found that all the 12 bm mutants had a reduction in the amount of C28 and C30 fatty acids that resulted in the reduction of total wax load relative to wild type [48]. On the basis of composition analysis, it was suggested that these sorghum mutants may have lesions that affect either C26 acyl-CoA elongation or acyl-CoA thioesterases. The molecular identity of these mutant loci still remains unknown. These wax mutants can be exploited for elucidating genes involved in the biosynthesis of the very long-chain fatty acids. Recently, a mapping population developed from a cross between BTx623 (wild type with profuse wax) and KFS2021 (a mutant with greatly reduced wax) was used for molecular mapping and characterization of a locus associated with production of profuse wax BLOOM-CUTICLE (BLMC) in sorghum [61]. The locus mapped to the terminal end of sorghum chromosome 10 was delimited to as small as 0.7 cM region. The analysis of putative genes in the BLMC region revealed the presence of an acyl CoA oxidase (a gene involved in lipid and wax biosynthesis) and seven other putative transcripts, among others [61]. Next to stomata, water loss from plants occurs through its cuticle. High cuticular wax minimizes nonstomatal water loss from the plants. The bloomless F2 progenies of the cross showed a significant negative correlation between leaf epicuticular wax load with epidermal permeability and night-time conductance, suggesting that epicuticular wax may enhance water use efficiency of sorghum by regulating night-time water loss [49]. In addition to disrupting the epicuticular wax production, blmc mutation also reduced culm and leaf cuticle, and increased plant death rate in the field at anthesis [61]. This phenotype was similar to bm22 mutant reported by Jenks et al. [60]. The bm 22 mutant reduced both epicuticular wax and cuticle deposition that in turn was associated with increased epidermal conductance to water vapor and increased susceptibility to the

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funga1 pathogen Exserohilum turcicum [60]. Thus, there seems to be a link between the pathways of epicuticular wax synthesis and cuticle formation. Cutin synthetic enzymes use C16 and C18 acyl-CoA pools as precursors, potentially the same precursors used in wax synthesis. As cuticle is involved in several different functions including inhibition of uncontrolled permeation of water, solutes, and gases, and protection from phytopathogens and so on, identification and characterization of gene affecting both cuticle and epicuticular wax can be of significant importance for both biotic and abiotic stress tolerance of sorghum. 36.2.1.3 Osmotic Adjustment Osmotic adjustment and antioxidant capacity are the two traits that have been associated with drought tolerance mechanisms. OA refers to the lowering of osmotic potential due to the net accumulation of compatible solutes in response to water deficits. These compatible solutes may be various amino acids (e.g., proline), sugars (e.g., sucrose and fructans), polyols (e.g., mannitol and pinitol), quaternary amines (e. g., glycine betaine), ions (e.g., potassium), and organic acids (e.g., malate and citrate) [62]. There is a wide variation in OA in crop plants, and the solutes accumulated also differ by plant species [63]. Osmotic adjustment is an inherited trait and has been associated with sustained yield in water-limiting conditions in many crop plants [15]. In sorghum, two independent major genes (OA1 and OA2), with some minor effects, have been reported to control the inheritance of OA in sorghum [64]. Glycine-betaine (GB) is an important osmoprotectant and its role in abiotic stress tolerance is demonstrated in several plant species. GB stabilizes the quaternary structure of proteins, stabilizes highly ordered state of membranes, and reduces lipid peroxidation under stress [65]. Betaine aldehyde dehydrogenase and choline monooxygenase catalyze the synthesis of GB in a two-step oxidation of choline via the intermediate betaine aldehyde. In sorghum, expression of BADH1 and BADH15, encoding betaine aldehyde dehydrogenase, was found to be induced by water deficit and their induced expression coincided with GB accumulation [66]. Among cereal crops, maize and sorghum synthesize GB, while rice does not [67]. Moreover within maize and sorghum, there are certain genotypes that do not accumulate GB [68, 69]. To study the GB accumulation in sorghum, near-isogenic lines (NILs) that differ in their ability to accumulate GB were analyzed [69]. Labeling studies in sorghum demonstrated that the deficiency in GB accumulation was at the choline oxidation step [69]. However, a recent study suggests that low GB accumulation may not be due to the absence of choline monooxygenase; rather, it may be due to the nonavailability of substrate or lack of choline transporter [70]. Thus, mechanism of GB synthesis and accumulation in these lines of sorghum and maize still remains an enigma. Besides GB, other solutes such as proline, K þ , sugars, Cl, and P, were also reported to contribute to osmotic adjustment in sorghum [66, 71]. Since phenotyping for OA trait is difficult due to methodological constrains of OA evaluation, it will be important to map OA QTL for different solutes, which can be transferred by markerassisted selection (MAS) or transgenic approach to incorporate this trait for improvement of OA and osmoprotection in sorghum.


36.2.2 Cold Tolerance

Sorghum being native to tropical and subtropical regions of Africa [72] is well adapted to warm growing conditions. Cool temperatures during the early growing season are, therefore, a major limitation to growing sorghum in temperate areas. The development of sorghum cultivars with improved early-season cold tolerance would allow expansion of sorghum to these more northerly latitudes and would also allow for earlier planting in areas where it is being grown [73]. Moreover, improved emergence and early-season vigor would enable better stand establishment and protect against loss of seedlings during unexpected cold periods that are likely to become frequent due to climate change scenario. Though most of the available sorghum germplasm is of tropical origin, some of the sorghum landraces from temperate regions of China, referred to as kaoliang, exhibit higher seedling emergence and greater seedling vigor under cold conditions than most sorghum cultivars [74–76]. However, these races lack desirable agronomic characteristics. Hence, efforts are being made to introgress desirable genes from Chinese landraces into elite lines by marker-assisted selection. A population developed from a cross between Chinese landrace Shan Qui Red (SQR, cold tolerant) and SRN39 (cold sensitive) was employed for QTL analysis of early-season cold performance in sorghum [77]. Two QTL, one on linkage group SBI-03 and the second on group SBI-07, for germination under cold and optimal temperatures were identified. Another QTL located on linkage group SBI-01 showed strong association with seedling emergence and seedling vigor scores under early and late field planting. The three QTL were validated across two populations [78]. Hence, these can be useful for marker-assisted breeding to improve early-season performance in sorghum. 36.2.3 Salt Tolerance

Salinity is one of the major abiotic stresses that adversely affect crop productivity and quality [5]. Saline soil is characterized by toxic levels of chlorides and sulphates of sodium. The problem of soil salinity exists in both irrigated and dry areas. In irrigated areas, poor quality of water or improper drainage or entry of seawater in coastal areas contributes to salinity. In arid and semiarid regions, it is the high evaporation and insufficient leaching of ions due to inadequate rainfall that leads to high salt accumulation in root zones [79]. Salinity restricts plant growth due to nutritional constrains, ion toxicity, and osmotic stress. Though sorghum has been characterized as moderately tolerant, it is more tolerant than maize [80, 81]. Moreover, its better suitability in arid and semiarid regions also makes it a suitable target for improvement in salt tolerance. The mechanism of salt tolerance has been studied in detail (reviewed in Refs [79, 82]), yet the complex genetic mechanism is a big hurdle to improvement of salt tolerance. In sorghum, diallel analysis, based on relative root length in salt-treated and control plants, showed both additive and dominance effects of NaCl [83]. A large genotypic variation for tolerance to salinity in sorghum has been reported [83–86]; however, no detailed studies have been carried out. Therefore, there is a need to explore this area of stress tolerance in sorghum.

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36.2.4 Aluminum Tolerance

Aluminum (Al) is a light metal that makes up 7% of the Earths crust and is the third most abundant element after oxygen and silicon [87]. Most of this Al occurs in the form of harmless oxides and aluminosilicates with only small amounts present in soluble forms in the rhizosphere. However, under acidic condition of soil (pH < 5), Al is solubilized into the phtotoxic trivalent cation, Al3 þ . Aluminum toxicity primarily affects the root growth resulting in limited absorption of water and mineral nutrients [88], leading to a significant reduction in the quality of the grains on acid soils [89]. Acidic soil accounts for up to 50% of the worlds potentially arable soils [90], of which larger part comes from tropic and subtropic areas of developing countries. A significant variation in Al tolerance is reported within some species [89]. In barley, Al tolerance appears to be monogenic [91], while in rice it is a quantitative trait [92]. Al tolerance is either simply inherited as single dominant gene in some genotypes of wheat or involves action of more than one gene in other genotypes [93–96]. Plants have evolved two physiological mechanisms to resist the effect of Al toxicity in acidic soils: exclusion of Al from the root apex and chelation mechanism. Exclusion mechanism is based on the external detoxification of Al, which protects the root apex against Al penetration. This is achieved by the secretion of organic acids from the root apex to the rhizosphere that modifies the pH and chelates the toxic Al3 þ [97]. Chelation mechanism works on compartmentalization of aluminum ions by specific proteins, short-chain organic acids, phenolic compounds, and tannins that can bind and form complexes with Al3 þ . These complexes are subsequently compartmentalized in the vacuole, thus reducing Al toxicity [98–100]. Among the two mechanisms, Al-activated exudation of organic acid – anions – from root apices is the best documented and characterized plant Al tolerance mechanism [87]. The exudation of organic acid may be species specific, such as malate from Al-tolerant cultivars of wheat [101], citrate from Al-tolerant cultivars of maize [102] and soybean [103], and oxalate from buckwheat [104] and taro [105]. However, some species such as Secale cereale (rye) may show exudation of both malate and citrate [106]. Transport of these organic acids occurs via anionic channels, the opening of which may be activated by Al. The first such transporter ALMT1 (aluminum-activated malate transporter 1), responsible for malate efflux, was identified in wheat [107]. ALMT1 represented a new family of membrane proteins and mapped to chromosome 4DL, corresponding to AltBH, a major aluminum tolerance locus in wheat and other members of the Triticeae tribe [108]. A new thrust came in to the Al tolerance research when Magalhaes et al. [109] reported a single locus, AltSB, which accounted for 80% of the Al tolerance phenotype in sorghum mapping population. Interestingly, the locus AltSB mapped on the sorghum chromosome 3, which is not homologous to the Triticeae group 4 chromosomes. Comparative mapping studies indicated that a major Al tolerance QTL on rice chromosome 1 might be orthologous to AltSB, whereas another QTL on chromosome 3 is likely to correspond to the Triticeae group 4 Al tolerance locus [109]. Therefore, it appeared that in rice that is one of the most Altolerant grasses [92, 110], the quantitative inheritance of Al tolerance may be a result of

36.3 Genetic and Genomics Resources of Sorghum

two major QTL, which act as two independent and distinct major Al tolerance genes in Andropogoneae and Triticeae [109]. As AltSB appeared to be distinct from AltBH, positional cloning of AltSB was taken up that led to the identification of the gene encoding aluminum-activated citrate transporter, a member of the multidrug and toxic compound extrusion (MATE) family from sorghum [111]. Transgenic expression of SbMATE gene conferred Al tolerance in both Arabidopsis and wheat [111]. Simultaneously, in the same year another MATE protein, HvAACT1, an Al-activated citrate transporter that confers Al tolerance to barley, was reported [112]. MATE proteins are members of a large and complex family of transporters; functional members of this family were found first in prokaryotic organisms and later in eukaryotic organisms and are generally involved in the efflux of small organic solutes. Their identification in sorghum and barley subsequently led to the identification of several other plant MATE members that were implicated in citrate transport. These include OsFRDL1 from rice [113], AtMATE from Arabidopsis [114], and ZmMATE1 in maize [115], and a MATE gene implicated in citrate efflux has also been reported from wheat [116]. Though overall studies indicate that Al tolerance in plants is predominantly contributed by orthologous series of at least two major loci, detection of additional QTL or genes in the genomes of maize [117], rice [92], oat [118], and rye [119] indicates that these Al tolerance genes may also play a role in Al tolerance of plants. In sorghum, Al tolerance appears to be a function of both allelic heterogeneity and nonallelic heterogeneity [120]. A wide range of phenotypic variation for Al tolerance was found, which was attributed to multiple alleles of AltSB. Even the two most tolerant sorghum cultivars, SC283 and SC566, which were found to rely on AltSB for their tolerance [109], showed a distinct phenotype, SC566, being significantly more tolerant than SC283 indicating that the SC566 allele is stronger than the SC283 allele [120]. As the correlation between SbMATE expression and Al tolerance in a panel having allelic diversity at the AltSB locus was highly significant [111], it was suggested that these allelic effects in part may be regulatory in nature. Moreover, transgressive segregation was also observed in a highly Al-tolerant breeding line, indicating the role of additive or codominant effects in sorghum Al tolerance [120]. Though identification of these nonorthologous and additive aluminum tolerance genes remains to be explored, the major gene AltSB from sorghum has been instrumental in revealing a new mechanism of aluminum tolerance in plant species. The major gene effect and allelic diversity at the AltSB locus can be exploited for improving Al tolerance of sensitive sorghum genotypes and other species.

36.3 Genetic and Genomics Resources of Sorghum 36.3.1 Germplasm Resources and Genetic Diversity

The plant genetic resources are defined as the Genetic material of plants that is of value as a resource for the present and future generations of people [121]. All

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accessions of a particular crop species are expected to contain essentially the same genes. Differences in agricultural performance between accessions are thought to be due to allelic differences within the same gene set. Thus, genetic diversity in a crop is an important asset for improvement of its adaptive and agronomic traits. Genetic diversity is essential both for evolutionary history and for future evolutionary trajectory of a species. Most of the modern cultivars are having narrow genetic base making them vulnerable to potentially new biotic and abiotic stresses, the best example being the 1970 southern corn leaf blight (Bipolarise maydays) epidemic [122]. With a changing global climate scenario, exploitation and preservation of genetic diversity may become more evident for survival and sustainability of a crop. Sorghum is a highly diverse species. There are three S. bicolor subspecies, cultivated types (ssp. bicolor), wild (ssp. verticilliflorum), and weedy types that are product of hybridization between domesticated and wild sorghums (ssp. drummondii). Furthermore, within ssp. bicolor, there are 5 races (i.e., bicolor, caudatum, durra, guinea, and kafir) and 10 intermediate races have been described on the basis of panicle and spikelet morphology [123]. Sorghum genetic resources are conserved at many centers around the world including India, China, the United States, Ethiopia, Sudan, and South Africa. At the global level, sorghum germplasm collections consist of approximately 168 500 accessions. International Crops Research Institute for Semi-Arid Tropics (ICRISAT), India, is a major repository for world sorghum germplasm with a total of 37 000 accessions from 91 countries [124]. To facilitate enhanced utilization of diverse germplasm in breeding program, a core collection of 2247 accessions was developed in 2001 [125]. As this core collection was found to be too large, a sorghum minicore with 242 accessions (10% of the core or 1% of the entire collection) was developed from the existing core collection [124]. A minicore collection thus may help in a precise evaluation and phenotyping for various traits. Different molecular markers (RFLP, RAPD, AFLP, or SSR) have been used for molecular analysis of genetic diversity in sorghum germplasm [126–131]. These studies revealed that genetic diversity in sorghum is mostly influenced by racial and geographic origins [126, 127, 129, 131]. A worldwide core collection of 210 landraces representative of race, latitude of origin, response to day length, and production system was analyzed with 74 restriction fragment length polymorphism (RFLP) probes dispersed throughout the genome indicating that along with the geographical and racial genetic diversity, there were varying levels of diversity within specific morphological races. Among races, the highest diversity was exhibited by bicolor race and least by kafir [132]. 36.3.2 Genetic Maps and QTL Mapping

Several studies identified QTL associated with various traits in sorghum including disease resistance [133], insect resistance [134], plant height and maturity [135], and drought tolerance (references given in Section 36.2.1). Two high-density linkage maps are also available [136, 137]. The linkage map created by Menz et al. [136] consists of 2926 loci on 10 linkage groups with a total genetic distance of 1713 cM, while map

36.3 Genetic and Genomics Resources of Sorghum

developed by Bowers et al. [137] contained 2512 loci on 10 linkage groups, with a total genetic distance of 1059.2 cM. Later, these two maps have been aligned by identifying and mapping markers common to both populations [138]. On the basis of fluorescent in situ hybridization (FISH) of sorghum genomic BAC clones, a size-based nomenclature for sorghum chromosomes (SBI-01–SBI-10) and linkage groups (LG-01–LG10) has been proposed [139]. A unified system of nomenclature for chromosome and linkage maps will benefit the validation and comparison of QTL across different backgrounds and environments. Recently, using the genome sequence more than 6500 simple sequence repeat (SSR) loci with publicly available primer sequences have been mapped in silico on sorghum genome [140]. This will facilitate the identification of markers representing the entire genome, which in turn will not only improve resolution in diversity analyses and linkage disequilibrium mapping but also help in fine mapping and marker-assisted breeding. Besides standard molecular markers such as RFLP and SSR, a new hybridization-based diversity array technology (DArTÔ) has also been developed for sorghum [141]. Recently, six-component mapping populations were used to integrate over 2000 unique loci, including 1190 unique DArTmarkers and 839 others, into a single consensus map with an average marker density of one marker/ 0.79 cM [142]. This consensus map, however, still has overall lower marker density compared to that one marker/0.59 cM and one marker/0.42 cM published by Menz et al. [136] and Bower et al. [137], respectively. DArT provides the advantage of being a cost-effective, high-throughput marker technology that is independent of sequence information and allows high multiplexing level for whole genome profiling. 36.3.3 Association Genetics

Association mapping, also called linkage disequilibrium (LD) mapping, refers to the analysis of statistical associations between genotypes, usually individual singlenucleotide polymorphisms (SNPs) or SNP haplotypes, determined in a collection of individuals, and the traits (phenotypes) of the same individuals [143]. First developed for human genetics, association genetics has now been used for dissecting complex traits in crop plants [144]. In plants, a collection of individuals refers to those that are derived from wild populations, germplasm collections, or subsets of breeding germplasm. The levels of genetic variation and linkage disequilibrium (LD) are critical factors both in association mapping and in identification of loci that have been targets of selection. Sorghum being largely a self-pollinating crop is expected to have higher levels of LD and homozygosity, which are suitable parameters for LD mapping [145]. Analysis of 27 diverse S. bicolor accessions for sequence variation at about 30 000 sites throughout the genome of S. bicolor indicates that the frequency of SNPs is about one-fourth of that observed in a comparable sample of maize accessions [146]. The extent of allelic associations, as assessed by pairwise measures of LD, is higher in S. bicolor than in maize, but lower than in rice and Arabidopsis. Hamblin et al. [147] demonstrated that in sorghum LD could extend up to 100 kb, but had largely decayed by 15 kb, meaning that targeted association mapping is possible in this species. To facilitate the association studies in sorghum, Casa et al. [148] have

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characterized a panel of 377 accessions. These accessions were phenotyped for eight traits, and levels of population structure and familial relatedness were assessed with 47 SSR loci. The genotypic data for this panel along with appropriate statistical models for correcting for population structure and kinship are available for the entire sorghum community. Furthermore, efforts are being made to develop recombinant inbred populations for carrying out nested association mapping strategies in sorghum [148]. Recently, a few candidate gene-based association studies have been reported for various traits in sorghum such as plant height, brix, starch metabolism, and grain quality [149–152]. However, for complex quantitative traits such as drought stress, a genome-wide association mapping may be more useful. This will also require a genome-wide coverage of markers. Owing to their high density, SNPs play an important role in genome-scale linkage disequilibrium and association studies. About 1402 SNP alleles were reported by Hamblin et al. [146, 147, 151] through direct sequencing, while 2217 SNPs were detected in sorghum from analysis of loci from public EST databases [153]. 36.3.4 Transcriptomics and Reverse Genetics

Besides sequence-based information, adaptive responses of sorghum have been monitored by genome-wide expression analysis under different stress conditions such as salinity, osmotic stress, or abscisic acid [154]. In addition, a sorghum Expressed Sequence Tags (ESTs) project has collected over 200 000 sequences from cDNA libraries derived from diverse tissues [155] and by December 2010, 209 828 ESTs were available at EST database of National Center for Biotechnological Information (NCBI). Various in silico genome-wide analyses of genes, promoters, or miRNAs are being performed that will help in identification and characterization of existing and new orthologues of these sequences [156, 157]. Additional resources for sorghum include mutant populations that are either being screened for target traits such epicuticular wax [158] or being developed as TILLING populations [159]. A TILLING population of 1600 lines has also been generated through EMS mutagenesis in sorghum genotype BTx 623 and its applicability has been evaluated on a subset of mutant lines [159]. Isolation of Candystripe1 (Cs1), first active transposable element from sorghum, has potential for insertion mutagenesis and transposon tagging in sorghum [160]. The possibility of genetic transformation in sorghum [161–163] provides equal opportunities for both functional validation and crop improvement strategies. Moreover, the results of interspecific hybridization have been encouraging that will allow inclusion of allelic diversity in cultivated sorghum [164, 165]. 36.3.5 Comparative Genomics

Besides using its own genetic and genomic resources, sorghum can be benefited by the high degree of genic colinearity and sequence conservation that prevails among

36.4 Prospects

cereals [166, 167]. The syntenic relationship of sorghum with other cereals has become instrumental in the construction of genetic maps, verification of certain quantitative trait loci, identification of candidate genes underlying QTL, and genome evolution [109, 168–170]. Postgenome sequencing, enormous information is emerging from rice. The knowledge gained from rice can be used to accelerate progress in sorghum and sorghum in turn can benefit closely related large genomes such as maize and sugarcane. For example, analysis of miRNA in sorghum genome indicates that rice miRNA 169 g, which is upregulated during drought stress, has five sorghum homologues. Similarly, cytochrome P450 domain-containing genes, often involved in scavenging toxins such as those accumulated in response to stress, are more abundant in sorghum than in rice [4]. A detailed analysis of these duplicated genes may shed light on the adaptive nature of sorghum. On the other hand, sorghum genome has been found to be an excellent template for assembling the genic DNA of the autopolyploid sugarcane genome and Miscanthus giganteus genome [171, 172]. Thus, with rice, sorghum and Brachypodium distachyon genome [173] sequences already available, and with impending maize genome sequence, there is an immense opportunity for comparative genetics and genomics to dissect abiotic stress tolerance mechanisms in cereals.

36.4 Prospects

Postgenome sequencing, there has been a phenomenal change in the prospects of sorghum research in general. The focus has been shifted to sorghum because of several inherent attributes that make it a highly promising system in this global climate change scenario. With the availability of whole-genome sequence, wide germplasm resource and diversity, high-density linkage maps, array of markers coupled with tolerance to drought and heat, and potential candidate as bioenergy crop, sorghum is poised for modeling a future crop. There are several traits that are best represented by sorghum and yet remain unexplored. For example, sorghum tends to arrest growth during periods of drought and grows rapidly when water is available, thus avoiding yield losses. The extensive root system of sorghum can penetrate 1.5–2.5 m into the soil and extend 1 m away from the stem. Roots harvest water and nutrients from soil and thus play an important role in adaptation to abiotic stresses. Several root QTL have been identified in rice and maize, yet no such efforts have been made in sorghum. Maybe the extensive root system of sorghum itself could pose difficulty in phenotyping. The availability of advanced phenotyping facilities and information generated from rice and maize root QTL studies can be exploited. Furthermore, sorghum apparently shows epicuticular wax values close to maximum that can be achieved by plants. Though genetic and chemical analyses of epicuticular wax mutants have been reported, molecular aspects are needed to be understood. Components such as membrane stability and water use efficiency require a thorough evaluation. Passioura [174] remarked, Drought tolerance is a nebulous term that becomes more nebulous the more closely we look at it, much as a newspaper

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photograph does when viewed through a magnifying glass. Thanks to the tremendous progress in understanding drought tolerance mechanisms during the past two decades, and the availability of high-throughput phenomics and genomics tools, today plant scientist hope that crop drought tolerance can be improved drop by drop, trait by trait, and gene by gene [175]. Hence, application of high-throughput omics approach to understand the abiotic stress-adaptive mechanisms of sorghum will help genetic improvement of abiotic stress tolerance in sorghum. The trait of seedling emergence and seed vigor under cold from Chinese landraces is associated with transfer of negative traits such as susceptibility to leaf diseases. Identification of QTL is being done; however, tightly linked markers need to be developed for precise introgression of this trait in elite cultivars. Though it has been claimed that sorghum is tolerant to heat, yet there is no systematic study to illustrate this trait in sorghum. Overall, the attributes of sorghum for abiotic stress tolerance are still unexplored. Though some physiological evidences are available and genetic studies have been initiated, yet detail understanding of molecular and physiological mechanism is necessary for improvement of sorghum and cereal family in general.

Acknowledgment

Our work related to drought stress was supported by grants from National Agricultural Innovation Project, Indian Council of Agricultural research, New Delhi, India.

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