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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.
j 36 Sorghum: Improvement of Abiotic Stress Tolerance
924
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.
36.2
Abiotic Stress Tolerance
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
36.2 Abiotic Stress Tolerance
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
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
RIL
RIL
RIL
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
36.2 Abiotic Stress Tolerance
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 Abiotic Stress Tolerance
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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940
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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