Responses of Sorghum to Abiotic Stresses

14 Pages·2012·0.2 MB·English

J A C 1 2 0 1 7 B Dispatch:1.12.12 Journal: JAC CE:PriyaC.
Journal Name ManuscriptNo. AuthorReceived: No.ofpages:11 PE:Vigneshwari
JAgroCropSci(2012)ISSN0931-2250
1 SALINITY STRESS
2
3 1 Responses of Sorghum to Abiotic Stresses: A Review
4 (cid:1) (cid:1)
I. Tari,G. Laskay,Z. Takacs&P. Poor
5
6 DepartmentofPlantBiology,UniversityofSzegedSzeged,Hungary
7
8
9
10
11 Keywords Abstract
12 aluminiumstress;nutrientsupplyand
Sorghum (Sorghum bicolor L. Moench) is a highly productive crop plant, which
13 deficiency;saltstress;Sorghumbicolor
(L.Moench);temperaturestress;waterstress canbeusedforalternativeenergyresource,humanfood,livestockfeedorindus-
14
trialpurposes.Thebiomassofsorghumcanbeutilizedassolidfuelviathermo-
15
Correspondence chemical routes or as a carbohydrate substrate via fermentation processes. The
16
I.Tari planthasagreatadaptationpotentialtodrought,highsalinityandhightempera-
17 DepartmentofPlantBiology
ture, which are important characteristics of genotypes growing in extreme envi-
18 UniversityofSzeged
19 Ko€z(cid:1)epfasor52 ronments.However,theclimatechangeinthe21stcenturymaybringaboutnew
challenges in the cultivated areas. In this review, we summarize the most recent
20 POBox654
H-6701Szeged literatureabouttheresponsesofsorghumtothemostimportantabioticstresses:
21
Hungary nutrient deficiency, aluminium stress, drought, high salinity, waterlogging or
22
Tel.:/Fax:[phone] temperaturestresstheplantshavetocopewithduringcultivation.Theadvanced
23 2 Email:[email protected] molecularandsystembiologicaltoolsprovidenewopportunitiesforbreedersto
24
selectstress-tolerantandhigh-yieldingcultivars.
25 AcceptedNovember16,2012
26
27 doi:10.1111/jac.12017
28
29
30 Germplasmresourcesofsorghumshowthatacompetition
Introduction
31 exists between grain yield and stem biomass production,
32 Sorghum (Sorghum bicolor L. Moench) is a multipurpose andthetaskofthebreedersistofindtheoptimumcondi-
33 cropbelongingtothePoaceaefamily,whichareC4carbon tionsforthedifferentproductivitiesintheplants.Breeding
34 cycle plants with high photosynthetic efficiency and pro- strategies for adaptation of sorghum to climatic variability
35 ductivity. Sorghumisoneof thefive major cultivatedspe- havebeenexcellentlyreviewedbyHausmannet al.(2012).
36 cies in the world because it has several economically
37 important potential uses such as food (grain), feed (grain
MorphologicalandPhysiologicalCharacteristicsof
38 andbiomass),fuel(ethanolproduction),fibre(paper),fer-
Sorghum
39 mentation (methane production) and fertilizer (utilization
40 3 of organic by-products) (ICRISAT 2009). Sorghum origi- Theplantisnativeintropicalareasandisalsowelladapted
41 nates from Africa, from the southern region of the Sahara totemperateclimate.Itishighlyresistanttodrought(Sted-
42 Desert,whereseveral closelyrelatedwildspeciesarefound uto et al. 1997), salinity (Almodares et al. 2008a,b) as well
43 (Legwaila et al. 2003). The cultivated genotypes and aswaterlogging(Promkhambutet al.2010),anditcanbe
44 hybridsareverydiverse.IntheEuropeanUnionandinthe grownandcanmaintainremarkableyieldpotentialinenvi-
45 USA, sweet sorghum has been bred as a promising energy ronments that are normally too extreme for other C4
46 crop (Berenji and Dahlberg 2004), and it is also suggested plants. Some of its morphological features are advanta-
47 asacandidateforbiofuelproductioninhotanddry(arid) geousfortheacclimationtospecificabioticstresses.
48 countries, such as Nigeria, India, Australia or Mexico (Al- The height of the plants ranges from 1.5 to 3.0 m,
49 4 modares and Hadi 2009). It is an important cereal in depending on the number and length of the internodes as
50 Africa,theMiddleEast,AsiaandCentralAmericaandisa wellasonthelengthofthepeduncleandthepanicle.Tillers
51 principal source of food for millions of people. The pur- maydevelopfromthelowernodes,whilelateralbranching
52 pose of breeders in China is to develop genotypes of both may occur higher up on the stem. In adult plants, lateral
53 high grain yield and high sugar content in the stem juice. branches usually develop when a significant amount of
©2012BlackwellVerlagGmbH 1
Tarietal.
1 moisture is available in the soil and more extensive tiller sorghum biomass at midgrowth. N concentration in plant
2 production can be observed during and after the anthesis tissues followed a common dilution curve, indicating that
3 ofthemainshoot(IsbellandMorgan1982). fertilizedsorghumefficientlyutilizedthesuppliedN,avoid-
4 Primary roots have a limited growth, and their function ing luxury consumption (Barbanti et al. 2011). However,
5 is taken over by the secondary root system, developing nitrogenfertilizationincreasedthestemdrymatterwithout
6 fromtherootcrowns.Therootsofanadultsorghumplant enhancing the sugar content of the tissues (Ferraris 1981).
7 are all secondary adventitious roots with numerous lateral Itwasaninterestingfindingthattheexpressionofthestay-
8 rootspenetratingthesoilinalldirections.Thedifferencein green phenotype in sorghum exhibited higher use and
9 totalwateruseduetochangesinrootmorphologyandbio- uptakeofnitrogen(Addyet al.2010).
10 mass was responsible for an increased yield of newly TheformofinorganicNalsodeterminesthedrymatter
11 released hybrids under rain-fed conditions (Assefa and accumulation of the plants. The tolerance of ammonium
12 Staggenborg 2011); likewise, the structure of the root sys- nutritiondependsontheammoniumdetoxificationcapac-
13 templaysanimportantroleinthedroughtstresstolerance ity of the root tissues via the cytosolic form of glutamine
14 oftherespectivecultivars(Salihet al.1999). synthetase, GS1 (GS, EC 6.3.1.2). It was shown that sor-
15 Sweet sorghum is a short-day plant, but large genotypic ghum-sudan grass (S. bicolor L. 9 S. bicolor var. sudan-
16 differences exist in the photoperiodic requirement for the ense) hybrids exhibited enhanced biomass production and
17 transition from the vegetative to the generative phase. increased capacity for N assimilation at increasing NO(cid:1)
3
18 There are varieties in Australia, which are insensitive to and NHþ supplies. In sorghum, the two distinct cytoplas-
4
19 photoperiods but late sorghum varieties are known to be micformsofGSwerefoundtobetheexpressionproducts
20 highly photoperiod sensitive. The choice of cultivar and of the SbGln1.2 and SbGln1.3 genes. The expression of the
21 sowing date should be combined in order that the plants SbGln1.3genewasup-regulatedbyhighlevelsofinorganic
22 flowerduringthelast20 daysofrainyseasonsensuringan N, with a maximal abundance of transcripts after NHþ
4
23 unperturbed grain-filling process. Experiments were con- treatment(ElOmariet al.2010).
24 ducted in three representative sites along a latitudinal gra- The different N forms supplied in the root medium
25 dient in Mali with seven sorghum cultivars (Abdulai et al. affected the uptake of K+ from low-K+ solutions. NHþ in
4
26 2012). Although the largest difference in day length was full nutrient solution increased the depletion of K+ from
27 8 minbetweentheexperimentalareas,eventheserelatively the incubation medium, which correlated with an
28 small differences caused variations in the duration of enhanced activity of the plasma membrane H+-ATPase in
29 vegetativephaseofupto3 weeks. sorghumroots,whileNO(cid:1) wasnotveryeffective(Alvarez-
3
30 The appearance of the panicle determines the distribu- Pizarroet al.2011).
31 tion of assimilates because it is a better sink than the leaf, TheinteractionbetweenKandZnsupplywasstudiedon
32 leafsheathandstalk.Beforestemelongation,thephotosyn- growth, yield and quality of forage sorghum grown in
33 thates accumulate mainly in the leaves, but after elonga- loamysandsoil(Moinuddin2010).IncreasingKlevelssig-
34 tion, the sugars begin to accumulate in the stalk and nificantly improved the yield and quality attributes, and
35 inflorescence. The dry matter distribution and sugar con- the beneficial effects of Zn application increased progres-
36 tentvaryalongthestalk.Thecentralpartofthestalkcon- sivelywithincreasedKsupply.
37 tains the most of soluble sugars, especially that of sucrose The uptake of the other macroelement, phosphorus, by
38 (Coleman1970,Eastin1972).Moreglucosecanbedetected sorghum depended on the concentration of the P forms
39 inthelowerpartofthestem,whiletheupperpartcontains available to plants in the soil (Khorasgani et al. 2009).
40 moresucroseandstarch(Ventreet al.1939). Phosphorus supply affects photosynthetic performance,
41 starch synthesis and transport of sugars across the chloro-
42 plast membrane and hence also plant growth and yield. P
EffectsofAppropriateNutrientSupplyand
43 deficiency seriously reduced the biomass production of
NutrientDeficiency
44 grain sorghum plants, decreased the performance of PSII,
45 The early and late application of fertilizers can promote the photosynthetic rate under light saturation, the effi-
46 growthandbiomassproductionofsweetsorghum,andthe ciency of carboxylation, ATP production and the rate of
47 plantsrespondwithhigheryieldtobothorganicandinor- ribulose-1,5-biphosphateregeneration(Ripleyet al.2004).
48 5 ganic fertilizers (Amuyojegbe et al. 2007). However, the Photosynthetic activity of plants is determined not only
49 effect of nitrogen fertilizers proved to be contradictory. by the availability of macroelements but also by that of
50 Increasing N supply in the form of composted bio-solids microelements. Critical Mn levels are needed for water
51 was expected to contribute to plant growth and nutrition; splitting in C3 and C4 plants and malate decarboxylation
52 thus, a mixed compost was prepared using (15)N-labelled forCO releaseinC4plants.NADP-malicenzyme(NADP-
2
53 materials.Itwasfoundthatthecompostenhancedthefibre ME) C4 plants, such as sorghum, reached maximum
2 ©2012BlackwellVerlagGmbH
EffectofAbioticStressesonSorghum
1 biomassproductionandphotosyntheticrateat2–5 lMMn (Magalhaes et al. 2004, Caniato et al. 2007). In two sor-
2 inthenutrientsolution(Keringet al.2009).IncreasingCu ghum cultivars, Magalhaes et al. (2004) found a major
3 supply for sweet sorghum in combination with ethylen- locus (Alt ) for Al3+ tolerance, which might be associated
sb
4 ediaminetetraaceticacid(EDTA)inhydroponiccultureled with citrate exudation from root apices. Most recently, a
5 to increased biomass production (Sz(cid:1)ekely et al. 2011) and gene encoding a member ofthemultidrug and toxic com-
6 increasedtheelongationgrowthofplants. pound extrusion (MATE) family, an aluminium-activated
7 Plants cannot easily acquire iron from the soil, so iron citrate transporter has been identified in sorghum plants
8 deficiencyisoneofthemajorlimitingfactorsaffectingcrop (Magalhaes et al. 2007). Genes controlling Al3+ resistance
9 yield.Graminaceousspeciescanenhanceironuptakefrom have already been cloned from various crop plants
10 inorganicFe(III)derivativesbyreleasingphytosiderophores includingsorghum(RyanandDelhaize2010).
11 (PS),theFe-chelatingcompounds.ThePSreleasebyroots
12 andtheuptakeofFe(III)PSbyrootcellsincreasebyafactor
DroughtStress
13 ofaboutfiveunderFedeficiency.Sorghumissusceptibleto
14 Fedeficiency,andthereforeanincreaseinitsresistancetoFe Thescarcityofwatermayexertanadverseeffectuponseed
15 deficiency(to‘limechlorosis’)canbeachievedbybreeding germination and embryo growth rate in the field, but sev-
16 the cultivars with high rates of PS release (Ro€mheld and eral sorghum cultivars adapted well to semi-arid areas
17 Marschner1990).Severalsimpleandeffectivesoilmanage- (Patan(cid:3)e et al. 2012). Although water-use efficiency and 8
18 ment practices, such as root feeding and bag fertilization, other physiological characteristics of sweet sorghum indi-
19 weredevelopedtoimprovetheFenutritionofplants(Zuo catethatthisspeciescansuccessfullyadapttodrought,the
20 6 andZhang2011).Singhet al.(2011)investigatedthetrans- research so far has mainly focused on biomass yield and
21 locationofradiolabellediron((59)Fe)suppliedthroughthe sugarcontentunderunfavourableconditions.
22 rootsystemtonon-chlorotic and chloroticsorghum.They Sorghumdevelopedtwoimportantstrategiesforadapta-
23 also treated the leaves with foliar spray of FeSO solution tion to water deficit. The primary way is the tolerance of
4
24 combined with various chelating compounds and found water potential decrease, while the second mechanism is
25 thatunderirondeficiencythedifferentialuptakeoflabelled theescapefromwaterstressduetodeepandextensiveroot
26 Fewasmarkedlyincreasedintheleavesandstemsofchlo- formation.
27 rotic plants as compared to non-chlorotic ones, and the Drought resistance of sorghum has been attributed to
28 foliar spray with FeSO + thiourea increased the (59)Fe morphological and physiological factors such as the dense
4
29 uptakethroughtheroots.IncontrasttotheFe-efficientbar- rootssystem(Mayakiet al.1976,JordanandMiller1980),
30 ley,whereironwasallocatedpreferentiallytothethylakoid theabilitytomaintainstomatalopeningandphotosynthe-
31 membranes during Fe deficiency, in the Fe-deficient sor- sis at low water potentials, and the ability for osmotic
32 ghum,thephotosyntheticapparatuswasseriouslydamaged, adjustment(Ludlowet al.1990).Sometimes,late-flowering
33 andtheproportionofleafFeallocatedtothethylakoidswas cultivars can tolerate water deficit more effectively (Hsiao
34 notaltered(Mikamiet al.2011). et al.1976).
35 Itwas reported that the high drought tolerance of sweet
36 sorghum cv. Gadambalia was associated with high water
AluminiumStress
37 extraction efficiency from the soil, fewer nodal roots
38 The rhizotoxicity of Al3+ is the major limitation to plant per plants and fewer metaxylem vessels in nodal roots.
39 production in acidic soils, a problem which is exacerbated The plants had a smaller leaf area and well-developed
40 by the use of ammonium fertilizers and acid rain (von sclerenchymaintheirleaftissues(Salihet al.1999).
41 Uexkull and Murtert 1995). Higher concentrations of Al3+ Drought-tolerantgenotypescanbecharacterizedbyhigh
42 werefoundinthesoilsolutionatpH3.7thanatpH5.8or epicuticular wax deposition on the leaf surface, which
43 6.3(Milleret al.2009). increases leaf reflectance in the visible and near-infrared
44 The resistance mechanism of plants to Al3+ toxicity can radiation and contributes to decreased transpiration (Sur-
45 be classified into two main groups: (i) the external toler- wenshiet al.2010).Anotherimportantfunctionoftheleaf
46 ance,thechelationofthemetalionbyorganicacidsinthe epicuticular wax is to reduce the cuticular conductance to
47 rhizosphere, or (ii) the chelation of Al3+ inside the cells water vapour and thus to increase water-use efficiency
48 7 (Inostrosa-Blancheteau et al. 2008). The main mechanism (WUE).
49 for the alleviation of Al3+ toxicity relies on the release of As a positive correlation was found between leaf photo-
50 organic anions from the root cells to the apoplast, which synthesis,totalbiomassandgrainproduction,theeffectsof
51 maybindanddetoxifytheharmfulAl3+cationsextracellu- droughtstressonphotosyntheticactivity,stomatalconduc-
52 larly. Sorghum bicolor belongs to the first group and uses tance and transpiration have been investigated by several
53 the exclusion mechanism through organic acid exudation authors(Youniset al.2000).
©2012BlackwellVerlagGmbH 3
Tarietal.
1 Drought stress decreased the transpiration rate and sto- the most sensitive to drought in the maturation stage,
2 matal conductance (Premachandra et al. 1994, Massacci whichwasprobablyduetotheirhighertranspirationrates.
3 et al. 1996), and these parameters varied among cultivars. They found accumulation of soluble carbohydrates,
4 Tsujiet al.(2003)characterizedthephysiologicalresponses sucrose, glucose and fructose in the leaf tissues during the
5 of an isohydric cultivar, which was able to maintain the vegetativeandreproductivestagesunderwaterstress.How-
6 water potential (cv. Gadambalia), and a desiccation-toler- ever, at maturation, significant decreases were observed.
7 ant one, which reduced the water potential under drought Thissuggeststhattheplantswereabletoadaptosmotically
8 stress (cv. Tabat). Drought tolerance of Gadambalia was duetotheaccelerateddegradationofstarchandformation
9 associatedwithhighleafwaterpotentialandrelativewater ofsolublesugarsduringthevegetativeandearlyreproduc-
10 content, while the reduction in net photosynthetic rate, tive stages. Both unstressed and drought-stressed plants
11 stomatal conductance and transpiration rate was low in accumulated sucrose and starch after the anthesis in the
12 Gadambaliaandhighincv.Tabat. stem. In the course of panicle maturation, sucrose and
13 Theeffectofmoderateandseriousdroughtstressonthe starch contents were higher in drought-stressed than in
14 diurnalchangesofphotosyntheticparametersaswellason unstressedstems(Massacciet al.1996).
15 their variation in various developmental phases has been It was also found that a silicon (Si) fertilizer improved
16 investigated in the sweet sorghum hybrid BJ0601. Photo- the growth of sorghum under water stress, increased the
17 synthesis declined in most plants around mid-day, which root water uptake and decreased the osmotic potential in
18 wasacombinedconsequenceofhighirradiationandwater the root cells indicating an osmotic adjustment. Under
19 deficit. This hybrid displayed a significantly lower water drought stress, silica is deposited in the endodermis of the
20 potential, the net photosynthetic rate (Pn) exhibited a root to avoid tissue collapse. An analysis of root solutes
21 depressionunderseriouswaterstressanditwascloselycor- showed that soluble sugars and amino acids (alanine and
22 related with stomatal conductance. With increasing glutamic acid) were accumulated as compatible osmolytes
23 drought stress, the light compensation point increased, in root tissues after Si application (Sonobe et al. 2010).
24 whereas the light saturation point, the apparent quantum Moreover, under water stress, silicon-treated seedlings
25 yieldanddarkrespirationdeclined.Thestemfreshbiomass exhibited higher stomatal conductance and photosynthetic
26 was the highest under moderate drought stress (Xie et al. ratethanuntreatedones(Sonobeet al.2009).
27 2010). Proline also acts as a compatible osmolyte and accumu-
28 Net CO assimilation rate (NAR), leaf area index (LAI), lates during abiotic stresses. D1-Pyrroline-5-carboxylate
2
29 whichisameasureofthetotalone-sidedareaofphotosyn- synthetase (P5CS, EC 2.7.2.11) is a key regulatory enzyme
30 theticleafsurfaceperunitgroundsurfacearea,andrelative of proline biosynthesis. Two closely related P5CS genes,
31 growth rate (RGR) are good indicators of the effectiveness SbP5CS1andSbP5CS2,wereisolatedfromsweetsorghum,
32 ofsolarradiationcapture(Patterson1982).Comparingfive which were located on chromosomes 3 and 9. Promoter
33 sweet sorghum cultivars and four lines, it was found that analysis of the two P5CS genes uncovered several stress-
34 exceptatpost-grainmaturitystage,thecorrelationsofLAI, responsive cis-acting elements. The expression analysis
35 NAR and RGR with sucrose and total sugar contents were revealed that the genes were up-regulated when the plants
36 positive,whereaswithglucose,fructose,maltoseandxylose wereexposedtodroughtstressandthatprolineconcentra-
37 contents,theywerenegative(Almodareset al.2007a).This tionwasincorrelationwiththeexpressionofSbP5CSgenes
38 meansthatasplantsgrow,LAI,NARandRGRincreasein (Suet al.2011).
39 parallel with sucrose accumulation and with the reduction Molecularvariation withinthedefinedgenes underlying
40 in invert sugars. Allen et al. (2011) found that canopy net specific biochemical and physiological functions provides
41 photosynthesis of grain sorghum was only 9 % lower at candidategene-basedmarkers,whichshowverycloseasso-
42 ambient (360 lmol mol(cid:1)1) and 7 % lower at elevated ciation with thetrait of interest. Srinivas et al. (2009) pre-
43 (720 lmol mol(cid:1)1)CO concentrationunderwater-limited sented a microsatellite linkage map containing 128
2
44 conditions than in well-watered plants. This suggests that microsatellite loci from subtracted drought stress ESTs in
45 effect of drought stress in C4 crop plants can be slightly S. bicolor(L.)Moench.ThedevelopedESTmarkersinclude
46 amelioratedatelevatedCO levels. genes coding for important regulatory proteins and
2
47 The sensitivity of sweet sorghum to water shortage enzymesthatarerelatedtodroughtstress.
48 dependedonthedevelopmentalstage.Theplantswerevery The transcriptome of sorghum shoot and root tissues
49 sensitive to drought in the vegetative and early reproduc- exposed to polyethylene glycol (PEG)-induced osmotic
50 tive stages. In the late reproductive phase, their water stress or to exogenous abscisic acid (ABA) was studied
51 requirement waslower, but theyielddecreased due to ter- using next-generation sequencing (NGS) technology to
52 minaldrought(Youniset al.2000,Xieet al.2010).Incon- revealthespecificgenesandgenenetworksthatcontribute
53 trast,OliveiraNetoet al.(2009)foundthattheplantswere tothedroughttoleranceofthiscrop(Dugaset al.2011).
4 ©2012BlackwellVerlagGmbH
EffectofAbioticStressesonSorghum
1 The authors found more than 28 000 unique genes that intheresponseoftherootsystemtowaterlogging,andsev-
2 showed transcriptional activities during osmotic stress or eralgenotypesrespondedwithaerenchymaformationfrom
3 ABA treatment. Expression analysis revealed 5156 unique the roots to the stalk base in flooded soils (Promkhambut
4 genes expressed differentially (DE genes) in treated and et al.2011b).Developmentofnewnodalrootsappearedto
5 controlsamples.Thegenescodingforthelateembryogene- be also an adaptive response of sorghum to waterlogging
6 sis abundant (LEA) proteins, WSI18, a water stress– (Pardales et al. 1991). The responses of three sweet sorgh-
7 induced protein and dehydrins were found in the top five umsandaforagecultivarwerecomparedaftertwentydays
8 genes up-regulated in response to both PEG and ABA. In of waterlogging (Promkhambut et al. 2010). This long-
9 contrast,agenecodingforperoxidase6andagenesimilar termfloodingcausedsignificantreductioninbiomasspro-
10 to OSIG-Ba010B08.10 coding for a sugar substrate trans- duction, increased the allocation of biomass to the roots
11 porter domain-containing protein were down-regulated. andreducedtheleafarea,andinthesweetcultivars,itsig-
12 Genes enriched in gene ontology (GO) categories, such as nificantly reduced photosynthetic rate, stomatal conduc-
13 response to drought, osmotic stress, cold and heat stress, tanceandtranspiration.Theabilitytoextendtheyoungest
14 were up-regulated in the roots and shoots after ABA and leaves, to produce new leaves, to increase the root length
15 PEG treatments, and only a small number of genes were and nodal root development indicated the high tolerance
16 down-regulated in these categories. The pathway enrich- ofasweetcultivar,Wray,towaterlogging.Thebiochemical
17 ment analysis revealed that both choline and the proline mechanismsunderlyingtheadaptationofplantstoO defi-
2
18 biosynthesis pathways contained DE genes in both shoots ciency are based on the ability of a genotype to maintain
19 and roots, but the authors did not observe enrichment for active fermentative metabolism under anaerobiosis. The
20 the glycine betaine biosynthesis pathway after ABA and rootsofaflood-tolerantsorghumcv.SSG-59-3exhibiteda
21 osmoticstresstreatments. ABAandosmoticstressaffected constant increase in alcohol dehydrogenase (EC 1.1.1.1)
22 thebiosynthetic pathways of other hormones, such as eth- and lactate dehydrogenase (EC 1.1.1.27) activities and
23 ylene, gibberellins, jasmonic acid and brassinosteroids; higher ethanol concentration than the sensitive variety
24 some of them also showing enrichment while cytokinin S-308, suggesting that the flood-tolerant variety tends to
25 and indoleacetic acid conjugation pathways, which render attaingreatercapacityforvariousfermentativepathwaysas
26 these hormones biologically inactive, also contained DE alternative means to sustain production of ATP under
27 genes. In PEG-treated roots, the up-regulated genes were floodedconditions(Jainet al.2010).
28 enrichedintheGOcategoriessuchasnodulation andepi-
29 dermal cell differentiation, while the genes coding for an
SaltStress
30 auxin efflux carrier and a phosphate transporter as well as
31 thegenesinvolvedinlateralrootdevelopmentweredown- Althoughsorghumisamoderatelysalt-tolerantcrop,geno-
32 regulated. Promoter analysis of the DE genes up-regulated typic differences exist among cultivars. High salinity is a
33 in theshoots due to ABA treatment revealed ABA-respon- consequence of the excess accumulation of various ions,
34 sive (ABRE) and dehydration-responsive (DRE) cis-acting first of all sodium, calcium, magnesium, chloride and sul-
35 elements, and the members of the AP2-EREBP transcrip- phate in the soil, and among them, sodium chloride is the
36 tionfactorfamily,whichcanbindthesecis-actingelements, mostharmfulforplantgrowthanddevelopment.Thereare
37 werealsoover-representedwithintheDEgenes. several classical methods for screening salt tolerance of
38 plants because the majority of the physiological processes,
39 for example, germination, K+ uptake, photosynthesis, bio-
Waterlogging
40 massproductionandbiochemicalparameters,suchaselec-
41 In tropical and sub-tropical regions, the crops may suffer trolyte leakage or chlorophyll content, are all highly
42 intermittentorlong-termwaterloggingduetoheavyrains, sensitivetosaltstress.Theresistanceofplantstosalinityis
43 storms, excessirrigation orflooding.Inthese areas,water- based on three strategies: (i) exclusion of Na+ from the
44 logging has a particularly deleterious effect on the crop, cytoplasm due to low uptake, or pumping out of the ion
45 because it does not only influence plant metabolism but from the cell by active mechanisms, (ii) sequestration of
46 also induces unfavourable changes in the soil texture. The Na+intothevacuoleand(iii)preferentialaccumulationin
47 harmful effects of flooding depend on the age of the seed- the leaf tissues. However, the genotypes with high leaf Na
48 lings(OrchardandJessop1984).Theplantsweremostsen- contentsprovedtobegenerallysaltsensitiveandonlythose
49 sitivetofloodingandrespondedwiththehighestreduction cantoleratehightissueconcentrations,whichcansequester
50 in growth and dry mass at the early vegetative and early Na+ into the vacuoles of leaf cells. The essential processes
51 reproductive stages (Promkhambut et al. 2011a).Flooding leading to plant adaptation to high salinity include ionic,
52 later than 30 days after emergence did not significantly metabolic and osmotic adjustments. The salt-resistant
53 affectshootgrowth.However,thereweregeneticvariations genotypes can successfully cope with osmotic and ionic
©2012BlackwellVerlagGmbH 5
Tarietal.
1 stresses caused by the excess of NaCl; they can effectively (APX, EC 1.11.1.11), catalase (CAT, 1.11.1.6), superoxide
2 reduce the oxidative damage and are able to detoxify the dismutase (SOD, EC 1.15.1.1), peroxidase (POX, EC
3 harmfulmetabolites(Zhu2001). 1.11.1.7), glutathione reductase (GR, EC 1.6.4.2) and total
4 Thetwo-phasemodelofgrowthreductioncausedbysalt antioxidantand phenolcontentsoftissues,suggesting that
5 stress divides theresponse ofplants into two distinct peri- the alleviation of salinity stress was associated with
6 ods (Munns 1993). The retardation of growth in the first enhanced antioxidant activity. Moreover, the plants accu-
7 phasewasshowntobeduetoosmoticstressandinthesec- mulated compatible osmolytes, soluble sugars and proline
8 ond phase to ion-related effects caused by high NaCl con- and exhibited higher osmotic adaptation after the applica-
9 centrations. It was observed by several authors that long- tion of silicon (Kafi et al. 2011). Increasing salinity levels
10 termsaltstressledtochlorosisandimpairedphotosynthe- decreasedthestemyieldandsolublecarbohydratelevelsin
11 sisinolderleaves(Munns1993,2002).Insorghumplants, twosweetsorghums(cvsKellerandSofra)andinonegrain
12 anotablesalt-stressphenotypewasobservedafter4 daysof sorghum cultivar (Kimia), but at the higher salinity level
13 growthin200 mMNaCl(Swamiet al.2011). the cv. Keller had the highest stem yield and sucrose
14 Salt stress decreased the percentage (Almodares et al. content(Almodareset al.2008b).
15 2007b) and increased the duration of germination (Gill Although the analyses of transcriptomes in response to
16 et al. 2003) in sweet sorghum. Significant differences can abiotic stresses have already been published by several
17 bedetectedinthesensitivityofgerminationtohighsalinity authors(seeinDugaset al.2011),studiesoncellularprote-
18 amongcultivars(Samadaniet al.1994). ome in sorghum are limited. Swami et al. (2011) investi-
19 The accumulation of toxic ions (Na+ and Cl(cid:1)) causes gated overall changes in the protein complement of
20 disturbancesinionuptakeandK+statusoftissues;thus,it sorghumleavesafter96-hexposureto200 mMNaCl.They
21 isthe high K+/Na+ discrimination and the maintenance of found 21 spots with altered expressions on 2-DE gels, and
22 lowNa+/K+ratiointissues,whichcharacterizethesalt-tol- after tryptic digestion of the excised spots, they identified
23 erant genotypes (Amtmann and Sanders 1999, Hasegawa them by MALDI-TOF/TOF mass spectrometer. One pro-
24 et al. 2000). The Na+ content of tissues in sorghum tein, the ATP synthase a-subunit, showed enhanced abun-
25 increased with increasing external sodium concentrations dance, which points to an impact of salt stress on the
26 (Lacerdaet al.2003),andthereweresignificantdifferences photosynthetic machinery. Eight of the up-regulated pro-
27 in root and shoot Na+ contents among genotypes (Bavei teins were involved inscavenging of ROS(POXand APX)
28 et al. 2011a). Lower accumulation of sodium in the shoot orinthedetoxificationofreactiveelectrophiliccompounds
29 results from either lower Na+ uptake by the root or from (glutathione S-transferase, EC 2.5.1.18). Other proteins,
30 the differences in the rate of Na+ transfer to the shoot. It such as lectin-like protein kinase, salt-inducible protein
31 was found that the salt-tolerant sorghum variety, Jambo, kinase, serine/threonine protein kinase, may be putative
32 accumulatedlessNa+intherootandshoottissuesthanthe components of the Na+-induced signal transduction. GS
33 salt-sensitive genotypes and maintained lower Na+/K+ was also an overexpressed protein in sorghum under salt
34 ratiosbothintherootandshoot(Baveiet al.2011a).Pref- stress, which corresponds to the findings of Pang et al.
35 erentialdepositionofNa+ionsintheshootoccurredinthe (2010)insalt-stressedThellungiella.Thissuggeststhatreas-
36 leafbase(Lacerdaet al.2003),andincreasinglevelsofCa2+ similation of ammonia is a crucial process under high
37 in the culture solution enhanced growth and lowered salinityinsorghum.
38 sodium uptake of sorghum plants (Asghar et al. 2009). It
39 was also observed that the salt-tolerant genotype Jambo
LowandHighTemperatureStresses
40 accumulated more Ca2+ both in the leaf and root tissues
41 than the sensitive varieties, Kimia and Payam (Bavei et al. The planting date determines the total sugar content and
42 2011b). biomass production of sweet sorghum: the later is the
43 The control of the excess accumulation of reactive oxy- planting, the lower are the yields of the stalk in arid envi-
44 gen species (ROS) generated as a secondary stress under ronments (Almodares and Mostafi Darany 2006). The
45 high salinity is also an essential component of salt toler- shortageinsoilwaterandtheheatstresssensitivityofculti-
46 ance. Many studies attributed the salt tolerance to an varsaretheprimary factorsfordecidingthedateofplant-
47 increase in the activity of antioxidant enzymes. However, ing in hot and dry climate zones (Teetor et al. 2011). In
48 salttolerancedidnotconsistentlydependonhigherantiox- these areas such as Arizona (USA), the growing season is
49 idant activities, and a fine tuning of both enzymatic and over 6 months long and sunlight is not limited. It was
50 non-enzymatic ROS-scavenging components can contrib- foundbyseveralresearchersthattheamountsofnon-struc-
51 ute to successful acclimation. Application of silicon to soil turalcarbohydratesincreasedfrompre-bootstagetoanthe-
52 alleviated salinity stress in two sorghum cultivars and sis (McBee and Miller 1982) and sucrose accumulation
53 caused an increase in the activities of ascorbate peroxidase reached the highest value at the ‘soft dough’ stage (Lingle
6 ©2012BlackwellVerlagGmbH
EffectofAbioticStressesonSorghum
1 1987).Duringadelayedharvestperiod,themaincarbohy- recently been found that the photosynthetic activity does
2 drate components in the stems in decreasing order were not depend only on the day temperature but also on the
3 sugar > cellulose > hemicellulose > starch in Chinese temperaturedetectedinthenightperiod(PrasadVaraand
4 sweetsorghumcultivars(Zhaoet al.2012). Djanaguiraman2011a).Theauthorscomparedtheeffectof 10
5 In temperate zones, the optimal growth can be con- an optimal day/night temperature combination (32/22 °C,
6 strained bychilling stressin earlyspring andit determines respectively) with an optimal day temperature (32 °C)/
7 theplantingdateintheseareas. high night temperature (HNT) (28 °C) combination and
8 Sweetsorghumisacold-sensitivecrop,andtheseedger- found that HNT adversely affected the photosynthetic
9 mination,seedlingemergenceandthegrowthofplantsare activity of plants. Exposure to HNT increased thylakoid
10 all sensitive to low temperatures (Alegre De La Soujeole membranedamageandnon-photochemicalquenchingbut
11 and Miller1984).Theseeds cannot germinate belowa soil decreasedthechlorophyllcontentofthetissues,thephoto-
12 temperature of 10 °C (Anda and Pint(cid:1)er 1994). Generally, chemical quenching parameter, the electron transport rate
13 stand establishment and early-season vigour are adversely and the photosynthetic activity of the leaves. The other
14 affected byair and soil temperatures below15 °C (Yu and interesting finding was that HNT increased ROS produc-
15 9 Tuinstra 2001). It was found that chilling stress caused a tioninleavesandpollengrains.Thelatterledtodecreased
16 significant decline in photosynthetic capacity (Taylor and pollen germination and lower seed set. It is in agreement
17 Rowley 1971) and photosynthetic rate was more severely with the results of Prasad et al. (2011b) who found that
18 affected than respiratory rate (Ercoli et al. 2004). After a grain sorghum pollen had shorter lifespan and exhibited
19 prolonged exposure to low temperature (8 °C), the plants much lower germination percentage on artificial growth
20 wereabletoadaptbyrestoringphotosynthesis,butatlower mediumathightemperatures.
21 temperatures the growth ceased. After screening for the High temperature stress (40/30 °C day/night tempera-
22 chillingtoleranceofsweetsorghumgenotypes,itwasfound tures)ingrainsorghumdecreasedthechlorophyllcontent,
23 that chilling temperatures drastically inhibited the photo- photosynthetic rate and antioxidant enzyme activities but
24 chemical quenching of chlorophyll a fluorescence. This increased oxidant production and membrane damage as
25 effect characterized the chilling-susceptible genotypes, and comparedtothecontrolplantsgrowingatoptimaltemper-
26 it was not observed in chilling-tolerant plants (Havaux atures(32/22 °C).Thisoxidativestresscanbemitigatedby
27 1989). sodium selenate sprayed onto the plant leaves, indicating
28 Chineselandraces‘kaoliangs’werefoundtoshowhigher that selenium can play a protective role during high tem-
29 seedling emergence and improved seedling vigour under perature stress by enhancing the antioxidant defence
30 cool conditions (Franks et al. 2006), but unfortunately system(Djanaguiramanet al.2010).
31 these landraces also harbour poor and undesirable agro- Heat shock proteins (HSPs) are synthesized in response
32 nomic traits. To produce elite sorghum lines with stable tohightemperatureorotherabioticstresses,andasmolec-
33 and good early-season cold tolerance, Burow et al. (2011) ular chaperones, they canprotect proteins fromtheharm-
34 identifiedsimplesequencerepeat(SSR)molecularmarkers ful effects of the stressors. The expression of hsp90 was
35 associated with various traits for early-season cold toler- comparedinvarioustypesofsorghum(ingrainandforage
36 ance. The mapping population consisting of 171 F -F sorghum hybrids and in a sweet sorghum cultivar) after
7 8
37 recombinant inbred lines (RILs) derived from the cross various durations of heat stress (Pavli et al. 2011). The
38 between RTX430 (cold-sensitive) and PI610727 (cold-tol- accumulation of hsp90 transcripts was determined by
39 erant) lines. PI610727 is also known as Gaigao Liang, a meansofRT-qPCRanalysis,anditwasfoundthatthelev-
40 landrace from a Chinese germplasm selected for early-sea- els of gene expression were significantly different in the
41 son cold tolerance. The RILs were evaluated for cold and investigatedgenotypes.
42 optimal temperature germinability in the laboratory, field The complete genom sequence for sorghum has been
43 emergence and seedling vigour in two locations during recently released (Paterson et al. 2009). This, in parallel
44 early-season planting. Two or more quantitative trait loci with the analysis of abiotic stress-induced transcriptomes,
45 (QTLs)weredetectedforalltraits, exceptforseedlingvig- proteomesandmetabolomes,providesanexcellenttoolfor
46 our;here,onlyoneQTLwasfound.Usinganewsourceof breeders to improve stress tolerance of this important
47 cold tolerance, PI610727, the authors tagged the genome energycrop.
48 regions of sorghum that have significant contributions to
49 traitsforearly-seasoncoldtolerance.
Acknowledgements
50 Hightemperaturestressmayalsoresultinthereduction
(cid:1)
51 in biomass and sugar yield. Photosynthetic activity, the The Project named ‘TAMOP-4.2.1/B-09/1/KONV-2010-
52 lightreactions andtheactivityofCalvin cycleenzymesare 0005 – Creating the Center of Excellence at the University
53 highlysensitivetoheatstress(Yanet al.2011,2012).Ithas of Szeged’ is supported by the European Union and
©2012BlackwellVerlagGmbH 7
Tarietal.
1 co-financedby theEuropeanRegionalFund(www.nfu.hu; Assefa,Y.,andS.A.Staggenborg,2011:Phenotypicchangesin
2 www.okmt.hu) and by the Hungarian Scientific Research grainsorghumoverthelastfivedecades.J.Agron.CropSci.
3 Fund(OTKACNK80781,K83642,K75528). 197,249–257.
4 Barbanti,L.,M.Grigatti,andC.Ciavatta,2011:Nitrogenrelease
5 froma(15)N-labeledcompostinasorghumgrowthexperi-
6 References ment.J.PlantNutr.SoilSci.174,240–248.
7 Abdulai,A.L.,M.Kouressy,M.Vaksmann,F.Asch,M.Giese, Bavei,V.,B.Shiran,M.Khodambashi,andA.Ranjbar,2011a:
Proteinelectrophoreticprofilesandphysiochemicalindicators
8 andB.Holger,2012:Latitudeanddateofsowinginfluences
ofsalinitytoleranceinsorghum(SorghumbicolorL.).Afr.J.
9 phenologyofphotoperiod-sensitivesorghums.J.Agric.Crop
10 Sci.198,340–348. Biotechnol.10,2683–2697.
Bavei,V.,B.Shiran,andA.Ahmad,2011b:Evaluationofsalinity
11 Addy,S.,C.E.JrNiedziela,andM.P.Reddy,2010:Effectof
toleranceinsorghum(SorghumbicolorL.)usingionaccumu-
12 nitrogenfertilizationonstay-greenandsenescentsorghum
13 hybridsinsandculture.J.PlantNutr.33,185–199. lation,prolineandperoxidasecriteria.PlantGrowthRegul.
64,275–285.
AlegreDeLaSoujeole,A.A.,andF.R.Miller,1984:Coldtoler-
14
Berenji,J.,andJ.Dahlberg,2004:Perspectivesofsorghumin
anceofsorghumduringearlydevelopmentalstages.Proc.
15 Ann.CornSorghumRes.Conf.39,18–32. Europe.J.Agron.CropSci.190,332–338.
16
Burow,G.,J.J.Burke,Z.Xin,andC.D.Franks,2011:Genetic
Allen,L.H.Jr,V.G.Kakani,J.C.V.Vu,andK.J.Boote,2011:
17
dissectionofearly-seasoncoldtoleranceinsorghum(Sorghum
ElevatedCO increaseswateruseefficiencybysustainingpho-
18 2 bicolor(L.)Moench).Mol.Breeding28,391–402.
tosynthesisofwater-limitedmaizeandsorghum.J.Plant
19 Physiol.168,1909–1918. Caniato,F.F.,C.T.Guimaraes,R.E.Shaffert,V.M.C.Alves,L.
20 V.Kochian,A.Borem,P.E.Klein,andJ.V.Magalhaes,2007:
Almodares,A.,andM.Hadi,2009:Productionofbioethanol
21 fromsweetsorghum.Areview.Afr.J.Agric.Res.4,772–778. Geneticdiversityforaluminiumtoleranceinsorghum.Theor.
22 Appl.Genet.114,863–876.
Almodares,A.,andS.M.MostafiDarany,2006:Effectsofplant-
23 Coleman,R.E.,1970:Sweetsorghumforsugarproduction.
ingdateandtimeofnitrogenapplicationonyieldandsugar
24 contentofsweetsorghum.J.Environ.Biol.27,601–605. Proc.Am.Soc.SugarCaneTech.17,1–9.
25 Almodares,A.,R.Taheri,andS.Adeli,2007a:Inter-relationship Djanaguiraman,M.,P.V.Prasad,andM.Seppanen,2010:Sele-
26 betweengrowthanalysisandcarbohydratecontentsofsweet niumprotectssorghumleavesfromoxidativedamageunder
27 sorghumcultivarsandlines.J.Environ.Biol.28,527–531. hightemperaturestressbyenhancingantioxidantdefensesys-
28 Almodares,A.,M.R.Hadi,andB.Dosti,2007b:Effectsofsalt tem.PlantPhysiol.Biochem.48,999–1007.
29 stressongerminationpercentageandseedlinggrowthinsweet Dugas, D. V., M. K. Monaco, A. Olson, R. R. Klein, S. Ku-
30 sorghumcultivars.J.Biol.Sci.7,1492–1495. mari, D. Ware, and P. E. Klein, 2011: Functional annota-
tion of the transcriptome of Sorghum bicolor in response
31 Almodares,A.,M.R.Hadi,andB.Dosti,2008a:Theeffectsof
to osmotic stress and abscisic acid. BMC Plant Genomics
32 saltstressongrowthparametersandcarbohydratecontentsin
33 sweetsorghum.Res.J.Environ.Sci.2,298–304. 12, 514–535.
Eastin,J.D.,1972:Photosynthesisandtranslocationinrelation
34 Almodares,A.,M.R.Hadi,andH.Ahmadpour,2008b:Sor-
toplantdevelopment.In:N.G.P.RaoandL.R.House,eds.
35 ghumstemyieldandsolublecarbohydratesunderdifferent
36 salinitylevels.Afr.J.Biotechnol.7,4051–4055. SorghumintheSeventies,pp.214–246.OxfordandIBHPub-
Alvarez-Pizarro,J.C.,E.Gomes-Filho,J.Tarqu(cid:1)ınioPrisco,M.F. lishingCo,NewDelhi,India.ICRISAT(InternationalCrops
37
Grossi-de-S(cid:1)a,andO.BrilhantedeOliveira-Neto,2011: ResearchInstituteforSemi-AridTropics)2009,http://www.
38
NH + -stimulatedlow-K+uptakeisassociatedwiththe icrisat.org. 11
39 4
inductionofH+extrusionbytheplasmamembraneH+-AT- ElOmari,R.,M.Rueda-Lopez,C.Avila,R.Crespillo,M.Nhiri,
40 PaseinsorghumrootsunderK+deficiency.J.PlantPhysiol. andF.M.C(cid:1)anovas,2010:Ammoniumtoleranceandtheregu-
41
168,1617–1626. lationoftwocytosolicglutaminesynthetasesintherootsof
42 Amtmann,A.,andD.Sanders,1999:MechanismsofNa+uptake sorghum.Funct.PlantBiol.37,55–63.
43 byplantcells.Adv.Bot.Res.29,76–104. Ercoli,L.,M.Mariotti,A.Masoni,andI.Arduini,2004:Growth
44 responsesofsorghumplantstochillingtemperatureand
Amuyojegbe,B.J.,J.T.Opabode,andA.Olayinka,2007:Effect
45 durationofexposure.Eur.J.Agron.2,93–103.
oforganicandinorganicfertilizeronyieldandchlorophyll
46 Ferraris,F.,1981:Earlyassessmentofsweetsorghumasanagro-
contentofmaize(ZeamaysL.)andsorghum(Sorghumbicolor
47 L.Moench).Afr.J.Biotechnol.6,1869–1873. industrialcrop.1.Varietalevaluation.Austr.J.Exp.Agric.
48 Anda,A.,andL.Pint(cid:1)er,1994:Sorghumgerminationanddevel- Anim.Husbandry21,75–82.
49 opmentasinfluencedbysoiltemperatureandwatercontent. Franks,C.,G.Burow,andJ.Burke,2006:AcomparisonofU.S.
50 Agron.J.86,621–624. andChinesesorghumgermplasmforearlyseasoncoldtoler-
51 Asghar,D.,A.A.Khan,andJ.C.Collins,2009:Effectsofsalinity ance.CropSci.43,1371–1376.
52 ongrowth,ionicrelationsandsolutecontentofSorghumbico- Gill,P.K.,A.D.Sharma,P.Singh,andS.S.Bhullar,2003:
53 lorL.Moench.J.PlantNutr.32,1219–1236. Changesingermination,growthandsolublesugarcontentsof
8 ©2012BlackwellVerlagGmbH
EffectofAbioticStressesonSorghum
1 Sorghumbicolor(L.)Moenchseedsundervariousabiotic Lingle,S.E.,1987:Sucrosemetabolismintheprimaryculmof
2 stresses.PlantGrowthRegul.40,157–162. sweetsorghumduringdevelopment.CropSci.27,1214–1219.
3 Hasegawa,P.M.,R.A.Bressan,J.K.Zhu,andH.J.Bohnert, Ludlow,M.M.,J.M.Santamaria,andS.Fukai,1990:Contribu-
4 2000:Plantcellularandmolecularresponsestohighsalinity. tionofosmoticadjustmenttograinyieldofSorghumbicolor
5 Annu.Rev.PlantPhysiol.PlantMol.Biol.51,463–499. (L.)Moenchunderwater-limitedconditions.II.Post-anthesis
6 Hausmann,B.I.G.,H.FredRattunde,E.Weltzien-Rattunde,P. waterstress.Aust.J.Agric.Res.41,67–78.
7 S.C.Traor(cid:1)e,K.vomBrocke,andH.K.Parzies,2012:Breed- Magalhaes, J. V., D. F. Garvin, Y. Wang, M. E. Sorrells, P. E.
ingstrategiesforadaptationofpearlmilletandsorghumto Klein, R. E. Shaffert, L. Li, and L. V. Kochian, 2004: Com-
8
climatevariabilityandchangeinWestAfrica.J.Agron.Crop parative mapping of a major aluminium tolerance gene in
9
Sci.198,327–339. sorghum and other species in the Poaceae. Genetics 167,
10
Havaux,M.,1989:Fluorometricdeterminationofthegenetic 1905–1914.
11
variabilityexistingforchillingtoleranceinsweetsorghumand Magalhaes,J.,????.Liu,C.T.Guiamaraes,G.P.Lana,M.C.
12
sudangrass.PlantBreeding102,327–332. Alves,Y.H.Wang,R.E.Shaffert,O.A.Hoekenga,M.A.
13
Hsiao,T.C.,E.Fereres,E.Acevedo,andD.W.Henderson, Pin~eros,J.E.Shaff,P.A.Klein,N.P.Carneiro,C.M.Coelho,
14
1976:Waterstressanddynamicsofgrowthandyieldincrop H.N.Trick,andL.V.Kochian,2007:Ageneinthemultidrug
15
plants.In:O.L.Lange,L.Kappen,andE.D.Schulze,eds. andtoxiccompoundextrusion(MATE)familyconfersalu-
16 WaterandPlantLife.ProblemsandModernApproaches,pp. miniumtoleranceinsorghum.Nat.Genet.9,1156–1162. 14
17 12 281–305.Springer-Verlag,Berlin-Heidelberg-NewYork. Massacci,A.,A.Battistelli,andF.Loreto,1996:Effectofdrought
18
Inostrosa-Blancheteau,C.,B.Soto,P.Ulloa,F.Aquea,andM. stressonphotosyntheticcharacteristics,growthandsugar
19 Reyes-D(cid:1)ıaz,2008:Resistancemechanismsofaluminium(Al3 accumulationoffield-grownsweetsorghum.Aust.J.Plant
20 +)phytotoxicityincereals:physiological,geneticandmolecu- Physiol.23,331–340.
21 larbases.J.SoilSci.PlantNutr.8,57–71. Mayaki,W.C.,L.R.Stone,andI.D.Teare,1976:Irrigatedand
22 Isbell,V.R.,andP.W.Morgan,1982:Manipulationofapical nonirrigatedsoybean,cornandgrainsorghumrootssystems.
23 dominanceofsorghumwithgrowthregulators.CropSci.22, Agron.J.68,532–534.
24 30–35. McBee,G.G.,andF.R.Miller,1982:Carbohydratesinsorghum
25 Jain,V.,N.K.Singla,S.Jain,andK.Gupta,2010:Activitiesof culmsasinfluencedbycultivars,spacings,andmaturityovera
26 enzymesoffermentationpathwaysintheleavesandrootsof diurnalperiod.CropSci.22,381–385.
27 contrastingcultivarsofsorghum(SorghumbicolorL.)during Mikami,Y.,A.Saito,E.Miwa,andK.Higuchi,2011:Allocation
28 flooding.Physiol.Mol.Biol.Plants163,241–247. ofFeandferricchelatereductaseactivitiesinmesophyllcells
29 Jordan,W.R.,andF.R.Miller,1980:Geneticvariabilityinsor- ofbarleyandsorghumunderFe-deficientconditions.Plant
30 ghumrootsystems.Implicationsfordroughttolerance.In:N. Physiol.Biochem.49,513–519.
C.TurnerandP.J.Kramer,eds.AdaptationofPlantsto Miller,G.,M.Mamo,R.Drijber,C.Wortmann,andR.Renken,
31
WaterandHighTemperatureStress,pp.383–399.Willey& 2009:Sorghumgrowth,rootresponsesandsoil-solutionalu-
32
Sons,NewYork,NY,USA. miniumandmanganeseonpH-stratifiedsandysoil.J.Plant
33
Kafi,M.,J.Nabati,A.Masoumi,andM.Z.Mehrgerdi,2011: Nutr.SoilSci.172,108–117.
34
Effectofsalinityandsiliconapplicationonoxidativedamage Moinuddin,I.P.,2010:Effectofzincnutritionongrowth,yield,
35
ofsorghum[(Sorghumbicolor(L.)Moench.]Pak.J.Bot.43, andqualityofforagesorghuminrespectwithincreasing
36
2457–2462. potassiumapplicationrates.J.PlantNutr.33,2062–2081.
37
Kering,M.K.,K.Lukasewska,andD.G.Blevins,2009:Manga- Munns,R.,1993:Physiologicalprocesseslimitingplantgrowth
38
neserequirementforoptimumphotosynthesisandgrowthin insalinesoils:somedogmasandhypotheses.Nat.Biotechnol.
39 NAD-malicenzymeC-4species.PlantSoil316,217–226. 21,255–261.
40
Khorasgani,M.N.,H.Shariatmadari,andB.Atarodi,2009: Munns,R.,2002:Comparativephysiologyofsaltandwater
41 Interrelationofinorganicphosphorusfractionsandsorghum stress.PlantCellEnviron.25,239–250.
42 availablephosphorusincalcareoussoilsofSouthernKhora- OliveiraNeto,C.F.,A.K.S.Lobato,M.C.Gon(cid:1)calves-Vidigal,
43 san.Commun.SoilSci.PlantAnal.40,2460–2473. R.C.L.Costa,B.G.SantosFilho,G.A.F.Alves,W.J.M.S.
44 Kochian,L.V.,2004:Comparativemappingofamajoralumin- Maia,F.J.R.Cruz,H.K.B.Neves,andM.J.S.Lopez,2009:
45 iumtolerancegeneinsorghumandotherspeciesinthePoa- Carboncompoundsandchlorophyllcontentsinsorghum
46 13 ceae.Genetics167,1905–1914. submittedtowaterdeficitduringthreegrowthstages.J.Food
47 Lacerda,C.F.,J.Cambraria,M.A.Oliva,H.A.Ruiz,andJ.T. Agric.Environ.7,588–593.
48 Prisco,2003:Soluteaccumulationanddistributionduring Orchard,P.W.,andR.S.Jessop,1984:Theresponseofsorghum
49 shootandleafdevelopmentintwosorghumgenotypesunder andsunflowertoshort-termwaterlogging.I.Effectsofstage
50 saltstress.Rev.Bras.Physiol.Veg.49,107–120. ofdevelopmentanddurationofwaterloggingongrowthand
51 Legwaila,G.M.,T.V.Balole,andS.K.Karikari,2003:Reviewof yield.PlantSoil81,119–132.
52 sweetsorghum:apotentialcashandforagecropinBotswana. Pang,Q.,S.Chen,S.Dai,Y.Chen,Y.Wang,andX.Yan,2010:
53 UNISWAJ.Agric.12,5–14. ComparativeproteomicsofsalttoleranceinArabidopsis
©2012BlackwellVerlagGmbH 9
Tarietal.
1 thalianaandThellungiellahalophyla.J.ProteomeRes.9, Ro€mheld,V.,andH.Marschner,1990:Genotypicaldifferences
2 2584–2599. amonggraminaceousspeciesinreleaseofphytosiderophores
3 Pardales,J.R.Jr,Y.Kono,andA.Yamaguchi,1991:Responseof anduptakeofironphytosiderophores.PlantSoil123,147–153.
4 differentrootsystemcomponentsofsorghumtoincidence Ryan,P.,andE.Delhaize,2010:Theconvergentevolutionof
5 waterlogging.Environ.Exp.Bot.31,107–115. aluminiumresistanceinplantsexploitsaconvenientcurrency.
6 Patan(cid:3)e,C.,A.Saita,andO.Sortino,2012:Comparativeeffects Funct.PlantBiol.37,275–284.
7 ofsaltandwaterstressonseedgerminationandearlyembryo Sahu,M.P.,2011:Differentialtranslocationof(59)ironiniron
growthintwocultivarsofsweetsorghum.J.Agron.CropSci. sufficientanddeficientsorghumplants.J.PlantNutr.34,
8
15 ????,????–????.doi:10.1111/j.1439-037X.2012.00531.x. 1723–1735. 16
9
Paterson,A.H.,J.E.Bowers,R.Bruggmann,I.Dubchak, Salih,A.A.,I.A.Ali,A.Lux,M.Luxov(cid:1)a,Y.Cohen,Y.Sugimoto,
10
J.Grimwood,H.Gundlach,G.Haberer,U.Hellsten,T.Mitros, andS.Inanaga,1999:Rooting,wateruptakeandxylemstruc-
11
A.Poliakov,J.Schmutz,M.Spannagl,H.Tang,X.Wang, tureadaptationtodroughtoftwosorghumcultivars.Crop
12
T.Wicker,A.K.Bharti,J.Chapman,F.A.Feltus,U.Gowik, Sci.39,168–173.
13
I.V.Grigoriev,E.Lyons,C.A.Maher,M.Martis,A.Narechania, Samadani,B.,B.Kholdbarin,andA.Almodares,1994:Salttoler-
14
R.P.Otillar,B.W.Penning,A.A.Salamov,Y.Wang,L.Zhang, anceofsweetsorghumcultivarsandtheirmechanisms.MSc
15
N.C.Carpita,M.Freeling,A.R.Gingle,C.T.Hash,B.Keller, Thesisinbiology(plantphysiology).ShirazUniversity,Iran,
16 P.Klein,S.Kresovich,M.C.McCann,R.Ming,D.Peterson, pp.45–62.
17
G.Mehboob-ur-Rahman,D.Ware,P.Westhoff,K.F.Mayer, Singh,G.,N.S.Nathawat,N.Kishore,S.Ramani,N.K.Ra-
18
J.Messing,andD.S.Rokhsar,2009:TheSorghumbicolorgen- mashwamy,S.R.D’Souza,andM.P.Sahu,2011:Differential
19 omeandthediversificationofgrasses.Nature457,551–556. translocationof59Ironinironsufficientanddeficientsor-
20 Patterson,D.T.,1982:Effectsoflightandtemperatureonweed/ ghumplants.J.PlantNutr.34,1723–1735.
21 cropgrowthandcompetition.In:J.L.HatfieldandI.J.Tho- Sonobe,K.,T.Hattori,P.An,W.Tsuji,E.Eneji,K.Tanaka,and
22 mason,eds.BiometeorologyinIntegratedPestManagement, S.Inanaga,2009:Diurnalvariationsinphotosynthesis,stoma-
23 pp.407–420.AcademicPress,NewYork,NY,USA. talconductanceandleafwaterrelationinsorghumgrown
24 Pavli,O.I.,D.V.Ghikas,A.Katsiotis,andG.N.Skaracis,2011: withorwithoutsiliconunderwaterstress.J.PlantNutr.32,
25 Differentialexpressionofheatshockproteingenesinsor- 433–442.
26 ghum(SorghumbicolorL.)genotypesunderheatstress.Austr. Sonobe,K.,T.Hattori,P.An,W.Tsuji,E.Eneji,S.Kobayashi,
27 J.CropSci.5,511–515. Y.Kawamura,K.Tanaka,andS.Inanaga,2010:Effectofsili-
28 PrasadVara,P.V.,andM.Djanaguiraman,2011a:Highnight conapplicationonsorghumrootresponsestowaterstress.
29 temperaturedecreasesleafphotosynthesisandpollenfunction J.PlantNutr.34,71–82.
30 ingrainsorghum.Funct.PlantBiol.38,993–1003. Srinivas,G.,K.Satish,R.Madhusudhana,andN.Seetharama,
Prasad,P.V.V.,K.J.Boote,andL.H.JrAllen,2011b:Longevity 2009:Explorationandmappingofmicrosatellitemarkers
31
andtemperatureresponseofpollenasaffectedbyelevated fromsubtracteddroughtstressESTsinSorghumbicolor(L.)
32
growthtemperatureandcarbondioxideinpeanutandgrain Moench.Theor.Appl.Genetics118,703–717.
33
sorghum.Environ.Exp.Bot.70,51–57. Steduto,P.,N.Katerji,H.Puertos-Molina,M.U€nlu€,M.Mast-
34
Premachandra,G.S.,D.T.Hahn,andR.J.Joly,1994:Leafwater rorilli,andG.Rana,1997:Water-useefficiencyofsweetsor-
35
relationsandgasexchangeintwograinsorghumgenotypes ghumunderwaterstressconditions:gas-exchange
36
differingintheirpre-andpostfloweringdroughttolerance. investigationsatleafandcanopyscales.FieldCropsRes.54,
37
J.PlantPhysiol.143,96–101. 221–234.
38
Promkhambut,A.,A.Younger,A.Polthanee,andC.Akkasaeng, Su,M.,X.-F.Li,X.-Y.Ma,X.J.Peng,A.G.Zhao,L.Q.Cheng,
39
2010:Morphologicalandphysiologicalresponsesofsorghum S.Y.Chen,andG.S.Liu,2011:CloningtwoP5CSgenesfrom
40
(SorghumbicolorL.Moench)towaterlogging.AsianJ.Plant bioenergysorghumandtheirexpressionprofilesunderabiotic
41 Sci.9,183–193. stressesandMeJAtreatment.PlantSci.181,652–659.
42 Promkhambut,A.,A.Polthanee,C.Akkasaeng,andA.Younger, Surwenshi, A., V. P. Chimmad, B. R. Jalageri, V. Kumar, M.
43 2011a:Growth,yieldandaerenchymaformationofsweetsor- Ganapathi, and H. T. Nakul, 2010: Characterization of sor-
44 ghum(SorghumbicolorL.Moench)asaffectedbyfloodingat ghum genotypes for physiological parameters and yield
45 differentgrowthstages.Aust.J.CropSci.5,954–965. under receding soil moisture conditions. Res. J. Agric. Sci.
46 Promkhambut,A.,A.Polthanee,C.Akkasaeng,andA.Younger, 1, 242–244.
47 2011b:Aflood-freeperiodcombinedwithearlyplantingis Swami,A.K.,S.I.Alam,N.Sengupta,andR.Sarin,2011:Dif-
48 requiredtosustainyieldofpre-ricesweetsorghum(Sorghum ferentialproteomicanalysisofsaltstressresponseinSorghum
49 bicolorL.Moench).ActaAgric.Scan.B61,345–355. bicolorleaves.Environ.Exp.Bot.71,321–328.
50 Ripley,B.S.,S.P.Redfern,andJ.Dames,2004:Quantification Sz(cid:1)ekely,A(cid:1).,P.Poo(cid:1)r,I.Bagi,J.Csisz(cid:1)ar,K.G(cid:1)emes,F.Horv(cid:1)ath,
51 ofthephotosyntheticperformanceofphosphorus-deficient andI.Tari,2011:EffectofEDTAonthegrowthandcopper
52 Sorghumbymeansofchlorophyll-afluorescence.S.Afr.J.Sci. accumulationofsweetsorghumandsudangrassseedlings.
53 100,615–618. ActaBiol.Szeged55,159–164.
10 ©2012BlackwellVerlagGmbH