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Sorghum pp 11-40 | Cite as

Mapping QTLs and Identification of Genes Associated with Drought Resistance in Sorghum

  • Karen R. Harris-ShultzEmail author
  • Chad M. Hayes
  • Joseph E. Knoll
Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 1931)

Abstract

Water limits global agricultural production. Increases in global aridity, a growing human population, and the depletion of aquifers will only increase the scarcity of water for agriculture. Water is essential for plant growth and in areas that are prone to drought, the use of drought-resistant crops is a long-term solution for growing more food for more people with less water. Sorghum is well adapted to hot and dry environments and has been used as a dietary staple for millions of people. Increasing the drought resistance in sorghum hybrids with no impact on yield is a continual objective for sorghum breeders. In this review, we describe the loci, quantitative trait loci (QTLs), or genes that have been identified for traits involved in drought avoidance (water-use efficiency, cuticular wax synthesis, trichome development and morphology, root system architecture) and drought tolerance (compatible solutes, pre- and post-flowering drought tolerance). Many of these identified genes and QTL regions have not been tested in hybrids and the effect of these genes, or their interactions, on yield must be understood in normal and drought-stressed conditions to understand the strength and weaknesses of their utility.

Key words

Drought avoidance Drought tolerance Drought escape Trichomes Epicuticular wax Stay-green Root architecture Water-use efficiency Compatible solutes 

Notes

Acknowledgments

The authors would like to thank Dr. Somashekhar Punnuri (Fort Valley State University, Fort Valley, GA) and Dr. Corley Holbook (USDA-ARS, Tifton, GA) for their critical comments in the development of this book chapter.

References

  1. 1.
    Boyer JS (1982) Plant productivity and environment. Science 218:444–448CrossRefGoogle Scholar
  2. 2.
    Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought-from genes to the whole plant. Funct Plant Biol 30:239–264CrossRefGoogle Scholar
  3. 3.
    Sanchez AC, Subudhi PK, Rosenow DT, Nguyen HT (2002) Mapping QTLs associated with drought resistance in sorghum (Sorghum bicolor L. Moench). Plant Mol Biol 48:713–726PubMedCrossRefGoogle Scholar
  4. 4.
    Kramer PJ, Boyer JS (1995) Water relations of plants and soils. Academic Press, San Diego, CAGoogle Scholar
  5. 5.
    Hu H, Xiong L (2014) Genetic engineering and breeding of drought-resistant crops. Annu Rev Plant Biol 65:715–741PubMedCrossRefGoogle Scholar
  6. 6.
    Blum A (1996) Crop responses to drought and the interpretation of adaptation. Plant Growth Regul 20:135–148CrossRefGoogle Scholar
  7. 7.
    Saini HS, Westgate ME (1999) Reproductive development in grain crops during drought. Adv Agron 68:59–96CrossRefGoogle Scholar
  8. 8.
    Lascano HR, Antonicelli GE, Luna CM, Melchiorre MN, Gómez LD, Racca RW, Trippi VS, Casano LM (2001) Antioxidant system response of different wheat cultivars under drought: field and in vitro studies. Funct Plant Biol 28:1095–1102CrossRefGoogle Scholar
  9. 9.
    Levitt J (1980) Responses of plants to environmental stresses, Physiological ecology series. Academic, MichiganGoogle Scholar
  10. 10.
    Fang Y, Xiong L (2015) General mechanisms of drought response and their application in drought resistance improvement in plants. Cell Mol Life Sci 72:673–689PubMedCrossRefGoogle Scholar
  11. 11.
    Mooney HA, Ehleringer J, Berry JA (1976) High photosynthetic capacity of a winter annual in Death Valley. Science 194:322–324PubMedCrossRefGoogle Scholar
  12. 12.
    Cattivelli L, Rizza F, Badeck F-W, Mazzucotelli E, Mastrangelo AM, Francia E, Marè C, Tondelli A, Michele Stanca A (2008) Drought tolerance improvement in crop plants: an integrated view from breeding to genomics. Field Crops Res 105:1–14CrossRefGoogle Scholar
  13. 13.
    Ebercon A, Blum A, Jordan WR (1977) A rapid colorimetric method for epicuticular wax contest of sorghum leaves. Crop Sci 17:179–180CrossRefGoogle Scholar
  14. 14.
    Grammatikopoulos G, Manetas Y (1994) Direct absorption of water by hairy leaves of Phlomis fruticosa and its contribution to drought avoidance. Can J Bot 11:1805–1811CrossRefGoogle Scholar
  15. 15.
    Munné-Bosch S, Alegre L (2004) Die and let live: leaf senescence contributes to plant survival under drought stress. Funct Plant Biol 31:203–216CrossRefGoogle Scholar
  16. 16.
    Rohde A, Bhalerao RP (2007) Plant dormancy in the perennial context. Trends Plant Sci 12:217–223PubMedCrossRefGoogle Scholar
  17. 17.
    O'Toole JC, Cruz RT, Singh TN (1979) Leaf rolling and transpiration. Plant Sci Lett 16:111–114CrossRefGoogle Scholar
  18. 18.
    Pearcy RW, Ehleringer J (1984) Comparative ecophysiology of C3 and C4 plants. Plant Cell Envir 7(1):11CrossRefGoogle Scholar
  19. 19.
    Malamy JE (2005) Intrinsic and environmental response pathways that regulate root system architecture. Plant Cell Environ 28:67–77PubMedCrossRefGoogle Scholar
  20. 20.
    Sawidis T, Sofia K, Delivopoulos S (2005) The root-tuber anatomy of Asphodelus aestivus. Flora 200:332–338CrossRefGoogle Scholar
  21. 21.
    Basu S, Ramegowda V, Kumar A, Pereira A (2016) Plant adaptation to drought stress. F1000Research 5:1554CrossRefGoogle Scholar
  22. 22.
    Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930PubMedCrossRefGoogle Scholar
  23. 23.
    Singh M, Kumar J, Singh S, Singh VP, Prasad SM (2015) Roles of osmoprotectants in improving salinity and drought tolerance in plants: a review. Rev Environ Sci Biotechnol 14:407–426CrossRefGoogle Scholar
  24. 24.
    Mundree SG, Baker B, Mowla S, Peters S, Marais S, Vander Willigen C, Govender K, Maredza A, Farrant JM, Thomson JA (2002) Physiological and molecular insights into drought tolerance. Afr J Biotech 1:28–38CrossRefGoogle Scholar
  25. 25.
    Price AH, Taylor A, Ripley SJ, Griffiths A, Trewavas AJ, Knight MR (1994) Oxidative signals in tobacco increase cytosolic calcium. Plant Cell 6:1301–1310PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K et al (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol 9:436–442PubMedCrossRefGoogle Scholar
  27. 27.
    Atkinson NJ, Urwin PE (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot 63:3523–3544CrossRefGoogle Scholar
  28. 28.
    Asselbergh B, Achuo AE, Hofte M, Van Gijsegem F (2008) Abscisic acid deficiency leads to rapid activation of tomato defence responses upon infection with Erwinia chrysanthemi. Mol Plant Pathol 9:11–24PubMedGoogle Scholar
  29. 29.
    Ton J, Flors V, Mauch-Mani B (2009) The multifaceted role of ABA in disease resistance. Trends Plant Sci 14:310–317PubMedCrossRefGoogle Scholar
  30. 30.
    Camejo D, Guzman-Cedeno A, Moreno A (2016) Reactive oxygen species, essential molecules, during plant-pathogen interactions. Plant Physiol Biochem 103:10–23PubMedCrossRefGoogle Scholar
  31. 31.
    Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498PubMedCrossRefGoogle Scholar
  32. 32.
    Rodriguez MCS, Petersen M, Mundy J (2010) Mitogen-activated protein kinase signaling in plants. Annu Rev Plant Biol 61:621–649PubMedCrossRefGoogle Scholar
  33. 33.
    Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nurnberger T, Jones JDG, Felix G, Boller T (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448:497–500PubMedCrossRefGoogle Scholar
  34. 34.
    Andreasson E, Ellis B (2010) Convergence and specificity in the Arabidopsis MAPK nexus. Trends Plant Sci 15:106–113PubMedCrossRefGoogle Scholar
  35. 35.
    Miller G, Mittler R (2006) Could heat shock transcription factors function as hydrogen peroxide sensors in plants? Ann Bot 98:279–288PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Jedmowski C, Ashoub A, Beckhaus T, Berberich T, Karas M, Brüggemann W (2014) Comparative analysis of Sorghum bicolor proteome in response to drought stress and following recovery. Int J Proteomics 2014:Article ID 395905.  https://doi.org/10.1155/2014/395905CrossRefGoogle Scholar
  37. 37.
    Kimber C (2000) Origins of domesticated sorghum and its early diffusion to India and China. In: Smith CW, Frederiksen RA (eds) Sorghum: origin, history, technology, and production. John Wiley, New York, pp 3–98Google Scholar
  38. 38.
    Rooney WL, Blumenthal J, Bean B, Mullet JE (2007) Designing sorghum as a dedicated bioenergy feedstock. Biofpr 1:147–157Google Scholar
  39. 39.
    Rao PS, Vinutha KS, Kumar GSA, Chiranjeevi T, Uma A, Lal P et al (2016) Sorghum: a multipurpose bioenergy crop. In: Ciampitti I, Prasad V (eds) Sorghum: state of the art and future perspectives, agronomy monographs, vol 58. American Society of Agronomy and Crop Science Society of America, Madison, WIGoogle Scholar
  40. 40.
    Williams RJ, Rao KN (1981) A review of sorghum grain moulds. Trop Pest Manage 27:200–211CrossRefGoogle Scholar
  41. 41.
    Hilley JL, Weers BD, Truong SK, McCormick RF, Mattison AJ, McKinley BA, Morishige DT, Mullet JE (2017) Sorghum Dw2 encodes a protein kinase regulator of stem internode length. Sci Rep 7:4616PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Blum A, Arkin GF (1984) Sorghum root growth and water-use as affected by water supply and growth duration. Field Crops Res 9:131–142CrossRefGoogle Scholar
  43. 43.
    Stout DG, Simpson GM (1978) Drought resistance of Sorghum bicolor. l. Drought avoidance mechanisms related to leaf water status. Can J Plant Sci 58:213–224CrossRefGoogle Scholar
  44. 44.
    Tari I, Laskay G, Takács Z, Poór P (2013) Response of sorghum to abiotic stress: a review. J Agro Crop Sci 199:264–274CrossRefGoogle Scholar
  45. 45.
    Brauer D, Baumhardt RL (2016) Future prospects for sorghum as a water-saving crop. In: Ciampitti I, Prasad V (eds) Sorghum: state of the art and future perspectives, Agron Monogr 58. ASA and CSSA, Madison, WIGoogle Scholar
  46. 46.
    International Crops Research Institute for the Semi-Arid Tropics (ICRISAT)/Food and Agriculture Organization (FAO) (1996) The world sorghum and millet economies. ICRISAT/FAO, Patancheru/RomeGoogle Scholar
  47. 47.
    O’Brien D (2017) Domestic and international sorghum marketing. In: Ciampitti I, Prasad V (eds) Sorghum: state of the art and future perspectives. Agron Monogr 58. ASA and CSSA, Madison, WIGoogle Scholar
  48. 48.
    Thompson LM (1963) Evaluation of weather factors in the production of grain sorghums. Agron J 55:182–185CrossRefGoogle Scholar
  49. 49.
    Gale F, Hansen J, Jewison M (2014) China’s growing demand for agricultural imports, EIB-136, U.S. Department of Agriculture, Economic Research Service, February 2014Google Scholar
  50. 50.
    Jewison M, Gale F (2012) China’s market for distillers dried grains and the key influences on its longer run potential, FDS-12g-01, U.S. Department of Agriculture, Economic Research ServiceGoogle Scholar
  51. 51.
    Pratt LH, Liang C, Shah M, Sun F, Wang H, Reid SP, Gingle AR, Paterson AH, Wing R, Dean R, Klein R, Nguyen HT, Ma H-M, Zhao X, Morishige DT, Mullet JE, Cordonnier-Pratt MM (2005) Sorghum expressed sequence tags identify signature genes for drought, pathogenesis, and skotomorphogenesis from a milestone set of 16,801 unique transcripts. Plant Physiol 139:869–884PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Soares MB, Bonaldo MF (1998) Constructing and screening normalized cDNA libraries. In: Birren B, Green ED, Klapholz S, Myers RM, Roskams J (eds) Genome analysis: a laboratory manual, vol 2. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  53. 53.
    Buchanan CD, Lim S, Salzman RA, Kagiampakis I, Morishige DT, Weers BD, Klein RR, Pratt LH, Cordonnier-Pratt MM, Klein PE, Mullet JE (2005) Sorghum bicolor’s transcriptome response to dehydration, high salinity and ABA. Plant Mol Biol 58:699–720PubMedCrossRefGoogle Scholar
  54. 54.
    Temnykh S, DeClerck G, Lukashova A, Lipovich L, Cartinhour S, McCouch S (2001) Computational and experimental analysis of microsatellites in rice (Oryza sativa L.): frequency, length variation, transposon associations, and genetic marker potential. Genome Res 11:1441–1452PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Srinivas G, Satish K, Madhusudhana R, Seetharama N (2009) Exploration and mapping of microsatellite markers from subtracted drought stress ESTs in Sorghum bicolor (L.) Moench. Theor Appl Genet 118:703–717PubMedCrossRefGoogle Scholar
  56. 56.
    Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang H, Wang X, Wicker T, Bharti AK, Chapman J, Feltus FA, Gowik U, Grigoriev IV, Lyons E, Maher CA, Martis M, Narechania A, Otillar RP, Penning BW, Salamov AA, Wang Y, Zhang L, Carpita NC, Freeling M, Gingle AR, Hash CT, Keller B, Klein P, Kresovich S, McCann MC, Ming R, Peterson DG, Mehboob-ur-Rahman WD, Westhoff P, Mayer KFX, Messing J, Rokhsar DS (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556PubMedCrossRefGoogle Scholar
  57. 57.
    Dugas DV, Monaco MK, Olsen A, Klein RR, Kumari S, Ware D, Klein PE (2011) Functional annotation of the transcriptome of Sorghum bicolor in response to osmotic stress and abscisic acid. BMC Genomics 12:514–510PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Johnson SM, Lim F-L, Finkler A, Fromm H, Slabas AR, Knight MR (2014) Transcriptomic analysis of Sorghum bicolor responding to combined heat and drought stress. BMC Genomics 15:456PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Groppa MD, Tomaro ML, Benavides MP (2001) Polyamines as protectors against cadmium or copper-induced oxidative damage in sunflower leaf discs. Plant Sci 161:481–488CrossRefGoogle Scholar
  60. 60.
    Kaspar S, Peukert M, Svatos A, Matros A, Mock H-P (2011) MALDI-imaging mass spectrometry–an emerging technique in plant biology. Proteomics 11:1840–1850PubMedCrossRefGoogle Scholar
  61. 61.
    Collard BCY, Jahufer MZZ, Brouwer JB et al (2005) An introduction to markers, quantitative trait loci (QTL) mapping and marker-assisted selection for crop improvement: the basic concepts. Euphytica 142:169CrossRefGoogle Scholar
  62. 62.
    Myles S, Peiffer J, Brown PJ, Ersoz ES, Zhang Z, Costich DE, Buckler ES (2009) Association mapping: critical considerations shift from genotyping to experimental design. Plant Cell 21:2194–2202PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES et al (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One 6:e19379PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Jiao Y, Burke JJ, Chopra R, Burow G, Chen J, Wang B, Hayes C, Emendack Y, Ware D, Xin Z (2016) A sorghum mutant resource as an efficient platform for gene discovery in grasses. Plant Cell 28:1551–1562PubMedPubMedCentralGoogle Scholar
  65. 65.
    Blum A (2005) Drought resistance, water-use efficiency, and yield potential-are they compatible, dissonant, or mutually exclusive? Aust J Agric Res 56:1159–1168CrossRefGoogle Scholar
  66. 66.
    Balota M, Payne WA, Rooney W, Rosenow D (2008) Gas exchange and transpiration ratio in sorghum. Crop Sci 48:2361–2371CrossRefGoogle Scholar
  67. 67.
    Kapanigowda MH, Payne WA, Rooney WL, Mullet JE, Balota M (2014) Quantitative trait locus mapping of the transpiration ratio related to preflowering drought tolerance in sorghum (Sorghum bicolor). Func Plant Biol 41:1049–1065CrossRefGoogle Scholar
  68. 68.
    Morishige DT, Klein PE, Hilley JL, Sahraeian SME, Sharma A, Mullet JE (2013) Digital genotyping of sorghum–a diverse plant species with a large repeat-rich genome. BMC Genomics 14:448PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Lopez JR, Erickson JE, Munoz P, Saballos A, Felderhoff TJ, Vermerris W (2017) QTLs associated with crown root angle, stomatal conductance, and maturity in sorghum. Plant Genome 10(2).  https://doi.org/10.3835/plantgenome2016.04.0038CrossRefGoogle Scholar
  70. 70.
    Maurel C, Verdoucq L, Luu D-T, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. An Rev Plant Biol 59:595–624CrossRefGoogle Scholar
  71. 71.
    Lu ZJ, Neumann PM (1999) Water stress inhibits hydraulic conductance and leaf growth in rice seedlings but not the transport of water via mercury-sensitive water channels in the root. Plant Physiol 120:143–151PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Hasan SA, Rabei SH, Nada RM, Abogadallah G (2016) Water use efficiency in the drought-stressed sorghum and maize in relation to expression of aquaporin genes. Biol Plantarum 61:127–137CrossRefGoogle Scholar
  73. 73.
    Liu P, Yin L, Deng X, Wang S, Tanaka K, Zhang S (2014) Aquaporin-mediated increase in root hydraulic conductance is involved in silicon-induced improved root water uptake under osmotic stress in Sorghum bicolor L. J Exp Bot 65:4747–4756PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Koch K, Ensikat HJ (2008) The hydrophobic coatings of plant surfaces: epicuticular wax crystals and their morphologies, crystallinity and molecular self-assembly. Micron 39:759–772PubMedCrossRefGoogle Scholar
  75. 75.
    Yeats TH, Rose JKC (2013) The formation and function of plant cuticles. Plant Physiol 163:5–20PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Becker M, Kerstiens G, Schönherr J (1986) Water permeability of plant cuticles: permeance, diffusion and partition coefficients. Trees 1:54CrossRefGoogle Scholar
  77. 77.
    Kerier F, Schönherr J (1988) Permeation of lipophilic chemicals across plant cuticles: prediction from partition coefficients and molar volumes. Arch Environ Contam Toxicol 17:7–12CrossRefGoogle Scholar
  78. 78.
    Lendzian KJ (1984) Permeability of plant cuticles to gaseous air pollutants. In: Koziot MJ, Whatley FR (eds) Gaseous air pollutants and plant metabolism, vol 36. Butterworths, London, pp 77–81CrossRefGoogle Scholar
  79. 79.
    Lendzian KJ, Kerstiens G (1991) Sorption and transport of gases and vapors in plant cuticles. Rev Environ Contam Toxicol 121:65–128Google Scholar
  80. 80.
    Peters PJ, Jenks MA, Rich PJ, Axtell JD, Ejeta G (2009) Mutagenesis, selection, and allelic analysis of epicuticular wax mutants in sorghum. Crop Sci 49:1250–1258CrossRefGoogle Scholar
  81. 81.
    Uttam GA, Praveen M, Rao YV, Tonapi VA, Madhusudhana R (2017) Molecular mapping and candidate gene analysis of a new epicuticular wax locus in sorghum (Sorghum bicolor L. Moench). Theor Appl Genet 130:2109–2125PubMedCrossRefGoogle Scholar
  82. 82.
    Jenks MA, Rich PJ, Rhodes D, Ashworth EN, Axtell JD, Ding C-K (2000) Leaf sheath cuticular waxes on bloomless and sparse-bloom mutants of Sorghum bicolor. Phytochemistry 54:577–584PubMedCrossRefGoogle Scholar
  83. 83.
    Agrawal VP, Lessiere R, Stumpf PK (1984) Biosynthesis of very-long-chain fatty acids in microsomes of epidermal cells of Allium porrum L. Arch Biochem Biophys 230:580–589PubMedCrossRefGoogle Scholar
  84. 84.
    Jenks MA, Joly RJ, Peters PJ, Rich PJ, Axtell JD, Ashworth EN (1994) Chemically-induced cuticle mutation affecting epidermal conductance to water vapor and disease susceptibility in Sorghum bicolor (L.). Moench. Plant Physiol 105:1239–1245PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Jenks MA, Rich PJ, Peters PJ, Axtell JD, Ashworth EN (1992) Epicuticular wax morphology of bloomless (bm) mutants in Sorghum bicolor. Int J Plant Sci 153:311–319CrossRefGoogle Scholar
  86. 86.
    Jordan WR, Shouse PJ, Blum A, Miller FR, Monk RL (1984) Environmental physiology of sorghum: II. Epicuticular wax load and cuticular transpiration. Crop Sci 24:1168–1173CrossRefGoogle Scholar
  87. 87.
    Peterson GC, Suksayretrup K, Weibel DE (1982) Inheritance of some bloomless and sparse-bloom mutants in sorghum. Crop Sci 22:63–67CrossRefGoogle Scholar
  88. 88.
    Burow GB, Franks CD, Xin Z (2008) Genetic and physiological analysis of an irradiated bloomless mutant (epicuticular wax mutant) of sorghum. Crop Sci 48:41–48CrossRefGoogle Scholar
  89. 89.
    Burow GB, Franks CD, Acosta-Martinez V, Xin ZG (2009) Molecular mapping and characterization of BLMC, a locus for profuse wax (bloom) and enhanced cuticular features of sorghum (Sorghum bicolor (L.) Moench.). Theor Appl Genet 118:423–431PubMedCrossRefGoogle Scholar
  90. 90.
    Punnuri S, Harris-Shultz K, Knoll J, Ni X, Wang H (2017) The genes Bm2 and Blmc that affect epicuticular wax deposition in sorghum are allelic. Crop Sci 57:1552–1556CrossRefGoogle Scholar
  91. 91.
    Reina JJ, Guerrero C, Heredia A (2007) Isolation, characterization, and localization of AgaSGNH cDNA: a new SGNH-motif plant hydrolase specific to Agave americana L. Leaf epidermis. J Exp Bot 58:2717–2731PubMedCrossRefGoogle Scholar
  92. 92.
    Mizuno H, Kawahigashi H, Ogata J et al (2013) Genomic inversion caused by gamma irradiation contributes to downregulation of a WBC11 homolog in bloomless sorghum. Theor Appl Genet 126:1513–1520PubMedCrossRefGoogle Scholar
  93. 93.
    Hülskamp M, Miséra S, Jürgens G (1994) Genetic dissection of trichome cell development in Arabidopsis. Cell 76:555–566PubMedCrossRefGoogle Scholar
  94. 94.
    Inamdar JA, Gangadhara M (1977) Studies on the trichomes of some Euphorbiaceae. Feddes Repert 88:103–111CrossRefGoogle Scholar
  95. 95.
    Ehleringer JR (1984) Ecology and ecophysiology of leaf pubescence in North American desert plants. In: Rodriguez E, Healy PL, Mehta I (eds) Biology and chemistry of plant trichomes. Plenum Press, New York, pp 113–132CrossRefGoogle Scholar
  96. 96.
    Levin DA (1973) The role of trichomes in plant defense. Q Rev Biol 48:3–15CrossRefGoogle Scholar
  97. 97.
    Buta JG, Lusby WR, Neal JW, Waters RM, Pittarelli GW (1993) Sucrose esters from Nicotianan gossei active against the greenhouse whitefly Trialeuroides vaporariorum. Phytochemistry 32:859–864CrossRefGoogle Scholar
  98. 98.
    Ehleringer JR, Björkman O, Mooney HA (1976) Leaf pubescence: effects on absorbance and photosynthesis in a desert shrub. Science 192:376–377PubMedCrossRefGoogle Scholar
  99. 99.
    Brewer CA, Smith WK, Vogelmann TC (1991) Functional interaction between leaf trichomes, leaf wettability and the optical properties of water droplets. Plant Cell Environ 14:955–962CrossRefGoogle Scholar
  100. 100.
    Gonzáles WL, Negritto MA, Suárez LH, Gianoli E (2008) Induction of glandular and non-glandular trichomes by damage in leaves of Madia sativa under contrasting water regimes. Acta Oecol 33:128–132CrossRefGoogle Scholar
  101. 101.
    Schreuder MDJ, Brewer CA, Heine C (2001) Modelled influences of non-exchanging trichomes on leaf boundary layers and gas exchange. J Theor Biol 210:23–32PubMedCrossRefGoogle Scholar
  102. 102.
    Satish K, Srinivas G, Madhusudhana R, Padmaja PG, Reddy RN, Mohan SM et al (2009) Identification of quantitative trait loci for resistance to shoot fly in sorghum [Sorghum bicolor (L.) Moench]. Theor Appl Genet 119:1425–1439PubMedCrossRefGoogle Scholar
  103. 103.
    Singh V, van Oosterom EJ, Jordan DR, Messina CD, Cooper M, Hammer GL (2010) Morphological and architectural development of root systems in sorghum and maize. Plant Soil 333:287–299CrossRefGoogle Scholar
  104. 104.
    Trachsel S, Kaeppler SM, Brown KM, Lynch JP (2011) Shovelomics: high throughput phenotyping of maize (Zea mays L.) root architecture in the field. Plant Soil 341:75–87CrossRefGoogle Scholar
  105. 105.
    Singh V, van Oosterom EJ, Jordan DR, Hammer GL (2012) Genetic control of nodal root angle in sorghum and its implications on water extraction. Eur J Agron 42:3–10CrossRefGoogle Scholar
  106. 106.
    Clark RT, Famoso AN, Zhao K, Shaff JE, Craft EJ, Bustamante CD, McCouch SR, Aneshansley DJ, Kochian LV (2013) High-throughput two-dimensional root system phenotyping platform facilitates genetic analysis of root growth and development. Plant Cell Environ 36:454–466PubMedCrossRefGoogle Scholar
  107. 107.
    Le Marié C, Kirchgessner N, Marschall D, Walter A, Hund A (2014) Rhizoslides: paper-based growth system for non-destructive, high throughput phenotyping of root development by means of image analysis. Plant Meth 10:13CrossRefGoogle Scholar
  108. 108.
    Mace ES, Singh V, Van Oosterom EJ, Hammer GL, Hunt CH, Jordan DR (2012) QTL for nodal root angle in sorghum (Sorghum bicolor L. Moench) co-locate with QTL for traits associated with drought adaptation. Theor Appl Genet 124:97–109PubMedCrossRefGoogle Scholar
  109. 109.
    Joshi DC, Singh V, Hunt C, Mace E, van Oosterom E, Sulman R, Jordan D, Hammer G (2017) Development of a phenotyping platform for high throughput screening of nodal root angle in sorghum. Plant Meth 13:56CrossRefGoogle Scholar
  110. 110.
    Rajkumar FB, Kavil SP, Girma Y, Arun SS, Dadakhalandar D, Gurusiddesh BH, Patil AM, Thudi M, Bhairappanavar SB, Narayana YD, Krishnaraj PU, Khadi BM, Kamatar MY (2013) Molecular mapping of genomic regions harbouring QTLs for root and yield traits in sorghum (Sorghum bicolor L. Moench). Physiol Mol Biol Plants 19:409–419PubMedPubMedCentralCrossRefGoogle Scholar
  111. 111.
    Li R, Han Y, Lv P, Du R, Liu G (2014) Molecular mapping of the brace root traits in sorghum (Sorghum bicolor L. Moench). Breeding Sci 64:193–198CrossRefGoogle Scholar
  112. 112.
    Coskun D, Britto DT, Huynh WQ, Kronzucker HJ (2016) The role of silicon in higher plants under salinity and drought stress. Front Plant Sci 7:1072PubMedPubMedCentralCrossRefGoogle Scholar
  113. 113.
    Soukup M, Martinka M, Bosnic D, Caplovicova M, Elbaum R, Lux A (2017) Formation of silica aggregates in sorghum root endodermis is predetermined by cell wall architecture and development. Ann Bot 120:739–753PubMedPubMedCentralCrossRefGoogle Scholar
  114. 114.
    Lux A, Luxova M, Hattori T, Inanaga S, Sugimoto Y (2002) Silicification in sorghum (Sorghum bicolor) cultivars with different drought tolerance. Physiol Plantarum 115:87–92CrossRefGoogle Scholar
  115. 115.
    McNeil SD, Nuccio ML, Hanson AD (1999) Betaines and related osmoprotectants. Targets for metabolic engineering of stress resistance. Plant Physiol 120:945–949PubMedPubMedCentralCrossRefGoogle Scholar
  116. 116.
    Nuccio ML, Rhodes D, McNeil SD, Hanson AD (1999) Metabolic engineering of plants for osmotic stress resistance. Curr Opin Plant Biol 2:128–134PubMedCrossRefGoogle Scholar
  117. 117.
    Mickelbart MV, Peel G, Joly RJ, Rhodes D, Ejeta G, Goldsbrough PB (2003) Development and characterization of near-isogenic lines of sorghum segregating for glycinebetaine accumulation. Physiol Plantarum 118:253–261CrossRefGoogle Scholar
  118. 118.
    Castro NS, Ortiz-Cereceres J, Mendoza-Castillo MD, Huerta AJ, Trejo-Lopez C, Zavala-Garcia F, Martinez-Garza A (2003) Accumulation of proline in leaves of sorghum genotypes (Sorghum bicolor L. Moench) which differ in their response to drought. Phyton Int J Exp Bot 72:49–57Google Scholar
  119. 119.
    Burke JJ, Payton P, Chen J, Xin Z, Burow G, Hayes C (2015) Metabolic responses of two contrasting sorghums to water-deficit stress. Crop Sci 55:344–353CrossRefGoogle Scholar
  120. 120.
    Nxele X, Klein A, Ndimba BK (2017) Drought and salinity stress alters ROS accumulation, water retention, and osmolyte content in sorghum plants. S Afr J Bot 108:261–266CrossRefGoogle Scholar
  121. 121.
    Yang W-J, Nadolska-Orczyk A, Wood KV, Hahn DT, Rich PJ, Wood AJ, Saneoka H, Premachandra GS, Bonham CC, Rhodes JC, Joly RJ, Samaras Y, Goldsbrough PB, Rhodes D (1995) Near-isogenic lines of maize differing for glycinebetaine. Plant Physiol 107:621–630PubMedPubMedCentralCrossRefGoogle Scholar
  122. 122.
    Yang W-J, Rich PJ, Axtell JD, Wood KV, Bonham CC, Ejeta G, Mickelbart MV, Rhodes D (2003) Genotypic variation for glycinebetaine in Sorghum bicolor. Crop Sci 43:162–169CrossRefGoogle Scholar
  123. 123.
    Peel GJ, Mickelbart MV, Rhodes D (2010) Choline metabolism in glycinebetaine accumulating and non-accumulating near-isogenic lines of Zea mays and Sorghum bicolor. Phytochemistry 71:404–414PubMedCrossRefGoogle Scholar
  124. 124.
    Rosenow DT, Quisenberry JE, Wendt CW, Clark LE (1983) Drought tolerant sorghum and cotton germplasm. Dev Agric Managed-For Ecol 12:207–222Google Scholar
  125. 125.
    Tuinstra MR, Grote EM, Goldsbrough PB, Ejeta G (1996) Identification of quantitative trait loci associated with pre-flowering drought tolerance in sorghum. Crop Sci 36:1337–1344CrossRefGoogle Scholar
  126. 126.
    Ludlow MM, Muchow RC (1990) A critical evaluation of traits for improving crop yields in water-limited environments. Adv Agron 43:107–153CrossRefGoogle Scholar
  127. 127.
    Kebede H, Subudhi PK, Rosenow DT, Nguyen HT (2001) Quantitative trait loci influencing drought tolerance in grain sorghum (Sorghum bicolor L. Moench). Theor Appl Genet 103:266–276CrossRefGoogle Scholar
  128. 128.
    Borrell AK, Hammer GL, Douglas ACL (2000) Does maintaining green leaf area in sorghum improve yield under drought? I. leaf growth and senescence. Crop Sci 40:1026–1037CrossRefGoogle Scholar
  129. 129.
    Borrell AK, Hammer GL, Henzell RG (2000) Does maintaining green leaf area in sorghum improve yield under drought? II. Dry matter production and yield. Crop Sci 40:1037–1048CrossRefGoogle Scholar
  130. 130.
    Rosenow DT, Ejeta G, Clark LE, Gilbert ML, Henzell RG, Borrell AK, Muchow RC (1996) Breeding for pre- and post-flowering drought stress resistance in sorghum. In: Rosenow D (ed) The international conference on genetic improvement of sorghum and millet, Lubbock, TX. 23–27 Sept 1996. Publication No. 97–5. International Sorghum and Millet, Lincoln, NE. p 400–424Google Scholar
  131. 131.
    Jordan DR, Hunt CH, Cruickshank AW, Borrell AK, Henzell RG (2012) The relationship between the stay-green trait and grain yield in elite sorghum hybrids grown in a range of environments. Crop Sci 52:1153–1161CrossRefGoogle Scholar
  132. 132.
    Rosenow DT, Clark LE (1981) Drought tolerance in sorghum. In: Loden HD, Wilkinson D (eds) Proceedings of the Annual Corn and Sorghum Industry Research Conference–American Seed Trade Association, Corn and Sorghum Division, Corn and Sorghum Research Conference, Washington, DC. 9–11 Dec. 1981. American Seed Trade Association, Alexandria, VA. p 18–30Google Scholar
  133. 133.
    Borrell AK, Hammer GL (2000) Nitrogen dynamics and the physiological basis of stay-green in sorghum. Crop Sci 40:129501307Google Scholar
  134. 134.
    Borell AK, Hammer G, Van Oosterom E (2001) Stay-green: a consequence of the balance between supply and demand for nitrogen during grain filling? Ann Appl Biol 138:91–95CrossRefGoogle Scholar
  135. 135.
    Thomas H, Ougham H, Canter P, Donnison I (2002) What stay-green mutants tell us about the nitrogen remobilization in leaf senescence. J Exp Bot 53(370)Google Scholar
  136. 136.
    Tuinstra MR, Grote EM, Goldsbrough PB, Ejeta G (1997) Genetic analysis of post-flowering drought tolerance and components of grain development in Sorghum bicolor (L.) Moench. Mol Breed 3:439–448CrossRefGoogle Scholar
  137. 137.
    Crasta OR, Xu WW, Rosenow DT, Mullet J, Nguyen HT (1999) Mapping of post-flowering drought resistance traits in grain sorghum: association between QTLs influencing premature senescence and maturity. Mol Gen Genet 262(3):579–588PubMedCrossRefGoogle Scholar
  138. 138.
    Subudhi PK, Rosenow DT, Nguyen HT (2000) Quantitative trait loci for the stay green trait in sorghum (Sorghum bicolor L. Moench): consistency across genetic backgrounds and environments. Theor Appl Genet 101:733–741CrossRefGoogle Scholar
  139. 139.
    Tao YZ, Henzell RG, Jordan DR, Butler DG, Kelly AM, McIntyre CL (2000) Identification of genomic regions associated with stay green in sorghum by testing RILs in multiple environments. Theor Appl Genet 100:1225–1232CrossRefGoogle Scholar
  140. 140.
    Xu W, Rosenow DT, Nguyen HT (2000a) Stay green trait in grain sorghum: relationship between visual rating and leaf chlorophyll concentration. Plant Breed 119:365–367CrossRefGoogle Scholar
  141. 141.
    Xu W, Subudhi PK, Crasta OR, Rosenow DT, Mullet JE, Nguyen HT (2000b) Molecular mapping of QTLs conferring stay-green in grain sorghum (Sorghum bicolor L. Moench). Genome 43:461–469PubMedCrossRefGoogle Scholar
  142. 142.
    Haussmann BIG, Mahalakshmi V, Reddy BVS, Seetharama N, Hash CT, Geiger HH (2002) QTL mapping of stay-green in two sorghum recombinant inbred populations. Theor Appl Genet 106:133–142PubMedCrossRefGoogle Scholar
  143. 143.
    Harris K (2007) Genetic analysis of the sorghum bicolor stay-green drought tolerance trait. Dissertation, Texas A&M University, College Station, TXGoogle Scholar
  144. 144.
    Walula RS, Rosenow DT, Wester DB, Nguyen H (1994) Inheritance of the stay-green trait in sorghum. Crop Sci 34:970–972CrossRefGoogle Scholar
  145. 145.
    Mace ES, Jordan DR (2010) Location of major effect genes in sorghum (Sorghum bicolor (L.) Moench). Theor Appl Genet 121:1339–1356PubMedCrossRefGoogle Scholar
  146. 146.
    Weers B (2011) Integrated analysis of phenology, traits, and QTL in the drought tolerant sorghum genotypes BTx642 and RTx7000. Dissertation, Texas A&M University, College Station, TXGoogle Scholar
  147. 147.
    Harris K, Subudhi P, Borrell A, Jordan D, Rosenow D, Nguyen H, Klein P, Klein R, Mullet J (2006) Sorghum stay-green QTL individually reduce post-flowering drought induced leaf senescence. J Exp Bot 58:327–338PubMedCrossRefGoogle Scholar
  148. 148.
    Borrell AK, Mullet JE, George-Jaeggli B, Oosterom EJV, Hammer GL, Klein PE, Jordan DR (2014) Drought adaptation of stay-green sorghum is associated with canopy development, leaf anatomy, root growth, and water uptake. J Exp Bot 65:6251–6263PubMedPubMedCentralCrossRefGoogle Scholar
  149. 149.
    Hayes CM, Weers B, Thakran M, Burow G, Xin Z, Emendack Y, Burke JJ, Rooney WL, Mullet JE (2015) Discovery of a dhurrin QTL in Sorghum bicolor: co-localization of dhurrin biosynthesis and a novel stay-green QTL. Crop Sci 56:104–112CrossRefGoogle Scholar
  150. 150.
    Gleadow RM, Møller BL (2014) Cyanogenic glycosides: synthesis, physiology, and phenotypic plasticity. Annu Rev Plant Biol 65:155–195PubMedCrossRefGoogle Scholar
  151. 151.
    Sakhi S, Shehzad T, Rehman S, Okuno K (2013) Mapping the QTLs underlying drought stress at developmental stage of sorghum (Sorghum bicolor (L.) Moench) by association analysis. Euphytica 193:433–450CrossRefGoogle Scholar
  152. 152.
    Upadhyaya HD, Dwivedi SL, Wang Y, Vetriventhan M (2016) Sorghum genetic resources. In: Ciampitti I, Prasad V (eds) Sorghum: state of the art and future perspectives. Agron Monogr, vol 58. ASA and CSSA, Madison, WIGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Karen R. Harris-Shultz
    • 1
    Email author
  • Chad M. Hayes
    • 2
  • Joseph E. Knoll
    • 1
  1. 1.Crop Genetics and Breeding Research UnitUSDA-ARSTiftonUSA
  2. 2.Plant Stress and Germplasm Development ResearchUSDA-ARSLubbockUSA

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