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Differential responses of sorghum genotypes to drought stress revealed by physio-chemical and transcriptional analysis

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Abstract

Sorghum is an essential food crop for millions of people in the semi-arid regions of the world, where its production is severely limited by drought stress. Drought in the early stages of crop growth and development irreversibly interferes, which leads to poor yield. The effect of drought stress in sorghum was studied at physiological, biochemical, and molecular levels in a set of two genotypes differing in their tolerance to drought. Drought stress was imposed by restraining water for 10 days on 25 days old seedlings. A significant influence of water stress was observed on the considered morpho-physiological and biochemical traits. The genotype DRT1019 exhibited physiological and biochemical indicators of drought avoidance through delayed leaf rolling, osmotic adjustment, ideal gas-exchange system, solute accumulation, an increased level of enzyme synthesis and root trait expression as compared to the ICSV95022 genotype. Furthermore, differences in the metabolite changes viz. total carbohydrate, total amides, and lipids were found between the two genotypes under drought stress. In addition, transcript profiling of potential candidate drought genes such as SbTIP3-1, SbDHN1, SbTPS, and SbDREB1A revealed up-regulation in DRT1019, which corresponded with other important physiological and biochemical parameters exhibited in the genotype. In conclusion, this study provides an improved understanding of whole plant response to drought stress in sorghum. Additionally, our results provide promising candidate genes for drought tolerance in sorghum that can be used as potential markers for drought tolerance breeding programs.

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References

  1. Comas L, Becker S, Cruz VMV et al (2013) Root traits contributing to plant productivity under drought. Front Plant Sci 4:442

    Article  PubMed  PubMed Central  Google Scholar 

  2. Wang Y, Ying J, Kuzma M et al (2005) Molecular tailoring of farnesylation for plant drought tolerance and yield protection. Plant J 43:413–424

    Article  CAS  PubMed  Google Scholar 

  3. McGuire S (2000) Farmers’ management of sorghum diversity in eastern Ethiopia. In: Encouraging diversity: the conservation and development of plant genetic resources. Intermediate Technology Publications, London, pp 43–48

    Google Scholar 

  4. ICRISAT (2012) ICRISAT annual report 2011. ICRISAT, Hyderabad

    Google Scholar 

  5. Derese SA, Shimelis H, Laing M, Mengistu F (2018) The impact of drought on sorghum production, and farmer’s varietal and trait preferences, in the north eastern Ethiopia: implications for breeding. ActaAgricScand Sect B Soil Plant Sci 68:424–436. https://doi.org/10.1080/09064710.2017.1418018

    Article  CAS  Google Scholar 

  6. Badigannavar A, Teme N, de Oliveira AC et al (2018) Physiological, genetic and molecular basis of drought resilience in sorghum [Sorghum bicolor (L.) Moench]. Indian J Plant Physiol 23:670–688. https://doi.org/10.1007/s40502-018-0416-2

    Article  CAS  Google Scholar 

  7. Baalbaki RZ, Zurayk RA, Bleik MM, Talhouk SN (1999) Germination and seedling development of drought tolerant and susceptible wheat under moisture stress. Seed SciTechnol 27:291–302

    Google Scholar 

  8. Ji XM, Raveendran M, Oane R et al (2005) Tissue-specific expression and drought responsiveness of cell-wall invertase genes of rice at flowering. Plant MolBiol 59:945–964

    CAS  Google Scholar 

  9. Burke JJ, Franks CD, Burow G, Xin Z (2010) Selection system for the stay-green drought tolerance trait in sorghum germplasm. Agron J 102:1118–1122

    Article  Google Scholar 

  10. Borrell A, Jordan D, Mullet J et al (2006) Drought adaptation in sorghum. In: Drought adaptation in cereals. Haworth Press Inc, Philadelphia, pp 335–399

    Google Scholar 

  11. Dingkuhn M, Audebert AY, Jones MP et al (1999) Control of stomatal conductance and leaf rolling in O. sativa and O. glaberrima upland rice. F Crop Res 61:223–236

    Article  Google Scholar 

  12. Hsiao TC, O’Toole JC, Yambao EB, Turner NC (1984) Influence of osmotic adjustment on leaf rolling and tissue death in rice (Oryza sativa L.). Plant Physiol 75:338–341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Izanloo A, Condon AG, Langridge P et al (2008) Different mechanisms of adaptation to cyclic water stress in two South Australian bread wheat cultivars. J Exp Bot 59:3327–3346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Farooq M, Wahid A, Kobayashi N et al (2009) Plant drought stress: effects, mechanisms and management. In: Sustainable agriculture. Springer, Berlin, pp 153–188

    Chapter  Google Scholar 

  15. Siddique MRB, Hamid A, Islam MS (2000) Drought stress effects on water relations of wheat. Bot Bull Acad Sin 41:35–39

    Google Scholar 

  16. Kavi Kishor PB, Sreenivasulu N (2014) Is proline accumulation per se correlated with stress tolerance or is proline homeostasis a more critical issue? Plant Cell Environ 37:300–311

    Article  CAS  PubMed  Google Scholar 

  17. Kishor PBK, Sangam S, Amrutha RN et al (2005) Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. CurrSci 88:424–438

    CAS  Google Scholar 

  18. Shankar A, Singh A, Kanwar P et al (2013) Gene expression analysis of rice seedling under potassium deprivation reveals major changes in metabolism and signaling components. PLoS ONE 8:e70321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Yang Z, Chi X, Guo F et al (2020) SbWRKY30 enhances the drought tolerance of plants and regulates a drought stress-responsive gene, SbRD19, in sorghum. J Plant Physiol 246:153142

    Article  PubMed  Google Scholar 

  20. Ghatak A, Chaturvedi P, Weckwerth W (2017) Cereal crop proteomics: systemic analysis of crop drought stress responses towards marker-assisted selection breeding. Front Plant Sci 8:757

    Article  PubMed  PubMed Central  Google Scholar 

  21. Fetter K, Van Wilder V, Moshelion M, Chaumont F (2004) Interactions between plasma membrane aquaporins modulate their water channel activity. Plant Cell 16:215–228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Gosal SS, Wani SH, Kang MS (2009) Biotechnology and drought tolerance. J Crop Improv 23:19–54

    Article  CAS  Google Scholar 

  23. Agarwal PK, Agarwal P, Reddy MK, Sopory SK (2006) Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep 25:1263–1274

    Article  CAS  PubMed  Google Scholar 

  24. Finkelstein RR, Lynch TJ (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12:599–609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Tyerman SD, Niemietz CM, Bramley H (2002) Plant aquaporins: multifunctional water and solute channels with expanding roles. Plant Cell Environ 25:173–194

    Article  CAS  PubMed  Google Scholar 

  26. Fracasso A, Trindade L, Amaducci S (2016) Drought tolerance strategies highlighted by two Sorghum bicolor races in a dry-down experiment. J Plant Physiol 190:1–14

    Article  CAS  PubMed  Google Scholar 

  27. El-Bashiti T, Hamamcı H, Öktem HA, Yücel M (2005) Biochemical analysis of trehalose and its metabolizing enzymes in wheat under abiotic stress conditions. Plant Sci 169:47–54

    Article  CAS  Google Scholar 

  28. Augustine SM, Syamaladevi DP, Premachandran MN et al (2015) Physiological and molecular insights to drought responsiveness in Erianthusspp. Sugar Tech 17:121–129

    Article  CAS  Google Scholar 

  29. Mir RR, Zaman-Allah M, Sreenivasulu N et al (2012) Integrated genomics, physiology and breeding approaches for improving drought tolerance in crops. TheorAppl Genet 125:625–645

    Article  CAS  Google Scholar 

  30. Gregersen PL, Culetic A, Boschian L, Krupinska K (2013) Plant senescence and crop productivity. Plant MolBiol 82:603–622

    CAS  Google Scholar 

  31. Rajarajan K (2017) Studies on drought tolerance mechanisms and identification of differentially regulated drought responsive candidate genes in sorghum (Sorghum bicolor). Tamil Nadu Agricultural University, Coimbatore

    Google Scholar 

  32. O’Toole JC, Cruz RT (1980) Response of leaf water potential, stomatal resistance, and leaf rolling to water stress. Plant Physiol 65:428–432

    Article  PubMed  PubMed Central  Google Scholar 

  33. Barrs HD, Weatherley PE (1962) A re-examination of the relative turgidity technique for estimating water deficits in leaves. Aust J BiolSci 15:413–428

    Article  Google Scholar 

  34. Resende RS, Rodrigues FÁ, Cavatte PC et al (2012) Leaf gas exchange and oxidative stress in sorghum plants supplied with silicon and infected by Colletotrichum sublineolum. Phytopathology 102:892–898

    Article  CAS  PubMed  Google Scholar 

  35. Ebercon A, Blum A, Jordan WR (1977) A rapid colorimetric method for epicuticular wax contest of sorghum leaves 1. Crop Sci 17:179–180

    Article  Google Scholar 

  36. Ball RA, Oosterhuis DM (2005) Measurement of root and leaf osmotic potential using the vapor-pressure osmometer. Environ Exp Bot 53:77–84

    Article  Google Scholar 

  37. Hageman RH, Hucklesby DP (1971) [45] Nitrate reductase from higher plants. In: Methods in enzymology. Elsevier, Amsterdam, pp 491–503

    Google Scholar 

  38. Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  39. Ogbaga CC, Stepien P, Dyson BC et al (2016) Biochemical analyses of sorghum varieties reveal differential responses to drought. PLoS ONE 11:1–20. https://doi.org/10.1371/journal.pone.0154423

    Article  CAS  Google Scholar 

  40. Allwood JW, Ellis DI, Goodacre R (2008) Metabolomic technologies and their application to the study of plants and plant–host interactions. Physiol Plant 132:117–135

    CAS  PubMed  Google Scholar 

  41. Correia I, Nunes A, Barros AS, Delgadillo I (2008) Protein profile and malt activity during sorghum germination. J Sci Food Agric 88:2598–2605

    Article  CAS  Google Scholar 

  42. Ellis DI, Goodacre R (2006) Metabolic fingerprinting in disease diagnosis: biomedical applications of infrared and Raman spectroscopy. Analyst 131:875–885

    Article  CAS  PubMed  Google Scholar 

  43. Chomzynski P (1987) Single-step method of RNA isolation by acid guanidiniumthiocyanate-phenol-chloroform extraction. Anal Biochem 162:156–159

    Article  Google Scholar 

  44. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. In: Bioinformatics methods and protocols. Springer, Berlin, pp 365–386

    Google Scholar 

  45. Kozera B, Rapacz M (2013) Reference genes in real-time PCR. J Appl Genet 54:391–406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Devnarain N, Crampton BG, Chikwamba R et al (2016) Physiological responses of selected African sorghum landraces to progressive water stress and re-watering. S Afr J Bot 103:61–69

    Article  Google Scholar 

  47. Sheoran S, Thakur V, Narwal S et al (2015) Differential activity and expression profile of antioxidant enzymes and physiological changes in wheat (Triticum aestivum L.) under drought. ApplBiochemBiotechnol 177:1282–1298. https://doi.org/10.1007/s12010-015-1813-x

    Article  CAS  Google Scholar 

  48. Kadioglu A, Terzi R (2007) A dehydration avoidance mechanism: leaf rolling. Bot Rev 73:290–302

    Article  Google Scholar 

  49. Rauf S, Al-Khayri JM, Zaharieva M et al (2016) Breeding strategies to enhance drought tolerance in crops. In: Advances in plant breeding strategies: agronomic, abiotic and biotic stress traits. Springer, Berlin, pp 397–445

    Chapter  Google Scholar 

  50. Hendry GAF, Price AH (1993) Stress indicators: chlorophylls and carotenoids. Chapman Hall, London

    Google Scholar 

  51. Al-Hamdani SH, Barger TW (2003) Influence of water stress on selected physiological responses of three sorghum genotypes. Italy J Agron 7:15–22

    Google Scholar 

  52. Ahmed F, Rafii MY, Ismail MR et al (2013) Waterlogging tolerance of crops: Breeding, mechanism of tolerance, molecular approaches, and future prospects. Biomed Res Int. https://doi.org/10.1155/2013/963525

    Article  PubMed  PubMed Central  Google Scholar 

  53. Kapanigowda MH (2011) Quantitative trait locus (QTL) mapping of transpiration efficiency related to pre-flower drought tolerance in sorghum [Sorghum bicolor (L.) Moench]. Texas A&M University, College Station

    Google Scholar 

  54. Xu W, Subudhi PK, Crasta OR et al (2000) Molecular mapping of QTLs conferring stay-green in grain sorghum (Sorghum bicolor L. Moench). Genome 43:461–469

    Article  CAS  PubMed  Google Scholar 

  55. Altinkut A, Kazan K, Ipekci Z, Gozukirmizi N (2001) Tolerance to paraquat is correlated with the traits associated with water stress tolerance in segregating F2 populations of barley and wheat. Euphytica 121:81

    Article  Google Scholar 

  56. Patwari P, Salewski V, Gutbrod K et al (2019) Surface wax esters contribute to drought tolerance in Arabidopsis. Plant J 98:727–744

    Article  CAS  PubMed  Google Scholar 

  57. Ludlow MM, Muchow RC (1990) A critical evaluation of traits for improving crop yields in water-limited environments. In: Advances in agronomy. Elsevier, Amsterdam, pp 107–153

    Google Scholar 

  58. Keyvan S (2010) The effects of drought stress on yield, relative water content, proline, soluble carbohydrates and chlorophyll of bread wheat cultivars. J Anim Plant Sci 8:1051–1060

    Google Scholar 

  59. Tsuji W, Ali MEK, Inanaga S, Sugimoto Y (2003) Growth and gas exchange of three sorghum cultivars under drought stress. Biol Plant 46:583–587

    Article  Google Scholar 

  60. Sinclair TR, Hammer GL, Van Oosterom EJ (2005) Potential yield and water-use efficiency benefits in sorghum from limited maximum transpiration rate. Funct Plant Biol 32:945–952

    Article  PubMed  Google Scholar 

  61. Ouyang W, Struik PC, Yin X, Yang J (2017) Stomatal conductance, mesophyll conductance, and transpiration efficiency in relation to leaf anatomy in rice and wheat genotypes under drought. J Exp Bot 68:5191–5205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Jordan WR, Shouse PJ, Blum A et al (1984) Environmental physiology of Sorghum. II. Epicuticular wax load and cuticular transpiration 1. Crop Sci 24:1168–1173

    Article  Google Scholar 

  63. Blum A (2017) Osmotic adjustment is a prime drought stress adaptive engine in support of plant production. Plant Cell Environ 40:4–10

    Article  CAS  PubMed  Google Scholar 

  64. Verslues PE (2019) Understanding plant water potential and drought response. Plant Cell Suppl comment http://www.plantcell.org/content/plantcell/suppl/2019/03/01/tpc18

  65. Price AH, Cairns JE, Horton P et al (2002) Linking drought-resistance mechanisms to drought avoidance in upland rice using a QTL approach: progress and new opportunities to integrate stomatal and mesophyll responses. J Exp Bot 53:989–1004

    Article  CAS  PubMed  Google Scholar 

  66. Habyarimana E, Laureti D, De Ninno M, Lorenzoni C (2004) Performances of biomass sorghum [Sorghum bicolor (L.) Moench] under different water regimes in Mediterranean region. Ind Crops Prod 20:23–28

    Article  Google Scholar 

  67. Nour AM, Weibel DE (1978) Evaluation of root characteristics in grain Sorghum 1. Agron J 70:217–218

    Article  Google Scholar 

  68. Plaut ZVI (1974) Nitrate reductase activity of wheat seedlings during exposure to and recovery from water stress and salinity. Physiol Plant 30:212–217

    Article  CAS  Google Scholar 

  69. Sinha SK, Nicholas DJD (1981) Nitrate reductase. In: The physiology and biochemistry of drought resistance in plants. Academic Press, Sydney, pp 145–169

    Google Scholar 

  70. Sivaramakrishnan S, Patell VZ, Flower DJ, Peacock JM (1988) Proline accumulation and nitrate reductase activity in contrasting sorghum lines during mid-season drought stress. Physiol Plant 74:418–426

    Article  CAS  Google Scholar 

  71. Rivas-Ubach A, Sardans J, Pérez-Trujillo M et al (2012) Strong relationship between elemental stoichiometry and metabolome in plants. ProcNatlAcadSci 109:4181–4186

    Article  CAS  Google Scholar 

  72. Silvente S, Sobolev AP, Lara M (2012) Metabolite adjustments in drought tolerant and sensitive soybean genotypes in response to water stress. PLoS ONE 7:e38554

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Suseela V, Tharayil N, Xing B, Dukes JS (2015) Warming and drought differentially influence the production and resorption of elemental and metabolic nitrogen pools in Quercus rubra. Glob Chang Biol 21:4177–4195

    Article  PubMed  Google Scholar 

  74. Nuccio ML, Wu J, Mowers R et al (2015) Expression of trehalose-6-phosphate phosphatase in maize ears improves yield in well-watered and drought conditions. Nat Biotechnol 33:862–869

    Article  CAS  PubMed  Google Scholar 

  75. Li H-W, Zang B-S, Deng X-W, Wang X-P (2011) Overexpression of the trehalose-6-phosphate synthase gene OsTPS1 enhances abiotic stress tolerance in rice. Planta 234:1007–1018

    Article  CAS  PubMed  Google Scholar 

  76. Taiz L, Zeiger E (2006) Stress physiology. In: Plant physiology, 4th edn. Sinauer Associates Inc, Sunderland

    Google Scholar 

  77. Lorenz WW, Alba R, Yu Y-S et al (2011) Microarray analysis and scale-free gene networks identify candidate regulators in drought-stressed roots of loblolly pine (P. taeda L.). BMC Genom 12:264

    Article  CAS  Google Scholar 

  78. Dubouzet JG, Sakuma Y, Ito Y et al (2003) OsDREB genes in rice, Oryzasativa L., encode transcription activators that function in drought-, high-salt-and cold-responsive gene expression. Plant J 33:751–763

    Article  CAS  PubMed  Google Scholar 

  79. Hoth S, Morgante M, Sanchez J-P et al (2002) Genome-wide gene expression profiling in Arabidopsis thaliana reveals new targets of abscisic acid and largely impaired gene regulation in the abi1-1 mutant. J Cell Sci 115:4891–4900

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors are grateful to Director, Centre for Plant Molecular Biology and Biotechnology, Tamil Nadu Agricultural University, Coimbatore, India and Indian Council of Agricultural Research (ICAR), New Delhi, India, for facilities to complete this work. We thank Dr. Bharathi Raja Ramadoss for helping with proof-editing and polishing the manuscript.

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  1. K. Rajarajan

    Present address: ICAR Central Agroforestry Research Institute, Jhansi, India

Authors and Affiliations

  1. Tamil Nadu Agricultural University, Coimbatore, India

    K. Rajarajan, K. Ganesamurthy, M. Raveendran, P. Jeyakumar, A. Yuvaraja & C. Senthilraja

  2. Agriculture and Agri-Food Canada (AAFC), 107 Science Place, Saskatoon, SK, S7N 0X2, Canada

    P. Sampath

  3. Genomics Lab, Sugarcane Breeding Institute, Coimbatore, India

    P. T. Prathima

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KR, KG, MR and PJ conceived the idea. KR, MR, and PS wrote the main manuscript text. KR, PTP, AY and CS prepared the manuscript. KR, KG, MR and PTP revised the manuscript at different stages of the writing process and read and approved the revised manuscript.

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Rajarajan, K., Ganesamurthy, K., Raveendran, M. et al. Differential responses of sorghum genotypes to drought stress revealed by physio-chemical and transcriptional analysis. Mol Biol Rep 48, 2453–2462 (2021). https://doi.org/10.1007/s11033-021-06279-z

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