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Comparative transcriptome analysis reveals the genes and pathways involved in terminal drought tolerance in pearl millet

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Abstract

Pearl millet is a widely cultivated grain and forage crop in areas frequented with hot and dry weather, and high temperature. Being cultivated in arid and semi-arid regions, the crop often encounters intermittent water stress either at early stages of development or flowering stage or both. However, its asynchronous tillering behavior and fast growth rate helps recovering from drought stress at vegetative stages while there is no such reprieve under terminal stress (flowering through grain filling). At present, the molecular basis of terminal drought tolerance of certain pearl millet genotypes remains elusive. In this study, a comparative transcriptome analysis has been performed at both vegetative and flowering stages of a terminal drought tolerant genotype, PRLT2/89-33, subjected to drought stress. The gene expression profiling analysis showed that PRLT2/89-33 has an inherent ability to sense drought at both developmental stages. Gene Ontology (GO) and MapMan pathway analyses underlined that flavanoid pathway, lignin biosynthesis, phenyl propanoid pathway, pigment biosynthesis, and other secondary metabolite pathways were enriched in control and drought stressed PRLT2/89-33 at flowering stage than at the vegetative stage. To our knowledge, this is the first report of comparative transcriptome analysis under drought stress at two different developmental stages which can facilitate fastidious discovery of drought tolerant genes leading to improved yield in pearl millet and other related crops.

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References

  • Agarwal PK, Agarwal P, Jain P, Jha B, Reddy MK, Sopory SK (2007) Constitutive overexpression of a stress-inducible small GTP-binding protein PgRab7 from Pennisetum glaucum enhances abiotic stress tolerance in transgenic tobacco. Plant Cell Rep 27:105–115

    PubMed  Google Scholar 

  • Agarwal P, Agarwal PK, Joshi AJ, Sopory SK, Reddy MK (2010) Overexpression of PgDREB2A transcription factor enhances abiotic stress tolerance and activates downstream stress-responsive genes. Mol Biol Rep 37:1125–1135

    CAS  PubMed  Google Scholar 

  • Aloni R, Wolf A, Feigenbaum P, Avni A, Klee HJ (1998) The Never ripe mutant provides evidence that tumor-induced ethylene controls the morphogenesis of Agrobacterium tumefaciens-induced crown galls on tomato stems. Plant Physiol 117:841–849

    CAS  PubMed  PubMed Central  Google Scholar 

  • Aparna K, Nepolean T, Srivastava RK, Kholova J, Rajaram V, Kumar S, Rekha B, Senthilvel S, Hash CT, VadeZ V (2015) Quantitative trait loci associated with constitutive traits controlling water use in pearl millet [Pennisetum glaucum (L.) R.Br.]. Plant Biol 5:1073–1084

    Google Scholar 

  • Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT et al (2000) Gene ontology: tool for the unification of biology. Nat Genet 25(1):25–29

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58

    CAS  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc 57:289–300

    Google Scholar 

  • Bidinger FR, Hash CT (2004) Pearl millet. In: Nguyen HT, Blum A (eds) Physiology and biotechnology integration for plant breeding. Marcel Dekker, New York, pp 225–270

    Google Scholar 

  • Bidinger FR, Mahalakshmi V, Rao GDP (1987) Assessment of drought resistance in pearl millet [Pennisetum americanum (L.) Leeke]. Estimation of genotype response to stress. Aust J Agric Res 38:49–59

    Google Scholar 

  • Botella MA, Rosada A, Bressan RA, Hasegawa PM (2008) Plant adaptive responses to salinity stress. In: Jenks MA, Hasegawa PM (eds) Plant abiotic stress. Blackwell, Oxford, pp 37–70

    Google Scholar 

  • Cattivelli L, Rizza F, Badeck FW, Mazzucotelli E, Mastrangelo AM, Francia E, Marè C, Tondelli A, Stanca AM (2008) Drought toleranceimprovement in crop plants: an integrated view from breeding to genomics. Field Crops Res 105:1–14

    Google Scholar 

  • Chakrabarty D, Chauhan PS, Chauhan AK, Indoliya Y, Lavania UM, Nautiyal CS (2015) De novo assembly and characterization of root transcriptome in two distinct morphotypes of vetiver, Chrysopogon zizaniodes (L.) roberty. Sci Rep 5:18630

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chauhan PS, Lata C, Tiwari S, Chauhan AS, Mishra SK, Agrawal L, Chakrabarty D, Nautiyal CS (2019) Transcriptional alterations reveal Bacillus amyloliquefaciens-rice cooperation under salt stress. Sci Rep 9:11912

    PubMed  PubMed Central  Google Scholar 

  • Choudhary M, Padaria JC (2015) Transcriptional profiling in pearl millet (Pennisetum glaucum L.) for identification of differentially expressed drought responsive genes. Physiol Mol Biol Plants 21(2):187

    CAS  PubMed  PubMed Central  Google Scholar 

  • Desai MK, Mishra RN, Verma D, Nair S, Sopory SK, Reddy MK (2006) Structural and functional analysis of a salt stress inducible gene encoding voltage dependent anion channel (VDAC) from pearl millet (Pennisetum glaucum). Plant Physiol Biochem 44:483–493

    CAS  PubMed  Google Scholar 

  • Dudhate A, Shinde H, Tsugama D, Liu S, Takano T (2018) Transcriptomic analysis reveals the differentially expressed genes and pathways involved in drought tolerance in pearl millet [Pennisetum glaucum (L.) R. Br]. PLoS ONE 13(4):e0195908

    PubMed  PubMed Central  Google Scholar 

  • Harvaux M, Kloppstech K (2001) The protective functions of carotenoid and flavonoid pigments against excess visible radiation at chilling temperature investigated in Arabidopsis npq and tt mutants. Planta 213(6):953–966

    CAS  PubMed  Google Scholar 

  • Houben M, Van de Poel B (2019) 1-Aminocyclopropane-1-Carboxylic Acid Oxidase (ACO): The enzyme that makes the plant hormone ethylene. Front Plant Sci 10:695

    PubMed  PubMed Central  Google Scholar 

  • Jaiswal S, Antala TJ, Mandavia MK, Chopra M, Jasrotia RS, Tomar RS, Kheni J, Angadi UB, Iquebal MA, Golakia BA, Rai A, Kumar D (2018) Transcriptomic signature of drought response in pearl millet [Pennisetum glaucum (L.)] and development of web-genomic resources. Sci Rep 8:3382

    PubMed  PubMed Central  Google Scholar 

  • Jatan R, Tiwari S, Asif MH, Lata C (2019) Genome-wide profiling reveals extensive alterations in Pseudomonas putidamediated miRNAs expression during drought stress in chickpea (Cicer arietinum L.). Environ Exp Bot 157:217–227

    CAS  Google Scholar 

  • Jha UC, Chaturvedi SK, Bohra A, Basu PS, Khan MS, Barh D (2014) Abiotic stresses, constraints and improvement strategies in chickpea. Plant Breed 133:163–178

    Google Scholar 

  • Kholova J, Hash CT, Kakkera A, Kocova M, Vadez V (2010) Constitutive water-conserving mechanisms are correlated with the terminal drought tolerance of pearl millet [Pennisetum glaucum (L.) R. Br.]. J Exp Biol 61:369–377

    CAS  Google Scholar 

  • Kholová J, Vadez V (2013) Water extraction under terminal drought explains the genotypic differences in yield, not the anti-oxidant changes in leaves of pearl millet (Pennisetum glaucum). Funct Plant Biol 40:44–53

    Google Scholar 

  • Kholova J, Hash CT, Koˇcová M, Vadez V (2011) Does a terminal drought tolerance QTL contribute to differences in ROS scavenging enzymes and photosynthetic pigments in pearl millet exposed to drought? Environ Exp Bot 71:91–106

    Google Scholar 

  • Lata C, Prasad M (2011) Role of DREBs in regulation of abiotic stress responses in plants. J Exp Bot 62:3387–3401

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lata C, Jha S, Dixit V, Sreenivasulu N, Prasad M (2011) Differential antioxidative responses to dehydration-induced oxidative stress in core set of foxtail millet cultivars [Setaria italica (L.)]. Protoplasma 248:817–828

    CAS  PubMed  Google Scholar 

  • Lata C (2015) Advances in omics for enhancing abiotic stress tolerance in millets. Proc Indian Natl Sci Acad 81:397–417

    Google Scholar 

  • Lata C, Muthamilarasan M, Prasad M (2015) Drought stress responses and signal transduction in plants. In: Pandey GK (ed) The elucidation of abiotic stress signaling in plants. Springer, New York, pp 195–225

    Google Scholar 

  • Larbi A, Mekliche A (2004) Relative water content (RWC) and leaf senescence as screening tools for drought tolerance in wheat. In: Mediterranean Rainfed Agriculture: Strategies for Sustainability: Final Seminar of the Regional Action Program on Rainfed Agriculture. 2–3 June 2003, Zaragoza,Spain. International Centre for Advanced Mediterranean Agronomic Studies 60: 193–196. Cantero-Martinez, C., and Cabina, D. eds., Options Mediterraneennes. Series A, Seminaires Mediterraneens. Paris

  • Lu M, Ying S, Zhang DF, Shi YS, Song YC, Wang TY (2012) A maize stress-responsive NAC transcription factor, ZmSNAC1, confers enhanced tolerance to dehydration in transgenic Arabidopsis. Plant Cell Rep 31:1701–1711

    CAS  PubMed  Google Scholar 

  • Mahalakshmi V, Bidinger FR (1986) Water deficit during panicle development in pearl millet: yield compensation by tillers. J Agric Sci Camb 106:113–119

    Google Scholar 

  • Mahalakshmi V, Bidinger FR, Rao GDP (1988) Timing and intensity of water deficits during flowering and grain filling in pearl millet. Agron J 80:130–135

    Google Scholar 

  • Mi G, Tang L, Zhang F, Zhang J (2002) Carbohydrate storage and utilization during grain filling as regulated by nitrogen application in two wheat cultivars. J Plant Nutr 25:213–229

    CAS  Google Scholar 

  • Mishra R, Reddy P, Nair S, Markandeya G, Reddy A, Sopory S, Reddy M (2007) Isolation and characterization of expressed sequence tags (ESTs) from subtracted cDNA libraries of Pennisetum glaucum seedlings. Plant Mol Biol 64:713–732

    CAS  PubMed  Google Scholar 

  • Nawaz A, Farooq M, Cheema SA, Yasmeen A, Wahid A (2013) Stay green character at grain filling ensures resistance against terminal drought in wheat. Int J Agric Biol 15:1272–1276

    Google Scholar 

  • Pateraki I, Kanellis AK (2010) Stress and developmental responses of terpenoid biosynthetic genes in Cistus creticus subsp. creticus. Plant Cell Rep 29:629–641

    CAS  PubMed  Google Scholar 

  • Rajaram V, Nepolean T, Senthilvel S, Varshney RK, Vadez V, Srivastava RK, Shah TM, Supriya A, Kumar S, Kumari BR et al (2013) Pearl millet [Pennisetum glaucum(L.) R. Br.] consensus linkage map constructed using four RIL mapping populations and newly developed EST-SSRs. BMC Genomics 14:159

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ranjan A, Nigam D, Asif MH, Singh R, Ranjan S, Mantri S, Pandey N, Trivedi I, Rai KM, Jena SN et al (2012) Genome wide expression profiling of two accession of G. herbaceum L. in response to drought. BMC Genomics 13:94

    CAS  PubMed  PubMed Central  Google Scholar 

  • Reddy PS, Thirulogachandar V, Vaishnavi CS, Aakrati A, Sopory SK, Reddy MK (2011) Molecular characterization and expression of a gene encoding cytosolic Hsp90 from Pennisetum glaucum and its role in abiotic stress adaptation. Gene 474:29–38

    CAS  PubMed  Google Scholar 

  • Reddy PK, Reddy GM, Pandey P, Chandrasekhar K, Reddy MK (2012) Cloning and molecular characterization of a gene encoding late embryogenesis abundant protein from Pennisetum glaucum: protection against abiotic stresses. Mol Biol Rep 39:7163–7174

    CAS  PubMed  Google Scholar 

  • Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, Sturn A, Snuffin M, Rezantsev A, Popov D, Ryltsov A, Kostukovich E, Borisovsky I, Liu Z, Vinsavich A, Trush V, Quackenbush J (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34(2):374–378

    CAS  PubMed  Google Scholar 

  • Sehgal D, Skot L, Singh R, Srivastava RK, Das SP, Taunk J, Sharma PC, Pal R, Raj B, Hash CT, Yadav RS (2015) Exploring potential of pearl millet germplasm association panel for association mapping of drought tolerance traits. PLoS ONE 10:e0122165

    PubMed  PubMed Central  Google Scholar 

  • Selmar D, Kleinwächter M (2013) Stress enhances the synthesis of secondary plant products: the impact of stress-related over-reduction on the accumulation. Plant Cell Physiol 54(6):817–826

    CAS  PubMed  Google Scholar 

  • Sharma A, Zheng B (2019) Melatonin mediated regulation of drought stress: physiological and molecular aspects. Plants (Basel) 8(7):190

    CAS  Google Scholar 

  • Shinde H, Tanaka DA, Tsugama D, Mine Y, Kamiya T, Gupta SK, Liu S, Takano T (2018) Comparative de novo transcriptomic profiling of the salinity stress responsiveness in contrasting pearl millet lines. Environ Exp Bot 155:619–627

    CAS  Google Scholar 

  • Shivhare R, Lata C (2016) Selection of suitable reference genes for assessing gene expression in pearl millet under different abiotic stresses and their combinations. Sci Rep 6:23036

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shivhare R, Lata C (2017) Exploration of genetic and genomic resources for biotic and biotic stress tolerance in pearl millet. Front Plant Sci 7:2069

    PubMed  PubMed Central  Google Scholar 

  • Shivhare R, Lata C (2019) Assessment of pearl millet genotypes for drought stress tolerance at early and late seedling stages. Acta Physiol Plant 41:39

    Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58(2):221–227

    CAS  PubMed  Google Scholar 

  • Singh J, Reddy PS, Reddy CS, Reddy MK (2015) Molecular cloning and characterization of salt inducible dehydrin gene from the C4 plant Pennisetum glaucum. Plant Gene 4:55–63

    CAS  Google Scholar 

  • Shinde H, Dudhate A, Tsugama D, Gupta SK, Liu S, Takano T (2019) Pearl millet stress-responsive NAC transcription factor PgNAC21 enhances salinity stress tolerance in Arabidopsis. Plant Physiol Biochem 135:546–553

    CAS  PubMed  Google Scholar 

  • Smigocki AC, Owens LD (1989) Cytokinin gene fused with a strong promoter enhances shoot organogenesis and zeatin levels in transformed plant cells. Proc Natl Acad Sci USA 85:5131–5135

    Google Scholar 

  • Sylvester-Bradley R, Scott RK, Wright CE (1990) Physiology in the production and improvement of cereals. Home-grown Cereals Authority Research Review 18. HGCA, London

  • Thimm O, Blasing O, Gibon Y, Nagel A, Meyer S, Kruger P, Selbig J, Muller LA, Rhee SY, Stitt M (2004) MAPMAN: a user-driven tool to display genomics data sets on to diagrams of metabolic pathways and other biological processes. Plant J 37:914–939

    CAS  PubMed  Google Scholar 

  • Islam SMT, Tammi RS, Singla-Pareek SL, Seraj ZI (2010) Enhanced salinity tolerance and improved yield properties in Bangladeshi rice Binnatoa through Agrobacterium-mediated transformation of PgNHX1 from Pennisetum glaucum. Acta Physiol Plant 32:657–663

    CAS  Google Scholar 

  • Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Biounformatics 25(9):1105–1111

    CAS  Google Scholar 

  • Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pacher L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7:562–578

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ubeda-Thomas S, Swarup R, Coates J, Swarup K, Laplaze L, Beemster GTS, Hedden P, Bhalerao R, Bennett MJ (2008) Root growth in Arabidopsis requires gibberellin/DELLA signalling in the endodermis. Nat Cell Biol 10:625–628

    Google Scholar 

  • Varshney RK, Shi C, Thudi M, Mariac C, Wallace J, Qi P, Zhang H, Zhao Y, Wang W, Rathore A et al (2017) Pearl millet genome sequence provides a resource to improve agronomic traits in arid environments. Nat Biotechnol 35:969–976

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vogt T (2010) Phenylpropanoid biosynthesis. Mol Plant 3(1):2–20

    CAS  PubMed  Google Scholar 

  • Xu FJ, Jin CW, Liu WJ, Zhang YS, Lin XY (2011) Pretreatment with H2O2 alleviates aluminum-induced oxidative stress in wheat seedlings. J Integr Plant Biol 53:44–53

    CAS  PubMed  Google Scholar 

  • Yadav RS, Sehgal D, Vadez V (2011) Using genetic mapping and genomics approaches in understanding and improving drought tolerance in pearl millet. J Exp Bot 62:397–408

    CAS  PubMed  Google Scholar 

  • Yang J, Zhang J, Wang Z, Zhu Q, Liu L (2001) Water deficit induced senescence and its relationship to the remobilization of pre-stored carbon in wheat during grain filling. Agron J 93:196–206

    CAS  Google Scholar 

  • Yoshida S (1972) Physiological aspects of grain yield. Ann Rev Plant Physiol 23:437–464

    Google Scholar 

  • Zheng J-X, Zhang H, Su HX, Jian SG, Zhang M (2018) Ipomoea pes-caprae IpASR improves salinity and drought tolerance in transgenic Escherichia coli and Arabidopsis. Int J Mol Sci 19(8):2252

    PubMed Central  Google Scholar 

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Acknowledgements

CL acknowledges the INSPIRE Faculty Award [IFA-11LSPA-01] from Department of Science & Technology (DST), GoI, New Delhi. The authors are thankful to Dr. Rakesh Srivastava, International Crops Research Institute for the Semi- Arid Tropics, Patancheru, India for providing pearl millet seed materials. Authors are also thankful to Dr. Muthamilarasan Mehanathan, University of Hyderabad, Telangana, India for assisting us in improvising the language of our manuscript.

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  1. Charu Lata

    Present address: CSIR-National Institute of Science Communication and Information Resources, 14 Satsang Vihar Marg, New Delhi, 110067, India

Authors and Affiliations

  1. CSIR- National Botanical Research Institute, Rana Pratap Marg, Lucknow, 226001, India

    Radha Shivhare, Mehar H. Asif & Charu Lata

  2. Academy of Scientific and Innovative Research (AcSIR), Ghaziabad, 201002, India

    Radha Shivhare, Mehar H. Asif & Charu Lata

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  1. Radha Shivhare
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CL conceived and designed the experiment. RS and CL conducted the experiments. RS, MHA and CL analyzed the data. RS and CL wrote the manuscript. All authors read and approved the manuscript.

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Correspondence to Charu Lata.

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Shivhare, R., Asif, M.H. & Lata, C. Comparative transcriptome analysis reveals the genes and pathways involved in terminal drought tolerance in pearl millet. Plant Mol Biol 103, 639–652 (2020). https://doi.org/10.1007/s11103-020-01015-w

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