Indian Journal of Plant Physiology

, Volume 23, Issue 4, pp 772–784 | Cite as

Physiological, biochemical and molecular responses of lentil (Lens culinaris Medik.) genotypes under drought stress

  • Ragini Sinha
  • Awadhesh Kumar Pal
  • Anil Kumar SinghEmail author
Original Article


Lentil (Lens culinaris Medik.) is an important pulse crop in India. It is moderately tolerant to drought, however intermittent and terminal drought significantly reduce lentil productivity. Selection of appropriate parent for breeding drought resistant variety is a challenging task. Thus, in the present work drought response of eight lentil genotypes (GP3690, LL1136, GP3643, NDL908, KLS218, IC248956, PL230, L4076) has been analysed, by imposing drought stress using PEG 6000 (18% w/v) for 15 days. Various physiological (stomatal density, relative water content) and biochemical parameters (total chlorophyll, total soluble sugar, anthocyanin and proline contents, lipid peroxidation, superoxide dismutase and catalase activities) were analysed under drought stress. These eight genotypes were further evaluated by analysing expression of drought stress marker genes (DREBs and RDs) which suggested genotypes GP3690 as drought susceptible (DS) and genotypes GP3643 and IC248956 as drought tolerant (DT). Relative expression of forty-three drought responsive genes related to various molecular functions, like biosynthetic process, redox homeostasis and defence related genes were evaluated in these three genotypes, which revealed that the tolerant genotypes alters the metabolic and biosynthesis processes of plant to overcome drought. This study provides basic information on drought tolerance capacity of the genotypes which may be further ascertained at field level.


Lentil Drought Physiological analysis Gene expression qRT-PCR 



RS acknowledges Science and Engineering Research Board, Department of Science and Technology, Government of India for the National-Postdoctoral Fellowship (PDF/2016/000924). AKS acknowledges Institute projects IXX12585 and IXX12644 funded by ICAR-Indian Institute of Agricultural Biotechnology, Ranchi. We thank Dr. Madhuparna Banerjee, Associate Professor, College of Biotechnology, Birsa Agricultural Biotechnology, Ranchi for granting access to her lab facilities during the course of this study.

Supplementary material

40502_2018_411_MOESM1_ESM.pdf (334 kb)
Supplementary material 1 (PDF 334 kb)


  1. Aubert, Y., Vile, D., Pervent, M., Aldon, D., Ranty, B., Simonneau, T., et al. (2010). RD20, a stress-inducible caleosin, participates in stomatal control, transpiration and drought tolerance in Arabidopsis thaliana. Plant and Cell Physiology, 51, 1975–1987.PubMedGoogle Scholar
  2. Barrs, H. D., & Weatherley, P. E. (1962). A re-examination of the relative turgidity techniques for estimating water deficits in leaves. Australian Journal of Biological Sciences, 15, 413–428.Google Scholar
  3. Bates, L. S., Waldren, R. P., & Teare, I. D. (1973). Rapid determination of free proline for water stress studies. Plant and Soil, 39, 205–207.Google Scholar
  4. Beauchamp, C., & Fridovich, I. (1971). Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels. Annals of Biochemistry, 44, 276–287.Google Scholar
  5. Cho, S. K., Kim, J. E., Park, J. A., Eom, T. J., & Kim, W. T. (2006). Constitutive expression of abiotic stress-inducible hot pepper CaXTH3, which encodes a xyloglucan endotransglucosylase/hydrolase homolog, improves drought and salt tolerance in transgenic Arabidopsis plants. FEBS Letter, 580, 3136–3144.Google Scholar
  6. Dobra, J., Motyka, V., Dobrev, P., Malbeck, J., Prasil, I. T., Haisel, D., et al. (2010). Comparison of hormonal responses to heat, drought and combined stress in tobacco plants with elevated proline content. Journal of Plant Physiology, 167, 1360–1370.PubMedGoogle Scholar
  7. Dos Santos, T. B., de Lima, R. B., Nagashima, G. T., de Oliveira, C. L., Carpentieri-Pipolo, V., Filipe, L., et al. (2015). Galactinol synthase transcriptional profile in two genotypes of Coffea canephora with contrasting tolerance to drought. Genetics and Molecular Biology, 38, 182–190.PubMedPubMedCentralGoogle Scholar
  8. DuBois, M., Gilles, K. A., Hamilton, J. K., Rebers, P. A., & Smith, F. (1956). Colorimetric method for determination of sugars and related substances. Annals of Chemistry, 28, 350–356.Google Scholar
  9. Ghawana, S., Paul, A., Kumar, H., Kumar, A., Singh, H., Bhardwaj, P. K., et al. (2011). An RNA isolation system for plant tissues rich in secondary metabolites. BMC Research Notes, 4, 85–89.PubMedPubMedCentralGoogle Scholar
  10. Good, A. G., & Zaplachinski, S. T. (1994). The effect of drought stress on free amino acid accumulation and protein synthesis in Brassica napus. Physiologia Plantarum, 90, 9–14.Google Scholar
  11. Grusak, M. A., & Coyne, C. J. (2009). Variation for seed minerals and protein concentration in diverse germplasm of lentil. Paper presented at North American Pulse Improvement Association, 20th Biennial Meeting (Fort Collins, CO), p. 11.Google Scholar
  12. Gunasekera, D., & Berkowitz, G. A. (1992). Evaluation of contrasting cellular-level acclimation responses to leaf water deficits in three wheat genotypes. Plant Science, 86, 1–12.Google Scholar
  13. Guo, P., Baum, M., Grando, S., Ceccarelli, S., Bai, G., Li, R., et al. (2009). Differentially expressed genes between drought-tolerant and drought-sensitive barley genotypes in response to drought stress during the reproductive stage. Journal of Experimental Botany, 60, 3531–3544.PubMedPubMedCentralGoogle Scholar
  14. Guo, L., Yang, H., Zhang, X., & Yang, S. (2013). Lipid transfer protein 3 as a target of MYB96 mediates freezing and drought stress in Arabidopsis. Journal of Experimental Botany, 64, 1755–1767.PubMedPubMedCentralGoogle Scholar
  15. Guo, J., Ling, H., Jingjing, M., Chen, Y., Su, Y., Lin, Q., et al. (2017). A sugarcane R2R3-MYB transcription factor gene is alternatively spliced during drought stress. Scientific Reports, 7, 41922.PubMedPubMedCentralGoogle Scholar
  16. Harb, A., Krishnan, A., Ambavaram, M. M. R., & Pereira, A. (2010). Molecular and physiological analysis of drought stress in Arabidopsis reveals early responses leading to acclimation in plant growth. Plant Physiology, 154, 1254–1271.PubMedPubMedCentralGoogle Scholar
  17. Hashimoto, M., Kisseleva, L., Sawa, S., Furukawa, T., Komatsu, S., & Koshiba, T. (2004). A novel rice PR10 protein, RSOsPR10, specifically induced in roots by biotic and abiotic stresses, possibly via the jasmonic acid signalling pathway. Plant and Cell Physiology, 45, 550–559.PubMedGoogle Scholar
  18. Heath, R. L., & Packer, L. (1968). Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics, 125, 189–198.PubMedGoogle Scholar
  19. Hiscox, J. D., & Israelstam, G. F. (1979). A method for the extraction of chlorophyll from leaf tissue without maceration. Canadian Journal of Botany, 57, 1332–1334.Google Scholar
  20. Hu, C. A., Delauney, A. J., & Verma, D. P. S. (1992). A bifunctional enzyme (Δ1-pyrroline-5-carboxylate synthase) catalyzes the first two steps in proline biosynthesis in plants. Proceedings of the National Academy of Sciences, United States of America, 89, 9354–9358.Google Scholar
  21. Huang, G.-T., Ma, S.-L., Bai, L.-P., Zhang, L., Ma, H., Jia, P., et al. (2011). Signal transduction during cold, salt, and drought stresses in plants. Molecular Biology Reports, 39, 969–987.PubMedGoogle Scholar
  22. Idrissi, O., Udupa, S. M., De Keyser, E., McGee, R. J., Coyne, C. J., Saha, G. C., et al. (2016). Identification of quantitative trait loci controlling root and shoot traits associated with drought tolerance in a lentil (Lens culinaris Medik.) recombinant inbred line population. Frontiers in Plant Science, 7, 1174.PubMedPubMedCentralGoogle Scholar
  23. Joshi, V., Joung, J. G., Fei, Z., & Jander, G. (2010). Interdependence of threonine, methionine and isoleucine metabolism in plants: accumulation and transcriptional regulation under abiotic stress. Amino Acids, 39(4), 933–947.PubMedGoogle Scholar
  24. Khedr, A. H., Abbas, M. A., Abdel Wahid, A. A., QuickGaber, W. P., & Abogadallah, M. (2003). Proline induces the expression of salt-stress-responsive proteins and may improve the adaptations of Pancratium maritimum L. to salt stress. Journal of Experimental Botany, 54, 2553–2562.PubMedGoogle Scholar
  25. Kim, J., Yi, H., Choi, G., Shin, B., Song, P.-S., & Choi, G. (2003). Functional characterisation of phytochrome interacting factor 3 in phytochrome-mediated light signal transduction. The Plant Cell, 15, 2399–2407.PubMedPubMedCentralGoogle Scholar
  26. Kim, S. T., Yu, S., Kang, Y. H., Kim, S. G., Kim, J. Y., Kim, S. H., et al. (2008). The rice pathogen-related protein 10 (JIOsPR10) is induced by abiotic and biotic stresses and exhibits ribonuclease activity. Plant Cell Reports, 27, 593–603.PubMedGoogle Scholar
  27. Koingshofer, H. L., & Oppert, H. G. (2015). Regulation of invertase activity in different root zones of wheat (Triticum aestivum L.) seedlings in the course of osmotic adjustment under water deficit conditions. Journal of Plant Physiology, 183, 130–137.Google Scholar
  28. Lata, C., & Prasad, M. (2011). Role of DREBs in regulating abiotic stress responses in plants. Journal of Experimental Botany, 62, 4731–4748.PubMedGoogle Scholar
  29. Lee, B.-R., Jung, W.-J., Lee, B.-H., Avice, J.-C., Ourry, A., & Kim, T.-H. (2007). Kinetics of drought induced pathogenesis-related proteins and its physiological significance in white clover leaves. Physiologia Plantarum, 132, 329–337.Google Scholar
  30. Luck, H. (1974). In Bergmeyer (Ed.), Methods in enzymatic analysis 2 (p. 885). New York: Academic.Google Scholar
  31. Martinez, J. P., Silva, H., Ledent, J. F., & Pinto, M. (2007). Effect of drought stress on the osmotic adjustment, cell wall elasticity and cell volume of six cultivars of common beans (Phaseolus vulgaris L.). European Journal of Agronomy, 26, 30–38.Google Scholar
  32. Mishra, B. K., Srivastava, J. P., Lal, J. P., & Sheshshayee, M. S. (2016). Physiological and biochemical adaptations in lentil genotypes under drought stress. Russian Journal of Plant Physiology, 63, 695–708.Google Scholar
  33. Mirouze, M., Sels, J., Richard, O., Czernic, P., Loubet, S., Jacquier, A., et al. (2006). A putative role of plant defensin from the zinc hyper-accumulating plant, Arabidopsis halleri confers zinc tolerance. The Plant Journal, 47, 329–342.PubMedGoogle Scholar
  34. Moller, I. M., Jensen, P. E., & Hansson, A. (2007). Oxidative modifications to cellular components in plants. Annual Review of Plant Biology, 58, 459–481.PubMedGoogle Scholar
  35. Monakhova, O. F., & Chemyadev, I. I. (2002). Protective role of kartolin-4 in wheat plants exposed to soil drought. Applied Biochemistry and Microbiology, 38, 373–380.Google Scholar
  36. Moussa, H. R., & Abdel-Aziz, S. M. (2008). Comparative response of drought tolerant and drought sensitive maize genotypes to water stress. Australian Journal of Crop Science, 1, 31–36.Google Scholar
  37. Munne-Bosch, S., Jubany-Mari, T., & Alegre, L. (2001). Drought induced senescence is characterised by a loss of antioxidant defences in chloroplasts. Plant, Cell and Environment, 24, 1319–1327.Google Scholar
  38. Muscolo, A., Sidari, M., Anastasi, U., Santonoceto, C., & Maggio, A. (2014). Effect of drought stress on germination of four lentil genotypes. Journal of Plant Interaction, 9, 354–363.Google Scholar
  39. Muscolo, A., Junker, A., Klukas, C., Weigelt-Fischer, K., Riewe, D., & Altmann, T. (2015). Phenotypic and metabolic responses to drought and salinity of four contrasting lentil accessions. Journal of Experimental Botany, 66, 5467–5480.PubMedPubMedCentralGoogle Scholar
  40. Nakashima, K., Kiyosue, T., Yamaguchi-Shinozaki, K., & Shinozaki, K. (1997). A nuclear gene, erd1, encoding a chloroplast-targeted Clp protease regulatory subunit homolog is not only induced by water stress but also developmentally up-regulated during senescence in Arabidopsis thaliana. Plant Journal, 12, 851–861.PubMedGoogle Scholar
  41. Nath, U. K., Rani, S., Paul, M. R., Alam, M. N., & Horneburg, B. (2014). Selection of superior lentil (Lens esculenta M.) genotypes by assessing character association and genetic diversity. Scientific World Journal, 2014, 372405.PubMedGoogle Scholar
  42. Nautiyal, C. S., Srivastava, S., Chauhan, P. S., Seem, K., Mishra, A., & Sopory, S. K. (2013). Plant growth-promoting bacteria Bacillus amyloliquefaciens NBRISN13 modulates gene expression profile of leaf and rhizosphere community in rice during salt stress. Plant Physiology and Biochemistry, 66, 1–9.PubMedGoogle Scholar
  43. Nishizawa, A., Yabuta, Y., & Shigeoka, S. (2008a). The contribution of carbohydrates including raffinose family oligosaccharides and sugar alcohols to protection of plant cells from oxidative damage. Plant Signalling and Behaviour, 11, 1016–1018.Google Scholar
  44. Nishizawa, A., Yabuta, Y., & Shigeoka, S. (2008b). Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiology, 147, 1251–1263.PubMedPubMedCentralGoogle Scholar
  45. Pulido, P., Llamas, E., Llorente, B., Ventura, S., Wright, L. P., & Rodriguez-Concepcion, M. (2016). Specific Hsp 100 chaperones determine the fate of the first enzymes of the plastidial isoprenoid pathway for either refolding or degradation by the stromal Clp proteases in Arabidopsis. PLoS Genetics, 12, e1005824.PubMedPubMedCentralGoogle Scholar
  46. Oktem, H. A., Eyidodan, F., Demirba, D., Bayrac, A. T., Oz, M. T., Ozgur, E., et al. (2008). Antioxidant responses of lentil to cold and drought stress. Journal of Plant Biochemistry and Biotechnology, 17, 15–21.Google Scholar
  47. Reda, A. (2015). Lentil (Lens culinaris Medikus) current status and future prospect of production in Ethiopia. Advances in Plants & Agriculture Research, 2, 00040.Google Scholar
  48. Renault, H., El-Amrani, A., Berger, A., Mouille, G., Soubigou-Taconnat, L., Bouchereau, A., et al. (2013). γ-Aminobutyric acid transaminase deficiency impairs central carbon metabolism and leads to cell wall defects during salt stress in Arabidopsis roots. Plant, Cell and Environment, 36, 1009–1018.PubMedGoogle Scholar
  49. Rose, J. K., Braam, J., Fry, S. C., & Nishitani, K. (2002). The XTH family of enzymes involved in xyloglucan endotransglucosylation and endohydrolysis: Current perspectives and a new unifying nomenclature. Plant and Cell Physiology, 43, 1421–1435.PubMedGoogle Scholar
  50. Saito, K., & Matsuda, F. (2010). Metabolomics for functional genomics, systems biology, and biotechnology. Annual Review of Plant Biology, 61, 463–489.PubMedGoogle Scholar
  51. Sengupta, S., Mukherjee, S., Basak, P., & Majumdar, A. L. (2015). Significance of galactinol and raffinose family oligosaccharide synthesis in plants. Frontiers in Plant Science, 6, 656.PubMedPubMedCentralGoogle Scholar
  52. Sehgal, A., Sita, K., Kumar, J., Kumar, S., Singh, S., Siddique, K. H. M., et al. (2017). Effects of drought, heat and their interaction on the growth, yield and photosynthetic function of lentil (Lens culinaris Medikus) genotypes varying in heat and drought sensitivity. Frontiers in Plant Science, 8, 1776.PubMedPubMedCentralGoogle Scholar
  53. Shah, Z. H., Rehman, H. M., Akhtar, T., Daur, I., Nawaz, M. A., Ahmad, M. Q., et al. (2017). Redox and ionic homeostasis regulation against oxidative, salinity and drought stress in wheat (a systems biology approach). Frontiers in Genetics, 8, 141.PubMedPubMedCentralGoogle Scholar
  54. Shavrukov, Y., Kurishbayev, A., Jatayev, S., Shvidchenko, V., Zotova, L., Koekemoer, F., et al. (2017). Early flowering as a drought escape mechanism in plants: How can it aid wheat production? Frontiers in Plant Science, 8, 1950.PubMedPubMedCentralGoogle Scholar
  55. Siddique, M. H., Al-Khaishany, M. Y., Al-Qutami, M. A., Al-Whaibi, M. H., Grover, A., Ali, H. M., et al. (2015). Responses of different genotypes of Faba bean plant to drought stress. International Journal of Molecular Sciences, 16, 10214–10227.Google Scholar
  56. Singh, A. K., Sopory, S. K., Wu, R., & Singla-Pareek, S. L. (2010). Transgenic approaches. In A. Pareek, S. K. Sopory, H. J. Bohnert, & Govindjee (Eds.), Abiotic stress adaptation in plants: Physiological molecular and genomic foundation (pp. 417–450). Dordrecht: Springer.Google Scholar
  57. Singh, D., Singh, C. K., Tomar, R. S. S., Taunk, J., Singh, R., Maurya, S., et al. (2016). Molecular assortment of Lens species with different adaptations to drought conditions using SSR markers. PLoS ONE, 11, e0147213.PubMedPubMedCentralGoogle Scholar
  58. Singh, D., Singh, C. K., Taunk, J., Tomar, R. S. S., Chaturvedi, A. K., Gaikwad, K., et al. (2017a). Transcriptome analysis of lentil (Lens culinaris) in response to seedling drought stress. BMC Genomics, 18, 206.PubMedPubMedCentralGoogle Scholar
  59. Singh, D., Singh, C. K., Kumari, S., Tomar, R. S. S., Karwa, S., Singh, R., et al. (2017b). Discerning morpho-anatomical, physiological and molecular multiformity in cultivated and wild genotypes of lentil with reconciliation to salinity stress. PLoS ONE, 12, e0190462.PubMedPubMedCentralGoogle Scholar
  60. Sinha, R., Sharma, T. R., & Singh, A. K. (2018). Validation of reference genes for qRT-PCR data normalisation in lentil (Lens culinaris) under leaf developmental stages and abiotic stresses. Physiology and Molecular Biology of Plants. Scholar
  61. Siopongco, J. D. L. C., Yamauchi, A., Salekdeh, H., Bennet, J., & Wade, L. J. (2006). Growth and water use response of doubled-haploid rice lines to drought and rewatering during the vegetative stage. Plant Production Science, 9, 141–151.Google Scholar
  62. Sita, K., Sehgal, A., Kumar, J., Kumar, S., Singh, S., Siddique, K. H. M., et al. (2017). Identification of high temperature tolerant lentil (Lens culinaris Medik.) genotypes through leaf and pollen traits. Frontiers in Plant Science, 8, 744.PubMedPubMedCentralGoogle Scholar
  63. Stolf-Moreira, R., Lemos, E., Carareto-Alves, L., Marcondes, J., Pereira, S., Rolla, A., et al. (2011). Transcriptional profiles of roots of different soybean genotypes subjected to drought stress. Plant Molecular Biology Reports, 29, 19–34.Google Scholar
  64. Sultan, M. A. R. F., Hui, L., Yang, L. J., & Xian, Z. H. (2012). Assessment of drought tolerance of some Triticum L. species through physiological indices. Czech Journal of Genetics and Plant Breeding, 48, 178–184.Google Scholar
  65. Szabadous, L., & Savoure, A. (2010). Proline: A multifunctional amino acid. Trends in Plant Science, 15, 89–97.Google Scholar
  66. Taji, T., Ohsumi, C., Iuchi, S., Seki, M., Kasuga, M., Kobayashi, M., et al. (2002). Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. The Plant Journal, 29, 417–426.PubMedGoogle Scholar
  67. Thameur, A., Lachiheb, B., & Ferchichi, A. (2012). Drought effect on growth, gas exchange and yield in two strains of local barley Ardhaoui, under water deficit conditions in southern Tunisia. Journal of Environmental Management, 113, 495–500.PubMedGoogle Scholar
  68. Tiwari, S., Lata, C., Chauhan, P. S., & Nautiyal, C. S. (2016). Pseudomonas putida attunes morphophysiological, biochemical and molecular responses in Cicer arietinum L. during drought stress and recovery. Plant Physiology and Biochemistry, 99, 108–117.PubMedGoogle Scholar
  69. van Wijk, K. J. (2015). Protein maturation and proteolysis in plant plastids, mitochondria, and peroxisomes. Annual Review of Plant Biology, 66, 75–111.PubMedGoogle Scholar
  70. Wang, Z., Zhu, Y., Wang, L., Liu, X., Liu, Y., Phillips, J., et al. (2009). A WRKY transcription factor participates in dehydration tolerance in Boea hygrometrica by binding to the W-box elements of the galactinol synthase (BhGolS1) promoter. Planta, 230, 1155–1166.PubMedGoogle Scholar
  71. Wang, L., Liu, Y., Feng, S., Yang, J., Li, D., & Zhang, J. (2017). Roles of plasmalemma aquaporin gene StPiP1 in enhancing drought tolerance in potato. Frontiers in Plant Science, 8, 616.PubMedPubMedCentralGoogle Scholar
  72. Wehner, G., Balko, C., Humbeck, K., Zyprian, E., & Ordon, F. (2016). Expression profiling of genes involved in drought stress and leaf senescence in juvenile barley. BMC Plant Biology, 16, 3.PubMedPubMedCentralGoogle Scholar
  73. Wei, T., Deng, K., Zhang, Q., Gao, Y., Liu, Y., Yang, M., et al. (2017). Modulating AtDREB1C expression improves drought tolerance in Salvia miltiorrhiza. Frontiers in Plant Science, 8, 52.PubMedPubMedCentralGoogle Scholar
  74. Wheeler, M. C., Tronconi, M. A., Drincovich, M. F., Andreo, C. S., Flugge, U. I., & Maurino, V. G. (2005). A comprehensive analysis of the NADP-malic enzyme gene family of Arabidopsis. Plant Physiology, 139, 39–51.PubMedGoogle Scholar
  75. Wu, Q. S., & Xia, R. X. (2006). Arbuscular mycorrhizal fungi influence growth, osmotic adjustment and water stress conditions. Journal of Plant Physiology, 163, 417–425.PubMedGoogle Scholar
  76. Xiu, Y., Iqbal, A., Zhu, C., Wu, G., Chang, Y., Li, N., et al. (2015). Improvement and transcriptome analysis of root architecture by overexpression of Fraxinus pennsylvanica DREB2A transcription factor in Robinia pseudoacacia L. ‘Idaho’. Plant Biotechnology Journal, 14, 1456–1469.Google Scholar
  77. Xu, Z., & Zhou, G. (2008). Responses of leaf stomatal density to water status and its relationship with photosynthesis in a grass. Journal of Experimental Botany, 59, 3317–3325.PubMedPubMedCentralGoogle Scholar
  78. Yamaguchi-Shinozaki, K., & Shinozaki, K. (2006). Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annual Review of Plant Biology, 57, 781–803.PubMedGoogle Scholar
  79. Yoshiba, Y., Kiyosue, T., Katagiri, T., Ueda, H., Mizoguchi, T., Yamaguchi-Shinozaki, K., et al. (1995). Correlation between the induction of a gene for δ 1-pyrroline-5-carboxylate synthetase and the accumulation of proline in Arabidopsis thaliana under osmotic stress. The Plant Journal, 7, 751–760.PubMedGoogle Scholar
  80. Yoshiba, Y., Nanjo, T., Miura, S., Yamaguchi-Shinozaki, K., & Shinozaki, K. (1999). Stress-responsive and developmental regulation of Δ 1-pyrroline-5-carboxylate synthetase 1 (P5CS1) gene expression in Arabidopsis thaliana. Biochemical and Biophysical Research Communication, 261, 766–772.Google Scholar
  81. Yusuf, M., Singh, N. P., & Dastane, N. G. (1979). Effect of frequency and timings of irrigation on grain yield and water use efficiency of lentil. Annals of Arid Zone, 18, 127–134.Google Scholar
  82. Zeigler, R. S., & Puckridge, D. W. (1995). Improving sustainable productivity in rice based rainfed lowland systems of South and Southeast Asia. Feeding four billion people: The challenge for rice research in the 21st century. GeoJournal, 35, 307324.Google Scholar
  83. Zhou, Q., & Yu, B. J. (2009). Accumulation of inorganic and organic osmolytes and their role in osmotic adjustment in NaCl-stresses vetiver grass seedlings. Russian Journal of Plant Physiology, 56, 678–685.Google Scholar
  84. Zinselmeier, C., Jeong, B. R., & Boyer, J. S. (1999). Starch and the control of kernel number in maize at low water potentials. Plant Physiology, 121, 25–35.PubMedPubMedCentralGoogle Scholar

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© Indian Society for Plant Physiology 2018

Authors and Affiliations

  1. 1.ICAR-Indian Institute of Agricultural BiotechnologyRanchiIndia
  2. 2.Department of Biochemistry and Crop PhysiologyBihar Agricultural UniversityBhagalpurIndia

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