Plant Physiology Reports

, Volume 24, Issue 3, pp 422–433 | Cite as

Effect of drought stress on the expression of genes linked to antioxidant enzymatic activity in landraces of Zea mays L. and Pennisetum glaucum (L.) R. Br.

  • Emmanuel Iwuala
  • Victor Odjegba
  • Abiodun Ajiboye
  • Caroline Umebese
  • Vinay Sharma
  • Afroz AlamEmail author
Original Article


Millets are usually considered more drought tolerant than other cereals. Pearl millet [Pennisetum glaucum (L.) R. Br.] could be an alternative to maize (Zea mays L.) for drought hit regions of the world. In this current study, the sensitivity of these two plants was evaluated under a simulated condition of drought stress. Genotypes IP35451 (pearl millet) and LRN1303 (maize) were compared for their tolerance to drought stress. The growth parameters viz., root/shoot ratio and relative water content were reduced drastically in LRN1303 than in IP35451. Photosystem II was also measured and the study revealed a decrease in electron transport rate and photosynthetically active photo flux density in LRN1303 as compared to IP35451 which had an efficient photosynthesis capacity during drought. Malondialdehyde content and concentration of antioxidant enzymes (Ascorbate peroxidase, Catalase, Glutathione reductase and Superoxide dismutase) revealed that the genotype IP35451 (pearl millet) is better adapted to drought as compared to LRN1303 (maize). Moreover, the gene expression study of three identified genes at transcript levels proved their occurrence as indicators for drought tolerance. GBSS11a in leaf and root displayed steady up-regulation under drought stress in IP35451 (pearl millet), and an initial increase with a subsequent down-regulation in LRN1303 (maize). Expression of antioxidant genes revealed that APX1 and CAT1 in leaves and roots were more remarkably sensitive to drought in IP35451 (pearl millet), however, not for LRN1303 (maize) where they might support better detoxifying action against reactive oxygen species effect under drought condition. The results showed different capacities of LRN1303 (maize) and IP35451 (pearl millet) to activate expression of drought related mRNA. The outcome of the study will be helpful to provide new avenues in future research related to attaining drought tolerant landraces and their genomics.


Antioxidant enzymes Chlorophyll fluorescence Pennisetum glaucum Relative water content Zea mays 



The authors are thankful to Prof. Aditya Shastri, Vice Chancellor, Banasthali (Rajasthan), India for his support. One of the authors (IE) also grateful to Centre of International Cooperation in Science in association with the Department of Biotechnology (DBT), India for providing the fund (Grant Number: 342) and Association of African Universities (AAU) (Ghana) for giving him opportunity to complete his Ph.D.

Author contributions

EI, VO, CU and AA designed the research; EI, AA and VS conducted the research; EI, VO and AA analyzed the data; EI, VO, CU and AA drafted the paper; AA had responsibility for the concluded statement. All authors have read and approved the final manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

Supplementary material

40502_2019_460_MOESM1_ESM.docx (30 kb)
Supplementary material 1 (DOCX 30 kb)


  1. Aebi, H. (1984). Catalase in vitro. Methods Enzymology,105, 121–126.Google Scholar
  2. Alia, K. V., Prasad, S. K., & Pardha, S. P. (1995). Effect of zinc on free radical and proline in Brassica juncea and Cajanus cajan. Phytochemistry,39, 45–47.Google Scholar
  3. Barata, R. M., Chapparro, S. M., Chabregas, R., Gonzalez, C. A., Labate, R. A., Azevedo, G., et al. (2000). Targeting of the soybean leghemoglobin to tobacco chloroplasts: Effects on aerobic metabolism in transgenic plants. Plant Science,155, 193–202.PubMedGoogle Scholar
  4. Bartels, D., & Sunkar, R. (2005). Drought and salt tolerance in plants. CRC Critical Review in Plant Science,24, 23–58.Google Scholar
  5. Beauchamp, C. H., & Fridovich, I. (1971). Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels. Anal Biochemistry,44, 276–287.Google Scholar
  6. Belder, P., Spiertz, J. H. J., Bouman, B. A. M., Lu, G., & Tuong, T. P. (2005). Nitrogen economy and water productivity of lowland rice under water saving irrigation. Field Crops Research,93, 169–185.Google Scholar
  7. Bota, H. M., Magdalena, T., Sebastià, M., Jaume, F., Esther, H., Joan, R., et al. (2015). From leaf to whole-plant water use efficiency (WUE) in complex canopies: Limitations of leaf WUE as a selection target. Crop Journal,3, 220–228.Google Scholar
  8. Bouman, B. A. M. (2007). A conceptual framework for the improvement of crop water productivity at different spatial scales. Agronomical System,93, 43–60.Google Scholar
  9. Bruce, W. B., Edmeades, G. O., & Barker, T. C. (2002). Molecular and physiological approaches to maize improvement for drought tolerance. Journal of Experimental Botany,53(366), 13–25.PubMedGoogle Scholar
  10. Cakir, R. (2004). Effect of water stress at different development stages on vegetative and reproductive growth of corn. Field Crops Research,89, 1–6.Google Scholar
  11. Caverzan, A., Passaia, G., Rosa, S. B., Rebeiro, C. W., Lazzarotto, F., & Margis-Pinheiro, M. (2012). Plant responses to stresses: role of ascorbate peroxidise in antioxidant protection. Genetic Molecular Biology,35(4), 1011–1019.Google Scholar
  12. Chaves, M. M., Maroco, J. P., & Pereira, J. S. (2003). Understanding plant responses to drought—from genes to the whole plant. Functional Plant Biology,30, 239–264.Google Scholar
  13. Davies, W. J., & Zhang, J. (1991). Root signals and the regulation of growth and development in plants in drying soils. Plant Molecular Biology,42, 55–70.Google Scholar
  14. Dietz, K. J. (2005). Plant thiol enzymes and thiolhomoestasis in relation to thiol dependent redox reaction and oxidative stress. In N. Smirnoff (Ed.), Antioxidant and reactive oxygen species in plants (pp. 25–52). Hoboken: Blackwell Publications.Google Scholar
  15. Feng, Q., Masayuki, K., & Yoh, S. (2014). Genome wide identification of housekeeping genes in maize. Plant Molecular Biology, 86, 543–554.Google Scholar
  16. Fracasso, A., Trindade, L., & Amaducci, S. (2016). Drought tolerance strategies highlighted by two Sorghum bicolor races in a dry-down experiment. Journal of Plant Physiology,190, 1–14.PubMedGoogle Scholar
  17. Genty, B., Briantails, J., & Baker, N. R. (1989). The relationship between the quenching yield of photosynthetic electron transport rate and quenching of chlorophyll fluorescence. Biochemistry Biophysics Acta,99, 87–92.Google Scholar
  18. Guo, J., Yang, Y., Wang, G., Yang, L., & Sun, X. (2010). Ecophysiological responses of Abies fabri seedlings to drought stress and nitrogen supply. Plant Physiology,139, 335–347.Google Scholar
  19. Harn, C., Knight, M., Ramakrishnan, A., Guan, H., Keeling, P. L., & Wasserman, B. P. (1998). Isolation and characterization of the zSSIIa and zSSIIb starch synthase cDNA clones from maize endosperm. Plant Molecular Biology,37, 639–649.PubMedGoogle Scholar
  20. Hasan, S. A., Rabei, S. H., Nada, R. M., & Abogadallah, G. M. (2017). Water use efficiency in drought-stressed sorghum and maize in relation to expression of aquaporin genes. Biologia Plantarum,61(1), 127–137.Google Scholar
  21. Hayano-Kanashiro, C., Calderon, C., Ibarra-Laclette, E., Herrera-Estrella, L., & Simpson, J. (2009). Analysis of gene expression and physiological responses in three mexican maize landraces under drought stress and recovery irrigation. PLoS ONE,4(10), e7531. Scholar
  22. Hong, Y., Xiao, P., & Guo, Wu. (2009). Comparison of the starch synthesis genes between maize and rice: Copies, chromosome location and expression divergence. Theoretical Applied Genetics,119, 815–825.Google Scholar
  23. ICAR-ICRP (All India Coordinated Research Project on Pearl Millet) (2014). Annual report 2013 2014. Retrieved [12th June 2014] from
  24. Knight, H., & Knight, M. R. (2011). Abiotic stress signaling pathways: Specificity and cross-talk. Trends in Plant Science,6, 262–267.Google Scholar
  25. Koch, K. E. (1996). Carbohydrate-modulated gene expression in plants. Plant Molecular Biology,47, 509–540.Google Scholar
  26. Lata, C., Gupta, S., & Prasad, M. (2013). Foxtail millet: A model crop for genetic and genomic studies inbioenergy grasses. Critical Review in Biotechnology,33, 328–343.Google Scholar
  27. Lata, C., Muthamilarasan, M., & Prasad, M. (2015). Drought stress responses and Signal transduction in plants. In G. K. Pandey (Ed.), Elucidation of abiotic stress signaling in plants (pp. 195–225). New York: Springer.Google Scholar
  28. Lawrence, C. J., Harper, L. C., Schaeffer, M. L., & Campbell, D. A. (2008). MaizeGDB: The maize model organism database for basic, translational and applied research. International Journal of Plant Genome,2008, 496957.Google Scholar
  29. Livak, K. J., & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2−CT method. Methods,25, 402–408.PubMedPubMedCentralGoogle Scholar
  30. Mishra, R. N., Reddy, P. S., Nair, S., Markandeya, G., & Reddy, M. K. (2007). Isolation and characterization of expressed sequence tags (ESTs) from subtracted cDNA libraries of Pennisetum glaucum seedlings. Plant Molecular Biology,64, 713–732.PubMedGoogle Scholar
  31. Mittal, S., Kumari, N., & Sharma, V. (2012). Differential response of salt stress on Brassica juncea; photosynthetic performance, protein, proline, D1 and antioxidant enzymes. Plant Physiology and Biochemistry,54, 17–26.PubMedGoogle Scholar
  32. Murata, N., Takahashi, S., Nishiyama, Y., & Allakhverdiev, S. I. (2007). Photoinhibition of photosystem II under environmental stress. Biochemistry Biophysics Acta,176, 414–421.Google Scholar
  33. Nakano, Y., & Asada, K. (1981). Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiology,22, 867–880.Google Scholar
  34. Nepolean, T., Shiriga, K., Sharma, R., Kumar, K., & Hossain, F. (2014). Genome-wide identification and expression pattern of drought-responsive members of the NAC family in maize. Meta Gene,2, 407–417.Google Scholar
  35. Odjegba, J., & Adeniyi, M. (2012). Responses of Celosia argentea L. to simulated drought and exogenous salicylic acid. Nature and Science,10(12), 2–6.Google Scholar
  36. Pandey, R. K., Maranville, J. W., & Admou, A. (2000). Deficit irrigation and nitrogen effects on maize in a sahelian environment Grain yield and yield components. Agricultural Water Management,46, 1–13.Google Scholar
  37. PoorMohammad Kiani, S., Grieu, P., Maury, P., Hewezi, T., Gentzbittel, L., & Sarrafia, A. (2007). Genetic variability for physiological traits under drought conditions and differential expression of water stress-associated genes in sunflower (Helianthus annuus L). Theoretical Applied Genetics,11(2), 193–207.Google Scholar
  38. Reddy, A. R., Chaitanya, K. V., & Vivekanandan, M. (2004). Drought induced responses of photosynthesis and antioxidant metabolism in higher plants. Journal of Plant Physiology,161, 1189–1202.Google Scholar
  39. Reddy, P. S., Srinivas, D., Kiran, K., Bhatnagar-Mathur, P., & Vadez, V. (2015). Cloning and validation of reference genes for normalization of gene expression studies in pearl millet [Pennisetum glaucum (L.) R. Br.] by quantitative real-time PCR. Plant Gene,1, 35–42.Google Scholar
  40. Ribaut, J. M., & Ragot, M. (2007). Marker-assisted selection to improve drought adaptation in maize: The backcross approach, perspectives, limitations, and alternatives. Journal of Experimental Botany,58, 351–360.PubMedGoogle Scholar
  41. Sairam, R. K., & Tyagi, A. (2004). Physiology and molecular biology of salinity stress tolerance in plants. Current Science,86, 407–421.Google Scholar
  42. Schittenhelm, S., & Schroetter, S. (2014). Comparison of drought tolerance of maize, sweet sorghum and sorghum-sudan grass hybrids. Journal of Agricultural Crop Science,200, 46–53.Google Scholar
  43. Schreiber, U., Bilger, W., & Neubauer, C. (1995). Chlorophyll Fluorescence as a nonintrusive indicator for rapid assessment for in vitro photosynthesis. In E. D. Byschulze & M. M. Cadwell (Eds.), Ecophysiology of photosynthesis (pp. 49–70). Berlin: Springer.Google Scholar
  44. Sehgal, D., Rajaram, V., Armstead, I., Vadez, V., Hash, T., & Yadav, R. (2010). Integration of gene-based markers in a pearl millet genetic map for identification of candidate genes underlying drought tolerance quantitative trait loci. BMC Plant Biology,12, 9–20.Google Scholar
  45. Sharma, I., Kumari, N., & Sharma, V. (2014). Defense gene expression in Sorghum bicolor against Macrophomina phaseolina in leaves and roots of susceptible and resistant cultivars. Journal of Plant Interaction, 9(1), 315–323.Google Scholar
  46. Sharma, V., Parmar, P., & Kumari, N. (2016). Differential cadmium stress tolerance in wheat genotypes under mycorrhizal association. Journal of Plant Nutrition,52, 1–12.Google Scholar
  47. Sharp, R. E., Poroyko, V., Hejlek, L. G., Spollen, W. G., Springer, G. K., & Bohnert, H. J. (2004). Root growth maintenance during water deficits: physiology to functional genomics. Journal of Experimental Botany,55(407), 2343–2351.PubMedGoogle Scholar
  48. Shinozaki, K., Yamaguchi-Shinozaki, K., & Seki, M. (2003). Regulatory network of gene expression in the drought and cold stress responses. Current Opinion in Plant Biology,6, 410–417.PubMedGoogle Scholar
  49. Vadez, V., Aparna, K., Rajaram, V., & Trushar, M. (2008). Identification of Aquaporin genes from pearlmillet [Pennisetum glaucum (L.) R. Br.]. An Open Access Journal Icrisat,12, 3–12.Google Scholar
  50. Vinocur, B., & Altman, A. (2005). Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Current Opinion in Biotechnology,16, 123–132.PubMedGoogle Scholar
  51. Wang, Y. J., Wisniewski, M., Melian, R., Cui, M. G., Webb, R., & Fuchigami, L. (2005). Over expression of cytosolic ascorbate peroxidase in tomato confers tolerance to chilling and salt stress. Journal of America Horticultural Science,130, 167–173.Google Scholar
  52. Xue, P., McIntyre, C., Glassop, D., & Shorter, R. (2008). Use of expression analysis to dissect alterationsin carbohydrate metabolism in wheat leaves during drought stress. Plant Molecular Biology,67, 197–214.PubMedGoogle Scholar
  53. Yamaguchi-Shinozaki, K., Kasuga, M., Liu, Q., Nakashima, K., Sakuma, Y., Abe, H., Shinwari, Z.K., Seki, M., & Shinozaki, K. (2003). Biological mechanisms of drought stress response. JIRCAS Working Report 1–8.Google Scholar
  54. Yao, L. M., Wang, B., Cheng, L. J., & Wu, T. L. (2013). Identification of key drought stress-related genes in the hyacinth bean. PLoS ONE,8(3), e58108. Scholar
  55. Zhang, M., Ara, N., Nakkanong, K., Lv, W., Yang, J., & Hu, Z. (2007). Antioxidant enzymatic activities and gene expression associated with heat tolerance in the stems and roots of two cucurbit species (“Cucurbita maxima” and “Cucurbita moschata”) and their interspecific inbred line “Maxchata”. International Journal of Molecular Science,14, 24008–24028. Scholar

Copyright information

© Indian Society for Plant Physiology 2019

Authors and Affiliations

  1. 1.Department of Plant Science and BiotechnologyFederal University Oye EkitiOye-EkitiNigeria
  2. 2.Department of BotanyUniversity of LagosAkokaNigeria
  3. 3.Centre for BiotechnologyAmity UniversityJaipurIndia
  4. 4.Department of BiotechnologyBanasthali VidyapithTonkIndia

Personalised recommendations