Biologia Plantarum 63: 519-528, 2019 | DOI: 10.32615/bp.2019.085

Physiology and proteomics of two maize genotypes with different drought resistance

Y.H. LI1,2, J.Y. CUI1, Q. ZHAO2, Y.Z. YANG2, L. WEI1, M.D. YANG1, F. LIANG2, S.T. DING2, T.C. WANG1,*
1 Collaborative Innovation Center of Henan Grain Crops, Agronomy College of Henan Agricultural University, Zhengzhou, 450002, Henan, P.R. China
2 College of Life Sciences, Zhengzhou Normal University, Zhengzhou 450044, Henan, P.R. China

The aim of this study was to investigate the physiological basis and molecular mechanism of genotypic variation in drought response of maize seedlings. Comparative physiological and proteomic analyses were conducted in the leaves of drought-tolerant Liyu 35 (LY) and drought-sensitive Denghai 605 (DH) maize genotype seedlings. Drought induced a significant decrease of relative water content and osmotic potential of leaves, length and volume of roots, and total dry weight, but significantly increased malondialdehyde in DH seedlings. However, root dry weight , proline content and antioxidant enzyme activities increased more in LY than in DH. Forty-two spots in LY and 17 spots in DH that showed significant abundance variations were identified by matrix-assisted laser desorption/ionization time-of-flight/time-of-flight mass spectrometry. These drought-responsive proteins were mainly involved in biological processes of photosynthesis, defense and oxidative stress, carbohydrate and energy metabolism, protein synthesis and processing, and cell wall biogenesis and degradation. Among them, proteins involved in defense and oxidative stress, and protein synthesis and processing were largely enriched in the LY genotype, which may contribute to a natural variation of drought resistance between LY and DH genotypes. The altered protein abundance and corresponding physiological-biochemical response shed some light on molecular mechanisms related to drought tolerance in drought-tolerant maize and provide key candidate proteins for genetic improvement of maize.

Keywords: maize, drought stress, relative water content, reactive oxygen species, proteomics, drought-responsive protein.

Received: August 29, 2018; Revised: October 18, 2018; Accepted: January 18, 2019; Published online: July 8, 2019Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
LI, Y.H., CUI, J.Y., ZHAO, Q., YANG, Y.Z., WEI, L., YANG, M.D., ... WANG, T.C. (2019). Physiology and proteomics of two maize genotypes with different drought resistance. Biologia plantarum, 63, 519-528. doi: 10.32615/bp.2019.085.
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    Supplementary files

    Download fileLi5935 Suppl.pdf

    File size: 839.2 kB

    References

    1. Ahn, J.C., Kim, D.W., You, Y.N., Seok, M.S., Park, J.M., Hwang, H., Kim, B.G., Luan, S., Park, H.S., Cho, H.S.: Classification of rice (Oryza sativa I. japonica nipponbare) immunophilins (FKBPs, CYPs) and expression patterns under water stress. - BMC Plant Biol. 10: 1-22, 2010. Go to original source...
    2. Anjum, S.A., Ashraf, U., Tanveer, M., Khan, I., Hussain, S., Shahzad, B., Zohaib, A., Abbas, F., Saleem, M.F., Ali, I., Wang, L.C.: Drought induced changes in growth, osmolyte accumulation and antioxidant metabolism of three maize hybrids. - Front. Plant Sci. 8: 69, 2017. Go to original source...
    3. Aranjuelo, I., Molero, G., Erice, G., Avice, J.C., Nogues, S.: Plant physiology and proteomics reveals the leaf response to drought in alfalfa (Medicago sativa L.). - J. exp. Bot. 62: 111-123, 2011. Go to original source...
    4. Ashraf, M.: Inducing drought tolerance in plants: Recent advances. - Biotechnol. Adv. 28: 169-183, 2010. Go to original source...
    5. Bates, L.S., Waldren, R.P., Teare, I.D.: Rapid determination of free proline for water-stress studies. - Plant Soil. 39: 205-207, 1973. Go to original source...
    6. Beauchamp, C., Fridovich, I.: Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels. - Anal. Biochem. 44: 276-287, 1971. Go to original source...
    7. Benesova, M., Hola, D., Fischer, L., Jedelsky, P.L., Hnilicka, F., Wilhelmova, N., Rothova, O., Kocova, M., Prochazkova, D., Honnerova, J., Fridrichova, L., Hnilickova, H.: The physiology and proteomics of drought tolerance in maize: early stomatal closure as a cause of lower tolerance to short-term dehydration? - PLoS ONE. 7: e38017, 2012. Go to original source...
    8. Boyer, J.S.: Grain yields with limited water. - J. exp. Bot. 55: 2385-2394, 2004. Go to original source...
    9. Brandts, J.F., Halvorson, H.R., Brennan, M.: Consideration of the possibility that the slow step in protein denaturation reactions is due to cis-trans isomerism of proline residues. - Biochemistry 14: 4953-4963, 1975. Go to original source...
    10. Budak, H., Akpinar, B.A., Unver, T., Turktas, M.: Proteome changes in wild and modern wheat leaves upon drought stress by two-dimensional electrophoresis and nanoLC-ESI-MS/MS. - Plant mol. Biol. 83: 89-103, 2013. Go to original source...
    11. Caruso, G., Cavaliere, C., Foglia, P., Gubbiotti, R., Samperi, R., Laganà, A.: Analysis of drought responsive proteins in wheat (Triticum durum) by 2D-PAGE and MALDI-TOF mass spectrometry. - Plant Sci. 177: 570-576, 2009. Go to original source...
    12. Chang, L.L., Guo, A.P., Jin, X., Yang, Q., Wang, D., Sun, Y., Huang, Q.X., Wang, L.M., Peng, C.Z., Wang, X.C.: The beta subunit of glyceraldehyde 3-phosphate dehydrogenase is an important factor for maintaining photosynthesis and plant development under salt stress-Based on an integrative analysis of the structural, physiological and proteomic changes in chloroplasts in Thellungiella halophila. - Plant Sci. 236: 223-238, 2015. Go to original source...
    13. Chen, D.Q., Wang, S.W., Cao, B.B., Cao, D., Leng, G.H., Li, H.B., Yin, L.N., Shan, L., Deng, X.P.: Genotypic variation in growth and physiological response to drought stress and re-watering reveals the critical role of recovery in drought adaptation in maize seedlings. - Front. Plant Sci. 6: 1241, 2016. Go to original source...
    14. Davidson, R.M., Reeves, P.A., Manosalva, P.M., Leach, J.E.: Germins: A diverse protein family important for crop improvement. - Plant Sci. 177: 499-510, 2009. Go to original source...
    15. Deeba, F., Pandey, A.K., Ranjan, S., Mishra, A., Singh, R., Sharma, Y.K., Shirke, P.A., Pandey, V.: Physiological and proteomic responses of cotton (Gossypium herbaceum L.) to drought stress. - Plant Physiol. Biochem. 53: 6-18, 2012. Go to original source...
    16. Dipierro, S., Leonardis, S.D.: The ascorbate system and lipid peroxidation in stored potato (Solanum tuberosum L. ) tubers. - J. exp. Bot. 48: 779 -783, 1997. Go to original source...
    17. Dooki, A.D., Mayer-Posner, F.J., Askari, H., Zaiee, A.A., Salekdeh, G.H.: Proteomic responses of rice young panicles to salinity. - Proteomics 6: 6498-6507, 2006. Go to original source...
    18. Faghani, E., Gharechahi, J., Komatsu, S., Mirzaei, M., Khavarinejad, R.A., Najafi, F., Farsad, L.K., Salekdeh, G.H.: Comparative physiology and proteomic analysis of two wheat genotypes contrasting in drought tolerance. - J. Proteom. 114: 1-15, 2015. Go to original source...
    19. Farooq, M., Wahid, A., Kobayashi, N., Fujita, D., Basra, S.M.A.: Plant drought stress: effects, mechanisms and management. - Agron. Sustain. Dev. 29: 185-212, 2009. Go to original source...
    20. Fujimori, N., Enoki, S., Suzuki, A., Naznin, H.A., Shimizu, M., Suzuki, S.: Grape apoplasmic β-1,3-glucanase confers fungal disease resistance in Arabidopsis. - Sci. Hort. 200: 105-110, 2016. Go to original source...
    21. Fukayama, H., Ueguchi, C., Nishikawa, K., Katoh, N., Ishikawa, C., Masumoto, C., Hatanaka, T., Misoo, S.: Overexpression of rubisco activase decreases the photosynthetic CO2 assimilation rate by reducing rubisco content in rice leaves. - Plant Cell Physiol. 53: 976-986, 2012. Go to original source...
    22. Gill, S.S., Tuteja, N.: Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. - Plant Physiol. Biochem. 48: 909-930, 2010. Go to original source...
    23. Guo, Z., Ou, W., Lu, S., Zhong, Q.: Differential responses of antioxidative system to chilling and drought in four rice cultivars differing in sensitivity. - Plant Physiol. Biochem. 44: 828-836, 2006. Go to original source...
    24. Hajheidari, M., Eivazi, A., Buchanan, B.B., Wong, J.H., Majidi, I.: Proteomics uncovers a role for redox in drought tolerance in wheat. - J. Proteome Res. 6: 1451-1460, 2007. Go to original source...
    25. Hajheidari, M., Abdollahian-Noghabi, M., Askari, H., Heidari, M., Sadeghian, S.Y., Ober, E.S., Salekdeh, G.H.: Proteome analysis of sugar beet leaves under drought stress. - Proteomics 5: 950-960, 2005. Go to original source...
    26. Hammerschmidt, R., Nuckles, E.M., Kuć, J.: Association of enhanced peroxidase activity with induced systemic resistance of cucumber to Colletotrichum lagenarium. - Physiol. Plant Pathol. 20: 73-82, 1982. Go to original source...
    27. He, Y., Yu, C.L., Zhou, L., Chen, Y., Liu, A., Jin, J.H., Hong, J., Qi, Y.H., Jiang, D.: Rubisco decrease is involved in chloroplast protrusion and Rubisco-containing body formation in soybean (Glycine max.) under salt stress. - Plant Physiol. Biochem. 74: 118-124, 2014. Go to original source...
    28. Hu, X.L., Lu, M.H., Li, C.H., Liu, T.X., Wang, W., Wu, J.Y., Tai, F.J., Li, X., Zhang, J.: Differential expression of proteins in maize roots in response to abscisic acid and drought. - Acta Physiol. Plant. 33: 2437-2446, 2011. Go to original source...
    29. Jones, H.G.: Monitoring plant and soil water status: established and novel methods revisited and their relevance to studies of drought tolerance. - J. exp. Bot. 58: 119-130, 2007.
    30. Kakumanu, A., Ambavaram, M.M., Klumas, C., Krishnan, A., Batlang, U., Myers, E., Grene, R., Pereira, A.: Effects of drought on gene expression in maize reproductive and leaf meristem tissue revealed by RNA-Seq. - Plant Physiol. 160: 846-867, 2012. Go to original source...
    31. Katam, R., Sakata, K., Suravajhala, P., Pechan, T., Kambiranda, D.M., Naik, K.S., Guo, B., Basha, S.M.: Comparative leaf proteomics of drought-tolerant and -susceptible peanut in response to water stress. - J. Proteom. 143: 209-226, 2016. Go to original source...
    32. Kausar, R., Arshad, M., Shahzad, A., Komatsu, S.: Proteomics analysis of sensitive and tolerant barley genotypes under drought stress. - Amino Acids. 44: 345-359, 2013. Go to original source...
    33. Kok, B., Forbush, B., McGloin, M.: Cooperation of charges in photosynthetic O2 evolution-I. A linear four step mechanism. - Photochem. Photobiol. 11: 457-475, 1970. Go to original source...
    34. Król, A., Weidner, S.: Changes in the proteome of grapevine leaves (Vitis vinifera L.) during long-term drought stress. - J. Plant Physiol. 211: 114-126, 2017. Go to original source...
    35. Kumari, S., Roy, S., Singh, P., Singla-Pareek, S.L., Pareek, A.: Cyclophilins: proteins in search of function. - Plant Signal. Behav. 8: e22734, 2013. Go to original source...
    36. Lascano, H.R., Antonicelli, G.E., Luna, C.M., Melchiorre, M.N., Gómez, L.D., Racca, R.W., Trippi, V.S., Casano, L.M.: Antioxidant system response of different wheat cultivars under drought: field and in vitro studies. - Funct. Plant Biol. 28: 1095-1102, 2001. Go to original source...
    37. Lee, B.R., Jung, W.J., Lee, B.H., Avice, J.C., Ourry, A., Kim, T.H.: Kinetics of drought-induced pathogenesis-related proteins and its physiological significance in white clover leaves. - Physiol. Plant. 132: 329-337, 2008. Go to original source...
    38. Lee, D.G., Ahsan, N., Lee, S.H., Kang, K.Y., Bahk, J.D., Lee, I.J., Lee, B.H.: A proteomic approach in analyzing heat-responsive proteins in rice leaves. - Proteomics 7: 3369-3383, 2007. Go to original source...
    39. Liu, T.X., Zhang, L., Yuan, Z.L., Hu, X.L., Lu, M.H., Wang, W., Wang, Y.: Identification of proteins regulated by ABA in response to combined drought and heat stress in maize roots. - Acta Physiol. Plant. 35: 501-513, 2012.
    40. Loggini, B., Scartazza, A., Brugnoli, E., Navari-Izzo, F.: Antioxidative defense system, pigment composition, and photosynthetic efficiency in two wheat cultivars subjected to drought. - Plant Physiol. 119: 1091-1099, 1999. Go to original source...
    41. Mahajan, S., Tuteja, N.: Cold, salinity and drought stresses: an overview. - Arch. Biochem. Biophys. 444: 139-158, 2005. Go to original source...
    42. Maheswari, M., Tekula, V.L., Yellisetty, V., Sarkar, B., Yadav, S.K., Singh, J., G, S.B., Kumar, A., Amirineni, S., Narayana, J., Maddi, V.: Functional mechanisms of drought tolerance in maize through phenotyping and genotyping under well watered and water stressed conditions. - Eur. J. Agron. 79: 43-57, 2016. Go to original source...
    43. Marok, M.A., Tarrago, L., Ksas, B., Henri, P., Abrous-Belbachir, O., Havaux, M., Rey, P.: A drought-sensitive barley variety displays oxidative stress and strongly increased contents in low-molecular weight antioxidant compounds during water deficit compared to a tolerant variety. - J. Plant Physiol. 170: 633-645, 2013. Go to original source...
    44. Mo, Y.L., Yang, R.P., Liu, L.H., Gu, X.R., Yang, X.Z., Wang, Y.Q., Zhang, X., Li, H.: Growth, photosynthesis and adaptive responses of wild and domesticated watermelon genotypes to drought stress and subsequent re-watering. - Plant Growth Regul. 79: 229-241, 2016. Go to original source...
    45. Nuccio, M.L., Wu, J., Mowers, R., Zhou, H.P., Meghji, M., Primavesi, L.F., Paul, M.J., Chen, X., Gao, Y., Haque, E., Basu, S.S., Lagrimini, L.M.: Expression of trehalose-6-phosphate phosphatase in maize ears improves yield in well-watered and drought conditions. - Nat. Biotechnol. 33: 862-869, 2015. Go to original source...
    46. Ogbonnaya, C.I., Nwalozie, M.C., Roy-Macauley, H., Annerose, D.J.M.: Growth and water relations of Kenaf (Hibiscus cannabinus L.) under water deficit on a sandy soil. - Ind. Crops. Products. 8: 65-76, 1998. Go to original source...
    47. Parida, A.K., Jha, B.: Salt tolerance mechanisms in mangroves: a review. - Trees 24: 199-217, 2010. Go to original source...
    48. Plomion, C., Lalanne, C., Claverol, S., Meddour, H., Kohler, A., Bogeat-Triboulot, M.B., Barre, A., Le Provost, G., Dumazet, H., Jacob, D., Bastien, C., Dreyer, E., de Daruvar, A., Guehl, J.M., Schmitter, J.M., Martin, F., Bonneu, M.: Mapping the proteome of poplar and application to the discovery of drought-stress responsive proteins. - Proteomics 6: 6509-6527, 2006. Go to original source...
    49. Ribaut, J.M., Jiang, C., Gonzalez-de-Leon, D., Edmeades, G.O., Hoisington, D.A.: Identification of quantitative trait loci under drought conditions in tropical maize. - Tag Theor. Appl. Genet. 94: 887-896, 1997. Go to original source...
    50. Souza, T.C., César, M.P., Castro, E.M., Albuquerque, P.E.P., Marabesi, M.A.: The influence of ABA on water relation, photosynthesis parameters, and chlorophyll fluorescence under drought conditions in two maize hybrids with contrasting drought resistance. - Acta Physiol. Plant. 35: 515-527, 2012.
    51. Spreitzer, R.J.: Questions about the complexity of chloroplast ribulose-1,5-bisphosphate carboxylase/oxygenase. - Photosynth. Res. 60: 29-42, 1999. Go to original source...
    52. Spreitzer, R.J., Salvucci, M.E.: Rubisco: structure, regulatory interactions, and possibilities for a better enzyme. - Annu. Rev. Plant Biol. 53: 449-475, 2002. Go to original source...
    53. Sugihara, K., Hanagata, N., Dubinsky, Z., Baba, S., Karube, I.: Molecular characterization of cDNA encoding oxygen evolving enhancer protein 1 increased by salt treatment in the mangrove Bruguiera gymnorrhiza. - Plant Cell Physiol. 41: 1279-1285, 2000. Go to original source...
    54. Takahashi, S., Murata, N.: How do environmental stresses accelerate photoinhibition? - Trends Plant Sci. 13: 178-182, 2008. Go to original source...
    55. Tang, L., Kim, M.D., Yang, K.S., Kwon, S.Y., Kim, S.H., Kim, J.S., Yun, D.J., Kwak, S.S., Lee, H.S.: Enhanced tolerance of transgenic potato plants overexpressing nucleoside diphosphate kinase 2 against multiple environmental stresses. - Transgenic. Res. 17: 705-715, 2008. Go to original source...
    56. Thatcher, S.R., Danilevskaya, O.N., Meng, X., Beatty, M., Zastrow-Hayes, G., Harris, C., Van Allen, B., Habben, J., Li, B.: Genome-wide analysis of alternative splicing during development and drought stress in maize. - Plant Physiol. 170: 586-599, 2016. Go to original source...
    57. Tikhonov, A.N.: pH-Dependent regulation of electron transport and ATP synthesis in chloroplasts. - Photosynth. Res. 116: 511-534, 2013. Go to original source...
    58. Urban, M.O., Vašek, J., Klíma, M., Krtková, J., Kosová, K., Prášil, I.T., Vítámvás, P.: Proteomic and physiological approach reveals drought-induced changes in rapeseeds: Water-saver and water-spender strategy. - J. Proteom. 152: 188-205, 2016.
    59. Vítámvás, P., Urban, M.O., Škodáček, Z., Kosová, K., Pitelková, I., Vítámvás, J., Renaut, J., Prášil, I.T.: Quantitative analysis of proteome extracted from barley crowns grown under different drought conditions. - Front. Plant Sci. 6: 479, 2015. Go to original source...
    60. Wang, W., Vignani, R., Scali, M., Cresti, M.: A universal and rapid protocol for protein extraction from recalcitrant plant tissues for proteomic analysis. - Electrophoresis 27: 2782-2786, 2006. Go to original source...
    61. Wang, Z., Wang, Z., Shi, L., Wang, L., Xu, F.: Proteomic alterations of Brassica napus root in response to boron deficiency. - Plant Mol.Biol. 74: 265-278, 2010. Go to original source...
    62. Xie, H., Yang, D.H., Yao, H., Bai, G., Zhang, Y.H., Xiao, B.G.: iTRAQ-based quantitative proteomic analysis reveals proteomic changes in leaves of cultivated tobacco (Nicotiana tabacum) in response to drought stress. - Biochem. Biophy. Res. Commun. 469: 768-775, 2016. Go to original source...
    63. Xu, J., Yuan, Y.B., Xu, Y.B., Zhang, G.Y., Guo, X.S., Wu, F.K., Wang, Q., Rong, T.Z., Pan, G.T., Cao, M.J., Tang, Q.L., Gao, S.B., Liu, Y.X., Wang, J., Lan, H., Lu, Y.L.: Identification of candidate genes for drought tolerance by whole-genome resequencing in maize. - BMC Plant Biol. 14: 1-15, 2014. Go to original source...
    64. Yang, L.M., Fountain, J.C., Wang, H., Ni, X.Z., Ji, P.S., Lee, R.D., Kemerait, R.C., Scully, B.T., Guo, B.Z.: Stress sensitivity is associated with differential accumulation of reactive oxygen and nitrogen species in maize genotypes with contrasting levels of drought tolerance. - Int. J. Mol. Sci. 16: 24791-24819, 2015. Go to original source...
    65. Zhao, F., Zhang, D., Zhao, Y., Wang, W., Yang, H., Tai, F., Li, C., Hu, X.: The difference of physiological andpProteomic changes in maize leaves adaptation to drought, heat, and combined both stresses. - Front. Plant Sci. 7: 1471, 2016. Go to original source...

    Return to the content