Abstract
Adoption of water-saving cultivation strategy for cereal crops benefits development of the sustainable agriculture worldwide. In this study, the effects of water supply on agronomic traits, ABA contents, drought response-associated physiological parameters, and expression patterns of the ABA receptor family genes during late stage were investigated. Under normal irrigation condition (NI, with irrigations performed prior to seed sowing, and at stages of jointing and flowering), the wheat cultivars, namely, the drought tolerant Cangmai 14 and the sensitive Jimai 325, displayed comparable agronomic traits (i.e. yields, yield components, and water use efficiencies), ABA contents, and the physiological traits associated with drought stress (i.e., proline and soluble sugar contents, and photosynthetic parameters). Under deficit irrigation (DI, without irrigation at flowering stage compared with NI), Cangmai 14 was much better on the agronomic traits, ABA contents, and the drought response-associated traits at late stage than Jimai 325. These results suggested that the improvement of drought response-associated traits contributed to the enhanced yield formation capacity of the drought-tolerant cultivars. Expression analysis on ABA receptor genes (i.e., PYL family ones) involving ABA signal perception indicated that TaPYL3, TaPYL5 and TaPYL8, three of the PYL family members, modified expression in the tested cultivars upon modified water supply copnditions, with more transcripts detected under DI than NI. Moreover, the expression levels of these genes were all shown to be higher in Cangmai 14 under DI than in Jimai 325. Transgene analysis on TaPYL3 validated that this gene exerted positive roles in modulating biomass production and photosynthetic function of plants under drought treatment. These results suggested the essential function of the ABA signaling genes in modulating plant drought response, whose enhanced transcription efficiencies positively impact on the drought response-associated physiological process, biomass production, and the yield formation capacity of wheat plants treated with DI through possibly an ABA-dependent pathway.
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References
Abid, M., Ali, S., Qi, L., Zahoor, R., Tian, Z., Jiang, D., Snider, J., & Dai, T. (2018). Physiological and biochemical changes during drought and recovery periods at tillering and jointing stages in wheat (Triticum aestivum L.). Scientific Reports, 8, 4615.
Abid, M., Tian, Z., Ata-Ul-Karim, S. T., Cui, Y., Liu, Y., Zahoor, R., Jiang, D., & Dai, T. (2016). Nitrogen nutrition improves the potential of wheat (Triticum aestivum L.) to alleviate the effects of drought stress during vegetative growth periods. Frontiers in Plant Science, 7, 981.
Abuauf, H., Haider, I., Jia, K. P., Ablazov, A., Mi, J., & Blilou, I. (2018). The Arabidopsis DWARF27 gene encodes an all-trans-/9-cis-β-carotene isomerase and is induced by auxin, abscisic acid and phosphate deficiency. Plant Science, 277, 33–42.
Anjum, S. A., Wang, L. C., Farooq, M., Hussain, M., Xue, L. L., & Zou, C. M. (2011). Brassinolide application improves the drought tolerance in maize through modulation of enzymatic antioxidants and leaf gas exchange. Journal of Agronomy and Crop Science, 197, 177–185.
Antoni, R., Gonzalez-Guzman, M., Rodriguez, L., Peirats-Llobet, M., Pizzio, G. A., Fernandez, M. A., De Winne, N., De Jaeger, G., Dietrich, D., & Bennett, M. J. (2013). PYRABACTIN RESISTANCE1-LIKE8 plays an important role for the regulation of abscisic acid signaling in root. Plant Physiology, 161, 931–941.
Bhaskara, G. B., Nguyen, T. T., & Verslues, P. E. (2012). Unique drought resistance functions of the highly ABA-induced clade A protein phosphatase 2Cs. Plant Physiology, 160, 379–395.
Blackman, C. J., Creek, D., Maier, C., Aspinwall, M. J., Drake, J. E., Pfautsch, S., O’Grady, A., Delzon, S., Medlyn, B. E., Tissue, D. T., Choat, B., Blackman, C. J., et al. (2019). Drought response strategies and hydraulic traits contribute to mechanistic understanding of plant dry-down to hydraulic failure. Tree Physiology, 39, 910–924.
Chong, L., Guo, P., Zhu, Y., Chong, L., et al. (2020). Mediator complex: A pivotal regulator of ABA signaling pathway and abiotic stress response in plants. International Journal of Molecular Sciences, 21(20), 7755.
Demirevska, K., Zasheva, D., Dimitrov, R., Simova-Stoilova, L., Stamenova, M., & Feller, U. (2009). Drought stress effects on Rubisco in wheat: Changes in the Rubisco large subunit. Acta Physiologae Plantarum, 31, 1129–1138.
Deng, X. P., Shan, L., Zhang, H. P., & Turner, N. C. (2006). Improving agricultural water use efficiency in arid and semiarid areas of China. Agricultural Water Managememt, 80, 23–40.
Du, X., Zhao, X., Liu, X., Guo, C., Lu, W., Gu, J., & Xiao, K. (2013). Overexpression of TaSRK2C1, wheat SNF1-related protein kinase gene, increases tolerance to dehydration, salt, and low temperature in transgenic tobacco. Plant Molecular Biology Reporter, 31, 810–821.
Duan, B., Yang, Y., Lu, Y., Korpelainen, H., Berninger, F., & Li, C. (2007). Interactions between drought stress, ABA and genotypes in Picea asperata. Journal of Experimental. Botany, 58, 3025–3036.
Earl, H., & Davis, R. F. (2003). Effect of drought stress on leaf and whole canopy radiation use efficiency and yield of maize. Agronomy Journal, 95, 688–696.
Farooq, M., Wahid, A., Kobayashi, N., Fujita, D., & Basra, S. M. A. (2009). Plant drought stress: Effects, mechanisms and management. Agronomy for Sustainable. Development, 29, 185–212.
Finkelstein, R. (2013). Abscisic acid synthesis and response. Arabidopsis Book, 11, e0166.
Fu, J., & Huang, B. (2001). Involvement of antioxidants and lipid peroxidation in the adaptation of two cool-season grasses to localized drought stress. Environmental and Experimental Botany, 45, 105–114.
Fujii, H., Chinnusamy, V., Rodrigues, A., Rubio, S., Antoni, R., Park, S. Y., Cutler, S. R., Sheen, J., Rodriguez, P. L., & Zhu, J. K. (2009). In vitro reconstitution of an abscisic acid signalling pathway. Nature, 462, 660–664.
Fujii, H., & Zhu, J. K. (2009). Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress. Proceedings of the National Academy of Sciences of USA, 106, 8380–8385.
Gholami, Z. A., Ehsanzadeh, P., Szumny, A., & Matkowski, A. (2018). Genotype-specific response of Foeniculum vulgare grain yield and essential oil composition to proline treatment under different irrigation conditions. Industrial Crops and Products, 124, 177–185.
Gonzalez-Guzman, M., Pizzio, G. A., Antoni, R., Vera-Sirera, F., Merilo, E., Bassel, G. W., Fernandez, M. A., Holdsworth, M. J., Perez-Amador, M. A., & Kollist, H. (2012). Arabidopsis PYR/PYL/RCAR receptors play a major role in quantitative regulation of stomatal aperture and transcriptional response to abscisic acid. The Plant Cell, 24, 2483–2496.
Guo, C., Zhao, X., Liu, X., Zhang, L., Gu, J., Li, X., Lu, W., & Xiao, K. (2013). Function of wheat phosphate transporter gene TaPHT2;1 in Pi translocation and plant growth regulation under replete and limited Pi supply conditions. Planta, 237, 1163–1178.
He, X., Xu, L., Pan, C., Gong, C., Wang, Y., Liu, X., Yu, Y., He, X., et al. (2020). Drought resistance of Camellia oleifera under drought stress: Changes in physiology and growth characteristics. PLoS ONE, 15(7), e0235795.
Khan, R., Ma, X., Shah, S., Wu, X., Shaheen, A., Xiao, L., Wu, Y., Wang, S., Khan, R., et al. (2020). Drought-hardening improves drought tolerance in Nicotiana tabacum at physiological, biochemical, and molecular levels. BMC Plant Biology, 20(1), 486.
Kim, H., Hwang, H., Hong, J. W., Lee, Y. N., Ahn, I. P., & Yoon, I. S. (2012). A rice orthologue of the ABA receptor, OsPYL/RCAR5, is a positive regulator of the ABA signal transduction pathway in seed germination and early seedling growth. Journal of Experimental Botany, 63, 1013–1024.
Kim, T.-H., Böhmer, M., Hu, H., Nishimura, N., & Schroeder, J. I. (2010). Guard cell signal transduction network: Advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annual Review of Plant Biology, 61, 561–591.
Ku, Y. S., Sintaha, M., Cheung, M. Y., Lam, H. M., Ku, Y. S., et al. (2018). Plant hormone signaling crosstalks between biotic and abiotic stress responses. International Journal of Molecular Sciences, 19(10), 3206.
Lawlor, D. W., & Cornic, G. (2002). Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. Plant Cell Environment, 25, 275–294.
Li, D., Batchelor, W. D., Zhang, D., Miao, H., Li, H., Song, S., Li, R., Li, D., et al. (2020). Analysis of melatonin regulation of germination and antioxidant metabolism in different wheat cultivars under polyethylene glycol stress. PLoS ONE, 15(8), e0237536.
Li, J., Li, Y., Yin, Z., Jiang, J., Zhang, M., Guo, X., Ye, Z., Zhao, Y., Xiong, H., Zhang, Z., Shao, Y., Jiang, C., Zhang, H., An, G., Paek, N. C., Ali, J., Li, Z., Li, J., et al. (2017). OsASR5 enhances drought tolerance through a stomatal closure pathway associated with ABA and H(2) O(2) signalling in rice. Plant Biotechnology Journal, 15, 183–196.
Liang, C., Liu, Y., Li, Y., Meng, Z., Rong, Y., Zhu, T., Wang, Y., Kang, S., Abid, M. A., Malik, W., Sun, G., Guo, S., & Zhang, R. (2017). Activation of ABA receptors gene GhPYL9-11A is positively correlated with cotton drought tolerance in transgenic Arabidopsis. Frontiers in Plant Science, 8, 1453.
Liu, F., Ma, H., Du, Z., Ma, B., Liu, X., Peng, L., Zhang, W., Liu, F., et al. (2019). Physiological response of North China red elder container seedlings to inoculation with plant growth-promoting rhizobacteria under drought stress. PLoS ONE, 14(12), e0226624.
Ludlow, M. M., & Muchow, R. C. (1990). A critical evaluation of traits for improving crop yields in water-limited environments. Advances in Agronomy, 43, 107–153.
Ma, Y., Szostkiewicz, I., Korte, A., Moes, D., Yang, Y., Christmann, A., & Grill, E. (2009). Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science, 324, 1064–1068.
Maryam, Y., & Parviz, E. (2017). Photosynthetic and antioxidative upregulation in drought-stressed sesame (Sesamum indicum L.) subjected to foliar-applied salicylic acid. Photosynthetica, 55, 611–622.
Mei, X. R., Zhong, X. L., Vadez, V., & Liu, X. Y. (2013). Improving water use efficiency of wheat crop varieties in the North China plain: Review and analysis. Journal of Integrative Agronomy, 12, 1243–1250.
Melcher, K., Ng, L. M., Zhou, X. E., Soon, F. F., Xu, Y., Suino-Powell, K. M., Park, S. Y., Weiner, J. J., Fujii, H., & Chinnusamy, V. (2009). A gate lock mechanism for hormone signalling by abscisic acid receptors. Nature, 462, 602–608.
Monakhova, O. F., & Chernyadev, I. I. (2002). Protective role of kartolin-4 in wheat plants exposed to soil drought. Applied Biochemistry and Microbiology, 38, 373–380.
Mustilli, A. C., Merlot, S., Vavasseur, A., Fenzi, F., & Giraudat, J. (2002). Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. The Plant Cell, 14, 3089–3099.
Park, S. Y., Fung, P., Nishimura, N., Jensen, D. R., Fujii, H., Zhao, Y., Lumba, S., Santiago, J., Rodrigues, A., & Chow, T. F. (2009). Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science, 324, 1068–1071.
Praba, M. L., Cairns, J. E., Babu, R. C., & Lafitte, H. R. (2009). Identification of physiological traits underlying cultivar differences in drought tolerance in rice and wheat. Journal of Agronomy and Crop Science, 195, 30–46.
Shokat, S., Großkinsky, D. K., Roitsch, T., Liu, F., Shokat, S., et al. (2020). Activities of leaf and spike carbohydrate-metabolic and antioxidant enzymes are linked with yield performance in three spring wheat genotypes grown under well-watered and drought conditions. BMC Plant Biology, 20(1), 400.
Soma, F., Takahashi, F., Suzuki, T., Shinozaki, K., Yamaguchi-Shinozaki, K., Soma, F., et al. (2020). Plant Raf-like kinases regulate the mRNA population upstream of ABA-unresponsive SnRK2 kinases under drought stress. Nature Communication, 11(1), 1373.
Sreenivasulu, N., Harshavardhan, V. T., Govind, G., Seiler, C., & Kohli, A. (2012). Contrapuntal role of ABA: Does it mediate stress tolerance or plant growth retardation under long-term drought stress? Gene, 506, 265–273.
Takahashi, F., Kuromori, T., Sato, H., Shinozaki, K., Takahashi, F., et al. (2018). Regulatory gene networks in drought stress responses and resistance in plants. Advances in Experimental Medicine and Biology, 1081, 189–214.
Takahashi, Y., Zhang, J., Hsu, P. K., Ceciliato, P. H. O., Zhang, L., Dubeaux, G., Munemasa, S., Ge, C., Zhao, Y., Hauser, F., Schroeder, J. I., Takahashi, Y., et al. (2020). MAP3Kinase-dependent SnRK2-kinase activation is required for abscisic acid signal transduction and rapid osmotic stress response. Nature Communication, 11, 12.
Tischer, S. V., Wunschel, C., Papacek, M., Kleigrewe, K., Hofmann, T., Christmann, A., & Grill, E. (2017). Combinatorial interaction network of abscisic acid receptors and coreceptors from Arabidopsis thaliana. Proceedings of the National Academy of Sciences of USA, 114, 10280–10285.
Turner, N. C., Wright, G. C., & Siddique, K. H. M. (2001). Adaptation of grain legumes (pulses) to water-limited environments. Advances in Agronomy, 71, 193–231.
Verma, R. K., Kumar, V. V., Yadav, S. K., Pushkar, S., Rao, M. V., Chinnusamy, V., Verma, R. K., et al. (2019). Overexpression of ABA receptor PYL10 gene confers drought and cold tolerance to Indica rice. Frontiers in Plant Science, 10, 1488.
Wahid, A., Gelani, S., Ashraf, M., & Foolad, M. R. (2007). Heat tolerance in plants: An overview. Environmental and Experimental Botany, 61, 199–223.
Wang, J. Q., Li, H., Liu, Q., Zeng, L. S., Wang, J. Q., et al. (2020). Effects of exogenous plant hormones on physiological characteristics and yield of sweet potato under drought stress. Ying Yong Sheng Tai Xue Bao, 31, 189–198.
Wang, P., Zhao, Y., Li, Z., Hsu, C. C., Liu, X., Fu, L., Hou, Y. J., Du, Y., Xie, S., Zhang, C., Gao, J., Cao, M., Huang, X., Zhu, Y., Tang, K., Wang, X., Tao, W. A., Xiong, Y., Zhu, J. K., Wang, P., et al. (2018). Reciprocal regulation of the TOR kinase and ABA receptor balances plant growth and stress response. Molecular Cell, 69, 100–112.
Wang, X. M., Wang, X. K., Su, Y. B., Zhang, H. X., Wang, X. M., et al. (2019). Land pavement depresses photosynthesis in urban trees especially under drought stress. Science of the Total Environment, 653, 120–130.
Wani, S. H., Kumar, V. 2015. Plant stress tolerance: engineering ABA: a Potent phytohormone. Transcriptomics: An Open Access 3:1000113 10.4172
Wu, J., Liu, M., Lü, A., & He, B. (2014). The variation of the water deficit during the winter wheat growing season and its impact on crop yield in the North China Plain. International Journal of Biometeorology, 58, 1951–1960.
Yu, J., Jiang, M., Guo, C., Yu, J., et al. (2019). Crop pollen development under drought: From the phenotype to the mechanism. International Journal of Molecular Sciences, 20(7), 1550.
Zhang, C., Liu, J., Shang, J., Cai, H., Zhang, C., et al. (2018a). Capability of crop water content for revealing variability of winter wheat grain yield and soil moisture under limited irrigation. Science of the Total Environment, 631, 677–687.
Zhang, D., Li, R., Batchelor, W. D., Ju, H., Li, Y., Zhang, D., et al. (2018b). Evaluation of limited irrigation strategies to improve water use efficiency and wheat yield in the North China Plain. PLoS ONE, 13(1), e0189989.
Zhang, J., Wang, G., Zhou, D., & Xiao, K. (2018c). Yield formation capacity, soil water consumption, property, and plant water use efficiency of wheat under water-saving conditions in North China plain. Turkish Journal of Field Crops, 23(2), 107–116.
Zhang, T., & Huang, Y. (2012). Impacts of climate change and inter-annual variability on cereal crops in China from 1980 to 2008. Journal of the Science of Food and Agriculture, 92, 1643–1652.
Zhao, Y., Chan, Z., Gao, J., Xing, L., Cao, M., Yu, C., Hu, Y., You, J., Shi, H., Zhu, Y., Gong, Y., Mu, Z., Wang, H., Deng, X., Wang, P., Bressan, R. A., Zhu, J. K., Zhao, Y., et al. (2016). ABA receptor PYL9 promotes drought resistance and leaf senescence. Proceedings of the National Academy of Sciences of USA, 113, 1949–1954.
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This work was financially supported by Chinese National Key Research and Development Project on Science and Technology (2017YFD0300902) and National Natural Science Foundation of China (31872869).
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Bai, X., Guo, L., Lin, R. et al. Characterization of Yields, Osmotic Stress-associated Traits, and Expression Patterns of ABA Receptor Genes in Winter Wheat Under Deficit Irrigation. Int. J. Plant Prod. 15, 419–429 (2021). https://doi.org/10.1007/s42106-021-00146-4
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DOI: https://doi.org/10.1007/s42106-021-00146-4