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MeSPL9 attenuates drought resistance by regulating JA signaling and protectant metabolite contents in cassava

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Analysis of drought-related genes in cassava shows the involvement of MeSPL9 in drought stress tolerance and overexpression of a dominant-negative form of this gene demonstrates its negative roles in drought stress resistance.

Abstract

Drought stress severely impairs crop yield and is considered a primary threat to food security worldwide. Although the SQUAMOSA promoter binding protein-like 9 (SPL9) gene participates extensively in numerous developmental processes and in plant response to abiotic stimuli, its role and regulatory pathway in cassava (Manihot esculenta) response to the drought condition remain elusive. In the current study, we show that cassava SPL9 (MeSPL9) plays negative roles in drought stress resistance. MeSPL9 expression was strongly repressed by drought treatment. Overexpression of a dominant-negative form of miR156-resistant MeSPL9, rMeSPL9-SRDX, in which a 12-amino acid repressor sequence was fused to rMeSPL9 at the C terminus, conferred drought tolerance without penalizing overall growth. rMeSPL9-SRDX-overexpressing lines not only exhibited increased osmoprotectant metabolites including proline and anthocyanin, but also accumulated more endogenous jasmonic acid (JA) and soluble sugars. Transcriptomic and real-time PCR analysis suggested that differentially expressed genes were involved in sugar or JA biosynthesis, signaling, and metabolism in transgenic cassava under drought conditions. Exogenous application of JA further confirmed that JA conferred improved drought resistance and promoted stomatal closure in cassava leaves. Taken together, our findings suggest that MeSPL9 affects drought resistance by modulating protectant metabolite levels and JA signaling, which have substantial implications for engineering drought tolerant crops.

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Acknowledgements

This work was supported by the Hainan Provincial Natural Science Foundation of China (320MS097), the National Key Research and Development Program of China (2019YFD1001105, 2019YFD1000500, 2018YFD1000500), and the Central Public-interest Scientific Institution Basal Research Fund for Chinese Academy of Tropical Agricultural Sciences (1630052021026).

Funding

Natural Science Foundation of Hainan Province, 320MS097, Shuxia Li

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  1. Shuxia Li and Zhihao Cheng are contributed equally to this work.

Authors and Affiliations

  1. Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Xueyuan Road 4, Haikou, 571101, China

    Shuxia Li, Zhibo Li, Shiman Dong, Xiaoling Yu, Pingjuan Zhao, Wenbin Liao & Ming Peng

  2. Haikou Experimental Station, Chinese Academy of Tropical Agricultural Sciences, Xueyuan Road 4, Haikou, 571101, China

    Zhihao Cheng

  3. School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Dongchuan Road 800, Shanghai, 200240, China

    Xiang Yu

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  1. Shuxia Li
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Contributions

M.P. and X.Y. designed the experiments; S.L., Z.L., S.D., X.Y., P.Z., Z.C., and W.L. conducted the experiments; S.L., X.Y., and Z.C. wrote the manuscript. We would like to thank TopEdit (www.topeditsci.com) for its linguistic assistance during the preparation of this manuscript.

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Correspondence to Shuxia Li, Xiang Yu or Ming Peng.

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Li, S., Cheng, Z., Li, Z. et al. MeSPL9 attenuates drought resistance by regulating JA signaling and protectant metabolite contents in cassava. Theor Appl Genet 135, 817–832 (2022). https://doi.org/10.1007/s00122-021-04000-z

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