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Improvement of multiple agronomic traits by a disease resistance gene via cell wall reinforcement

Abstract

The major disease resistance gene Xa4 confers race-specific durable resistance against Xanthomonas oryzae pv. oryzae, which causes the most damaging bacterial disease in rice worldwide. Although Xa4 has been one of the most widely exploited resistance genes in rice production worldwide, its molecular nature remains unknown. Here we show that Xa4, encoding a cell wall-associated kinase, improves multiple traits of agronomic importance without compromising grain yield by strengthening the cell wall via promoting cellulose synthesis and suppressing cell wall loosening. Strengthening of the cell wall by Xa4 enhances resistance to bacterial infection, and also increases mechanical strength of the culm with slightly reduced plant height, which may improve lodging resistance of the rice plant. The simultaneous improvement of multiple agronomic traits conferred by Xa4 may account for its widespread and lasting utilization in rice breeding programmes globally.

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Figure 1: Responses of transgenic plants to Xoo.
Figure 2: Effects of Xa4 on mechanical strength.
Figure 3: Effects of Xa4 on plant height.
Figure 4: Effects of Xa4 on CesA and EXPA gene expression in the rice–Xoo (PXO61) interaction.
Figure 5: Effects of an incompatible reaction on Xa4 expression.
Figure 6: Effects of Xa4 on the accumulation of JA-Ile and phytoalexins after PXO61 infection.

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Acknowledgements

We thank Y. Zhou of the Institute of Genetics and Developmental Biology, Chinese Academy of Science and M. Gu of the Yangzhou University for providing rice cesa4 mutant seeds, M. Xu of the China Agricultural University for providing the ZmWAK construct and L. Peng of the Huazhong Agricultural University for helping with the analysis of the cell wall composition. We also thank the RIKEN Yokohama Institute for providing CesA4 (J023093O20), CesA7 (J023009D02) and CesA9 (J023081B08) cDNA clones. This work was supported by grants from the National Natural Science Foundation of China (31330062), the National Key Research and Development Program of China (2016YFD0100903), and the National Program of High Technology Development of China (2014AA10A600).

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Authors

Contributions

K.H. designed and performed most of the experiments, analysed the data and drafted the manuscript; J.C., J.Z., F.X., Y.K., H.Z., W.X., H.L., Y.Cui., Y.Cao. and X.S. helped to perform histology, electron microscopy, protein subcellular localization, DNA hybridization and metabolite analyses and to generate some transgenic rice plants; J.X., X.L. and Q.Z. provided biochemical and molecular analysis support and field management; S.W. supervised the project, designed some of the experiments, interpreted data and revised the manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Shiping Wang.

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The authors declare no competing financial interests.

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Hu, K., Cao, J., Zhang, J. et al. Improvement of multiple agronomic traits by a disease resistance gene via cell wall reinforcement. Nature Plants 3, 17009 (2017). https://doi.org/10.1038/nplants.2017.9

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