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SPL6 represses signalling outputs of ER stress in control of panicle cell death in rice

Nature Plants volume 4, pages 280–288 (2018)Cite this article

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Abstract

Inositol-requiring enzyme 1 (IRE1) is the most conserved transducer of the unfolded protein response that produces either adaptive or death signals depending on the amplitude and duration of its activation. Here, we report that SQUAMOSA PROMOTER-BINDING PROTEIN-LIKE 6 (SPL6)-deficient plants displayed hyperactivation of the endoplasmic reticulum (ER) stress sensor IRE1, leading to cell death in rice panicles, indicating that SPL6 is an essential survival factor for the suppression of persistent or intense ER stress conditions. Importantly, knockdown of the hyperactivated mRNA level of IRE1 rescues panicle apical abortion in the spl6-1 transgenic plants harbouring the IRE1-RNAi constructs, establishing the genetic linkage between the hyperactivation of IRE1 and cell death in spl6-1. Our findings reveal a novel cell survival machinery in which SPL6 represses the transcriptional activation of the ER stress sensor IRE1 in control of ER stress signalling outputs that hinge on a balance between adaptive and death signals for determining cell fates during ER stress.

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Fig. 1: Loss of function of SPL6 causes panicle apical abortion.
Fig. 2: SPL6 regulates panicle development.
Fig. 3: Knockout of SPL6 leads to precocious cell death.
Fig. 4: Loss of function of SPL6 induces hyperactivation of IRE1.
Fig. 5: Knockdown of the hyperactivated mRNA level of IRE1 rescues panicle apical abortion in spl6-1.
Fig. 6: SPL6 represses the transcriptional activation of IRE1.

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Acknowledgements

This study was supported by the Chinese Academy of Sciences (Strategic Priority Research Program XDPB0404), the Ministry of Science and Technology of China (National Key R&D Program of China, 2016YFD0100405), the National Natural Science Foundation of China (31770314 and 31570260) and the Chinese Academy of Sciences (XDA08010203). We thank the Rice T-DNA Insertion Sequence Database for providing the rice mutant lines; H.-T. Liu, X.-F. Yang and S.-Q. Zhao for suggestions and technical assistance; X.-Y. Gao, X.-S. Gao, J.-Q. Li and Z.-P. Zhang for assistance with electron microscopy and confocal microscopy.

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  1. National Key Laboratory of Plant Molecular Genetics, Institute of Plant Physiology & Ecology, Chinese Academy of Sciences, Shanghai, China

    Qing-Long Wang, Ai-Zhen Sun, Si-Ting Chen, Li-Sha Chen & Fang-Qing Guo

  2. CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology & Ecology, Chinese Academy of Sciences, Shanghai, China

    Fang-Qing Guo

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  1. Qing-Long Wang
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Contributions

F.-Q.G. and Q.-L.W. supervised the project and designed the experiments. Q.-L.W., A.-Z.S., S.-T.C. and L.-S.C. performed the experiments. Q.-L.W., A.-Z.S. and S.-T.C. analysed the data and interpreted the results. F.-Q.G. and Q.-L.W. wrote the manuscript.

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Correspondence to Fang-Qing Guo.

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Wang, QL., Sun, AZ., Chen, ST. et al. SPL6 represses signalling outputs of ER stress in control of panicle cell death in rice. Nature Plants 4, 280–288 (2018). https://doi.org/10.1038/s41477-018-0131-z

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