A MAPK cascade downstream of IDA–HAE/HSL2 ligand–receptor pair in lateral root emergence

Abstract

Lateral root (LR) emergence is a highly coordinated process involving precise cell–cell communication. Here, we show that MITOGEN-ACTIVATED PROTEIN KINASE3 (MPK3) and MPK6, and their upstream MAP-kinase kinases (MAPKKs), MKK4 and MKK5, function downstream of HAESA (HAE)/HAESA-LIKE2 (HSL2) and their ligand INFLORESCENCE DEFICIENT IN ABSCISSION (IDA) during LR emergence. Loss of function of MKK4/MKK5 or MPK3/MPK6 results in restricted passage of the growing lateral root primordia (LRP) through the overlaying endodermal, cortical and epidermal cell layers, leading to reduced LR density. The MKK4/MKK5–MPK3/MPK6 module regulates the expression of cell wall remodelling genes in cells overlaying LRP and therefore controls pectin degradation in the middle lamella. Expression of constitutively active MKK4 or MKK5 driven by the HAE or HSL2 promoter fully rescues the LR emergence defect in the ida and hae hsl2 mutants. In addition, the MKK4/MKK5–MPK3/MPK6 module is indispensable in auxin-facilitated LR emergence. Our study provides insights into the auxin-governed and IDA–HAE/HLS2 ligand–receptor pair-mediated LR emergence process.

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Fig. 1: Loss of function of MPK3/MPK6 or MKK4/MKK5 results in reduced LR density.
Fig. 2: Loss of function of MKK4/MKK5 or MPK3/MPK6 leads to a delayed LR emergence and ruptured epidermal cells as the growing LRP push their way out.
Fig. 3: Mutation of MKK4/MKK5 and MPK3/MPK6 results in a pectin degradation defect in cells overlaying LRP.
Fig. 4: Loss of function of MKK4/MKK5 and MPK3/MPK6 results in compromised expression of CWR genes.
Fig. 5: MKK4/MKK5–MPK3/MPK6 module functions downstream of IDA and HAE/HSL2 during LR emergence.
Fig. 6: Functional MKK4/MKK5 and MPK3/MPK6 are required for auxin-facilitated LR emergence.

Data availability

All data generated or analysed in this study are included in this article and Supplementary Information files. The data that support the findings of this study are available from the corresponding author upon request.

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Acknowledgements

This research was supported by the grants from Zhejiang Provincial Natural Science Foundation of China (no. LR18C020001), 111 project (no. B14027), National Natural Science Foundation of China (no. 31570297) and Zhejiang University Special Fund for Young Researchers (no. 2018QNA6002) to J.X. We thank W. Lukowitz (University of Georgia, Athens, Georgia, USA) for mkk4 and mkk5 single TILLING mutant seeds.

Author information

Q.Z., J.X. and S.Z. designed the project. Q.Z., Y.S., S.G., M.Z., T.Z., X.H. and Y.L. ran the experiments. Q.Z., J.W., S.Z. and J.X. analysed the results. Q.Z., S.Z. and J.X. wrote the manuscript.

Correspondence to Shuqun Zhang or Juan Xu.

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The authors declare no competing interests.

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Journal peer review information Nature Plants thanks Tom Beeckman, Melinka Butenko, Jean Colcombet and other anonymous reviewers for their contribution to the peer review of this work.

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Supplementary Figures 1–22 and Supplementary Tables 1–3.

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Zhu, Q., Shao, Y., Ge, S. et al. A MAPK cascade downstream of IDA–HAE/HSL2 ligand–receptor pair in lateral root emergence. Nat. Plants 5, 414–423 (2019). https://doi.org/10.1038/s41477-019-0396-x

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