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CLE2 regulates light-dependent carbohydrate metabolism in Arabidopsis shoots

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A Correction to this article was published on 02 April 2021

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Key message

This study focused on the role of CLE1-CLE7 peptides as environmental mediators and indicated that root-induced CLE2 functions systemically in light-dependent carbohydrate metabolism in shoots.

Abstract

Plants sense environmental stimuli and convert them into cellular signals, which are transmitted to distinct cells and tissues to induce adequate responses. Plant hormones and small secretory peptides often function as environmental stress mediators. In this study, we investigated whether CLAVATA3/EMBRYO SURROUNDING REGION-RELATED proteins, CLE1–CLE7, which share closely related CLE domains, mediate environmental stimuli in Arabidopsis thaliana. Expression analysis of CLE1–CLE7 revealed that these genes respond to different environmental stimuli, such as nitrogen deprivation, nitrogen replenishment, cold, salt, dark, and sugar starvation, in a sophisticated manner. To further investigate the function of CLE2, we generated transgenic Arabidopsis lines expressing the β-glucuronidase gene under the control of the CLE2 promoter or expressing the CLE2 gene under the control of an estradiol-inducible promoter. We also generated cle2-1 and cle2-2 mutants using the CRISPR/Cas9 technology. In these transgenic lines, dark induced the expression of CLE2 in the root vasculature. Additionally, induction of CLE2 in roots induced the expression of various genes not only in roots but also in shoots, and genes related to light-dependent carbohydrate metabolism were particularly induced in shoots. In addition, cle2 mutant plants showed chlorosis when subjected to a shade treatment. These results suggest that root-induced CLE2 functions systemically in light-dependent carbohydrate metabolism in shoots.

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Data availability

The National Center for Biotechnology Information (NCBI) Gene Expression Omnibus (GEO) accession number for the microarray data reported in this paper is GSE149015.

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Acknowledgements

We thank Yukiko Sugisawa and Kuninori Iwamoto for technical support. We also thank Kyoko Ohashi-Ito, Yuki Kondo, Tomoyuki Furuya, Yumi Iwai and Alif Meem Nurani for discussion. This work was supported in part by Grants-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology (15H05958) and from Japan Society for the Promotion of Science (16H06377) to HF.

Funding

This work was supported in part by Grant-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology (15H05958) and from the Japan Society for the Promotion of Science (16H06377) to HF.

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Author notes

  1. Dichao Ma and Satoshi Endo have contributed equally to this work.

Authors and Affiliations

  1. Department of Biological Sciences, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-0033, Japan

    Dichao Ma, Satoshi Endo, Akie Shimotohno & Hiroo Fukuda

  2. Faculty of Life and Environmental Sciences, University of Tsukuba, 1-1-1 Tennodai, Tsukuba, Ibaraki, 305-8577, Japan

    Shigeyuki Betsuyaku

  3. Microbiology Research Center for Sustainability, University of Tsukuba, 1-1-1 Tennodai, Tsukuba, Ibaraki, 305-8572, Japan

    Shigeyuki Betsuyaku

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  1. Dichao Ma
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  4. Akie Shimotohno
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  5. Hiroo Fukuda
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DM, SE, SB, AS and HF designed the research; DM and SE performed the research; DM, SE and HF wrote the manuscript.

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Correspondence to Dichao Ma or Hiroo Fukuda.

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Ma, D., Endo, S., Betsuyaku, S. et al. CLE2 regulates light-dependent carbohydrate metabolism in Arabidopsis shoots. Plant Mol Biol 104, 561–574 (2020). https://doi.org/10.1007/s11103-020-01059-y

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