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Ubiquitin E3 ligase AtCHYR2 functions in glucose regulation of germination and post-germinative growth in Arabidopsis thaliana

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Abstract

Key message

Cytoplasm-localized RING ubiquitin E3 ligase AtCHYR2 involved in plant glucose responses during germination and post-germinative growth.

Abstract

CHY ZINC FINGER AND RING PROTEIN (CHYR) containing both a CHY zinc finger and a C3H2C3-type RING domain plays important roles in plant drought tolerance and the abscisic acid (ABA) response; however, their functions in sugar signaling pathways are less studied. Here, we report a glucose (Glc) response gene AtCHYR2, a homolog of RZFP34/CHYR1, which is induced by various abiotic stresses, ABA, and sugar treatments. In vitro, we demonstrated that AtCHYR2 is a cytoplasm-localized RING ubiquitin E3 ligase. Overexpression of AtCHYR2 led to hypersensitivity to Glc and enhanced Glc-mediated inhibition of cotyledon greening and post-germinative growth. Contrastingly, AtCHYR2 loss-of-function plants were insensitive to Glc-regulated seed germination and primary root growth, suggesting that AtCHYR2 is a positively regulator of the plant glucose response. Additionally, physiological analyses showed that overexpression AtCHYR2 increased stomata aperture and photosynthesis under normal condition, and promoted accumulation of endogenous soluble sugar and starch in response to high Glc. Genome-wide RNA sequencing analysis showed that AtCHYR2 affects a major proportion of Glc-responsive genes. Particularly, sugar marker gene expression analysis suggested that AtCHYR2 enhances the Glc response via a signaling pathway dependent on glucose metabolism. Taken together, our findings show that a novel RING ubiquitin E3 ligase, AtCHYR2, plays an important role in glucose responses in Arabidopsis.

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Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request. The RNA sequencing data for this research have been deposited in the NCBI Sequence Read Archive under accession code PRJNA912374.

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Acknowledgements

We wish to thank Bin Zhang of Beijing Vegetable Research Center (BVRC), Beijing Academy of Agriculture and Forestry Sciences (BAAFS) for detection of in vitro self-ubiquitination assay.

Funding

This work was supported by the National Natural Science Foundation (31701062, 31701439 and 31771801), the Engineering Research Center of Ecology and Agricultural Use of Wetland, Ministry of Education (KFT202012), the open funds of the State Key Laboratory of Plant Physiology and Biochemistry (SKLPPBKF2112), and the Plan in Scientific and Technological Innovation Team of Outstanding Young (T201704).

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  1. Shengyong Wang and Huili Chen contributed equally to this work.

Authors and Affiliations

  1. MARA Key Laboratory of Sustainable Crop Production in the Middle Reaches of the Yangtze River (Co-Construction by Ministry and Province), College of Agriculture, Yangtze University, 1 Jingmi Road, Jingzhou, 434025, Hubei, China

    Shengyong Wang, Huili Chen, Yujie Huang, Xiaotian Zhang, Yuhang Chen, Hongwei Wang & Shuangcheng Ding

  2. Engineering Research Center of Ecology and Agricultural Use of Wetland, Ministry of Education, Yangtze University, Jingzhou, 434025, China

    Shuangcheng Ding

  3. College of Life Science, Yangtze University, Jingzhou, 434025, China

    Hewei Du

  4. Center for Crop Functional Genomics and Molecular Breeding, China Agricultural University, Beijing, 100193, China

    Feng Qin

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  1. Shengyong Wang
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Contributions

Conceptualization, S.Y., H.W., F.Q., and S.D.; investigation, S.Y., H.L. and S.D.; data curation, Y.H., X.Z., Y.C., H. D., and S.D.; writing—original draft preparation, S.D.; writing—review and editing, H.W., F.Q., and S.D.; funding acquisition, H.W. and S.D. All authors have read and agreed to the published version of the manuscript.

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Correspondence to Hongwei Wang, Feng Qin or Shuangcheng Ding.

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Wang, S., Chen, H., Huang, Y. et al. Ubiquitin E3 ligase AtCHYR2 functions in glucose regulation of germination and post-germinative growth in Arabidopsis thaliana. Plant Cell Rep 42, 989–1002 (2023). https://doi.org/10.1007/s00299-023-03008-7

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