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In rose, transcription factor PTM balances growth and drought survival via PIP2;1 aquaporin

Nature Plants volume 5, pages 290–299 (2019)Cite this article

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Abstract

Plants have evolved sophisticated systems in response to environmental changes, and growth arrest is a common strategy used to enhance stress tolerance. Despite the growth–survival trade-off being essential to the shaping of plant productivity, the mechanisms balancing growth and survival remain largely unknown. Aquaporins play a crucial role in growth and stress responses by controlling water transport across membranes. Here, we show that RhPIP2;1, an aquaporin from rose (Rosa sp.), interacts with a membrane-tethered MYB protein, RhPTM. Water deficiency triggers nuclear translocation of the RhPTM C terminus. Silencing of RhPTM causes continuous growth under drought stress and a consequent decrease in survival rate. RNA sequencing (RNA-seq) indicated that RhPTM influences the expression of genes related to carbohydrate metabolism. Water deficiency induces phosphorylation of RhPIP2;1 at Ser 273, which is sufficient to promote nuclear translocation of the RhPTM C terminus. These results indicate that the RhPIP2;1-RhPTM module serves as a key player in orchestrating the trade-off between growth and stress survival in Rosa.

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Fig. 1: RhPIP2;1 interacts with RhPTM.
Fig. 2: Dehydration stimulates nuclear accumulation of the RhPTM C-terminal region.
Fig. 3: Silencing of RhPTM in rose enhances growth.
Fig. 4: Silencing of RhPTM reduces tolerance of rose plants to drought stress.
Fig. 5: RhPTM influences expression of genes related to carbohydrate metabolism and signalling of auxin and cytokinin in rose plants.
Fig. 6: Nuclear translocation of RhPTM CEND is regulated by phosphorylation of RhPIP2;1.

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Data availability

The data that support the findings of this study are available from the corresponding author upon request. All primers used in this study are described in Supplementary Table 3. Information on the genes used in this study is given in Supplementary Table 4. RNA-Seq data that support the findings of this study have been deposited in the NCBI Bioproject database under the accession number PRJNA486271 (https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA486271). The proteomic data of validation for anti-RhPTM antibody and RhPIP2;1 phosphorylation have been deposited in the PRIDE archive (Nos. PXD011942 and PXD011943, respectively; https://www.ebi.ac.uk/pride/archive).

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Acknowledgements

We thank Z. Li (Biological Mass Spectrometry Laboratory of the Functional Genomic Technology Centre of China Agricultural University) for LC–MS experiments. We thank J. Zhu (Jingjie PTM Biolabs, Inc.) for analysis of LC–MS data. We thank Z. Gong (China Agricultural University) for providing the pSuper1300 vector. We thank D. Zhang (Tsinghua University) for his generous help with MYTH screening. We thank PlantScribe (www.plantscribe.com) for careful editing of this article. This work was supported by the National Natural Science Foundation of China (grant Nos. 31520103913, 31522049, 31730079 and 31401914) and the 111 Project of the Ministry of Education (No. B17043).

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  1. These authors contributed equally: Shuai Zhang, Ming Feng, Wen Chen.

Authors and Affiliations

  1. Beijing Key Laboratory of Development and Quality Control of Ornamental Crops, Department of Ornamental Horticulture, China Agricultural University, Beijing, China

    Shuai Zhang, Ming Feng, Xiaofeng Zhou, Jingyun Lu, Yaru Wang, Nan Ma & Junping Gao

  2. The Key Laboratory for Quality Improvement of Agricultural Products of Zhejiang Province, School of Agriculture and Food Science, Zhejiang Agriculture & Forestry University, Lin’an, China

    Wen Chen

  3. School of Applied Chemistry and Biotechnology, Shenzhen Polytechnic, Shenzhen, China

    Yonghong Li

  4. Crop Pathology and Genetic Research Unit, United States Department of Agriculture, Agricultural Research Service, Davis, CA, USA

    Cai-Zhong Jiang

  5. Department of Plant Sciences, University of California, Davis, CA, USA

    Cai-Zhong Jiang

  6. Plant Biology Section, School of Integrative Plant Science, College of Agriculture and Life Sciences, Cornell University, Ithaca, NY, USA

    Su-Sheng Gan

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Contributions

S.Z., M.F., W.C., J.L., Y.W. and Y.L. performed the experiments. N.M. and J.G. designed the research. X.Z., C.J., S.G. and N.M. provided technical support, conceptual advice and data analysis. S.Z., N.M. and J.G. wrote the article.

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Correspondence to Nan Ma or Junping Gao.

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Supplementary information

Supplementary Information

Supplementary Figures 1–10, Supplementary Methods, Supplementary References, legends for Supplementary Tables and Datasets, and Supplementary Tables 1–3.

Reporting Summary

Supplementary Dataset 1

The entire database search results for validation of anti-RhPTM antibody by LC–MS.

Supplementary Dataset 2

Differentially expressed genes in RhPTM-silenced rose plants.

Supplementary Dataset 3

The entire database search results for phosphorylation of RhPIP2;1 by LC–MS.

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Zhang, S., Feng, M., Chen, W. et al. In rose, transcription factor PTM balances growth and drought survival via PIP2;1 aquaporin. Nat. Plants 5, 290–299 (2019). https://doi.org/10.1038/s41477-019-0376-1

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