A subset of plasma membrane-localized PP2C.D phosphatases negatively regulate SAUR-mediated cell expansion in Arabidopsis

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The plant hormone auxin regulates numerous growth and developmental processes throughout the plant life cycle. One major function of auxin in plant growth and development is the regulation of cell expansion. Our previous studies have shown that SMALL AUXIN UP RNA (SAUR) proteins promote auxin-induced cell expansion via an acid growth mechanism. These proteins inhibit the PP2C.D family phosphatases to activate plasma membrane (PM) H+-ATPases and thereby promote cell expansion. However, the functions of individual PP2C.D phosphatases are poorly understood. Here, we investigated PP2C.D-mediated control of cell expansion and other aspects of plant growth and development. The nine PP2C.D family members exhibit distinct subcellular localization patterns. Our genetic findings demonstrate that the three plasma membrane-localized members, PP2C.D2, PP2C.D5, and PP2C.D6, are the major regulators of cell expansion. These phosphatases physically interact with SAUR19 and PM H+-ATPases, and inhibit cell expansion by dephosphorylating the penultimate threonine of PM H+-ATPases. PP2C.D genes are broadly expressed and are crucial for diverse plant growth and developmental processes, including apical hook development, phototropism, and organ growth. GFP-SAUR19 overexpression suppresses the growth defects conferred by PP2C.D5 overexpression, indicating that SAUR proteins antagonize the growth inhibition conferred by the plasma membrane-localized PP2C.D phosphatases. Auxin and high temperature upregulate the expression of some PP2C.D family members, which may provide an additional layer of regulation to prevent plant overgrowth. Our findings provide novel insights into auxin-induced cell expansion, and provide crucial loss-of-function genetic support for SAUR-PP2C.D regulatory modules controlling key aspects of plant growth.

Original languageEnglish (US)
Article numbere1007455
JournalPLoS genetics
Issue number6
StatePublished - Jun 2018

Bibliographical note

Funding Information:
This work was supported by the National Institutes of Health (https://www.nih.gov, GM067203 to WMG) and the National Science Foundation (https://www.nsf.gov, MCB-1613809 to WMG). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We thank the University of Minnesota University Imaging Center for the Nikon A1 spectral confocal microscope and Dr. Clay Carter for the StepOnePlus Real-Time PCR System. We also thank the members of the Carter and Olszewski labs for helpful discussions, Dr. Min Ni for the help with the phototropism experiment, and Dr. Tony Sanderfoot (University of Wisconsin-La Crosse) for providing the SEC12 antibody.

Publisher Copyright:
© 2018 Ren et al. http://creativecommons.org/licenses/by/4.0/


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