SAUR Inhibition of PP2C-D Phosphatases Activates Plasma Membrane H⁺-ATPases to Promote Cell Expansion in Arabidopsis

The plant hormone auxin promotes cell expansion. Forty years ago, the acid growth theory was proposed, whereby auxin promotes proton efflux to acidify the apoplast and facilitate the uptake of solutes and water to drive plant cell expansion. However, the underlying molecular and genetic bases of thi...

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Published inThe Plant cell Vol. 26; no. 5; pp. 2129 - 2142
Main Authors Spartz, Angela K., Ren, Hong, Park, Mee Yeon, Grandt, Kristin N., Lee, Sang Ho, Murphy, Angus S., Sussman, Michael R., Overvoorde, Paul J., Gray, William M.
Format Journal Article
LanguageEnglish
Published United States American Society of Plant Biologists 01.05.2014
Subjects
Auxins
Cell membranes
Hypocotyls
Phenotypes
Phosphatases
Phosphorylation
Plant cells
Plants
Proteins
Seedlings
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Summary:The plant hormone auxin promotes cell expansion. Forty years ago, the acid growth theory was proposed, whereby auxin promotes proton efflux to acidify the apoplast and facilitate the uptake of solutes and water to drive plant cell expansion. However, the underlying molecular and genetic bases of this process remain unclear. We have previously shown that the SAUR19-24 subfamily of auxin-induced SMALL AUXIN UP-RNA (SAUR) genes promotes cell expansion. Here, we demonstrate that SAUR proteins provide a mechanistic link between auxin and plasma membrane H⁺-ATPases (PM H⁺-ATPases) in Arabidopsis thaliana. Plants overexpressing stabilized SAUR19 fusion proteins exhibit increased PM H⁺-ATPase activity, and the increased growth phenotypes conferred by SAUR19 overexpression are dependent upon normal PM H⁺-ATPase function. We find that SAUR19 stimulates PM H⁺-ATPase activity by promoting phosphorylation of the C-terminal autoinhibitory domain. Additionally, we identify a regulatory mechanism by which SAUR19 modulates PM H⁺-ATPase phosphorylation status. SAUR19 as well as additional SAUR proteins interact with the PP2C-D subfamily of type 2C protein phosphatases. We demonstrate that these phosphatases are inhibited upon SAUR binding, act antagonistically to SAURs in vivo, can physically interact with PM H⁺-ATPases, and negatively regulate PM H⁺-ATPase activity. Our findings provide a molecular framework for elucidating auxin-mediated control of plant cell expansion.
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Current address: College of Techno-Sciences, Mokwon University, 88 Doanbuk-ro, Daejeon, 302-729, South Korea.
These authors contributed equally to this work.
The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantcell.org) is: William M. Gray (grayx051@umn.edu).
www.plantcell.org/cgi/doi/10.1105/tpc.114.126037
ISSN:1040-4651
1532-298X
DOI:10.1105/tpc.114.126037