Phosphate-dependent regulation of vacuolar trafficking of OsSPX-MFSs is critical for maintaining intracellular phosphate homeostasis in rice.


Journal

Molecular plant
ISSN: 1752-9867
Titre abrégé: Mol Plant
Pays: England
ID NLM: 101465514

Informations de publication

Date de publication:
07 08 2023
Historique:
received: 01 04 2023
revised: 26 06 2023
accepted: 13 07 2023
medline: 24 8 2023
pubmed: 19 7 2023
entrez: 19 7 2023
Statut: ppublish

Résumé

Vacuolar storage of inorganic phosphate (Pi) is essential for Pi homeostasis in plants. The SPX-MFS family proteins have been demonstrated to be vacuolar Pi transporters in many plant species. Transcriptional regulation of the predominant transporter among rice SPX-MFSs, OsSPX-MFS3, was only moderately suppressed by Pi starvation. Thus, post-transcriptional mechanisms were hypothesized to regulate the activity of OsSPX-MFS3. In this study, we found that the tonoplast localization of OsSPX-MFSs is inhibited under Pi-depleted conditions, resulting in their retention in the pre-vacuolar compartments (PVCs). A yeast two-hybrid screen identified that two SNARE proteins, OsSYP21 and OsSYP22, interact with the MFS domain of OsSPX-MFS3. Further genetic and cytological analyses indicate that OsSYP21 and OsSYP22 facilitate trafficking of OsSPX-MFS3 from PVCs to the tonoplast. Although a homozygous frameshift mutation in OsSYP22 appeared to be lethal, tonoplast localization of OsSPX-MFS3 was significantly inhibited in transgenic plants expressing a negative-dominant form of OsSYP22 (OsSYP22-ND), resulting in reduced vacuolar Pi concentrations in OsSYP22-ND plants. Under Pi-depleted conditions, the interaction between OsSYP22 and OsSPX-MFS3 was disrupted, and this process depended on the presence of the SPX domain. Deleting the SPX domains of OsSPX-MFSs resulted in their tonoplast localization under both Pi-depleted and Pi-replete conditions. Complementation of the osspx-mfs1/2/3 triple mutants with the MFS domain or the SPX domain of OsSPX-MFS3 confirmed that the MFS and SPX domains are responsive to Pi transport activity and Pi-dependent regulation, respectively. These data indicated that the SPX domains of OsSPX-MFSs sense cellular Pi (InsP) levels and, under Pi-depleted conditions, inhibit the interaction between OsSPX-MFSs and OsSYP21/22 and subsequent trafficking of OsSPX-MFSs from PVCs to the tonoplast.

Identifiants

pubmed: 37464739
pii: S1674-2052(23)00206-X
doi: 10.1016/j.molp.2023.07.004
pii:
doi:

Substances chimiques

Phosphates 0
Plant Proteins 0
Phosphate Transport Proteins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1304-1320

Informations de copyright

Copyright © 2023 The Author. Published by Elsevier Inc. All rights reserved.

Auteurs

Runze Guo (R)

State Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang 310058, P.R. China; Hainan Institute, Zhejiang University, Sanya 572025, China; The Provincial International Science and Technology Cooperation Base on Engineering Biology, International Campus of Zhejiang University, Haining, Zhejiang 314400, China.

Qi Zhang (Q)

State Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang 310058, P.R. China; The Provincial International Science and Technology Cooperation Base on Engineering Biology, International Campus of Zhejiang University, Haining, Zhejiang 314400, China; Zhijiang lab, Hangzhou 310012, China.

Kun Qian (K)

State Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang 310058, P.R. China; The Provincial International Science and Technology Cooperation Base on Engineering Biology, International Campus of Zhejiang University, Haining, Zhejiang 314400, China.

Yinghui Ying (Y)

State Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang 310058, P.R. China.

Wenying Liao (W)

State Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang 310058, P.R. China; Hainan Institute, Zhejiang University, Sanya 572025, China.

Lening Gan (L)

State Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang 310058, P.R. China; Hainan Institute, Zhejiang University, Sanya 572025, China.

Chuanzao Mao (C)

State Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang 310058, P.R. China.

Yong Wang (Y)

The Provincial International Science and Technology Cooperation Base on Engineering Biology, International Campus of Zhejiang University, Haining, Zhejiang 314400, China.

James Whelan (J)

State Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang 310058, P.R. China; The Provincial International Science and Technology Cooperation Base on Engineering Biology, International Campus of Zhejiang University, Haining, Zhejiang 314400, China.

Huixia Shou (H)

State Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang 310058, P.R. China; Hainan Institute, Zhejiang University, Sanya 572025, China; The Provincial International Science and Technology Cooperation Base on Engineering Biology, International Campus of Zhejiang University, Haining, Zhejiang 314400, China. Electronic address: huixia@zju.edu.cn.

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