A phosphate starvation response-centered network regulates mycorrhizal symbiosis

Jincai Shi; Boyu Zhao; Shuang Zheng; Xiaowei Zhang; Xiaolin Wang; Wentao Dong; Qiujin Xie; Gang Wang; Yunping Xiao; Fan Chen; Nan Yu; Ertao Wang

doi:10.1016/j.cell.2021.09.030

A phosphate starvation response-centered network regulates mycorrhizal symbiosis

Cell. 2021 Oct 28;184(22):5527-5540.e18. doi: 10.1016/j.cell.2021.09.030. Epub 2021 Oct 12.

Authors

Jincai Shi¹, Boyu Zhao², Shuang Zheng¹, Xiaowei Zhang³, Xiaolin Wang³, Wentao Dong³, Qiujin Xie³, Gang Wang³, Yunping Xiao⁴, Fan Chen⁵, Nan Yu⁶, Ertao Wang⁷

Affiliations

¹ National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, SIBS, Chinese Academy of Sciences, Shanghai 200032, China; University of Chinese Academy of Sciences, Beijing 100039, China.
² National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, SIBS, Chinese Academy of Sciences, Shanghai 200032, China; Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai 200234, China.
³ National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, SIBS, Chinese Academy of Sciences, Shanghai 200032, China.
⁴ Shanghai OE Biotech Co., Ltd., Shanghai 201114, China.
⁵ Institute of Genetics and Developmental Biology, Innovation Academy for Seed Design, Chinese Academy of Sciences, Beijing 100101, China.
⁶ Shanghai Key Laboratory of Plant Molecular Sciences, College of Life Sciences, Shanghai Normal University, Shanghai 200234, China.
⁷ National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, SIBS, Chinese Academy of Sciences, Shanghai 200032, China. Electronic address: [email protected].

PMID: 34644527
DOI: 10.1016/j.cell.2021.09.030

Abstract

To secure phosphorus (P) from soil, most land plants use a direct phosphate uptake pathway via root hairs and epidermis and an indirect phosphate uptake pathway via mycorrhizal symbiosis. The interaction between these two pathways is unclear. Here, we mapped a network between transcription factors and mycorrhizal symbiosis-related genes using Y1H. Intriguingly, this gene regulatory network is governed by the conserved P-sensing pathway, centered on phosphate starvation response (PHR) transcription factors. PHRs are required for mycorrhizal symbiosis and regulate symbiosis-related genes via the P1BS motif. SPX-domain proteins suppress OsPHR2-mediated induction of symbiosis-related genes and inhibit mycorrhizal infection. In contrast, plants overexpressing OsPHR2 show improved mycorrhizal infection and are partially resistant to P-mediated inhibition of symbiosis. Functional analyses of network nodes revealed co-regulation of hormonal signaling and mycorrhizal symbiosis. This network deciphers extensive regulation of mycorrhizal symbiosis by endogenous and exogenous signals and highlights co-option of the P-sensing pathway for mycorrhizal symbiosis.

Keywords: P1BS motif; PHR2; SPX; endogenous and exogenous signals; gene network; mycorrhizal symbiosis; phosphate starvation response.

Publication types

Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Base Sequence
Gene Expression Regulation, Plant
Gene Regulatory Networks*
Mutation / genetics
Mycorrhizae / genetics*
Mycorrhizae / physiology*
Oryza / genetics
Oryza / microbiology
Phosphates / deficiency*
Phylogeny
Plant Proteins / genetics
Plant Proteins / metabolism
Promoter Regions, Genetic / genetics
Saccharomyces cerevisiae / metabolism
Symbiosis / genetics*
Symbiosis / physiology*
Two-Hybrid System Techniques

Substances

Phosphates
Plant Proteins