Characterization of the PHOSPHATE RESPONSE 2-dependent and -independent Pi-starvation response secretome in rice

Abstract

Many proteins secreted from plant cells into the surrounding extracellular space help maintain cell structure and regulate stress responses in the external environment. In this study, under Pi replete and deplete conditions, 652 high-confidence secreted proteins were quantified from wild type (WT) and OsPHR2-overexpressing suspension-cultured cells (SCCs). These proteins were functionally grouped as phosphatases, signal transduction proteins, pathogen-related (PR) proteins, cell wall remodeling proteins and reactive oxygen species (ROS) metabolism proteins. Although phosphate response (PHR) transcription factors regulate two-thirds of Pi-responsive genes at the transcriptional level, only 30.6% of the Pi-starvation-regulated secreted proteins showed significant changes in OsPHR2 overexpressing SCCs. The OsPHR2-dependent systemic Pi signaling pathway mainly regulates phosphatases and pathogen-related proteins, which are involved in the utilization of organophosphate, pathogen resistance, and rhizosphere microorganisms’ colonization. The OsPHR2-independent local Pi signaling pathway, on the other hand, largely regulated ROS metabolism proteins, cell wall remodeling proteins, and signal transduction proteins, which are involved in modifying cell wall structure and root architecture. The functions of differentially expressed secreted proteins between WT and OsPHR2 overexpressing plants under Pi-sufficient and Pi-deficient conditions were further confirmed by analysis of the acid phosphatase activity, ROS content, and cell wall composition.

Brassinosteroid signaling regulates phosphate starvation‐induced malate secretion in plants

“…Local Pi signaling, which is controlled by the Pi level in the environment, regulates the secretion of organic acids and root architecture remodeling (Thibaud et al, 2010). Hormone and ROS signals mediate the local Pi signaling pathway (Abel, 2017; Du et al, 2022; Li et al, 2022). Unlike other hormones, BRs cannot be transported over long distances in plants, making them suitable for regulating local Pi signaling (Symons and Reid, 2004; Symons et al, 2008).…”

“…As a result, plants have evolved various responses to improve Pi uptake from the soil, including secretion of organic acids and acid phosphatases into the rhizosphere, adjustment of root architecture, and elevated expression of phosphate transporter genes (He et al, 2019; Deng et al, 2020). These physiological and biochemical responses are regulated by integrating systemic and local Pi signaling (Puga et al, 2017; Du et al, 2022).…”

“…Secretion of acid phosphatases, accumulation of Pi transporters, and expression of phospholipid remodeling genes is mainly regulated by systemic Pi signaling, whereas stress and hormone response genes are mainly regulated by local Pi signaling (Thibaud et al, 2010; Du et al, 2022; Li et al, 2022). The systemic signal sensed by Suppressor of Yeast gpa1 (Syg1), yeast Phosphatase 81 (Pho81), and human Xenotropic and Polytropic Retrovirus receptor 1 (Xpr1) (SPX) domain‐containing proteins, which negatively regulate the activity of PHOSPHATE RESPONSE 1 (PHR1) and closely related transcription factors, is determined by the intracellular Pi status (Wild et al, 2016; Puga et al, 2017).…”

“…These physiological and biochemical responses are regulated by integrating systemic and local Pi signaling (Puga et al, 2017;Du et al, 2022).…”

Trade‐offs between root‐secreted acid phosphatase and root morphology traits, and their contribution to phosphorus acquisition in Brassica napus

“…3.1.3.2) catalyse the cleavage of a broad array of phosphomonoesters (Po sources) with optimal activity below pH 7.0 to release Pi (Bhadouria & Giri, 2022; Vincent et al, 1992; Wang & Liu, 2018). It is a common response to low soil P availability to increase the activity of root‐secreted APases in most crops, such as oilseed rape ( Brassica napus ), wheat, rice ( Oryza sative ), soybean ( Glycine max ) and common bean ( Phaseolus vulgaris ) (Bhadouria et al, 2023; Ciereszko et al, 2011; Du et al, 2022; Duan et al, 2020; Liang et al, 2010; Wu et al, 2018). Pi is released from Po by root‐secreted APases in the rhizosphere, which is closely related to the efficiency of P acquisition in crops (Deng et al, 2020; Duff et al, 1994; Lu et al, 2016; Mehra et al, 2017).…”