Chloroplastic Sec14-like proteins modulate growth and phosphate deficiency responses in Arabidopsis and rice

Abstract

Phosphorus is an essential nutrient acquired from soil as phosphate (Pi), and its deficiency severely reduces plant growth and crop yield. Here, we show that single nucleotide polymorphisms (SNPs) at the PHOSPHATIDYLINOSITOL TRANSFER PROTEIN7 (AtPITP7) locus, which encodes a chloroplastic Sec14-like protein, are associated with genetic diversity regarding Pi uptake activity in Arabidopsis (Arabidopsis thaliana). Inactivation of AtPITP7 and its rice (Oryza sativa) homolog (OsPITP6) through T-DNA insertion and CRISPR/Cas9-mediated gene editing, respectively, decreased Pi uptake and plant growth, regardless of Pi availability. By contrast, overexpression of AtPITP7 and OsPITP6 enhanced Pi uptake and plant growth, especially under limited Pi supply. Importantly, overexpression of OsPITP6 increased tiller number and grain yield in rice. Targeted metabolome analysis of glycerolipids in leaves and chloroplasts revealed that inactivation of OsPITP6 alters phospholipid contents, independent of Pi availability, diminishing the reduction in phospholipid content and increase in glycolipid content induced by Pi deficiency; meanwhile, overexpression of OsPITP6 enhanced Pi deficiency induced metabolic alterations. Together with transcriptome analysis of ospitp6 rice plants and phenotypic analysis of grafted Arabidopsis chimeras, these results suggest that chloroplastic Sec14-like proteins play an essential role in growth modulations in response to changes in Pi availability, although their function is critical for plant growth under any Pi condition. The superior traits of OsPITP6-overexpressing rice plants also highlight the potential of OsPITP6 and its homologs in other crops as additional tools for improving Pi uptake and plant growth in low Pi environments.

Comparative transcriptomic and physiological analyses unravel wheat source root adaptation to phosphorous deficiency

“…Moreover, other Pi-responsive transcription factors like WRKY, MYB, and bHLH families have been identified in several plant species 11 . Furthermore, miR399 decreases the transcript level of PHO2 , which encodes a ubiquitin-conjugating E2 enzyme involved in the ubiquitination and degradation of PHT proteins 12 .…”

Sec14-like proteins to the rescue: Improving plant performance in low-phosphate conditions

“…Despite these advances in understanding plant responses to phosphate limitation, much of the mechanism and regulation of membrane remodeling in this context remains unknown. In this issue of Plant Physiology , Yang et al reveal a new role for Sec14-like proteins AtPITP7 and OsPITP6 in regulating phosphorous utilization in chloroplasts and present exciting possibilities for manipulating OsPITP6 expression to improve growth and yield in phosphate-limiting conditions ( Yang et al 2023 ). In yeast, Sec14 family proteins are some of the most extensively studied lipid transfer proteins ( Holič et al 2021 ).…”

“…This function has been linked to phospholipid metabolism, membrane trafficking, and polarized membrane growth, and in mammalian cells, disruption of Sec14 family protein function contributes to a number of different diseases ( Holič et al 2021 ). Arabidopsis contains 32 Sec14-like proteins and rice contains 29, some of which have been shown to bind phospholipids and regulate membrane trafficking ( Yang et al 2023 ), similar to Sec14 family protein function in yeast and mammalian cells. Intriguingly, Arabidopsis and rice each contain only one Sec14-like protein with known localization in chloroplasts: AtPITP7 and OsPITP6 ( Yang et al 2023 ).…”

“…Arabidopsis contains 32 Sec14-like proteins and rice contains 29, some of which have been shown to bind phospholipids and regulate membrane trafficking ( Yang et al 2023 ), similar to Sec14 family protein function in yeast and mammalian cells. Intriguingly, Arabidopsis and rice each contain only one Sec14-like protein with known localization in chloroplasts: AtPITP7 and OsPITP6 ( Yang et al 2023 ). Deactivating or overexpressing this gene results in significant changes in fresh shoot and root weight, primary root length, phosphate uptake activity and content, and photosynthetic capacity in both Arabidopsis and rice ( Yang et al 2023 ).…”

“…Intriguingly, Arabidopsis and rice each contain only one Sec14-like protein with known localization in chloroplasts: AtPITP7 and OsPITP6 ( Yang et al 2023 ). Deactivating or overexpressing this gene results in significant changes in fresh shoot and root weight, primary root length, phosphate uptake activity and content, and photosynthetic capacity in both Arabidopsis and rice ( Yang et al 2023 ). These phenotypes are even more apparent under limited phosphate conditions, which suggests that AtPITP7 and OsPITP6 play roles in chloroplast phosphate metabolism and could be novel targets for improving crop productivity in soils with low phosphate availability ( Yang et al 2023 ).…”