The paralogous SPX3 and SPX5 genes redundantly modulate Pi homeostasis in rice

Jing Shi,Ping Wu,Zhongchang Wu,Han Hu,Yanan Yu,Keming Zhang,Wei Zhang

doi:10.1093/jxb/ert424

Abstract

The importance of SPX-domain-containing proteins to phosphate (Pi) homeostasis and signalling transduction has been established in plants. In this study, phylogenetic analysis revealed that OsSPX3 and OsSPX5 (SPX3/5) are paralogous SPX genes (SYG1/Pho81/XPR1) in cereal crops. SPX3/5 are specifically responsive to Pi starvation at both the transcriptional and post-transcriptional levels. Similar tissue expression patterns of the two genes and proteins were identified by in situ hybridization and the transgenic plants harbouring SPX3pro-SPX3-GUS or SPX5pro-SPX5-GUS fusions, respectively. Both SPX3/5 are localized in the nucleus and cytoplasm in rice protoplasts and plants. SPX3/5 negatively regulate root-to-shoot Pi translocation with redundant function. The data showed that the Pi-starvation-accumulated SPX3/5 proteins are players in restoring phosphate balance following phosphate starvation. In vitro and in vivo protein–protein interaction analyses indicated that these two proteins can form homodimers and heterodimers, also implying their functional redundancy. Genetic interaction analysis indicated that SPX3/5 are functional repressors of OsPHR2 (PHR2), the rice orthologue of the central regulator AtPHR1 for Pi homeostasis and Pi signalling. These results suggest that the evolution of the additional redundant paralogous SPX genes is beneficial to plants recovering Pi homeostasis after Pi starvation by PHR2 pathway.

Highlights

The maintenance of phosphate (Pi) homeostasis in plants is crucial for plant growth and development
The current data further showed that SPX3, SPX5, and SPX6 are induced by Pi starvation, which was remarkably reduced in the phr2 mutant (Supplementary Fig. S1; Chen et al, 2011)
This work reports that SPX3/5 evolved in cereal crops redundantly modulate Pi homeostasis and signalling

Summary

Introduction

The maintenance of phosphate (Pi) homeostasis in plants is crucial for plant growth and development. Increasing evidence shows that the proteins containing the SPX domain are key players controlling a set of processes involved in Pi homeostasis (Hamburger et al, 2002; Duan et al, 2008; Wang et al, 2009a; Lin et al, 2010; Liu et al, 2010, 2012; Kant et al, 2011). Proteins exclusively harbouring the SPX domain are referred to as SPX proteins and fall into class I, with four members in Arabidopsis and six members in rice (Duan et al, 2008; Secco et al, 2012). Phylogenetic analysis has revealed three evolutionary clades of these SPX proteins: clade I contains SPX1 and SPX2, clade III contains SPX4, and clade II contains SPX3 in Arabidopsis (AtSPX3) and three paralogous proteins in rice, designated SPX3, SPX5, and SPX6 (Secco et al, 2012)

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Conclusion