New insights into the evolution of SPX gene family from algae to legumes; a focus on soybean

Mahnaz Nezamivand-Chegini,Ahmad Tahmasebi,Manijeh Mohammadi-Dehchesmeh,Saeid Eshghi,Esmaeil Ebrahimie,Stanislav Kopriva,Ali Moghadam,Ali Niazi

doi:10.1186/s12864-021-08242-5

Abstract

BackgroundSPX-containing proteins have been known as key players in phosphate signaling and homeostasis. In Arabidopsis and rice, functions of some SPXs have been characterized, but little is known about their function in other plants, especially in the legumes.ResultsWe analyzed SPX gene family evolution in legumes and in a number of key species from algae to angiosperms. We found that SPX harboring proteins showed fluctuations in domain fusions from algae to the angiosperms with, finally, four classes appearing and being retained in the land plants. Despite these fluctuations, Lysine Surface Cluster (KSC), and the third residue of Phosphate Binding Sites (PBS) showed complete conservation in almost all of SPXs except few proteins in Selaginella moellendorffii and Papaver sumniferum, suggesting they might have different ligand preferences. In addition, we found that the WGD/segmentally or dispersed duplication types were the most frequent contributors to the SPX expansion, and that there is a positive correlation between the amount of WGD contribution to the SPX expansion in individual species and its number of EXS genes. We could also reveal that except SPX class genes, other classes lost the collinearity relationships among Arabidopsis and legume genomes. The sub- or neo-functionalization of the duplicated genes in the legumes makes it difficult to find the functional orthologous genes. Therefore, we used two different methods to identify functional orthologs in soybean and Medicago. High variance in the dynamic and spatial expression pattern of GmSPXs proved the new or sub-functionalization in the paralogs.ConclusionThis comprehensive analysis revealed how SPX gene family evolved from algae to legumes and also discovered several new domains fused to SPX domain in algae. In addition, we hypothesized that there different phosphate sensing mechanisms might occur in S. moellendorffii and P. sumniferum. Finally, we predicted putative functional orthologs of AtSPXs in the legumes, especially, orthologs of AtPHO1, involved in long-distance Pi transportation. These findings help to understand evolution of phosphate signaling and might underpin development of new legume varieties with improved phosphate use efficiency.

Highlights

SPX-containing proteins have been known as key players in phosphate signaling and homeostasis
With the combination of these two methods, we identified the functional orthologs of key regulators AtPHO1 (GLYMA_02G003700, GLYMA_10G004800), AtSPX4 (GLYMA_06G069000), AtPHO1;H10 (GLYMA_02G110600), and AtNLA2 (GLYMA_19G203000) in soybean
Identification of SPX domain proteins from algae to legumes While in several plant species four families of SPX proteins were characterized, much less is known about these proteins in legumes: in soybean and common bean just 10 and 3 members of class 1 were characterized and no SPX proteins in M. truncatula

Summary

Introduction

SPX-containing proteins have been known as key players in phosphate signaling and homeostasis. In high P availability, inositol polyphosphates (PP-InsPs) bind to the basic surface of SPX domain proteins and facilitate their binding to PHR. This interaction may sequester PHR1 in the cytosol or prevent its association with DNA in the nucleus [10]. In low P supply, low availability of PP-InsPs-SPX results in the release of PHR1 to translocate to nucleus and to activate Pi starvation induced (PSI) genes [8]. SPX domain proteins were shown to be involved in nitrate-phosphate signaling crosstalk in rice where nitrate-dependent interaction with NRT1.1B caused ubiquitination and degradation of OsSPX4 and translocation of OsPHR2 and OsNLP3 into nucleus to induce PSI genes and nitrate inducible genes, respectively [11]

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