Loss of two families of SPX domain-containing proteins required for vacuolar polyphosphate accumulation coincides with the transition to phosphate storage in green plants

Abstract

Phosphorus is an essential nutrient for plants. It is stored as inorganic phosphate (Pi) in the vacuoles of land plants but as inorganic polyphosphate (polyP) in chlorophyte algae. Although it is recognized that the SPX-Major Facilitator Superfamily (MFS) and VPE proteins are responsible for Pi influx and efflux, respectively, across the tonoplast in land plants, the mechanisms that underlie polyP homeostasis and the transition of phosphorus storage forms during the evolution of green plants remain unclear. In this study, we showed that CrPTC1, encoding a protein with both SPX and SLC (permease solute carrier 13) domains for Pi transport, and CrVTC4, encoding a protein with both SPX and vacuolar transporter chaperone (VTC) domains for polyP synthesis, are required for vacuolar polyP accumulation in the chlorophyte Chlamydomonas reinhardtii. Phylogenetic analysis showed that the SPX-SLC, SPX-VTC, and SPX-MFS proteins were present in the common ancestor of green plants (Viridiplantae). The SPX-SLC and SPX-VTC proteins are conserved among species that store phosphorus as vacuolar polyP and absent from genomes of plants that store phosphorus as vacuolar Pi. By contrast, SPX-MFS genes are present in the genomes of streptophytes that store phosphorus as Pi in the vacuoles. These results suggest that loss of SPX-SLC and SPX-VTC genes and functional conservation of SPX-MFS proteins during the evolution of streptophytes accompanied the change from ancestral polyP storage to Pi storage.

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

“…The outgroup genes used in this study were grouped in box E clustered with EXS clade. Overall, topology of EXS class is consistent with He et al, (2013), in that basal plants (lycophytes and moss) EXS homologs were grouped separately from the angiosperms, and also with the previous reports on EXS genes that monocots only possess homologs for AtPHO1 and AtPHO1;H1 [6, 24, 35].…”

“…Although Wang et al [24] reported one SPX-MFS in M. polymorpha genome, we could not find an intact SPX-MFS domain, but SPX-Sugar_tr domain with a highly similar motif composition with other MFSs was identified (Additional file 1: Figure S3). As it has previously been reported, PHT5 genes in B. napus have SPX domain connected to overlapping MFS and Sugar_tr domains [36], however, we only found SPX and Sugar-tr domains in M. polymorpha genome.…”

“…Meanwhile, some other classes have been revealed in the basal plants and algae such as SPX-SLC and SPX-VTC [24]. Here we report other functional protein domains being fused to SPX domains, Interestingly, some of these new domains have been lost in the land plants and all of them in angiosperms.…”

“…The role of SPX domain-containing proteins in Pi homeostasis in Arabidopsis, rice, rapeseed, and wheat and to some extent in soybean and common bean were studied previously [3,13,27,[29][30][31]35]. While an evolutionary analysis of SPX-EXS [47] and SPX-MFS [24] classes has been reported, as far as we know, the evolution of all classes of SPX gene family from algae to higher plants has not been explored. In addition, despite legume crops requiring a relatively high amount of P, no systematic study of SPX gene family has been reported in legume crops.…”

Insights of intracellular/intercellular phosphate transport and signaling in unicellular green algae and multicellular land plants

“…However, when and how this transition occurs during plant evolution remained unclear until recently. Wang et al (2021) showed that the transition of vacuolar P storage form from polyP to Pi occurred in the ancestor of later diverging streptophytes It was also suggested that this transition is a consequence of the loss of two gene families (SPX-SLC and SPX-VTC) involved in polyP homeostasis (Wang et al, 2021). Given that vacuolar polyP has not been documented in land plants, the transition of vacuolar P storage form from polyP to Pi is a vital node during plant evolution.…”