Phosphorus is an essential nutrient for plants. It is stored as inorganic phosphate (Pi) in vacuoles of land plants but as inorganic polyphosphate (polyP) in chlorophyte algae. Although it has been known that the SPX-MFS and VPE proteins are respectively responsible for Pi influx and efflux across the tonoplast in land plants, the mechanisms underlying 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 transporter, and CrVTC4, encoding a protein with both SPX and 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 are 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 of Pi storage mechanism from the ancestral form by which phosphorus was stored as polyP.
Proposed scenario of the stepwise evolution of SPX-containing genes and vacuolar phosphorus storage forms
The SPX-VTC and SPX-SLC proteins were present in the ancestor of Chlorophyta algae and participate in vacuolar polyP synthesis and accumulation, respectively. It is unknown if GlpT/VPE and SPX-MFS proteins mediate vacuolar Pi accumulation among the Chlorophyte algae. SPX-MFS proteins were lost in the early diverging streptophyte alga. The later-diverging streptophyte algae, which use GlpT/VPE and SPX-MFS for vacuolar Pi homeostasis, have lost SPX-VTC and SPX-SLC proteins, and had their vacuolar phosphorus storage form changed into Pi. Question masks and dashed arrows mean transporters without solid functional identification.
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