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

Long Wang (1, 2, 3) , Xianqing Jia (1, 2) , Yuxin Zhang (1, 2) , Lei Xu (1, 2) , Benoît Menand (4) , Hongyu Zhao (1, 2) , Houqing Zeng (5) , Liam Dolan (6) , Yiyong Zhu (7, 3) , Keke Yi (1, 2)

1 Key Laboratory of Plant Nutrition and Fertilizers, Ministry of Agriculture and Rural Affairs, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences
2 CAAS - Chinese Academy of Agricultural Sciences
3 NAU - Nanjing Agricultural University
4 LGBP - Luminy Génétique et Biophysique des Plantes
5 College of Life and Environmental Sciences, Hangzhou Normal University,
6 GMI - Gregor Mendel Institute of Molecular Plant Biology
7 Jiangsu Provincial Key Lab for Organic Solid Waste Utilization, National Engineering Research Center for Organic-based Fertilizers, Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, Nanjing Agricultural University, Nanjing, 210095, China

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 SPXMajor 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.

Keywords: Chlamydomonas; polyphosphate; SPX-SLC; SPX-VTC; vacuolar phosphate; plant evolution

Domains: Life Sciences [q-bio]

Long Wang, Xianqing Jia, Yuxin Zhang, Lei Xu, Benoît Menand, et al.. Loss of two families of SPX domain-containing proteins required for vacuolar polyphosphate accumulation coincides with the transition to phosphate storage in green plants. Molecular Plant, 2021, ⟨10.1016/j.molp.2021.01.015⟩. ⟨cea-03125841⟩