Mechanistic insights into the regulation of plant phosphate homeostasis by the rice SPX2 – PHR2 complex

Abstract

Phosphate (Pi) is a key macronutrient limiting plant growth and crop productivity. In response to the nutrient deficiency, Pi starvation response (PHR) transcription factors activate Pi starvation induced (PSI) genes. PHR transcription factors are negatively regulated by stand-alone SPX proteins, cellular receptors for inositol pyrophosphate (PP-InsP) nutrient messengers. How PP-InsP-bound SPX domains interact with PHR transcription factors is poorly understood. Here, we report crystal structures of the rice SPX2/InsP6/PHR2 complex and of the PHR2 DNA binding (MYB) domain in complex with its target DNA at resolutions of 3.1 Å and 2.7 Å, respectively. Inositol polyphosphate binding causes SPX2 to assemble into a domain-swapped dimer. The signalling-active SPX2 dimer binds two copies of PHR2, targeting both its coiled-coil (CC) oligomerisation domain and its MYB domain. Structural comparisons, biochemical analyses and genetic characterizations reveal that the SPX2 senses InsP6 / PP-InsPs to inactivate PHR2 by establishing severe steric clashes with the PHR2 MYB domain, preventing DNA binding, and by disrupting oligomerisation of the PHR2 CC domain, attenuating promoter binding. The complex structure rationalizes how PP-InsPs activate SPX receptor proteins to target PHR family transcription factors and provides a mechanistic framework to engineer crops with improved phosphate use efficiency.

Inositol pyrophosphate-controlled kinetochore architecture and mitotic entry in S. pombe

“…The functions of these molecules are very diverse, ranging from defense against pathogens in humans and plants, to mammalian organ development and fungal morphogenesis and pathogenicity [2][3][4][5][6][7][8]. Additionally, IPPs play an important function in cell adaptation to adverse environmental conditions, including a predominant role in maintaining phosphate homeostasis in mammals, plants and fungi [4,[9][10][11][12][13][14][15][16][17][18][19]. Although, IPPs appear to have rather pleiotropic effects, evidence is accumulating that different phenotypes are connected such as fungal virulence and phosphate homeostasis [20].…”

Phosphate starvation response precedes abscisic acid response under progressive mild drought in plants

“…The genetic basis of the PSR has been intensively studied in the model experimental plant Arabidopsis 16 . PSR is controlled by a conserved pathway centered on the SPX receptors and PHR transcription factors [17][18][19] . PHR transcription factors regulate the expression of PSR genes (e.g., those encoding phosphate transporters, phosphatases, and lipid modification proteins) to enhance Pi uptake under Pideficit conditions 20 .…”