On Dec 30, 2022, the Yi Keke team of the Institute of Agricultural Resources and Regional Planning (IARRP) of the Chinese Academy of Agricultural Sciences (CAAS) was invited to publish a review article entitled "Cracking the code of plant central phosphate signaling" in Trends in Plant Science, which systematically summarizes the latest progress in the analysis of the core modules of phosphorus signal regulation and its mode of action, and provides an outlook on the research in the field.

Phosphorus (P) is an essential element for all organisms on earth to sustain life. Phosphorus is not only a component of many important compounds in plants, but also participates in various of their biological pathways, such as the synthesis and metabolism of fats and sugars. Plants can only absorb free soluble inorganic phosphate (inorganic phosphate, Pi), and because phosphate is easily fixed by the soil, it is often necessary to apply a large amount of phosphorus fertilizer to meet the needs of crops, which results in low efficiency of phosphorus fertilizer use in the field and brings risk of environmental pollution. In order to effectively acquire phosphorus and maintain its homeostasis in cells, plants have evolved complex phosphorus signaling regulation mechanisms to deal with the uneven distribution of phosphorus in soil. Therefore, exploring the regulatory mechanism of phosphorus signaling is very important for improving plant phosphorus use efficiency and avoiding crop weight loss while achieving stable yield.

The core regulatory signal of the phosphorus nutrient in plants is mediated by a class of MYB transcription factors PHRs (PHOSPHATE STARVATION RESPONSE), and the transcriptional regulatory activity of PHRs is regulated by SPXs (SYG1/Pho81/XPR1) proteins. In recent years, studies have found that InsPs (Inositol polyphosphates) molecules act as "signaling translators" of intracellular phosphorus levels, and their content is controlled by a class of bifunctional enzymes VIHs (Vip1 homologs), and InsPs molecules change the interaction between PHRs and SPXs to regulate plant responses to phosphorus deficiency.

With the analysis of the crystal structure of the SPX-InsP-PHR complex in recent years, the working mode of the SPX-InsP-PHR module has been gradually established: when the phosphorus supply is sufficient, the ATP content in the cell increases, and the VIHs exert kinase activity to synthesize InsP8 , and InsP8 forms a 2:2:2 complex with SPXs and PHRs, inhibiting PHRs from activating phosphorus deficiency signals; but when phosphorus is deficient, VIHs exert phosphatase activity, the content of InsP8 in cells decreases, and the SPX-InsP-PHR complex depolymerizes , and PHRs transcription factors form dimers to activate the expression of downstream phosphorus deficiency response genes and initiate a phosphorus deficiency response.

This paper also puts forward a series of profound questions and prospects for future research directions in the field:

1.There are homologous genes of different PHRs genes and other MYB transcription factors (such as NIGTs, RLI1s, PAP1s, etc.) in plants, which are also involved in the regulation of phosphorus signaling. Will they also form SPX-InsP-PHR in plants, namely complex structures that exercise similar modes of action?

2.In addition to SPXs proteins, plants contain a variety of proteins containing SPX structures, most of which are related to phosphorus transport or transporter degradation, such as SPX-EXS, SPX-MFS, SPX-SLC, SPX-VTC and SPX-RING. Do they also have InsPs binding activity and competitive binding, and will they will form heterodimers with SPXs protein?

3.There are many isomers of InsPs molecules. Will they also participate in the regulation of phosphorus signaling in plants and compete with SPXs?

4.There are obvious differences in the structure of PHRs between algae and terrestrial plants, so does the working model of SPX-InsP-PHR complex also exist in lower plants? Are the functions of VIHs also conserved in lower plants?

5.PHRs directly repress the expression of defense-related genes, thereby favoring the assembly of the root microbiota, so what is the mechanism by which the SPX-InsP-PHR complex regulates Pi-starvation-suppressed genes, especially in the presence of microbes?

Discovery of the core module of plant phosphorus signaling regulation and its mode of action [Photo/IARRP]

Postdoctoral worker Jia Xianqing of the IARRP is the first author of the paper, researcher Yi Keke is the corresponding author of the paper, and postdoctoral Wang Long and Professor Laurent Nussaume of Aix-Marseille University are co-authors of the paper. Relevant work has been supported by key projects of the National Natural Science Foundation of China, youth projects of the National Natural Science Foundation of China, innovation projects of the Chinese Academy of Agricultural Sciences, and the China Postdoctoral Science Foundation.

Paper link:

https://www.sciencedirect.com/science/article/pii/S1360138522003296