The phosphate starvation response regulator PHR2 antagonizes arbuscule maintenance in Medicago

• Published in: The New phytologist 2024-12, Vol.244 (5), p.1979-1993
• Main Authors: Wang, Peng, Zhong, Yanan, Li, Yan, Zhu, Wenqian, Zhang, Yuexuan, Li, Jingyang, Chen, Zuohong, Limpens, Erik
• Format: Article
• Language: English
• Subjects: Alfalfa; arbuscular mycorrhiza; Arbuscular mycorrhizas; arbuscule development; Biodegradation; Colonization; Degradation; Gene expression; Gene Expression Regulation, Plant; Genes; Maintenance; Medicago; Medicago - genetics; Medicago - microbiology; Medicago truncatula; Medicago truncatula - genetics; Medicago truncatula - metabolism; Medicago truncatula - microbiology; Mycorrhizae - physiology; P1BS element; Phosphate starvation response; Phosphate transporter; Phosphates; Phosphates - deficiency; Phosphates - metabolism; Plant Proteins - genetics; Plant Proteins - metabolism; Promoters; Proteins; Starvation; Symbionts; Symbiosis; Symbiosis - genetics; Transcription factors; Transcription Factors - genetics; Transcription Factors - metabolism
• ISSN: 0028-646X; 1469-8137; 1469-8137
• DOI: 10.1111/nph.19869

Summary Phosphate starvation response (PHR) transcription factors play essential roles in regulating phosphate uptake in plants through binding to the P1BS cis‐element in the promoter of phosphate starvation response genes. Recently, PHRs were also shown to positively regulate arbuscular mycorrhizal colonization in rice and lotus by controlling the expression of many symbiotic genes. However, their role in arbuscule development has remained unclear. In Medicago, we previously showed that arbuscule degradation is controlled by two SPX proteins that are highly expressed in arbuscule‐containing cells. Since SPX proteins bind to PHRs and repress their activity in a phosphate‐dependent manner, we investigated whether arbuscule maintenance is also regulated by PHR. Here, we show that PHR2 is a major regulator of the phosphate starvation response in Medicago. Knockout of phr2 showed reduced phosphate starvation response, symbiotic gene expression, and fungal colonization levels. However, the arbuscules that formed showed less degradation, suggesting a negative role for PHR2 in arbuscule maintenance. This was supported by the observation that overexpression of PHR2 led to enhanced degradation of arbuscules. Although many arbuscule‐induced genes contain P1BS elements in their promoters, we found that the P1BS cis‐elements in the promoter of the symbiotic phosphate transporter PT4 are not required for arbuscule‐containing cell expression. Since both PHR2 and SPX1/3 negatively affect arbuscule maintenance, our results indicate that they control arbuscule maintenance partly via different mechanisms. While PHR2 potentiates symbiotic gene expression and colonization, its activity in arbuscule‐containing cells needs to be tightly controlled to maintain a successful symbiosis in Medicago. See also the Commentary on this article by Bashyal et al., 244: 1684–1686.