Plant immunity suppression via PHR1‐RALF‐FERONIA shapes the root microbiome to alleviate phosphate starvation

Abstract

The microbiome plays an important role in shaping plant growth and immunity, but few plant genes and pathways impacting plant microbiome composition have been reported. In Arabidopsis thaliana, the phosphate starvation response (PSR) was recently found to modulate the root microbiome upon phosphate (Pi) starvation through the transcriptional regulator PHR1. Here, we report that A. thaliana PHR1 directly binds to the promoters of rapid alkalinization factor (RALF) genes, and activates their expression under phosphate‐starvation conditions. RALFs in turn suppress complex formation of pathogen‐associated molecular pattern (PAMP)‐triggered immunity (PTI) receptor through FERONIA, a previously‐identified PTI modulator that increases resistance to certain detrimental microorganisms. Suppression of immunity via the PHR1‐RALF‐FERONIA axis allows colonization by specialized root microbiota that help to alleviate phosphate starvation by upregulating the expression of PSR genes. These findings provide a new paradigm for coordination of host‐microbe homeostasis through modulating plant innate immunity after environmental perturbations.

P Starvation in Roses Leads to Strongly Genotype-Dependent Induction of P-Transporter Genes during Black Spot Leaf Disease

“…This indicates a signalling crosstalk between the stress response to phosphate starvation and the response to pathogens in a genotype-specific manner. Examples of this can be found in the literature, e.g., Tang et al [ 46 ], Castrillo et al [ 47 ] and Dong et al [ 48 ] observed a negative influence of Pi Stress on the immune response, Khan et al [ 49 ] detected a positive effect, and Campos-Soriano et al [ 50 ] observed a negative influence with an excess of Pi.…”

A fungal secondary metabolism gene cluster enables mutualist-pathogen transition in root endophyteColletotrichum tofieldiae

“…Our evidence attributes PHR1/PHL1 -mediated alleviation of Ct3 pathogenesis to the suppression of fungal ABA-BOT expression, under low Pi and at high temperatures. Plant transcriptome data not detecting differential defense gene regulation, imply that PHR1/PHL1 -mediated control of fungal growth is also distinct from the previously described suppression of pattern-triggered immunity (Castrillo et al ., 2017; Tang et al ., 2022).…”

“…PHR1 and PHL1 positively regulate phosphate transporter genes during Ct colonization and are required for Ct -mediated plant growth promotion under low Pi (Hiruma et al ., 2016). PHR1/PHL1 restricts fungal overgrowth and potential virulence during beneficial interactions with Ct , whereas negatively regulating plant immunity against bacteria (Castrillo et al ., 2017; Tang et al ., 2022). However, our knowledge on the mechanisms by which PHR1/PHL1 play varied roles in different plant–microbe associations or host PSR influences microbial lifestyles is limited.…”

FERONIA Receptor Kinase Integrates with Hormone Signaling to Regulate Plant Growth, Development, and Responses to Environmental Stimuli

“…Recent findings confirm that FER is a receptor to both RALF1 and RALF23 [ 27 , 52 , 53 , 54 ]. The RALF–FER module has been shown to be involved in many different processes, including stress responses, cell growth, and immunity [ 54 , 75 , 76 ]. Among these functions, RALFs are involved in BR-regulated plant growth, and the two factors are generally functional in antagonism [ 77 , 78 , 79 ].…”