Root microbiota drive direct integration of phosphate stress and immunity

Abstract

Plants live in biogeochemically diverse soils that harbor extraordinarily diverse microbiota. Plant organs associate intimately with a subset of these microbes; this community’s structure can be altered by soil nutrient content. Plant-associated microbes can compete with the plant and with each other for nutrients; they can also provide traits that increase plant productivity. It is unknown how the plant immune system coordinates microbial recognition with nutritional cues during microbiome assembly. We establish that a genetic network controlling phosphate stress response influences root microbiome community structure, even under non-stress phosphate conditions. We define a molecular mechanism regulating coordination between nutrition and defense in the presence of a synthetic bacterial community. We demonstrate that the master transcriptional regulators of phosphate stress response in Arabidopsis also directly repress defense, consistent with plant prioritization of nutritional stress over defense. Our work will impact efforts to define and deploy useful microbes to enhance plant performance.

Phosphate excess increases susceptibility to pathogen infection in rice

“…During infection of SAP11 AYWB Arabidopsis plants with the bacterial pathogen Pseudomonas syringae , the induction of defence responses was suppressed and the SAP11 AYWB plants exhibited susceptibility to bacterial infection (Lu et al , ). In other studies, cross‐talk between Pi starvation and salt and drought stress signalling pathways, or hormone‐signalling pathways, has been described (Song and Liu, ; Abbas Khan et al ., ; Baek et al , ; Castrillo et al , ). Knowing that the defence‐related hormones JA and ethylene (ET) function as signalling hormones in the rice defence against M. oryzae (Nasir et al , ), a major future challenge is to determine whether Pi content affects defence hormone signalling in rice for the control of immune responses.…”

Root type and soil phosphate determine the taxonomic landscape of colonizing fungi and the transcriptome of field‐grown maize roots

“…In Arabidopsis, P sufficiency has been associated with increased defense gene expression in roots. This was shown to be responsible for changes in a synthetic bacterial rhizosphere and root community (Castrillo et al ., ) and suppression of the endophytic fungus Colletotrichum tofieldiae , which delivers P under LP conditions (Hacquard et al ., ; Hiruma et al ., ). We hypothesize that P‐induced defense responses in lateral roots could also be responsible for the fungal community shifts observed in field‐grown maize roots grown at HP (Fig.…”

Understanding and exploiting plant beneficial microbes

“…Experiments using both wild soil and a synthetic bacterial community demonstrated that Arabidopsis PSR mutants assemble a different root microbiome than wild type plants, even when grown in phosphate-sufficient soil. Further, the master transcriptional regulator of PSR directly integrates this nutritional stress response and immune system outputs [97]. These early examples suggest that the coordination of defense and nutrition is critical to driving microbiome function.…”

“…Purple: Firmicutes, Blue: Actinobacteria, Yellow: Bacteroidetes, Pink: Deinococcus-thermus and Orange: Proteobacteria. The tree was constructed using a concatenated filtered alignment of 31 single copy genes [97]. The genome assemblies of each of the three different sequencing projects can be accessed via the IMG/JGI portal by using the following project IDs:…”