Plant latent defense response to microbial non-pathogenic factors antagonizes compatibility

Abstract

Unlike microbe-associated molecular patterns (MAMPs) that are readily targeted by host immunity, microbial non-pathogenic factors (NPFs) appear negligible as they do not elicit defense. Little is known about whether and how NPFs may be monitored by hosts to control compatibility. Herein a forward genetic screen isolated an Arabidopsis mutant with a loss of plant-rhizobacteria mutualism, leading to the disclosure of plant latent defense response (LDR) to NPFs. The activation of LDR in the mutant, named rol1 for regulator of LDR 1, is triggered by several non-pathogenic volatile organic compounds (VOCs) and antagonizes plant compatibility with the beneficial bacterium Bacillus amyloliquefaciens GB03. The activation of LDR in rol1 is mediated through the prokaryotic pathway of chloroplastic lipid biosynthesis. The rol1 root microbiome showed reduced proportion of the Bacillaece family. We propose that, in parallel to the forefront immunity to MAMPs, LDR to certain NPFs provides a hidden layer of defense for controlling compatibility with commensal or beneficial microbes.

History of a model plant growth-promoting rhizobacterium, Bacillus velezensis GB03: from isolation to commercialization

“…This interesting phenomenon was attributed to the VOC diacetyl. Together with another study on the transition from mutualism to incompatibility ( Yang et al., 2022 ), it has led to the discovery of a new research area known as plant latent defense response (LDR), which is conditionally activated by certain non-pathogenic microbial factors and thus guards against potential risks from beneficial or commensal microbes ( Zhang, 2023 ). This hidden layer of defense increases the complexity in comprehending PGPR-mediated plant nutrient uptake, owing to the crosstalk between immunity and nutrient-related processes.…”

Plant latent defense response against compatibility

“…While it remains unclear how the volatile signals initiate plant cellular responses, the known downstream mechanisms include modulation of auxin and abscisic acid signaling [ 18 , 19 ], enhancement of iron and sulfur assimilation [ 20 , 21 ], enhancement of photosynthetic apparatus production [ 19 ], protection of chlorophylls from stress-induced degradation [ 22 ], and the requirement of AGP19 that is important for cell division and expansion [ 23 ]. The Arabidopsis plants defected in salicylic acid accumulation ( nahG ) or signaling ( eds1 ) showed similar fresh weights as the wild type plants [ 24 ], indicating that decreasing the basal immunity is not sufficient to cause PGP; in contrast, several NPFs in the GB03 volatile emissions strongly elicited plant immunity under certain conditions and compromised the PGP, showing not only the trade-off between growth and immunity, but also the antagonism against compatibility as evidenced by the immunity-dependent impairment of bacterial colonization [ 24 , 25 ].…”

“…Plant regulation of the compatibility with beneficial microbes through the perception of NPFs was also observed in the Arabidopsis mutant rol1 ( regulator of LDR 1 ), which was isolated from a forward genetic screen for mutants with defective plant growth promotion triggered by B. amyloliquefaciens GB03 [ 24 ]. In wild-type plants, GB03 enhanced chloroplastic lipid biosynthesis that consumed oleic acid.…”

“…This hidden layer of plant defense highlights the importance of NPFs in mediating plant regulation of mutualism, leading to the concept of the latent defense response (LDR), which is conditionally activated by certain NPFs and antagonizes compatibility [ 24 ]. LDR indicates the plant’s initiative in determining the plant-microbe association for optimized benefits, because the conditional activation of LDR avoids unnecessary hostility to beneficial or commensal microbes while enabling plants to deter the same microbes when the microbial association is unfavorable to the plants.…”

“…Similarly, how different LDR pathways may interact with each other is also to be explored. For instance, the diacetyl-triggered LDR is mediated through a mechanism different from the LDR in rol1 , because the latter is not induced by diacetyl [ 24 , 25 ]. Moreover, the activation of LDR by its eliciting NPFs may be interfered indirectly by the plant developmental regulation or environmental responses, as well as by other factors from the NPF-producing microbes or the other microbes present in the same plant-associated community.…”