Plant-Microbe Interactions Facing Environmental Challenge

Abstract

In the past four decades, tremendous progress has been made in understanding how plants respond to microbial colonization and how microbial pathogens and symbionts reprogram plant cellular processes. In contrast, our knowledge of how environmental conditions impact plant-microbe interactions is less understood at the mechanistic level, as most molecular studies are performed under simple and static laboratory conditions. In this review, we highlight research that begins to shed light on the mechanisms by which environmental conditions influence diverse plant-pathogen, plant-symbiont, and plant-microbiota interactions. There is a great need to increase efforts in this important area of research in order to reach a systems-level understanding of plant-microbe interactions that are more reflective of what occurs in nature.

Keywords: abiotic stress; circadian clock; climate change; humidity; innate immunity; light; nutrient; plant pathogen; symbiosis; temperature.

Figure 1.

(A) An overview diagram depicting environmental conditions that are known to affect plant-microbe interactions in plants. (B) The dynamic nature of environmental conditions that fluctuate and influence one another.

Figure 2.

Schematic diagram of temperature-, circadian- and humidity-mediated effects on plant immunity. (A) Effect of elevated temperature on immune signaling in plants. At elevated temperature, PTI responsive genes and phosphorylation of MPKs and BIK1 are activated more robustly. Elevated temperature suppresses ETI through (i) dampening expression of ETI-responsive genes, (ii) disruption of nuclear localization of NLR proteins, including SNC1 and RPS4, possibly through an ABA-dependent mechanism, (iii) reduced transcripts of SNC1 by the action of the ZRK-TCP module, and (iv) PIF4-mediated growth-defense tradeoff. Elevated temperature inhibits SA accumulation and defense gene expression via an unknown mechanism. (B) Effects of circadian clock on immune signaling in plants. The slave oscillator, GRP7, acting downstream of CCA1 and LHY, binds to the transcripts of FLS2 and EFR. Bacterial effector protein HopU1 blocks this interaction and reduces FLS2 protein level. GRP7 could also interact with FLS2 or EFR protein and translational machinery components. RPP4-mediated plant defense against avirulent Hpa isolates is modulated by CCA1 or LHY via transcriptional regulation. Clock protein TIC interacts with and contributes to the reduction of MYC2 protein accumulation. Clock protein CHE either directly regulates the expression of ICS1 gene or through CBP60g and SARD1. (C) Effects of humidity on immune signaling in plants. Left panel, under high atmospheric humidity, water-soaked lesions can be caused by two Pst DC3000 effectors, AvrE and HopM1. While how AvrE induces water-soaking remains unknown, HopM1 causes water-soaking in part through mediating the removal of HopM1-interactor7 (MIN7) in the host (Nomura et al., 2006). Right panel, AvrHah1, effector secreted by X. gardneri, transcriptionally activates bHLH3 and bHLH6. bHLH3 and bHLH6 regulate the induction of pectinesterase (PE) and pectate lyase (PL) that likely changes/loosens plant cell wall structure to create water soaking lesions.

Figure 3.

Nutrient status and plant-microbe interactions. (A) Phosphate status and Arabidopsis-root microbiome interaction. Under phosphate-limiting state, C. tofieldiae (Ct) colonization activates phosphate starvation response (PSR) genes and promotes phosphate uptake, which requires a functional PHR1. Additionally, PHR1 represses immune-related gene expression and is required for assembling root endophytic microbiome. (B) Nitrogen status and legume-Rhizobium interaction. Under nitrogen-sufficient condition, nodule formation is repressed through autoregulation of nodulation (AON; left panel). When plant is nitrogen-depleted (right panel), shoot-produced miR2111 post-transcriptionally downregulates TML (a positive regulator of AON) in the root to maintains host susceptibility to rhizobium for nodulation. (C) Iron status and Arabidopsis-root microbiome interaction. MYB72- and BGLU42-mediated production and exudation of scopoletin is induced by iron deficiency and during induced systemic resistance (ISR). Scopoletin is hypothesized to solubilize iron for uptake and to select plant-associated microbes.