New Insights into the Connections between Flooding/Hypoxia Response and Plant Defenses against Pathogens

Abstract

The impact of global climate change has highlighted the need for a better understanding of how plants respond to multiple simultaneous or sequential stresses, not only to gain fundamental knowledge of how plants integrate signals and mount a coordinated response to stresses but also for applications to improve crop resilience to environmental stresses. In recent years, there has been a stronger emphasis on understanding how plants integrate stresses and the molecular mechanisms underlying the crosstalk between the signaling pathways and transcriptional programs that underpin plant responses to multiple stresses. The combination of flooding (or resulting hypoxic stress) with pathogen infection is particularly relevant due to the frequent co-occurrence of both stresses in nature. This review focuses on (i) experimental approaches and challenges associated with the study of combined and sequential flooding/hypoxia and pathogen infection, (ii) how flooding (or resulting hypoxic stress) influences plant immunity and defense responses to pathogens, and (iii) how flooding contributes to shaping the soil microbiome and is linked to plants' ability to fight pathogen infection.

Keywords: combined stress; flooding; hypoxia; plant defenses against pathogens; plant immunity.

Figure 1

Overview of signaling events downstream of PAMP perception. Pathogens are detected via either PAMPs or pathogen effectors. PAMPs bind to and activate PRRs at the plant cell surface (1). This leads to the generation of second messengers such as Ca²⁺ (blue circles) or ROS (red circles) (2). These second messengers contribute to initiating phosphorylation cascades that result in the activation of transcription factors (3) which trigger the expression of defense genes (4 and 5). This transcriptional reprogramming results in the activation of the defense response and of hormone signaling pathways (6–7) that further contribute to plant defenses against pathogens. Steps (1) to (6) also apply to the perception of and response to abiotic stresses.

Figure 2

Hypoxia and flg22 stress sensing. (a) In its non-activated state, FLS2 interacts with BIK1 and cycles between the plasma membrane (PM) and endosomal compartments. Upon flg22 binding, FLS2 forms a stable complex with BAK1 stimulating phosphorylation (orange circles), which, in turn, triggers the release of BIK1 and the production of second messengers. (b) Under normal oxygen (O₂) levels, the N-degron pathway targets ERF-VII transcription factors for degradation through the action of methionine amino peptidases (MAPs), which remove the initial methionine (M) of ERF-VII transcription factors; plant cysteine oxidases (PCOs), which oxidize the newly exposed N-terminal cysteine (C* denotes oxidized cysteine); arginyl transferases (ATE1 and ATE2) that conjugate arginine (R) to the N-terminus; and the E3 ubiquitin ligase PRT6, leading to the polyubiquitination of the ERF-VII transcription factors and their degradation by the 26 proteasome. Under low oxygen levels (red dashed square and arrow), the N-degron pathway is inhibited at the PCO level, thus enabling the stabilization of the ERF-VII transcription factors, their accumulation in the nucleus, and the activation of hypoxia response genes. NO is known to stabilize ERF-VII transcription factors through an as-of-yet unknown mechanism involving PCOs.

Figure 3

Second messengers and signaling pathways downstream of pathogen or hypoxia sensing. (a) After sensing flg22, phosphorylated BIK1 interacts with RBOHD, as well as with other proteins such as GPA1 or AGB1, which are alpha and beta subunitsof a G-protein complex. Small molecules such as phosphatidic acid (PA) can also interact with RBOHD, inducing its activity and producing O₂-, which is rapidly dismutated into H₂O₂ in the apoplast. (b) HYPOXIA-RESPONSIVE UNIVERSAL STRESS PROTEIN 1 (HRU1)-HRU1 dimers are monomerized under hypoxic conditions. HRU1 migrates to the plasma membrane and interacts with RBOHD, thus contributing to its activation. ROP2 is also known to act upstream of RBOHD through an unknown mechanism. Common regulatory mechanisms of RBOHD include the direct binding of Ca²⁺ to RBOHD’s EF hands and CPKs such as CPK5, which interacts with RBOHD’s N-terminus.

Figure 4

MAPK signaling and transcriptional regulation. The induction of MAPK signaling upon pathogen/PAMP or hypoxia sensing involves different mechanisms, including Ca²⁺ (purple circles) signaling, ROS (red circles), and PA. MAPK signaling triggers the phosphorylation (orange circles: phosphate groups) of different transcription factors such as RAP2.12, RAP2.3, or WRKY33, regulating their activity and sub-cellular localization. Several transcription factors that act downstream of MAPK signaling have been shown to play dual roles in pathogen defense and response to hypoxia.