Action Mechanisms of Effectors in Plant-Pathogen Interaction

Abstract

Plant pathogens are one of the main factors hindering the breeding of cash crops. Pathogens, including oomycetes, fungus, and bacteria, secrete effectors as invasion weapons to successfully invade and propagate in host plants. Here, we review recent advances made in the field of plant-pathogen interaction models and the action mechanisms of phytopathogenic effectors. The review illustrates how effectors from different species use similar and distinct strategies to infect host plants. We classify the main action mechanisms of effectors in plant-pathogen interactions according to the infestation process: targeting physical barriers for disruption, creating conditions conducive to infestation, protecting or masking themselves, interfering with host cell physiological activity, and manipulating plant downstream immune responses. The investigation of the functioning of plant pathogen effectors contributes to improved understanding of the molecular mechanisms of plant-pathogen interactions. This understanding has important theoretical value and is of practical significance in plant pathology and disease resistance genetics and breeding.

Keywords: effector; infestation process; pathogen; plant immunity; virulence promotion.

Figure 1

Plant immune system. PRRs of plant cells recognize PAMPs and trigger the first layer of plant immune response PTI, which triggers responses such as calcium inward flow and reactive oxygen species burst. Pathogens produce effectors to inhibit PTI, and plant R proteins, such as NB-LRR proteins, are activated by effectors to produce the second layer of immune response ETI, which disrupts effectors and causes cell death.

Figure 2

Schematic diagram of effectors that break physical barriers to infestation and regulate the infestation environment. Effectors promote infestation by regulating stomata, degrading cell walls, regulating intercellular filament function, disrupting the cytoskeleton, and creating conditions conducive to infestation. P. syringae AvrB interacts with RIN4 protein to promote COI1 and JAZ protein binding and enhance plasma membrane H⁺-ATPase AHA1 activity. HopX1 inhibits stomatal immunity by degrading multiple JAZ transcriptional repressors leading to JA activation. xopS stabilizes WRKY40 and decreases JAZ expression. HopM1 and AvrE1 target the ABA signaling pathway, increase ABA accumulation, and induce stomatal closure. Fusarium oxysporum Avr2 and Six5 interact with intercellular filaments to enlarge the pore size. The oomycete pathogen Phytophthora brassicae RxLR3 effector physically interacts with callus synthases CalS1, CalS2 and CalS3 to impede callus accumulation in intercellular hyphae. P. syringae HopO1-1 interacts with and destabilizes the PD proteins PDLP7 and PDLP5. HopW1 disrupts the actin cytoskeleton by forming complexes with actin. Bradyrhizobium graminearum ROPIP targets the barley ROP GTPase HvRACB and manipulates host cell microtubule organization to facilitate its own cell entry. Xanthomonas oleifera T3E XopR binds to actin in the cell cortex to manipulate actin assembly and disrupt the host actin cytoskeleton. The hydrophobic protein MPG1 in Fusarium inermis, FgHyd1~FgHyd4 in F. graminearum, and the extracellular matrix protein EMP1 in F. graminearum can create hydrophobic spaces and participate in appressorium development. Ralf-like effectors can cause an increase in extracellular pH to promote the invasive growth of the fungus. Overall, effectors favor their own infestation by modifying the structural properties of plant cells and environmental conditions.

Figure 3

Inhibition of PAMP-triggered immunity by pathogens. Pathogens have developed different strategies to suppress PAMP-triggered immunity. For chitin, the main means used by pathogens are: (i) protection of the mycelium from degradation by plant chitinases, with representative effectors being the CBM family and CPP proteins; (ii) inhibition of LysM receptor recognition, with representative effectors being AvrPto, AvrPtoB, CoNIS1 and MoNIS1; (iii) isolation and masking of chitin oligosaccharides, representative effectors are Slp6, Ecp6, MpChi and ChELP1/2; (iv) targeting chitinases for degradation, representative effectors are FoMep1, SSEP1, FoSep1 and Umfly; and (v) modification and transformation of cell wall components, representative effectors are VdPDA1, FovPDA, UmCDA.

Figure 4

Effectors interfere with host plant cell physiological activities. AvrBs3, VdSCP41, TALE, PpEC23, HaRxL21, and RipAB have transcriptional activator-like activity and act as transcription factors that interfere with host cell degradation pathways, host protein function, and host vesicle transport, through regulating transcription of different genes, thus directly inducing the expression of plant genes. Nuclear effectors of M. oryzae MoHTR1 and MoHTR2 also reprogram the expression of immune-related genes in rice. In addition, the wheat stripe rust effector protein Pst_A23 suppresses host immune responses by regulating variable splicing of host disease-resistance-associated genes. Fusarium graminearum CSEP0064/BEC1054, F. graminearum Fg12, the secreted ribonuclease VdRTX1 of V. dahliae, C. orbiculare SRN1 and SRN2, and the wheat leaf blight effector Zt6 degrade host RNA and cause cell death. Phytophthora infestans effector PexRD54, P. syringae bacterial effectors HrpZ1, HopF3, and AvrPtoB employ different molecular strategies to regulate autophagy. P. syringae HopZ4, avrPiz-t, the U. maydis effector Tin2 launch an attack on the host ubiquitin-proteasome system to inhibit proteasome activity. Osp24 in F. graminearum, ZymosepVictoria tritici effector ZtSSP2, P. syringae effector HopI1, HopN1, wheat stripe rust Pst_12806, PstGSRE1, nucleophile integrin-like effector SsITL, Phytophthora sojae effector PsAvh262, AvrPiz-t, V. dahliae effector PevD1 and Phytophthora infestans effector Pi04314 act on different protein targets to exert pathogenic effects. P. syringae effector HopM1, rice blast fungus zinc finger transcription factor MoCRZ1, Blumeria graminis BEC4, Phytophthora brassicae RxLR24 effector and RXLR-WY effector PexRD31 in Phytophthora infestans are involved in the regulation of vesicle secretion.

Figure 5

Effectors manipulate downstream immune responses in host plants. Effectors mainly manipulate plant downstream immune responses by interfering with plant hormone transduction, disrupting plant RNA silencing, regulating ROS generation, and manipulating plant cell death. The effector chorismate mutase Cmu1 of Ustilago maydis, the oomycete pathogen Phytophthora sojae and the fungus Verticillium dahliae effectors PsIsc1 and VdIsc1, POPs in Ralstonia solanecearum, P. striiformis f.sp. effector PNPi, P. syringae effector AvrPtoB, HopZ1a, HopBB1, HopX1, HopAF1, AvrRpt2, HopQ1, Phytophthora capsicum effector RxLR48, F. oxysporum Fo5176-SIX4, rice blast effector ABM, LASA of L. medterranea, Phytophthora sojae RxLR effector PsAvh238, Phytophthora effector PSE1 and EqCSEP01276 of Erysiphe quercicola SnTox3, interfere with the transduction of different hormone signals in plants. The wheat stem rust Puccinia graminis f. sp. tritici effector protein PgtSR1, PsPSR1 and PsPSR2 in Phytophthora sojae, Botrytis cinerea BC-DCL1 and BC-DCL2 and PST-milR1 are gene silencing mechanisms. The maize smut effector PEP1, the biotrophic pathogen Puccinia striiformis PsSOD1 and avirulent proteins AVR-PII, AVR-PITA in M. oryzae, inhibit ROS accumulation. The M. oryzae effector enhances COX activity by interacting with mitochondrial OsCOX11; OsCOX11 is a key regulator of mitochondrial ROS metabolism in rice. RxLR207 in Phytophthora capsici can promote the degradation of BPA1, BPL1, BPL2, and BPL4, and destabilize ACD11 in a 26S proteasome-dependent manner to promote ROS accumulation and PCD activation. F. oxysporum apoplasts (SIX1 and Foa1) and cytoplasmic effectors (Avr2, Foa2 and Foa3) promote host colonization by inhibiting flg22-induced or chitin-induced ROS. There are four main types of effectors that cause cell death, namely effectors that trigger HR responses, host-selective toxins, cell wall-degrading enzyme effectors, and effectors with conserved necrosis-inducing domains.