Plant Disease Resistance-Related Signaling Pathways: Recent Progress and Future Prospects

Abstract

Plant-pathogen interactions induce a signal transmission series that stimulates the plant's host defense system against pathogens and this, in turn, leads to disease resistance responses. Plant innate immunity mainly includes two lines of the defense system, called pathogen-associated molecular pattern-triggered immunity (PTI) and effector-triggered immunity (ETI). There is extensive signal exchange and recognition in the process of triggering the plant immune signaling network. Plant messenger signaling molecules, such as calcium ions, reactive oxygen species, and nitric oxide, and plant hormone signaling molecules, such as salicylic acid, jasmonic acid, and ethylene, play key roles in inducing plant defense responses. In addition, heterotrimeric G proteins, the mitogen-activated protein kinase cascade, and non-coding RNAs (ncRNAs) play important roles in regulating disease resistance and the defense signal transduction network. This paper summarizes the status and progress in plant disease resistance and disease resistance signal transduction pathway research in recent years; discusses the complexities of, and interactions among, defense signal pathways; and forecasts future research prospects to provide new ideas for the prevention and control of plant diseases.

Keywords: disease resistance; plant hormone; signal molecule; signaling pathway.

Figure 1

A model of immune responses in plant–pathogen interactions. A plant’s innate immune system consists of PTI and ETI. PTI induced through the recognition of PAMPs by PRRs can inhibit the growth of most pathogens. Then, downstream signaling pathways such as Ca²⁺ signaling, the MAPK cascade, and ROS signaling are activated. Some pathogens can release pathogenic effectors to interfere with PTI, causing susceptibility triggered by effectors. The disease R proteins with conserved NB-LRR can directly or indirectly identify specific effectors to trigger ETI, which often causes an HR at the infection site of the pathogen, and then inhibit the growth of the pathogens again. The SA and JA/ET signaling pathways are also involved in PTI and ETI activation and the resistance response to pathogen infections, thereby stimulating downstream transcription factors and initiating plant defense responses. Many ncRNAs play critical roles in PTI or ETI responses by regulating various biological processes, such as the MAPK cascade, the expression of signaling components, ROS production, plant hormone biosynthesis, and signaling. NB-LRR, nucleotide-binding leucine-rich repeat; PRRs, pattern recognition receptors; SA, salicylic acid; JA/ET, jasmonic acid/ethylene; HR, hypersensitive response; PCD, programmed cell death; SAR, systemic acquired resistance; R, resistance; ROS, reactive oxygen species; MAPK, mitogen-activated protein kinase; PAMPs, pathogen-associated molecular pattern; PTI, PAMP-triggered immunity; ETI, effector-triggered immunity; ncRNAs, non-coding RNAs. The arrows indicate positive regulation, and open blocks indicate negative regulation.

Figure 2

Schematic representation of the plant defense signal transduction network. In the process of plant–pathogen interactions, a series of signals are triggered to induce plant defense responses. The complex and diverse signal pathways interact with each other and form signal transduction networks in plants. After the resistant host recognizes the elicitors produced by pathogens, it activates the signal transduction system, causing the release of Ca²⁺, an MAPK cascade reaction, and the activation of R genes. Ca²⁺ flowing into the cytoplasm can activate CaMs and CMLs, induce downstream NO synthesis, and then induce a primary immune response, including HR. Moreover, NO may regulate an HR/PCD through a synergistic effect with ROS. Besides being a signal to activate SAR, ROS can directly act as antibacterial effectors and enhance the structural resistance of the host. The interaction between the R gene and the avirulent gene (Avr) can stimulate a series of defense responses, such as the HR/PCD and SAR, which are induced by SA and give a strong resistance against some biotrophic pathogens. GDG1 is necessary for pathogen-induced SA biosynthesis, and its expression is regulated by EDS1 and PAD4. SA can also control the expression of GDG1, EDS1, and PAD4 through a positive feedback loop. The positive feedback regulation of GDG1 lies in the high level of SA accumulation. JA/ET signaling pathways mainly regulate plant resistance to necrotic pathogens and wounds. JA and ET also mediate the resistance induced by root microorganisms, which is called induced systemic resistance (ISR). SA inhibits the JA/ET pathway by activating NPRl, a positive regulatory gene of the SA pathway. ERF1 is located at the intersection of the JA and ET signaling pathway defense against pathogen infections and in wound responses. A JA signal can promote the interaction between JAZ and the SCF^COI1 ubiquitin ligase, resulting in the ubiquitination of the JAZ protein and degradation by the 26S proteasome, and then the activation of transcription factors such as MYC2 to induce JA responses. Ultimately, a series of downstream responses, such as the reinforcement of physical defensive structures, the production of secondary metabolites, the inhibition of growth pathogens by the induction of defensive proteins, the activation of the ROS scavenging system, and other disease resistance factors, are activated to fight against pathogen infection. CNGCs, cyclic nucleotide-gated channels; CaMs, calmodulins; CPKs, calcium-dependent protein kinases; GLR, glutamate receptor-like genes; NO, nitric oxide; POD, peroxidase; SOD, superoxide dismutase; CAT, catalase; APX, ascorbate peroxidase; GST, glutathione S-transferase; ROS, reactive oxygen species; RBOHD, respiratory burst oxidase homolog D; H₂O₂, hydrogen peroxide; O₂⁻, superoxide ion; OH, hydroxyl radical; BIK1, BOTRYTIS-INDUCED KINASE1; MAPK, mitogen-activated protein kinase; R-Avr, interaction between an avirulence (Avr) gene in the pathogen and the corresponding resistance (R) gene in the host; EDS1, enhanced disease susceptibility; PAD4, phytoalexin-deficient 4; NPR1, non-expresser of PR genes 1; GDG1, GH3-like defense gene 1; EIN2, ethylene-insensitive 2; ISR, induced systemic resistance; SCF, Skp/Cullin/F-box; COI1, coronatine-insensitive 1; LOX2, lipoxygenase 2; VSP2, vegetative storage protein 2; JAZ, jasmonate ZIM-domain; CTR1, copper transport protein 1; ETR1, ethylene receptor gene 1; ERF, ethylene response factor; PR, pathogenesis-related protein; PGIP, polygalacturonase-inhibitory protein; OXO, oxalate oxidase. The arrows indicate positive regulation, and open blocks indicate negative regulation. Dashed lines indicate possible or indirect interactions.

Figure 3

The function of SA in the formation of local resistance and SAR. Plants can accumulate a large amount of SA after being infected by many pathogens. In addition to the SA accumulated at the infection site, SA is also associated with the SAR of uninfected tissues. NPR1 is critical for SA-dependent PR gene expression and SAR. The inhibition of SA accumulation or biosynthesis will inhibit the formation of SAR. NahG is an inhibitor of SA synthesis, which can convert SA into inactive catechol. Therefore, the overexpression of this gene can inhibit SAR formation and PR gene expressions. INA and BTH are analogues of SA, which are also plant defense activators and can induce SAR and the expression of PR genes. MeSA is a derivative of SA, which can act as a mobile inducer of SAR and induce the expression of defense genes in adjacent plants. SAR, systemic acquired resistance; MeSA, methyl salicylate; BTH, benzothiadiazole; INA, 2,6-dichloroisonicotinic acid; NahG, salicylate hydroxylase; BSMT1, benzoic acid/salicylic acid carboxyl methyltransferases; MES, methylesterases.