Plant Immune Pathways Research Articles

Natural SNP Variation in GbOSM1 Promotor Enhances Verticillium Wilt Resistance in Cotton.

Osmotin is classified as the pathogenesis-related protein 5 group. However, its molecular mechanism involved in plant disease resistance remains largely unknown. Here, a Verticillium wilt (VW) resistance-related osmotin gene is identified in Gossypium barbadense (Gb), GbOSM1. GbOSM1 is preferentially expressed in the roots of disease-resistant G. barbadense acc. Hai7124 and highly induced by Verticillium dahliae (Vd). Silencing GbOSM1 reduces the VW resistance of Hai7124, while overexpression of GbOSM1 in disease-susceptible G. hirsutum improves tolerance. GbOSM1 predominantly localizes in tonoplasts, while it relocates to the apoplast upon exposure to osmotic stress or Vd infection. GbOSM1 confers VW resistance by hydrolyzing cell wall polysaccharides of Vd and activating plant immune pathways. Natural variation contributes to a differential CCAAT/CCGAT elements in the OSM1 promoter in cotton accessions. All G. hirsutum (Gh) exhibit the CCAAT haplotype, while there are two haplotypes of CCAAT/CCGAT in G. barbadense, with higher expression and stronger VW resistance in CCGAT haplotype. A NFYA5 transcription factor binds to the CCAAT element of GhOSM1 promoter and inhibits its transcription. Silencing GhNFYA5 results in higher GhOSM1 expression and enhances VW resistance. These results broaden the insights into the functional mechanisms of osmotin and provide an effective strategy to breed VW-resistant cotton.

TaTHI2 interacts with Ca2+-dependent protein kinase TaCPK5 to suppress virus infection by regulating ROS accumulation.

Thiamine (vitamin B1) biosynthesis involves key enzymes known as thiazole moieties (THI1/THI2), which have been shown to participate in plant responses to abiotic stress. However, the role of THI1/THI2 in plant immunity remains unclear. In this study, we cloned TaTHI2 from wheat and investigated its function in Chinese wheat mosaic virus (CWMV) infection. Overexpression of TaTHI2 (TaTHI2-OE) inhibited CWMV infection, while TaTHI2 silencing enhanced viral infection in wheat. Interestingly, the membrane-localized TaTHI2 protein was increased during CWMV infection. TaTHI2 also interacted with the Ca2+-dependent protein kinase 5 (TaCPK5), which is localized in the plasma membrane, and promoted reactive oxygen species (ROS) production by repressing TaCPK5-mediated activity of the catalase protein TaCAT1. CWMV CP disrupted the interaction between TaTHI2 and TaCAT1, reducing ROS accumulation and facilitating viral infection. Additionally, transgenic plants overexpressing TaTHI2 showed increased seed number per ear and 1000-kernel weight compared to control plants. Our findings reveal a novel function of TaTHI2 in plant immunity and suggest its potential as a valuable gene for balancing disease resistance and wheat yield. Furthermore, the disruption of the TaTHI2-mediated plant immune pathway by CWMV CP provides further evidence for the evolutionary arms race between plants and viruses.

Breaking Boundaries: The Perpetual Interplay Between Tobamoviruses and Plant Immunity.

Plant viruses of the genus Tobamovirus cause significant economic losses in various crops. The emergence of new tobamoviruses such as the tomato brown rugose fruit virus (ToBRFV) poses a major threat to global agriculture. Upon infection, plants mount a complex immune response to restrict virus replication and spread, involving a multilayered defense system that includes defense hormones, RNA silencing, and immune receptors. To counter these defenses, tobamoviruses have evolved various strategies to evade or suppress the different immune pathways. Understanding the interactions between tobamoviruses and the plant immune pathways is crucial for the development of effective control measures and genetic resistance to these viruses. In this review, we discuss past and current knowledge of the intricate relationship between tobamoviruses and host immunity. We use this knowledge to understand the emergence of ToBRFV and discuss potential approaches for the development of new resistance strategies to cope with emerging tobamoviruses.

Manipulation of plant immunity via an mRNA decapping pathogen effector.

This article is a Commentary on McCombe et al. (2023), 239: 222–239.

A rust-fungus Nudix hydrolase effector decaps mRNA invitro and interferes with plant immune pathways.

To infect plants, pathogenic fungi secrete small proteins called effectors. Here, we describe the catalytic activity and potential virulence function of the Nudix hydrolase effector AvrM14 from the flax rust fungus (Melampsora lini). We completed extensive invitro assays to characterise the enzymatic activity of the AvrM14 effector. Additionally, we used in planta transient expression of wild-type and catalytically dead AvrM14 versions followed by biochemical assays, phenotypic analysis and RNA sequencing to unravel how the catalytic activity of AvrM14 impacts plant immunity. AvrM14 is an extremely selective enzyme capable of removing the protective 5' cap from mRNA transcripts invitro. Homodimerisation of AvrM14 promoted biologically relevant mRNA cap cleavage invitro and this activity was conserved in related effectors from other Melampsora spp. In planta expression of wild-type AvrM14, but not the catalytically dead version, suppressed immune-related reactive oxygen species production, altered the abundance of some circadian-rhythm-associated mRNA transcripts and reduced the hypersensitive cell-death response triggered by the flax disease resistance protein M1. To date, the decapping of host mRNA as a virulence strategy has not been described beyond viruses. Our results indicate that some fungal pathogens produce Nudix hydrolase effectors with invitro mRNA-decapping activity capable of interfering with plant immunity.

Activation and turnover of the plant immune signaling kinase BIK1: a fine balance.

Mechanisms to sense and respond to pathogens have evolved in all species. The plant immune pathway is initiated by the activation of transmembrane receptor kinases that trigger phosphorylation relays resulting in cellular reprogramming. BOTRYTIS-INDUCED KINASE 1 (BIK1) is a direct substrate of multiple immune receptors in Arabidopsis thaliana and is a central regulator of plant immunity. Here, we review how BIK1 activity and protein stability are regulated by a dynamic interplay between phosphorylation and ubiquitination.

An angiosperm NLR Atlas reveals that NLR gene reduction is associated with ecological specialization and signal transduction component deletion

Nucleotide-binding leucine-rich-repeat (NLR) genes comprise the largest family of plant disease-resistance genes. Angiosperm NLR genes are phylogenetically divided into the TNL, CNL, and RNL subclasses. NLR copy numbers and subclass composition vary tremendously across angiosperm genomes. However, the evolutionary associations between genomic NLR content and ecological adaptation, or between NLR content and signal transduction components, are poorly characterized because of limited genome availability. In this study, we established an angiosperm NLR atlas (ANNA, https://biobigdata.nju.edu.cn/ANNA/) that includes NLR genes from over 300 angiosperm genomes. Using ANNA, we revealed that NLR copy numbers differ up to 66-fold among closely related species owing to rapid gene loss and gain. Interestingly, NLR contraction was associated with adaptations to aquatic, parasitic, and carnivorous lifestyles. The convergent NLR reduction in aquatic plants resembles the lack of NLR expansion during the long-term evolution of green algae before the colonization of land. A co-evolutionary pattern between NLR subclasses and plant immune pathway components was also identified, suggesting that immune pathway deficiencies may drive TNL loss. Finally, we identified a conserved TNL lineage that may function independently of the EDS1–SAG101–NRG1 module. Collectively, these findings provide new insights into the evolution of NLR genes in the context of ecological adaptation and genome content variation.

Pathogen-secreted proteases activate a novel plant immune pathway.

Mitogen-Activated Protein Kinase (MAPK) cascades play central roles in innate immune signaling networks in plants and animals1,2. In plants, however, the molecular mechanisms of how signal perception is transduced to MAPK activation remain elusive1. We report that pathogen-secreted proteases activate a previously unknown signaling pathway in Arabidopsis thaliana involving the Gα, Gβ and Gγ subunits of heterotrimeric G-protein complexes, which function upstream of a MAPK cascade. In this pathway, Receptor for Activated C Kinase 1 (RACK1) functions as a novel scaffold that binds to the Gβ subunit as well as to all three tiers of the MAPK cascade, thereby linking upstream G protein signaling to downstream activation of a MAPK cascade. The protease-G protein-RACK1-MAPK cascade modules identified in these studies are distinct from previously described plant immune signaling pathways such as the one elicited by bacterial flagellin, in which G proteins function downstream of or in parallel to a MAPK cascade without the involvement of the RACK1 scaffolding protein. The discovery of the novel protease-mediated immune signaling pathway described here was facilitated by the use of the broad host range, opportunistic bacterial pathogen Pseudomonas aeruginosa. The ability of P. aeruginosa to infect both plants and animals makes it an excellent model to identify novel types of immunoregulatory strategies that account for its niche adaptation to diverse host tissues and immune systems.

Two Prp19-Like U-Box Proteins in the MOS4-Associated Complex Play Redundant Roles in Plant Innate Immunity

Plant Resistance (R) proteins play an integral role in defense against pathogen infection. A unique gain-of-function mutation in the R gene SNC1, snc1, results in constitutive activation of plant immune pathways and enhanced resistance against pathogen infection. We previously found that mutations in MOS4 suppress the autoimmune phenotypes of snc1, and that MOS4 is part of a nuclear complex called the MOS4-Associated Complex (MAC) along with the transcription factor AtCDC5 and the WD-40 protein PRL1. Here we report the immuno-affinity purification of the MAC using HA-tagged MOS4 followed by protein sequence analysis by mass spectrometry. A total of 24 MAC proteins were identified, 19 of which have predicted roles in RNA processing based on their homology to proteins in the Prp19-Complex, an evolutionarily conserved spliceosome-associated complex containing homologs of MOS4, AtCDC5, and PRL1. Among these were two highly similar U-box proteins with homology to the yeast and human E3 ubiquitin ligase Prp19, which we named MAC3A and MAC3B. MAC3B was recently shown to exhibit E3 ligase activity in vitro. Through reverse genetics analysis we show that MAC3A and MAC3B are functionally redundant and are required for basal and R protein–mediated resistance in Arabidopsis. Like mos4-1 and Atcdc5-1, mac3a mac3b suppresses snc1-mediated autoimmunity. MAC3 localizes to the nucleus and interacts with AtCDC5 in planta. Our results suggest that MAC3A and MAC3B are members of the MAC that function redundantly in the regulation of plant innate immunity.

New Plant Immune Pathway

The plant gene NIM1 encodes a protein with similarity to members of the IκB family of proteins, which are transcriptional regulators that function in mammalian immune system. Plants with mutations in NIM1 are unresponsive to salicylic acid signaling, which is required for the systemic acquired resistance (SAR) response to pathogens. To search for new regulators of plant immune responses, Kim and Delaney screened for genetic suppressor mutations in Arabidopsis that relieved susceptibility to pathogens in nim1-1 mutants. The suppressor of nim1-1 (son1) mutant they isolated revealed a previously uncharacterized defense pathway independent of the SAR response. Resistance was restored in son1 mutants without activation of the pathogenesis-related genes normally regulated during SAR. The Son-1 gene was found to encode a protein with an NH2-terminal F-box characteristic of proteins that target specific proteins to E3 ubiquitin ligase complexes for subsequent destruction. The SON1 protein thus appears to be a negative regulator of a plant defense response that may target other proteins for destruction in the ubiquitin-proteasome pathway.H. S. Kim, T. P Delaney, Arabidopsis SON1 Is an F-Box Protein That Regulates a Novel Induced Defense Response Independent of Both Salicylic Acid and Systemic Acquired Resistance. Plant Cell 14, 1469-1482 (2002).[Abstract][Full Text]

New Plant Immune Pathway

The plant gene NIM1 encodes a protein with similarity to members of the IκB family of proteins, which are transcriptional regulators that function in mammalian immune system. Plants with mutations in NIM1 are unresponsive to salicylic acid signaling, which is required for the systemic acquired resistance (SAR) response to pathogens. To search for new regulators of plant immune responses, Kim and Delaney screened for genetic suppressor mutations in Arabidopsis that relieved susceptibility to pathogens in nim1-1 mutants. The suppressor of nim1-1 ( son1 ) mutant they isolated revealed a previously uncharacterized defense pathway independent of the SAR response. Resistance was restored in son1 mutants without activation of the pathogenesis-related genes normally regulated during SAR. The Son-1 gene was found to encode a protein with an NH 2 -terminal F-box characteristic of proteins that target specific proteins to E3 ubiquitin ligase complexes for subsequent destruction. The SON1 protein thus appears to be a negative regulator of a plant defense response that may target other proteins for destruction in the ubiquitin-proteasome pathway. H. S. Kim, T. P Delaney, Arabidopsis SON1 Is an F-Box Protein That Regulates a Novel Induced Defense Response Independent of Both Salicylic Acid and Systemic Acquired Resistance. Plant Cell 14 , 1469-1482 (2002). [Abstract] [Full Text]