Plant genomes encode large numbers of nucleotide-binding, leucine-rich repeat (NB-LRR) proteins, many of which are active in pathogen detection and defense response induction. NB-LRR proteins fall into two broad classes: those with a Toll and interleukin-1 receptor (TIR) domain at their N-terminus and those with a coiled-coil (CC) domain at the N-terminus. Within CC-NB-LRR-encoding genes, one basal clade is distinguished by having CC domains resembling the Arabidopsis thaliana RPW8 protein, which we refer to as CCR domains. Here, we show that CCR-NB-LRR-encoding genes are present in the genomes of all higher plants surveyed, and that they comprise two distinct subgroups: one typified by the Nicotiana benthamiana N-required gene 1 (NRG1) protein and the other typified by the Arabidopsis activated disease resistance gene 1 (ADR1) protein. We further report that, in contrast to CC-NB-LRR proteins, the CCR domains of both NRG1- and ADR1-like proteins are sufficient for the induction of defense responses, and that this activity appears to be SGT1-independent. Additionally, we report the apparent absence of both NRG1 homologs and TIR-NB-LRR-encoding genes from the dicot Aquilegia coerulea and the dicotyledonous order Lamiales as well as from monocotyledonous species. This strong correlation in occurrence is suggestive of a functional relationship between these two classes of NB-LRR proteins.
Mitogen-activated protein kinases (MAPKs) are evolutionarily conserved proteins that function as key signal transduction components in fungi, plants, and mammals. During interaction between phytopathogenic fungi and plants, fungal MAPKs help to promote mechanical and/or enzymatic penetration of host tissues, while plant MAPKs are required for activation of plant immunity. However, new insights suggest that MAPK cascades in both organisms do not operate independently but that they mutually contribute to a highly interconnected molecular dialogue between the plant and the fungus. As a result, some pathogenesis-related processes controlled by fungal MAPKs lead to the activation of plant signaling, including the recruitment of plant MAPK cascades. Conversely, plant MAPKs promote defense mechanisms that threaten the survival of fungal cells, leading to a stress response mediated in part by fungal MAPK cascades. In this review, we make use of the genomic data available following completion of whole-genome sequencing projects to analyze the structure of MAPK protein families in 24 fungal taxa, including both plant pathogens and mycorrhizal symbionts. Based on conserved patterns of sequence diversification, we also propose the adoption of a unified fungal MAPK nomenclature derived from that established for the model species Saccharomyces cerevisiae. Finally, we summarize current knowledge of the functions of MAPK cascades in phytopathogenic fungi and highlight the central role played by MAPK signaling during the molecular dialogue between plants and invading fungal pathogens.
Calcium-dependent protein kinases (CDPKs) are multifunctional proteins combining calcium-binding and signaling capabilities within a single gene product. This unique versatility enables multiple plant biological processes to be controlled, including developmental programs and stress responses. The genome of flowering plants typically encodes around 30 CDPK homologs that cluster in four conserved clades. In this Review, we take advantage of the recent availability of genome sequences from green algae and early land plants to examine how well the previously described CDPK family from angiosperms compares to the broader evolutionary states associated with early diverging green plant lineages. Our analysis suggests that the current architecture of the CDPK family was shaped during the colonization of the land by plants, whereas CDPKs from ancestor green algae have continued to evolve independently.
In plants, short chitin oligosaccharides and chitosan fragments (collectively referred to as chitooligosaccharides) are well-known elicitors that trigger defense gene expression, synthesis of antimicrobial compounds, and cell wall strengthening. Recent findings have shed new light on chitin-sensing mechanisms and downstream activation of intracellular signaling networks that mediate plant defense responses. Interestingly, chitin receptors possess several lysin motif domains that are also found in several legume Nod factor receptors. Nod factors are chitin-related molecules produced by nitrogen-fixing rhizobia to induce root nodulation. The fact that chitin and Nod factor receptors share structural similarity suggests an evolutionary conserved relationship between mechanisms enabling recognition of both deleterious and beneficial microorganisms. Here, we will present an update on molecular events involved in chitooligosaccharide sensing and downstream signaling pathways in plants and will discuss how structurally related signals may lead to such contrasted outcomes during plant-microbe interactions.
Background: As in other eukaryotes, plant mitogen-activated protein kinase (MAPK) cascades are composed of three classes of hierarchically organized protein kinases, namely MAPKKKs, MAPKKs, and MAPKs. These modules rapidly amplify and transduce extracellular signals into various appropriate intracellular responses. While extensive work has been conducted on the post-translational regulation of specific MAPKKs and MAPKs in various plant species, there has been no systematic investigation of the genomic organization and transcriptional regulation of these genes.
One branch of plant immunity is mediated through nucleotide-binding/Leu-rich repeat (NB-LRR) family proteins that recognize specific effectors encoded by pathogens. Members of the I2-like family constitute a well-conserved subgroup of NB-LRRs from Solanaceae possessing a coiled-coil (CC) domain at their N termini. We show here that the CC domains of several I2-like proteins are able to induce a hypersensitive response (HR), a form of programmed cell death associated with disease resistance. Using yeast two-hybrid screens, we identified the chloroplastic protein Thylakoid Formation1 (THF1) as an interacting partner for several I2-like CC domains. Co-immunoprecipitations and bimolecular fluorescence complementation assays confirmed that THF1 and I2-like CC domains interact in planta and that these interactions take place in the cytosol. Several HR-inducing I2-like CC domains have a negative effect on the accumulation of THF1, suggesting that the latter is destabilized by active CC domains. To confirm this model, we investigated N9, which recognizes the coat protein of most Tobamoviruses, as a prototypical member of the I2-like family. Transient expression and gene silencing data indicated that THF1 functions as a negative regulator of cell death and that activation of full-length N9 results in the destabilization of THF1. Consistent with the known function of THF1 in maintaining chloroplast homeostasis, we show that the HR induced by N9 is light-dependent. Together, our results define, to our knowledge, novel molecular mechanisms linking light and chloroplasts to the induction of cell death by a subgroup of NB-LRR proteins.
Plant mitogen-activated protein kinase (MAPK) cascades are important amplifying modules that can rapidly transduce stress signals into various appropriate intracellular responses. Several extracellular regulated kinase (ERK)-type MAPKs involved in plant defense signaling have been identified in herbaceous species, but no MAPK cascade has yet been characterized in a tree species. We examined the signal transduction events that lead to activation of defense mechanisms in poplar, a major forest species of economic and ecological importance which is becoming the model tree system for studying stress and adaptation responses. We show that, in poplar cell suspensions and leaf tissue, chitosan, a non-host-specific elicitor, and ozone, a strong oxidant and atmospheric pollutant, induce rapid and transient activation of at least two myelin basic protein (MBP) kinases with apparent molecular masses of 44 and 47 kD. The chitosan- and ozone-activated kinases have characteristics of MAPKs-they preferentially phosphorylate MBP, require tyrosine and threonine phosphorylation to be activated and are specifically recognized by anti-ERK and anti-pERK antibodies. Moreover, activation of these poplar MAPKs by chitosan or ozone is dependent on the production of reactive oxygen species; the influx of calcium ions via membrane channels; the activation of an upstream, membrane-localized component; and a cognate MAPK kinase (MAPKK). These data suggest that biotic and abiotic challenges activate MAPKs in poplar, as in herbaceous species, which then function as a convergence point for pathogen defense and oxidant stress signaling cascades.
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