Plants coexist with a diverse array of microorganisms, predominantly bacteria and fungi, in both natural and agricultural environments. While some microorganisms positively influence plant development and yield, others can cause harm to the host, leading to significant adverse impacts on the environment and the economy. Plant growth-promoting microorganisms (PGPM), including plant growth-promoting bacteria, arbuscular mycorrhizal fungus (AMF), and rhizobia, have been found to increase plant biomass production by synthesizing hormones, fixing nitrogen, and solubilizing phosphate and potassium. Numerous studies have contributed to unraveling the complex process of plant-microbe interactions in recent decades. In light of the increasing global challenges such as population growth, climate change, and resource scarcity, it has become imperative to explore the potential of plant-bacteria-fungi crosstalk in promoting sustainability. This review aims to bridge existing knowledge gaps, providing a roadmap for future research in this dynamic field by synthesizing current knowledge and identifying emerging trends.

Embedded in the plasma membrane of plant cells, receptor kinases (RKs) and receptor proteins (RPs) act as key sentinels, responsible for detecting potential pathogenic invaders. These proteins were originally characterized more than three decades ago as disease resistance (R) proteins, a concept that was formulated based on Harold Flor\'s gene-for-gene theory. This theory implies genetic interaction between specific plant R proteins and corresponding pathogenic effectors, eliciting effector-triggered immunity (ETI). Over the years, extensive research has unraveled their intricate roles in pathogen sensing and immune response modulation. RKs and RPs recognize molecular patterns from microbes as well as dangers from plant cells in initiating pattern-triggered immunity (PTI) and danger-triggered immunity (DTI), which have intricate connections with ETI. Moreover, these proteins are involved in maintaining immune homeostasis and preventing autoimmunity. This review showcases seminal studies in discovering RKs and RPs as R proteins and discusses the recent advances in understanding their functions in sensing pathogen signals and the plant cell integrity and in preventing autoimmunity, ultimately contributing to a robust and balanced plant defense response. [Formula: see text] The author(s) have dedicated the work to the public domain under the Creative Commons CC0 \"No Rights Reserved\" license by waiving all of his or her rights to the work worldwide under copyright law, including all related and neighboring rights, to the extent allowed by law, 2024.

Along with the emergence of green plants on this planet one billion years ago, the nucleotide binding site leucine-rich repeat (NLR) gene family originated and diverged into at least three subclasses. Two of them, with either characterized N-terminal toll/interleukin-1 receptor (TIR) or coiled-coil (CC) domain, serve as major types of immune receptor of effector-triggered immunity (ETI) in plants, whereas the one having a N-terminal Resistance to powdery mildew8 (RPW8) domain, functions as signal transfer component to them. In this review, we briefly summarized the history of identification of diverse NLR subclasses across Viridiplantae lineages during the establishment of NLR category, and highlighted recent advances on the evolution of NLR genes and several key downstream signal components under the background of ecological adaption.

The chemical diversity of sphingolipids in plants allows the assignment of specific roles to special molecular species. These roles include NaCl receptors for glycosylinositolphosphoceramides or second messengers for long-chain bases (LCBs), free or in their acylated forms. Such signaling function has been associated with plant immunity, with an apparent connection to mitogen-activated protein kinase 6 (MPK6) and reactive oxygen species (ROS). This work used in planta assays with mutants and fumonisin B1 (FB1) to generate varying levels of endogenous sphingolipids. This was complemented with in planta pathogenicity tests using virulent and avirulent Pseudomonas syringae strains. Our results indicate that the surge of specific free LCBs and ceramides induced by FB1 or an avirulent strain trigger a biphasic ROS production. The first transient phase is partially produced by NADPH oxidase, and the second is sustained and is related to programmed cell death. MPK6 acts downstream of LCB buildup and upstream of late ROS and is required to selectively inhibit the growth of the avirulent but not the virulent strain. Altogether, these results provide evidence that a LCB- MPK6- ROS signaling pathway contributes differentially to the two forms of immunity described in plants, upregulating the defense scheme of a non-compatible interaction.

Accumulating evidence suggests that chloroplasts are an important battleground during various microbe-host interactions. Plants have evolved layered strategies to reprogram chloroplasts to promote de novo biosynthesis of defense-related phytohormones and the accumulation of reactive oxygen species (ROS). In this minireview, we will discuss how the host controls chloroplast ROS accumulation during effector-triggered immunity (ETI) at the level of selective mRNA decay, translational regulation, and autophagy-dependent formation of Rubisco-containing bodies (RCBs). We hypothesize that regulation at the level of cytoplasmic mRNA decay impairs the repair cycle of photosystem II (PSII) and thus facilitates ROS generation at PSII. Meanwhile, removing Rubisco from chloroplasts potentially reduces both O2 and NADPH consumption. As a consequence, an over-reduced stroma would further exacerbate PSII excitation pressure and enhance ROS production at photosystem I.

As a destructive plant pathogen, Phytophthora infestans secretes diverse host-entering RxLR effectors to facilitate infection. One critical RxLR effector, PiAvr3b, not only induces effector-triggered immunity (ETI), which is associated with the potato resistance protein StR3b, but also suppresses pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI). To date, the molecular basis underlying such dual activities remains unknown. Based on phylogenetic analysis of global P. infestans isolates, we found two PiAvr3b isoforms that differ by three amino acids. Despite this sequence variation, the two isoforms retain the same properties in activating the StR3b-mediated hypersensitive response (HR) and inhibiting necrosis induced by three PAMPs (PiNpp, PiINF1, and PsXeg1) and an RxLR effector (Pi10232). Using a combined mutagenesis approach, we found that the dual activities of PiAvr3b were tightly linked and determined by 88 amino acids at the C-terminus. We further determined that either the W60 or the E134 residue of PiAvr3b was essential for triggering StR3b-associated HR and inhibiting PiNpp- and Pi10232-associated necrosis, while the S99 residue partially contributed to PTI suppression. Additionally, nuclear localization of PiAvr3b was required to stimulate HR and suppress PTI, but not to inhibit Pi10232-associated cell death. Our study revealed that PiAvr3b suppresses the plant immune response at different subcellular locations and provides an example in which a single amino acid of an RxLR effector links ETI induction and cell death suppression.

The transcriptomic and metabolomic responses of peach to Myzus persicae infestation were studied in Rubira, an accession carrying the major resistance gene Rm2 causing antixenosis, and GF305, a susceptible accession. Transcriptome and metabolome showed both a massive reconfiguration in Rubira 48 hours after infestation while GF305 displayed very limited changes. The Rubira immune system was massively stimulated, with simultaneous activation of genes encoding cell surface receptors involved in pattern-triggered immunity and cytoplasmic NLRs (nucleotide-binding domain, leucine-rich repeat containing proteins) involved in effector-triggered immunity. Hypersensitive reaction featured by necrotic lesions surrounding stylet punctures was supported by the induction of cell death stimulating NLRs/helpers couples, as well as the activation of H2O2-generating metabolic pathways: photorespiratory glyoxylate synthesis and activation of the futile P5C/proline cycle. The triggering of systemic acquired resistance was suggested by the activation of pipecolate pathway and accumulation of this defense hormone together with salicylate. Important reduction in carbon, nitrogen and sulphur metabolic pools and the repression of many genes related to cell division and growth, consistent with reduced apices elongation, suggested a decline in the nutritional value of apices. Finally, the accumulation of caffeic acid conjugates pointed toward their contribution as deterrent and/or toxic compounds in the mechanisms of resistance.

Abiotic and biotic environments influence a myriad of plant-related processes, including growth, development, and the establishment and maintenance of interaction(s) with microbes. In the case of the latter, elevated temperature has been shown to be a key factor that underpins host resistance and pathogen virulence. In this study, we elucidate a role for Arabidopsis NON-RACE-SPECIFIC DISEASE RESISTANCE1 (NDR1) by exploiting effector-triggered immunity to define the regulation of plant host immunity in response to both pathogen infection and elevated temperature. We generated time-series RNA sequencing data of WT Col-0, an NDR1 overexpression line, and ndr1 and ics1-2 mutant plants under elevated temperature. Not surprisingly, the NDR1-overexpression line showed genotype-specific gene expression changes related to defense response and immune system function. The results described herein support a role for NDR1 in maintaining cell signaling during simultaneous exposure to elevated temperature and avirulent pathogen stressors.

Plants have both cell-surface and intracellular receptors to recognize diverse self- and non-self molecules. Cell-surface pattern recognition receptors (PRRs) recognize extracellular pathogen-/damage-derived molecules or apoplastic pathogen-derived effectors. Intracellular nucleotide-binding leucine-rich repeat proteins (NLRs) recognize pathogen effectors. Activation of both PRRs and NLRs elevates defense gene expression and accumulation of the phytohormone salicylic acid (SA), which results in SA-dependent transcriptional reprogramming. These receptors, together with their coreceptors, form networks to mediate downstream immune responses. In addition, cell-surface and intracellular immune systems are interdependent and function synergistically to provide robust resistance against pathogens. Here, we summarize the interactions between these immune systems and attempt to provide a holistic picture of plant immune networks. We highlight current challenges and discuss potential new research directions.

In the plant immune system, according to the \'gene-for-gene\' model, a resistance (R) gene product in the plant specifically surveils a corresponding effector protein functioning as an avirulence (Avr) gene product. This system differs from other plant-pathogen interaction systems, in which plant R genes recognize a single type of gene or gene family because almost all virus genes with distinct structures and functions can also interact with R genes as Avr determinants. Thus, research conducted on viral Avr-R systems can provide a novel understanding of Avr and R gene product interactions and identify mechanisms that enable rapid co-evolution of plants and phytopathogens. In this review, we intend to provide a brief overview of virus-encoded proteins and their roles in triggering plant resistance, and we also summarize current progress in understanding plant resistance against virus Avr genes. Moreover, we present applications of Avr gene-mediated phenotyping in R gene identification and screening of segregating populations during breeding processes.