Plants constantly monitor and cope with the fluctuating environment while hosting a diversity of plant-inhabiting microbes. The mode and outcome of plant–microbe interactions, including plant disease ...epidemics, are dynamically and profoundly influenced by abiotic factors, such as light, temperature, water and nutrients. Plants also utilize associations with beneficial microbes during adaptation to adverse conditions. Elucidation of the molecular bases for the plant–microbe–environment interactions is therefore of fundamental importance in the plant sciences. Following advances into individual stress signaling pathways, recent studies are beginning to reveal molecular intersections between biotic and abiotic stress responses and regulatory principles in combined stress responses. We outline mechanisms underlying environmental modulation of plant immunity and emerging roles for immune regulators in abiotic stress tolerance. Furthermore, we discuss how plants coordinate conflicting demands when exposed to combinations of different stresses, with attention to a possible determinant that links initial stress response to broad-spectrum stress tolerance or prioritization of specific stress tolerance.
Summary
Plants solely rely on innate immunity of each individual cell to deal with a diversity of microbes in the environment. Extracellular recognition of microbe‐ and host damage‐associated ...molecular patterns leads to the first layer of inducible defenses, termed pattern‐triggered immunity (PTI). In plants, pattern recognition receptors (PRRs) described to date are all membrane‐associated receptor‐like kinases or receptor‐like proteins, reflecting the prevalence of apoplastic colonization of plant‐infecting microbes. An increasing inventory of elicitor‐active patterns and PRRs indicates that a large number of them are limited to a certain range of plant groups/species, pointing to dynamic and convergent evolution of pattern recognition specificities. In addition to common molecular principles of PRR signaling, recent studies have revealed substantial diversification between PRRs in their functions and regulatory mechanisms. This serves to confer robustness and plasticity to the whole PTI system in natural infections, wherein different PRRs are simultaneously engaged and faced with microbial assaults. We review the functional significance and molecular basis of PRR‐mediated pathogen recognition and disease resistance, and also an emerging role for PRRs in homeostatic association with beneficial or commensal microbes.
Significance Statement
In plants, pattern recognition receptors detect microbe‐associated and host damage‐associated molecular patterns in the extracellular spaces, and thereby trigger intracellular signaling that culminates in an enhanced state of immunity. An increasing inventory of elicitor‐active patterns and their receptors helps us to learn the molecular principles with which plants recognize and deal with a rich diversity of infectious microorganisms, ranging from pathogens, symbionts and commensals, in fluctuating environments.
Summary
Like in animals, cell surface and intracellular receptors mediate immune recognition of potential microbial intruders in plants. Membrane‐localized pattern recognition receptors (PRRs) ...initiate immune responses upon perception of cognate microbe‐associated molecular patterns (MAMPs). MAMP‐triggered immunity provides a first line of defence that restricts the invasion and propagation of both adapted and non‐adapted pathogens. The Leu‐rich repeat (LRR) receptor protein kinases (RKs) define a major class of trans‐membrane receptors in plants, of which some members are engaged in MAMP recognition and/or defence signalling. The endoplasmic reticulum (ER) quality control (QC) systems monitor N‐glycosylation and folding states of the extracellular, ligand‐binding LRR domains of LRR‐RKs. Recent progress reveals a critical role of evolutionarily conserved ERQC components for different layers of plant immunity. N‐glycosylation appears to play a role in ERQC fidelity rather than in ligand binding of LRR‐RKs. Moreover, even closely related PRRs show receptor‐specific requirements for N‐glycosylation. These findings are reminiscent of the earlier defined function of the cytosolic chaperon complex for LRR domain‐containing intracellular immune receptors. QC of the LRR domains might provide a basis not only for the maintenance but also for diversification of recognition specificities for immune receptors in plants.
•BAK1 acts as a shared coreceptor for LRR-RLKs/RLPs in pattern recognition.•Use of bak1-5 hypoactive allele facilitates to reveal PRR-related BAK1 function.•PRR- and NLR-related mechanisms activate ...immunity following BAK1/SERK4 depletion.•BAK1 depletion is not favored by host plants and pathogens as a means to attenuate PTI.•PRR complexes may access and phosphorylate PTI regulators on scaffold proteins.
Recognition of microbe- and danger-associated molecular patterns (MAMPs and DAMPs, respectively) by pattern recognition receptors (PRRs) is central to innate immunity in both plants and animals. The plant PRRs described to date are all cell surface-localized receptors. According to their ligand-binding ectodomains, each PRR engages a specific coreceptor or adaptor kinase in its signaling complexes to regulate defense signaling. With a focus on the coreceptor RLK BRI1-ASSOCIATED RECEPTOR KINASE1 (BAK1) and related SOMATIC EMBRYOGENESIS RECEPTOR KINASEs (SERKs), here we review the increasing inventory of BAK1 partners and their functions in plant immunity. We also discuss the significance of autoimmunity triggered by BAK1/SERK4 disintegration in shaping the strategies for attenuation of PRR signaling by infectious microbes and host plants.
Immune recognition of pathogen-associated molecular patterns or effectors leads to defense activation at the pathogen challenged sites. This is followed by systemic defense activation at distant ...non-challenged sites, termed systemic acquired resistance (SAR). These inducible defenses are accompanied by extensive transcriptional reprogramming of defense-related genes. SAR is associated with priming, in which a subset of these genes is kept at a poised state to facilitate subsequent transcriptional regulation. Transgenerational inheritance of defense-related priming in plants indicates the stability of such primed states. Recent studies have revealed the importance and dynamic engagement of epigenetic mechanisms, such as DNA methylation and histone modifications that are closely linked to chromatin reconfiguration, in plant adaptation to different biotic stresses. Herein we review current knowledge regarding the biological significance and underlying mechanisms of epigenetic control for immune responses in plants. We also argue for the importance of host transposable elements as critical regulators of interactions in the evolutionary "arms race" between plants and pathogens.
P-type conversion of n−-GaN by Mg-ion implantation was successfully performed using high quality GaN epitaxial layers grown on free-standing low-dislocation-density GaN substrates. These samples ...showed low-temperature PL spectra quite similar to those observed from Mg-doped MOVPE-grown p-type GaN, consisting of Mg related donor–acceptor pair (DAP) and acceptor bound exciton (ABE) emission. P–n diodes fabricated by the Mg-ion implantation showed clear rectifying I–V characteristics and UV and blue light emissions were observed at forward biased conditions for the first time.
Phosphorus (P) is an essential macronutrient for plant life and growth. P is primarily acquired in the form of inorganic phosphate (Pi) from soil. To cope with Pi deficiency, plants have evolved an ...elaborate system to improve Pi acquisition and utilization through an array of developmental and physiological changes, termed Pi starvation response (PSR). Plants also assemble and manage mutualistic microbes to enhance Pi uptake, through integrating PSR and immunity signaling. A trade-off between plant growth and defense favors the notion that plants lower a cellular state of immunity to accommodate host-beneficial microbes for nutrition and growth at the cost of infection risk. However, the existing data indicate that plants selectively activate defense responses against pathogens, but do not or less against non-pathogens, even under nutrient deficiency. In this review, we highlight recent advances in the principles and mechanisms with which plants balance immunity and growth-related processes to optimize their adaptation to Pi deficiency.
Summary
In Arabidopsis thaliana, PROPEPs and their derived elicitor‐active Pep epitopes provide damage‐associated molecular patterns (DAMPs), which trigger defence responses through cell‐surface ...receptors PEPR1 and PEPR2. In addition, Pep peptides induce root growth inhibition and root hair formation, however their relationships and coordinating mechanisms are poorly understood.
Here, we reveal that Pep1‐mediated root hair formation requires PEPR‐associated kinases BAK1/BKK1 and BIK1/PBL1, ethylene, auxin and root hair differentiation regulators, in addition to PEPR2.
Our analysis on 69 accessions unravels intraspecies variations in Pep1‐induced root hair formation and growth inhibition. The absence of a positive correlation between the two traits suggests their separate regulation and diversification in natural populations of A. thaliana.
Restricted PEPR2 expression to certain root tissues is sufficient to induce root hair formation and growth inhibition in response to Pep1, indicating the capacity of non‐cell‐autonomous receptor signalling in different root tissues. Of particular note, root hair cell‐specific PEPR2 expression uncouples defence activation from root growth inhibition and root hair formation, suggesting a unique property of root hairs in root defence activation following Pep1 recognition.
Recognition of molecular patterns characteristic of microbes or altered-self leads to immune activation in multicellular eukaryotes. In Arabidopsis thaliana , the leucine-rich-repeat receptor kinases ...FLAGELLIN-SENSING2 (FLS2) and EF-TU RECEPTOR (EFR) recognize bacterial flagellin and elongation factor EF-Tu (and their elicitor-active epitopes flg22 and elf18), respectively. Likewise, PEP1 RECEPTOR1 (PEPR1) and PEPR2 recognize the elicitor-active Pep epitopes conserved in Arabidopsis ELICITOR PEPTIDE PRECURSOR s (PROPEP s). Here we reveal that loss of ETHYLENE-INSENSITIVE2 (EIN2), a master signaling regulator of the phytohormone ethylene (ET), lowers sensitivity to both elf18 and flg22 in different defense-related outputs. Remarkably, in contrast to a large decrease in FLS2 expression, EFR expression and receptor accumulation remain unaffected in ein2 plants. Genome-wide transcriptome profiling has uncovered an inventory of EIN2-dependent and EFR-regulated genes. This dataset highlights important aspects of how ET modulates EFR-triggered immunity: the potentiation of salicylate-based immunity and the repression of a jasmonate-related branch. EFR requires ET signaling components for PROPEP2 activation but not for PROPEP3 activation, pointing to both ET-dependent and -independent engagement of the PEPR pathway during EFR-triggered immunity. Moreover, PEPR activation compensates the ein2 defects for a subset of EFR-regulated genes. Accordingly, ein2 pepr1 pepr2 plants exhibit additive defects in EFR-triggered antibacterial immunity, compared with ein2 or pepr1 pepr2 plants. Our findings suggest that the PEPR pathway not only mediates ET signaling but also compensates for its absence in enhancing plant immunity.
Recognition of microbial challenges leads to enhanced immunity at both the local and systemic levels. In Arabidopsis, EFR and PEPR1/PEPR2 act as the receptor for the bacterial elongation factor EF‐Tu ...(elf18 epitope) and for the endogenous PROPEP‐derived Pep epitopes, respectively. The PEPR pathway has been described to mediate defence signalling following microbial recognition. Here we show that PROPEP2/PROPEP3 induction upon pathogen challenges is robust against jasmonate, salicylate, or ethylene dysfunction. Comparative transcriptome profiling between Pep2‐ and elf18‐treated plants points to co‐activation of otherwise antagonistic jasmonate‐ and salicylate‐mediated immune branches as a key output of PEPR signalling. Accordingly, as well as basal defences against hemibiotrophic pathogens, systemic immunity is reduced in pepr1 pepr2 plants. Remarkably, PROPEP2/PROPEP3 induction is essentially restricted to the pathogen challenge sites during pathogen‐induced systemic immunity. Localized Pep application activates genetically separable jasmonate and salicylate branches in systemic leaves without significant PROPEP2/PROPEP3 induction. Our results suggest that local PEPR activation provides a critical step in connecting local to systemic immunity by reinforcing separate defence signalling pathways.
Synopsis
Local microbial recognition involving PEPR pattern recognition receptors leads to a systemic immune response via the Salicylate and Jasmonate hormone signaling pathways.
Genome‐wide profiling for Pep2‐responsive genes in Arabidopsis thaliana shows co‐activation of salicylate (SA)‐ and jasmonate (JA) pathways as an important output of PEPR‐mediated signalling.
Molecular genetic studies indicate a critical role for PEPRs in pathogen‐ and microbial pattern‐induced systemic immunity.
Activation of a PEPR‐PROPEP feedback loop is restricted to the pathogen‐challenged sites during pathogen‐induced systemic immunity.
Exogenous application of Pep peptides confers systemic immunity through distinct defence signalling branches.
Local microbial recognition involving PEPR pattern recognition receptors leads to a systemic immune response via the Salicylate and Jasmonate hormone signaling pathways.
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