Abstract Understanding the plant immune system is crucial for using genetics to protect crops from diseases. Plants resist pathogens via a two-tiered innate immune detection-and-response system. The first plant Resistance (R) gene was cloned in 1992 . Since then, many cell-surface pattern recognition receptors (PRRs) have been identified, and R genes that encode intracellular nucleotide-binding leucine-rich repeat receptors (NLRs) have been cloned. Here, we provide a list of characterized PRRs and NLRs. In addition to immune receptors, many components of immune signaling networks were discovered over the last 30 years. We review the signaling pathways, physiological responses, and molecular regulation of both PRR- and NLR-mediated immunity. Recent studies have reinforced the importance of interactions between the two immune systems. We provide an overview of interactions between PRR- and NLR-mediated immunity, highlighting challenges and perspectives for future research.

/pdf/thirty-years-of-resistance-zig-zag-through-the-plant-immune-2s6pdgpg.pdf

Thirty years of resistance: Zig-zag through the plant immune system

Salicylic acid (SA) is an essential plant defense hormone that promotes immunity against biotrophic and semibiotrophic pathogens. It plays crucial roles in basal defense and the amplification of local immune responses, as well as the establishment of systemic acquired resistance. During the past three decades, immense progress has been made in understanding the biosynthesis, homeostasis, perception, and functions of SA. This review summarizes the current knowledge regarding SA in plant immunity and other biological processes. We highlight recent breakthroughs that substantially advanced our understanding of how SA is biosynthesized from isochorismate, how it is perceived, and how SA receptors regulate different aspects of plant immunity. Some key questions in SA biosynthesis and signaling, such as how SA is produced via another intermediate, benzoic acid, and how SA affects the activities of its receptors in the transcriptional regulation of defense genes, remain to be addressed.

Salicylic Acid: Biosynthesis and Signaling

Abstract Understanding the plant immune system is crucial for using genetics to protect crops from diseases. Plants resist pathogens via a two-tiered innate immune detection-and-response system. The first plant Resistance (R) gene was cloned in 1992 . Since then, many cell-surface pattern recognition receptors (PRRs) have been identified, and R genes that encode intracellular nucleotide-binding leucine-rich repeat receptors (NLRs) have been cloned. Here, we provide a list of characterized PRRs and NLRs. In addition to immune receptors, many components of immune signaling networks were discovered over the last 30 years. We review the signaling pathways, physiological responses, and molecular regulation of both PRR- and NLR-mediated immunity. Recent studies have reinforced the importance of interactions between the two immune systems. We provide an overview of interactions between PRR- and NLR-mediated immunity, highlighting challenges and perspectives for future research. 

/pdf/oup-accepted-manuscript-1lfjzrt2.pdf

OUP accepted manuscript

The nucleotide-binding domain and leucine-rich repeats containing proteins (NLRs) serve as immune receptors in both plants and animals. Overaccumulation of NLRs often leads to autoimmune responses, suggesting that the levels of these immune receptors must be tightly controlled. However, the mechanism by which NLR protein levels are regulated is unknown. Here we report that the F-box protein CPR1 controls the stability of plant NLR resistance proteins. Loss-of-function mutations in CPR1 lead to higher accumulation of the NLR proteins SNC1 and RPS2, as well as autoactivation of immune responses. The autoimmune responses in cpr1 mutant plants can be largely suppressed by knocking out SNC1. Furthermore, CPR1 interacts with SNC1 and RPS2 in vivo, and overexpressing CPR1 results in reduced accumulation of SNC1 and RPS2, as well as suppression of immunity mediated by these two NLR proteins. Our data suggest that SKP1-CULLIN1-F-box (SCF) complex-mediated stability control of plant NLR proteins plays an important role in regulating their protein levels and preventing autoimmunity.

Stability of plant immune-receptor resistance proteins is controlled by SKP1-CULLIN1-F-box (SCF)-mediated protein degradation

Calcium ions function as a key second messenger ion in eukaryotes. Spatially and temporally defined cytoplasmic Ca2+ signals are shaped through the concerted activity of ion channels, exchangers, and pumps in response to diverse stimuli; these signals are then decoded through the activity of Ca2+‐binding sensor proteins. In plants, Ca2+ signaling is central to both pattern‐ and effector‐triggered immunity, with the generation of characteristic cytoplasmic Ca2+ elevations in response to potential pathogens being common to both. However, despite their importance, and a long history of scientific interest, the transport proteins that shape Ca2+ signals and their integration remain poorly characterized. Here, we discuss recent work that has both shed light on and deepened the mysteries of Ca2+ signaling in plant immunity.

/pdf/ca2-signals-in-plant-immunity-17gr08ac.pdf

Ca2+ signals in plant immunity

The study of plant diseases is almost as old as agriculture itself. Advancements in molecular biology have given us much more insight into the plant immune system and how it detects the many pathogens plants may encounter. Members of the primary family of plant resistance (R) proteins, NLRs, contain three distinct domains, and appear to use several different mechanisms to recognize pathogen effectors and trigger immunity. Understanding the molecular process of NLR recognition and activation has been greatly aided by advancements in structural studies, with ZAR1 recently becoming the first full-length NLR to be visualized. Genetic and biochemical analysis identified many critical components for NLR activation and homeostasis control. The increased study of helper NLRs has also provided insights into the downstream signaling pathways of NLRs. This review summarizes the progress in the last decades on plant NLR research, focusing on the mechanistic understanding that has been achieved.

Plant NLRs: The Whistleblowers of Plant Immunity.

Ascomycete Sclerotinia sclerotiorum (Lib.) de Bary is one of the most damaging soilborne fungal pathogens affecting hundreds of plant hosts, including many economically important crops. Its genomic sequence has been available for less than a decade, and it was recently updated with higher completion and better gene annotation. Here, we review key molecular findings on the unique biology and pathogenesis process of S. sclerotiorum, focusing on genes that have been studied in depth using mutant analysis. Analyses of these genes have revealed critical players in the basic biological processes of this unique pathogen, including mycelial growth, appressorium establishment, sclerotial formation, apothecial and ascospore development, and virulence. Additionally, the synthesis has uncovered gaps in the current knowledge regarding this fungus. We hope that this review will serve to build a better current understanding of the biology of this under-studied notorious soilborne pathogenic fungus.

https://www.mdpi.com/2076-0817/9/1/27/pdf

The Notorious Soilborne Pathogenic Fungus Sclerotinia sclerotiorum: An Update on Genes Studied with Mutant Analysis

The homeostasis of resistance (R) proteins in plants must be tightly regulated to ensure precise activation of plant immune response upon pathogen infection, while avoiding autoimmunity and growth defects when plants are uninfected. The ubiquitin-proteasome system (UPS) is a universal mechanism of protein homeostasis control in eukaryotes, and it was shown to be one of the mechanisms that regulate R protein levels. In particular, E3 ubiquitin ligase directly interacts with substrate proteins and largely determines the substrate specificity targeted for ubiquitination and proteasomal degradation. It was known that CPR1, an F-box protein in the SCF E3 complex, functions as a negative regulator of plant immunity through targeting R proteins SNC1 and RPS2 for degradation. However, whether or not those R proteins are targeted by other E3 ligases is unclear. In this paper, MUSE16, which encodes a RING-type E3 ligase, was isolated from a forward genetic screen and suggested to be a negative regulator of plant immunity. Unlike CPR1, knocking out MUSE16 in Arabidopsis thaliana alone is not enough to result in defense related dwarfism, since only RPS2 out of the tested R proteins accumulated in muse16. Thus, our study identified another E3 ligase involved in NLR R protein degradation, supporting that Ub-mediated degradation is a fine-tuned mechanism for regulating the turnover of R proteins in plants, and the same R protein can be targeted by different E3 ligases for its homeostasis regulation.

The homeostasis of R protein RPS2 is negatively regulated by the RING-type E3 ligase MUSE16.

Two transcriptional co-repressors physically interact with a transcription factor that is known to recruit a multi-protein complex, which promotes the repression of seed maturation genes by depositing trimethylation marks on lysine 27 of the histone 3 tails.

Co-repressors AtSDR4L and DIG1 interact with transcription factor VAL2 and promote Arabidopsis seed-to-seedling transition.

Repression of embryonic traits during the seed-to-seedling phase transition requires the inactivation of master transcription factors associated with embryogenesis. How the timing of such inactivation is controlled is unclear. Here, we report on a novel transcriptional co-repressor, Arabidopsis thaliana SDR4L, that forms a feedback inhibition loop with the master transcription factors LEC1 and ABI3 to repress embryonic traits post-imbibition. LEC1 and ABI3 regulate their own expression by inducing AtSDR4L during mid- to late embryogenesis. AtSDR4L binds to the upstream of LEC1 and ABI4, and these transcripts are upregulated in Atsdr4l seedlings. Atsdr4l seedlings phenocopy a LEC1 overexpressor. The embryonic traits of Atsdr4l can be partially rescued by impairing LEC1 or ABI3. The penetrance and expressivity of the Atsdr4l phenotypes depend on both developmental and external cues, demonstrating the importance of AtSDR4L in seedling establishment under suboptimal conditions. This article is protected by copyright. All rights reserved.

https://onlinelibrary.wiley.com/doi/pdfdirect/10.1111/jipb.13360

The transcriptional co-repressor SEED DORMANCY 4-LIKE (AtSDR4L) promotes embryonic-to-vegetative transition in Arabidopsis thaliana.

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