scholarly journals A molecular roadmap to the plant immune system

2020 ◽  
Vol 295 (44) ◽  
pp. 14916-14935 ◽  
Author(s):  
Adam R. Bentham ◽  
Juan Carlos De la Concepcion ◽  
Nitika Mukhi ◽  
Rafał Zdrzałek ◽  
Markus Draeger ◽  
...  

Plant diseases caused by pathogens and pests are a constant threat to global food security. Direct crop losses and the measures used to control disease (e.g. application of pesticides) have significant agricultural, economic, and societal impacts. Therefore, it is essential that we understand the molecular mechanisms of the plant immune system, a system that allows plants to resist attack from a wide variety of organisms ranging from viruses to insects. Here, we provide a roadmap to plant immunity, with a focus on cell-surface and intracellular immune receptors. We describe how these receptors perceive signatures of pathogens and pests and initiate immune pathways. We merge existing concepts with new insights gained from recent breakthroughs on the structure and function of plant immune receptors, which have generated a shift in our understanding of cell-surface and intracellular immunity and the interplay between the two. Finally, we use our current understanding of plant immunity as context to discuss the potential of engineering the plant immune system with the aim of bolstering plant defenses against disease.

Science ◽  
2013 ◽  
Vol 341 (6147) ◽  
pp. 746-751 ◽  
Author(s):  
Jeffery L. Dangl ◽  
Diana M. Horvath ◽  
Brian J. Staskawicz

Diverse and rapidly evolving pathogens cause plant diseases and epidemics that threaten crop yield and food security around the world. Research over the last 25 years has led to an increasingly clear conceptual understanding of the molecular components of the plant immune system. Combined with ever-cheaper DNA-sequencing technology and the rich diversity of germ plasm manipulated for over a century by plant breeders, we now have the means to begin development of durable (long-lasting) disease resistance beyond the limits imposed by conventional breeding and in a manner that will replace costly and unsustainable chemical controls.


2020 ◽  
Author(s):  
Christopher M. Garner ◽  
Benjamin J. Spears ◽  
Jianbin Su ◽  
Leland Cseke ◽  
Samantha N. Smith ◽  
...  

AbstractRegulation of the plant immune system is important for controlling the specificity and amplitude of responses to pathogens and in preventing growth-inhibiting autoimmunity that leads to reductions in plant fitness. In previous work, we reported that SRFR1, a negative regulator of effector-triggered immunity, interacts with SNC1 and EDS1. When SRFR1 is non-functional in the Arabidopsis accession Col-0, SNC1 levels increase, causing a cascade of events that lead to autoimmunity phenotypes. Previous work showed that some members of the transcriptional co-repressor family TOPLESS interact with SNC1 to repress negative regulators of immunity. Therefore, to explore potential connections between SRFR1 and TOPLESS family members, we took a genetic approach that examined the effect of each TOPLESS member in the srfr1 mutant background. The data indicated that an additive genetic interaction exists between SRFR1 and two members of the TOPLESS family, TPR2 and TPR3, as demonstrated by increased stunting and elevated PR2 expression in srfr1 tpr2 and srfr1 tpr2 tpr3 mutants. Furthermore, the tpr2 mutation intensifies autoimmunity in the auto-active snc1-1 mutant, indicating a novel role of these TOPLESS family members in negatively regulating SNC1-dependent phenotypes. This negative regulation can also be reversed by overexpressing TPR2 in the srfr1 tpr2 background. Thus, this work uncovers diverse functions of individual members of the TOPLESS family in Arabidopsis and provides evidence for the additive effect of transcriptional and post-transcriptional regulation of SNC1.Author SummaryThe immune system is a double-edged sword that affords organisms with protection against infectious diseases but can also lead to negative effects if not properly controlled. Plants only possess an innate antimicrobial immune system that relies on rapid upregulation of defenses once immune receptors detect the presence of microbes. Plant immune receptors known as resistance proteins play a key role in rapidly triggering defenses if pathogens breach other defenses. A common model of unregulated immunity in the reference Arabidopsis variety Columbia-0 involves a resistance gene called SNC1. When the SNC1 protein accumulates to unnaturally high levels or possesses auto-activating mutations, the visible manifestations of immune overactivity include stunted growth and low biomass and seedset. Consequently, expression of this gene and accumulation of the encoded protein are tightly regulated on multiple levels. Despite careful study the mechanisms of SNC1 gene regulation are not fully understood. Here we present data on members of the well-known TOPLESS family of transcriptional repressors. While previously characterized members were shown to function in indirect activation of defenses, TPR2 and TPR3 are shown here to function in preventing high defense activity. This study therefore contributes to the understanding of complex regulatory processes in plant immunity.


2011 ◽  
Vol 286 (41) ◽  
pp. 35834-35842 ◽  
Author(s):  
Laurence S. Boutemy ◽  
Stuart R. F. King ◽  
Joe Win ◽  
Richard K. Hughes ◽  
Thomas A. Clarke ◽  
...  

Phytopathogens deliver effector proteins inside host plant cells to promote infection. These proteins can also be sensed by the plant immune system, leading to restriction of pathogen growth. Effector genes can display signatures of positive selection and rapid evolution, presumably a consequence of their co-evolutionary arms race with plants. The molecular mechanisms underlying how effectors evolve to gain new virulence functions and/or evade the plant immune system are poorly understood. Here, we report the crystal structures of the effector domains from two oomycete RXLR proteins, Phytophthora capsici AVR3a11 and Phytophthora infestans PexRD2. Despite sharing <20% sequence identity in their effector domains, they display a conserved core α-helical fold. Bioinformatic analyses suggest that the core fold occurs in ∼44% of annotated Phytophthora RXLR effectors, both as a single domain and in tandem repeats of up to 11 units. Functionally important and polymorphic residues map to the surface of the structures, and PexRD2, but not AVR3a11, oligomerizes in planta. We conclude that the core α-helical fold enables functional adaptation of these fast evolving effectors through (i) insertion/deletions in loop regions between α-helices, (ii) extensions to the N and C termini, (iii) amino acid replacements in surface residues, (iv) tandem domain duplications, and (v) oligomerization. We hypothesize that the molecular stability provided by this core fold, combined with considerable potential for plasticity, underlies the evolution of effectors that maintain their virulence activities while evading recognition by the plant immune system.


2021 ◽  
Vol 22 (17) ◽  
pp. 9535
Author(s):  
Yuhuai Xie ◽  
Yuanyuan Wei

Long non-coding RNAs (lncRNAs) represent crucial transcriptional and post-transcriptional gene regulators during antimicrobial responses in the host innate immune system. Studies have shown that lncRNAs are expressed in a highly tissue- and cell-specific- manner and are involved in the differentiation and function of innate immune cells, as well as inflammatory and antiviral processes, through versatile molecular mechanisms. These lncRNAs function via the interactions with DNA, RNA, or protein in either cis or trans pattern, relying on their specific sequences or their transcriptions and processing. The dysregulation of lncRNA function is associated with various human non-infectious diseases, such as inflammatory bowel disease, cardiovascular diseases, and diabetes mellitus. Here, we provide an overview of the regulation and mechanisms of lncRNA function in the development and differentiation of innate immune cells, and during the activation or repression of innate immune responses. These elucidations might be beneficial for the development of therapeutic strategies targeting inflammatory and innate immune-mediated diseases.


Author(s):  
Alexandra Margets ◽  
Sharmin Rima ◽  
Mathew Helm ◽  
Morgan E Carter

The first of three International Society for Molecular Plant Microbe Interactions (IS-MPMI) eSymposia was convened on July 12-13, 2021, with the theme “Molecular Mechanism & Structure - Zooming in on Plant Immunity”. Hosted by Jian-Min Zhou (Beijing, China) and Jane Parker (Cologne, Germany), the eSymposium centered on “Top 10 Unanswered Questions in MPMI” number five: Does effector-triggered immunity (ETI) potentiate and restore pattern-triggered immunity (PTI) — or is there really a binary distinction between ETI and PTI? Since the previous International Congress of IS-MPMI in 2019, substantial progress has been made in untangling the complex signaling underlying plant immunity, including a greater understanding of the structure and function of key proteins. A clear need emerged for the MPMI community to come together virtually to share new knowledge around plant immunity. Over the course of two synchronous, half-days of programming, participants from 32 countries attended two plenary sessions with engaging panel discussions and networked through interactive hours and poster break out rooms. In this report, we summarize the concerted effort by multiple laboratories to study the molecular mechanisms underlying ETI and PTI, highlighting the essential role of plant resistosomes in the formation of calcium channels during an immune response. We conclude our report by forming new questions about how overlapping signaling mechanisms are controlled.


mBio ◽  
2016 ◽  
Vol 7 (2) ◽  
Author(s):  
Takafumi Mukaihara ◽  
Tadashi Hatanaka ◽  
Masahito Nakano ◽  
Kenji Oda

ABSTRACT The plant pathogen Ralstonia solanacearum uses a large repertoire of type III effector proteins to succeed in infection. To clarify the function of effector proteins in host eukaryote cells, we expressed effectors in yeast cells and identified seven effector proteins that interfere with yeast growth. One of the effector proteins, RipAY, was found to share homology with the ChaC family proteins that function as γ-glutamyl cyclotransferases, which degrade glutathione (GSH), a tripeptide that plays important roles in the plant immune system. RipAY significantly inhibited yeast growth and simultaneously induced rapid GSH depletion when expressed in yeast cells. The in vitro GSH degradation activity of RipAY is specifically activated by eukaryotic factors in the yeast and plant extracts. Biochemical purification of the yeast protein identified that RipAY is activated by thioredoxin TRX2. On the other hand, RipAY was not activated by bacterial thioredoxins. Interestingly, RipAY was activated by plant h -type thioredoxins that exist in large amounts in the plant cytosol, but not by chloroplastic m -, f -, x -, y - and z -type thioredoxins, in a thiol-independent manner. The transient expression of RipAY decreased the GSH level in plant cells and affected the flg22-triggered production of reactive oxygen species (ROS) and expression of pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) marker genes in Nicotiana benthamiana leaves. These results indicate that RipAY is activated by host cytosolic thioredoxins and degrades GSH specifically in plant cells to suppress plant immunity. IMPORTANCE Ralstonia solanacearum is the causal agent of bacterial wilt disease of plants. This pathogen injects virulence effector proteins into host cells to suppress disease resistance responses of plants. In this article, we report a biochemical activity of R. solanacearum effector protein RipAY. RipAY can degrade GSH, a tripeptide that plays important roles in the plant immune system, with its γ-glutamyl cyclotransferase activity. The high GSH degradation activity of RipAY is considered to be a good weapon for this bacterium to suppress plant immunity. However, GSH also plays important roles in bacterial tolerance to various stresses and growth. Interestingly, RipAY has an excellent safety mechanism to prevent unwanted firing of its enzyme activity in bacterial cells because RipAY is specifically activated by host eukaryotic thioredoxins. This study also reveals a novel host plant protein acting as a molecular switch for effector activation.


2021 ◽  
Vol 9 ◽  
Author(s):  
Meirav Leibman-Markus ◽  
Maya Bar

Much like humans, plants suffer from all kinds of diseases. In our lab, we study the immune system of plants. Using a technology called CRISPR, which enables us to edit the DNA of different creatures, we made changes in the plant immune system, with the goal of strengthening it. We succeeded in strengthening the plant immune system, and produced plants that are more resistant to diseases. Producing plants with a more active immune system could help us deal with plant diseases and improve agricultural crops.


2020 ◽  
Vol 42 (4) ◽  
pp. 14-18
Author(s):  
Hiroaki Adachi ◽  
Aleksandra Białas ◽  
Sophien Kamoun

Plants can get sick too. In fact, they get infected by all types of microbes and little critters. But plants have evolved an effective immune system to fight off pathogen invasion. Amazingly, nearly every single plant cell is able to protect itself and its neighbours against infections. The plant immune system gets switched on when one of its many immune receptors matches a ligand in the pathogen. As a consequence of a long evolutionary history of fighting off pathogens, immune receptors are now encoded by hundreds of genes that populate the majority of plant genomes. Understanding how the plant immune system functions and how it has evolved can give invaluable insights that would benefit modern agriculture and help breeding disease-resistant crops.


Author(s):  
Bruno Pok Man Ngou ◽  
Hee-Kyung Ahn ◽  
Pingtao Ding ◽  
Jonathan DG Jones

The plant immune system involves cell-surface receptors that detect intercellular pathogen-derived molecules, and intracellular receptors that activate immunity upon detection of pathogen-secreted effectors that act inside the plant cell. Surface receptor-mediated immunity has been extensively studied but in authentic interactions between plants and microbial pathogens, its presence impedes study of intracellular receptor-mediated immunity alone. How these two immune pathways interact is poorly understood. Here, we reveal mutual potentiation between these two recognition-dependent defense pathways. Recognition by surface receptors activates multiple protein kinases and NADPH oxidases, whereas intracellular receptors primarily elevate abundance of these proteins. Reciprocally, the intracellular receptor-dependent hypersensitive cell death response is strongly enhanced by activation of surface receptors. Activation of either immune system alone is insufficient to provide effective resistance against Pseudomonas syringae. Thus, immune pathways activated by cell-surface and intracellular receptors mutually potentiate to activate strong defense that thwarts pathogens. By studying the activation of intracellular receptors in the absence of surface receptor-mediated immunity, we have dissected the relationship between the two distinct immune systems. These findings reshape our understanding of plant immunity and have broad implications for crop improvement.


Viruses ◽  
2021 ◽  
Vol 13 (5) ◽  
pp. 840
Author(s):  
Marco Aurélio Ferreira ◽  
Ruan M. Teixeira ◽  
Elizabeth P. B. Fontes

In plant−virus interactions, the plant immune system and virulence strategies are under constant pressure for dominance, and the balance of these opposing selection pressures can result in disease or resistance. The naturally evolving plant antiviral immune defense consists of a multilayered perception system represented by pattern recognition receptors (PRR) and resistance (R) proteins similarly to the nonviral pathogen innate defenses. Another layer of antiviral immunity, signaling via a cell surface receptor-like kinase to inhibit host and viral mRNA translation, has been identified as a virulence target of the geminivirus nuclear shuttle protein. The Geminiviridae family comprises broad-host range viruses that cause devastating plant diseases in a large variety of relevant crops and vegetables and hence have evolved a repertoire of immune-suppressing functions. In this review, we discuss the primary layers of the receptor-mediated antiviral immune system, focusing on the mechanisms developed by geminiviruses to overcome plant immunity.


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