scholarly journals SUMOylation in Phytopathogen Interactions: Balancing Invasion and Resistance

Author(s):  
Manisha Sharma ◽  
Diana Fuertes ◽  
Jordi Perez-Gil ◽  
L. Maria Lois

Plants are constantly confronted by a multitude of biotic stresses involving a myriad of pathogens. In crops, pathogen infections result in significant agronomical losses worldwide posing a threat to food security. In order to enter plant tissues and establish a successful infection, phytopathogens have to surpass several physical, and chemical defense barriers. In recent years, post-translational modification (PTM) mechanisms have emerged as key players in plant defense against pathogens. PTMs allow a highly dynamic and rapid response in front of external challenges, increasing the complexity and precision of cellular responses. In this review, we focus on the role of SUMO conjugation (SUMOylation) in plant immunity against fungi, bacteria, and viruses. In plants, SUMO regulates multiple biological processes, ranging from development to responses arising from environmental challenges. During pathogen attack, SUMO not only modulates the activity of plant defense components, but also serves as a target of pathogen effectors, highlighting its broad role in plant immunity. Here, we summarize known pathogenic strategies targeting plant SUMOylation and, the plant SUMO conjugates involved in host-pathogen interactions. We also provide a catalog of candidate SUMO conjugates according to their role in defense responses. Finally, we discuss the complex role of SUMO in plant defense, focusing on key biological and experimental aspects that contribute to some controversial conclusions, and the opportunities for improving agricultural productivity by engineering SUMOylation in crop species.

2021 ◽  
Vol 22 (8) ◽  
pp. 4214
Author(s):  
Gautam Anand ◽  
Meirav Leibman-Markus ◽  
Dorin Elkabetz ◽  
Maya Bar

Plants lack a circulating adaptive immune system to protect themselves against pathogens. Therefore, they have evolved an innate immune system based upon complicated and efficient defense mechanisms, either constitutive or inducible. Plant defense responses are triggered by elicitors such as microbe-associated molecular patterns (MAMPs). These components are recognized by pattern recognition receptors (PRRs) which include plant cell surface receptors. Upon recognition, PRRs trigger pattern-triggered immunity (PTI). Ethylene Inducing Xylanase (EIX) is a fungal MAMP protein from the plant-growth-promoting fungi (PGPF)–Trichoderma. It elicits plant defense responses in tobacco (Nicotiana tabacum) and tomato (Solanum lycopersicum), making it an excellent tool in the studies of plant immunity. Xylanases such as EIX are hydrolytic enzymes that act on xylan in hemicellulose. There are two types of xylanases: the endo-1, 4-β-xylanases that hydrolyze within the xylan structure, and the β-d-xylosidases that hydrolyze the ends of the xylan chain. Xylanases are mainly synthesized by fungi and bacteria. Filamentous fungi produce xylanases in high amounts and secrete them in liquid cultures, making them an ideal system for xylanase purification. Here, we describe a method for cost- and yield-effective xylanase production from Trichoderma using wheat bran as a growth substrate. Xylanase produced by this method possessed xylanase activity and immunogenic activity, effectively inducing a hypersensitive response, ethylene biosynthesis, and ROS burst.


2008 ◽  
Vol 36 (5) ◽  
pp. 868-873 ◽  
Author(s):  
Ana Talamillo ◽  
Jonatan Sánchez ◽  
Rosa Barrio

SUMOylation, a reversible process used as a ‘fine-tuning’ mechanism to regulate the role of multiple proteins, is conserved throughout evolution. This post-translational modification affects several cellular processes by the modulation of subcellular localization, activity or stability of a variety of substrates. A growing number of proteins have been identified as targets for SUMOylation, although, for many of them, the role of SUMO conjugation on their function is unknown. The use of model systems might facilitate the study of SUMOylation implications in vivo. In the present paper, we have compiled what is known about SUMOylation in Drosophila melanogaster, where the use of genetics provides new insights on SUMOylation's biological roles.


2020 ◽  
Author(s):  
Abraham Más ◽  
Laura Castaño-Miquel ◽  
Lorenzo Carretero-Paulet ◽  
Núria Colomé ◽  
Francesc Canals ◽  
...  

AbstractPost-translational modification by Small Ubiquitin-related Modifier (SUMO) is an essential regulatory mechanism in eukaryotes. In the cell, SUMO conjugates are highly enriched in the nucleus and, consistently, SUMOylation machinery components are mainly nuclear. Nonetheless, cytosolic SUMO targets also exist and the mechanisms that facilitate SUMO conjugation in the cytosol are unknown. Here, we show that the nuclear localization of the Arabidopsis SUMO activating enzyme large subunit SAE2 is dependent on two nuclear localization signals, the canonical NLS1 and the non-canonical NLS2 identified and validated here. NLS2 is proteolytic processed from SAE2 during seed development, facilitating SAE2 enrichment in the cytosol. Results obtained using transgenic plants expressing different SAE2 proteoforms suggest that SAE2 cytosolic enrichment could constitute a rapid signal for growth arrest. Phylogenetic studies indicated that the Arabidopsis NLS1-NLS2 structural organization is conserved only in seed plants, providing a potential evolutionary role of cytosolic SUMOylation in seed appearance.


1991 ◽  
Vol 46 (11-12) ◽  
pp. 969-981 ◽  
Author(s):  
Wolfgang Knogge

The complex biological phenomenon “resistance” can be reduced to single Mendelian traits acting on both the plant and the pathogen side in a number of pathosystems. According to the “gene-for-gene hypothesis”, the outcome of a plant/pathogen interaction in these cases is incompatibility if a plant carrying a particular resistance gene and a pathogen with the complementary avirulence gene meet. This suggests a causal role of resistance genes in a recognition process initiating active plant defense responses. Fundamentally different strategies are followed to identify these genes molecularly depending on the plant and pathogen species involved. Fungal diseases of crop plants, especially those of cereals, cause dramatic yield losses worldwide. It is assumed that a molecular characterization of plant genes conferring resistance to fungal pathogens will lead to a better understanding of the plant defense system in general permitting the development of new methods of crop plant protection.


2020 ◽  
Vol 71 (17) ◽  
pp. 5256-5268 ◽  
Author(s):  
Jian Chen ◽  
Michael Clinton ◽  
Guang Qi ◽  
Daowen Wang ◽  
Fengquan Liu ◽  
...  

Abstract As a plant hormone, salicylic acid (SA) plays essential roles in plant defense against biotrophic and hemibiotrophic pathogens. Significant progress has been made in understanding the SA biosynthesis pathways and SA-mediated defense signaling networks in the past two decades. Plant defense responses involve rapid and massive transcriptional reprogramming upon the recognition of pathogens. Plant transcription factors and their co-regulators are critical players in establishing a transcription regulatory network and boosting plant immunity. A multitude of transcription factors and epigenetic regulators have been discovered, and their roles in SA-mediated defense responses have been reported. However, our understanding of plant transcriptional networks is still limited. As such, novel genomic tools and bioinformatic techniques will be necessary if we are to fully understand the mechanisms behind plant immunity. Here, we discuss current knowledge, provide an update on the SA biosynthesis pathway, and describe the transcriptional and epigenetic regulation of SA-mediated plant immune responses.


2015 ◽  
Vol 28 (2) ◽  
pp. 180-194 ◽  
Author(s):  
William Stork ◽  
Jung-Gun Kim ◽  
Mary Beth Mudgett

Many phytopathogenic type III secretion effector proteins (T3Es) have been shown to target and suppress plant immune signaling but perturbation of the plant immune system by T3Es can also elicit a plant response. XopX is a “core” Xanthomonas T3E that contributes to growth and symptom development during Xanthomonas euvesicatoria infection of tomato but its functional role is undefined. We tested the effect of XopX on several aspects of plant immune signaling. XopX promoted ethylene production and plant cell death (PCD) during X. euvesicatoria infection of susceptible tomato and in transient expression assays in Nicotiana benthamiana, which is consistent with its requirement for the development of X. euvesicatoria-induced disease symptoms. Additionally, although XopX suppressed flagellin-induced reactive oxygen species, it promoted the accumulation of pattern-triggered immunity (PTI) gene transcripts. Surprisingly, XopX coexpression with other PCD elicitors resulted in delayed PCD, suggesting antagonism between XopX-dependent PCD and other PCD pathways. However, we found no evidence that XopX contributed to the suppression of effector-triggered immunity during X. euvesicatoria–tomato interactions, suggesting that XopX's primary virulence role is to modulate PTI. These results highlight the dual role of a core Xanthomonas T3E in simultaneously suppressing and activating plant defense responses.


2021 ◽  
Vol 12 ◽  
Author(s):  
Beibei Li ◽  
Ruolin Wang ◽  
Shiya Wang ◽  
Jiang Zhang ◽  
Ling Chang

Cytokinins (CKs) can modulate plant immunity to various pathogens, but how CKs are involved in plant defense responses to the necrotrophic pathogen Botrytis cinerea is still unknown. Here, we found that B. cinerea infection induced transcriptional changes in multiple genes involved in the biosynthesis, degradation, and signaling of CKs, as well as their contents, in pathogen-infected Arabidopsis leaves. Among the CKs, the gene expression of CYTOKININ OXIDASE/DEHYDROGENASE 5 (CKX5) was remarkably induced in the local infected leaves and the distant leaves of the same plant without pathogen inoculation. Cis-zeatin (cZ) and its riboside (cZR) accumulated considerably in infected leaves, suggesting an important role of the cis-zeatin type of CKs in the plant response to B. cinerea. Cytokinin double-receptor mutants were more susceptible to B. cinerea infection, whereas an exogenous CK treatment enhanced the expression levels of defense-related genes and of jasmonic acid (JA) and ethylene (ET), but not salicylic acid (SA), resulting in higher resistance of Arabidopsis to B. cinerea. Investigation of CK responses to B. cinerea infection in the JA biosynthesis mutant, jar1-1, and ET-insensitive mutant, ein2-1, showed that CK signaling and levels of CKs, namely, those of isopentenyladenine (iP), isopentenyladenine riboside (iPR), and trans-zeatin (tZ), were enhanced in jar1-1-infected leaves. By contrast, reductions in iP, iPR, tZ, and tZ riboside (tZR) as well as cZR contents occurred in ein2-1-infected leaves, whose transcript levels of CK signaling genes were likewise differentially regulated. The Arabidopsis Response Regulator 5 (ARR5) gene was upregulated in infected leaves of ein2-1 whereas another type-A response regulator, ARR16, was significantly downregulated, suggesting the existence of a complex regulation of CK signaling via the ET pathway. Accumulation of the cis-zeatin type of CKs in B. cinerea-infected leaves depended on ET but not JA pathways. Collectively, our findings provide evidence that CK responds to B. cinerea infection in a variety of ways that are differently modulated by JA and ET pathways in Arabidopsis.


2019 ◽  
Vol 116 (34) ◽  
pp. 17090-17095 ◽  
Author(s):  
Michael J. Skelly ◽  
Saad I. Malik ◽  
Thierry Le Bihan ◽  
Yuan Bo ◽  
Jihong Jiang ◽  
...  

SUMOylation, the covalent attachment of the small ubiquitin-like modifier (SUMO) to target proteins, is emerging as a key modulator of eukaryotic immune function. In plants, a SUMO1/2-dependent process has been proposed to control the deployment of host defense responses. The molecular mechanism underpinning this activity remains to be determined, however. Here we show that increasing nitric oxide levels following pathogen recognition promote S-nitrosylation of the Arabidopsis SUMO E2 enzyme, SCE1, at Cys139. The SUMO-conjugating activities of both SCE1 and its human homolog, UBC9, were inhibited following this modification. Accordingly, mutation of Cys139 resulted in increased levels of SUMO1/2 conjugates, disabled immune responses, and enhanced pathogen susceptibility. Our findings imply that S-nitrosylation of SCE1 at Cys139 enables NO bioactivity to drive immune activation by relieving SUMO1/2-mediated suppression. The control of global SUMOylation is thought to occur predominantly at the level of each substrate via complex local machineries. Our findings uncover a parallel and complementary mechanism by suggesting that total SUMO conjugation may also be regulated directly by SNO formation at SCE1 Cys139. This Cys is evolutionary conserved and specifically S-nitrosylated in UBC9, implying that this immune-related regulatory process might be conserved across phylogenetic kingdoms.


2020 ◽  
Vol 21 (20) ◽  
pp. 7482
Author(s):  
Aarti Gupta ◽  
Mamta Bhardwaj ◽  
Lam-Son Phan Tran

Sensing of pathogen infection by plants elicits early signals that are transduced to affect defense mechanisms, such as effective blockage of pathogen entry by regulation of stomatal closure, cuticle, or callose deposition, change in water potential, and resource acquisition among many others. Pathogens, on the other hand, interfere with plant physiology and protein functioning to counteract plant defense responses. In plants, hormonal homeostasis and signaling are tightly regulated; thus, the phytohormones are qualified as a major group of signaling molecules controlling the most widely tinkered regulatory networks of defense and counter-defense strategies. Notably, the phytohormone jasmonic acid mediates plant defense responses to a wide array of pathogens. In this review, we present the synopsis on the jasmonic acid metabolism and signaling, and the regulatory roles of this hormone in plant defense against the hemibiotrophic bacterial pathogen Pseudomonas syringae. We also elaborate on how this pathogen releases virulence factors and effectors to gain control over plant jasmonic acid signaling to effectively cause disease. The findings discussed in this review may lead to ideas for the development of crop cultivars with enhanced disease resistance by genetic manipulation.


2017 ◽  
Vol 30 (4) ◽  
pp. 325-333 ◽  
Author(s):  
Shuai Wang ◽  
Shu Wang ◽  
Qi Sun ◽  
Leiyun Yang ◽  
Ying Zhu ◽  
...  

The phytohormone cytokinin (CK) is not only essential for plant growth and development but also impacts plant immunity. A mutant screen in a constitutively active plant immune receptor mutant snc1 (suppressor of npr1, constitutive1) identified a suppressor mutation of SNC1-induced defense responses in an ABC transporter coding gene ABCG14. ABCG14 transports CK from roots to the shoots, and the suppression of the SNC1-mediated defense response by the loss of ABCG14 is due to a deficiency of trans-zeatin (tZ)-type CK in the shoot. In addition, exogenous application of the tZ-type CK enhances disease resistance associated with increased expression of the plant immune receptor gene SNC1. Taken together, this study further established the role of tZ-type CK in disease resistance and suggests a new intersection of CKs with plant immunity at the expression regulation of a plant immune receptor gene.


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