scholarly journals Overexpressed BSR1-Mediated Enhancement of Disease Resistance Depends on the MAMP-Recognition System

2020 ◽  
Vol 21 (15) ◽  
pp. 5397
Author(s):  
Yasukazu Kanda ◽  
Yoko Nishizawa ◽  
Takashi Kamakura ◽  
Masaki Mori

Plant plasma membrane-localized receptors recognize microbe-associated molecular patterns (MAMPs) and activate immune responses via various signaling pathways. Receptor-like cytoplasmic kinases (RLCKs) are considered key signaling factors in plant immunity. BROAD-SPECTRUM RESISTANCE 1 (BSR1), a rice RLCK, plays a significant role in disease resistance. Overexpression of BSR1 confers strong resistance against fungal and bacterial pathogens. Our recent study revealed that MAMP-triggered immune responses are mediated by BSR1 in wild-type rice and are hyperactivated in BSR1-overexpressing rice. It was suggested that hyperactivated immune responses were responsible for the enhancement of broad-spectrum disease resistance; however, this remained to be experimentally validated. In this study, we verified the above hypothesis by disrupting the MAMP-recognition system in BSR1-overexpressing rice. To this end, we knocked out OsCERK1, which encodes a well-characterized MAMP-receptor-like protein kinase. In the background of BSR1 overaccumulation, the knockout of OsCERK1 nearly abolished the enhancement of blast resistance. This finding indicates that overexpressed BSR1-mediated enhancement of disease resistance depends on the MAMP-triggered immune system, corroborating our previously suggested model.

2019 ◽  
Vol 20 (22) ◽  
pp. 5523 ◽  
Author(s):  
Yasukazu Kanda ◽  
Hitoshi Nakagawa ◽  
Yoko Nishizawa ◽  
Takashi Kamakura ◽  
Masaki Mori

Plants activate their immune system through intracellular signaling pathways after perceiving microbe-associated molecular patterns (MAMPs). Receptor-like cytoplasmic kinases mediate the intracellular signaling downstream of pattern-recognition receptors. BROAD-SPECTRUM RESISTANCE 1 (BSR1), a rice (Oryza sativa) receptor-like cytoplasmic kinase subfamily-VII protein, contributes to chitin-triggered immune responses. It is valuable for agriculture because its overexpression confers strong disease resistance to fungal and bacterial pathogens. However, it remains unclear how overexpressed BSR1 reinforces plant immunity. Here we analyzed immune responses using rice suspension-cultured cells and sliced leaf blades overexpressing BSR1. BSR1 overexpression enhances MAMP-triggered production of hydrogen peroxide (H2O2) and transcriptional activation of the defense-related gene in cultured cells and leaf strips. Furthermore, the co-cultivation of leaves with conidia of the blast fungus revealed that BSR1 overexpression allowed host plants to produce detectable oxidative bursts against compatible pathogens. BSR1 was also involved in the immune responses triggered by peptidoglycan and lipopolysaccharide. Thus, we concluded that the hyperactivation of MAMP-triggered immune responses confers BSR1-mediated robust resistance to broad-spectrum pathogens.


2021 ◽  
Author(s):  
Xingyu An ◽  
Hui Zhang ◽  
Jinlu Li ◽  
Rui Yang ◽  
Qianchun Zeng ◽  
...  

Abstract Background: The molecular mechanism of durable and broad-spectrum resistance to rice blast disease in japonica rice variety is still very little known. Ziyu44, a local japonica rice variety in Yunnan Province of China, has shown durable broad-spectrum blast resistance for more than 30 years, and provides an opportunity for us to explore the molecular basis of broad-spectrum resistance to rice blast in japonica rice variety.Methods and Results: We conducted a comparative study of mycelium growth, aposporium formation, the accumulation of salicylate(SA), jasmonate(JA) and H2O2, the expression of SA- and JA-associated genes between Ziyu44 and susceptible variety Jiangnanxiangnuo (JNXN) upon M. oryzae infection. We found that appressorium formation and invasive hyphae extention were greatly inhibited in Ziyu 44 leaves compared with that in JNXN leaves. Both Ziyu 44 and JNXN plants maintained high levels of baseline SA and did not show increased accumulation of SA after inoculation with M. oryzae, while the levels of baseline JA in Ziyu 44 and JNXN plants were relatively low, and the accumulation of JA exhibited markedly increased in Ziyu 44 plants upon M. oryzae infection. The expression levels of key genes involving JA and SA signaling pathway OsCOI1b, OsNPR1, OsMPK6 as well as pathogenesis-related (PR) genes OsPR1a, OsPR1b and OsPBZ1, were markedly up-regulated in Ziyu44. Conclusions: The level of endogenous JA is critical for synchronous activation of SA and JA signaling pathway, up-regulating PR gene expression and enhancing disease resistance against rice blast in Ziyu44.


2020 ◽  
Vol 33 (5) ◽  
pp. 767-780 ◽  
Author(s):  
Laura Bacete ◽  
Hugo Mélida ◽  
Gemma López ◽  
Patrick Dabos ◽  
Dominique Tremousaygue ◽  
...  

The cytokinin signaling pathway, which is mediated by Arabidopsis response regulator (ARR) proteins, has been involved in the modulation of some disease-resistance responses. Here, we describe novel functions of ARR6 in the control of plant disease-resistance and cell-wall composition. Plants impaired in ARR6 function (arr6) were more resistant and susceptible, respectively, to the necrotrophic fungus Plectosphaerella cucumerina and to the vascular bacterium Ralstonia solanacearum, whereas Arabidopsis plants that overexpress ARR6 showed the opposite phenotypes, which further support a role of ARR6 in the modulation of disease-resistance responses against these pathogens. Transcriptomics and metabolomics analyses revealed that, in arr6 plants, canonical disease-resistance pathways, like those activated by defensive phytohormones, were not altered, whereas immune responses triggered by microbe-associated molecular patterns were slightly enhanced. Cell-wall composition of arr6 plants was found to be severely altered compared with that of wild-type plants. Remarkably, pectin-enriched cell-wall fractions extracted from arr6 walls triggered more intense immune responses than those activated by similar wall fractions from wild-type plants, suggesting that arr6 pectin fraction is enriched in wall-related damage-associated molecular patterns, which trigger immune responses. This work supports a novel function of ARR6 in the control of cell-wall composition and disease resistance and reinforces the role of the plant cell wall in the modulation of specific immune responses.


2021 ◽  
Author(s):  
Chen Chen ◽  
Chengguang Zhang ◽  
Haoqi Li ◽  
Zongmei Wang ◽  
Yueming Yuan ◽  
...  

Rabies, caused by rabies virus (RABV), is fatal to both humans and animals around the world. Effective clinical therapy for rabies has not been achieved, and vaccination is the most effective means of preventing and controlling rabies. Although different vaccines, such as live attenuated and inactivated vaccines, can induce different immune responses, different expression of pattern recognition receptors (PRRs) also causes diverse immune responses. Toll-like receptor 4 (TLR4) is a pivotal PRR that induces cytokine production and bridges innate and adaptive immunity. Importantly, TLR4 recognizes various virus-derived pathogen-associated molecular patterns (PAMPs) and virus-induced damage-associated molecular patterns (DAMPs), usually leading to the activation of immune cells. However, the role of TLR4 in the humoral immune response induced by RABV has not been revealed yet. Based on TLR4-deficient ( TLR4 -/- ) and wild-type (WT) mouse models, we report that TLR4-dependent recruitment of the conventional type-2 dendritic cells (CD8α - CD11b + cDC2) into secondary lymph organs (SLOs) is critical for antigen presentation. cDC2-initiated differentiation of Tfh cells promotes the proliferation of germinal centre (GC) B cells, the formation of GCs, and the production of plasma cells (PCs), all of which contribute to the production of RABV-specific IgG and virus-neutralizing antibodies (VNAs). Collectively, our work demonstrates that TLR4 is necessary for the recruitment of cDC2 and for the induction of RABV-induced humoral immunity, which is regulated by the cDC2-Tfh-GC B axis. IMPORTANCE Vaccination is the most efficient method to prevent rabies. TLR4, a well-known immune sensor, plays a critical role in initiating innate immune response. Here, we found that TLR4 deficiency ( TLR4 -/- ) mice suppressed the induction of humoral immune response after immunization with rabies virus (RABV), including reduced production of VNAs and RABV-specific IgG, compared with that occurred in wild-type (WT) mice. As a consequence, TLR4 -/- mice exhibited higher mortality than WT mice after challenge with virulent RABV. Importantly, further investigation found that TLR4 signaling promoted the recruitment of cDC2 (CD8α + CD11b - ), a subset of cDCs known to induce CD4 + T cell immunity through their MHC-II presentation machinery. Our results imply that TLR4 is indispensable for an efficient humoral response to rabies vaccine, which provides new insight into the development of novel rabies vaccines.


2018 ◽  
Vol 218 (2) ◽  
pp. 661-680 ◽  
Author(s):  
Sara Sopeña-Torres ◽  
Lucía Jordá ◽  
Clara Sánchez-Rodríguez ◽  
Eva Miedes ◽  
Viviana Escudero ◽  
...  

mBio ◽  
2020 ◽  
Vol 11 (3) ◽  
Author(s):  
Xiao Lin ◽  
Shumei Wang ◽  
Laura de Rond ◽  
Nicoletta Bertolin ◽  
Roland H. M. Wouters ◽  
...  

ABSTRACT Plants deploy cell surface receptors known as pattern-recognition receptors (PRRs) that recognize non-self molecules from pathogens and microbes to defend against invaders. PRRs typically recognize microbe-associated molecular patterns (MAMPs) that are usually widely conserved, some even across kingdoms. Here, we report an oomycete-specific family of small secreted cysteine-rich (SCR) proteins that displays divergent patterns of sequence variation in the Irish potato famine pathogen Phytophthora infestans. A subclass that includes the conserved effector PcF from Phytophthora cactorum activates immunity in a wide range of plant species. In contrast, the more diverse SCR74 subclass is specific to P. infestans and tends to trigger immune responses only in a limited number of wild potato genotypes. The SCR74 response was recently mapped to a G-type lectin receptor kinase (G-LecRK) locus in the wild potato Solanum microdontum subsp. gigantophyllum. The G-LecRK locus displays a high diversity in Solanum host species compared to other solanaceous plants. We propose that the diversification of the SCR74 proteins in P. infestans is driven by a fast coevolutionary arms race with cell surface immune receptors in wild potato, which contrasts the presumed slower dynamics between conserved apoplastic effectors and PRRs. Understanding the molecular determinants of plant immune responses to these divergent molecular patterns in oomycetes is expected to contribute to deploying multiple layers of disease resistance in crop plants. IMPORTANCE Immune receptors at the plant cell surface can recognize invading microbes. The perceived microbial molecules are typically widely conserved and therefore the matching surface receptors can detect a broad spectrum of pathogens. Here we describe a family of Phytophthora small extracellular proteins that consists of conserved subfamilies that are widely recognized by solanaceous plants. Remarkably, one subclass of SCR74 proteins is highly diverse, restricted to the late blight pathogen Phytophthora infestans and is specifically detected in wild potato plants. The diversification of this subfamily exhibits signatures of a coevolutionary arms race with surface receptors in potato. Insights into the molecular interaction between these potato-specific receptors and the recognized Phytophthora proteins are expected to contribute to disease resistance breeding in potato.


2017 ◽  
Vol 107 (1) ◽  
pp. 84-91 ◽  
Author(s):  
Wanwan He ◽  
Nengyan Fang ◽  
Ruisen Wang ◽  
Yunyu Wu ◽  
Guoying Zeng ◽  
...  

Heikezijing, a japonica rice landrace from the Taihu region of China, exhibited broad-spectrum resistance to more than 300 isolates of the blast pathogen (Magnaporthe oryzae). In our previous research, we fine mapped a broad-spectrum resistance gene, Pi-hk1, in chromosome 11. In this research, 2010-9(G1), one of the predominant races of blast in the Taihu Lake region of China, was inoculated into 162 recombinant inbred lines (RIL) and two parents, Heikezijing and Suyunuo, for mapping the resistance-blast quantitative trait loci (QTL). Three QTL (Lsqtl4-1, Lsqtl9-1, and Lsqtl11-1) associated with lesion scores were detected on chromosomes 4, 9, and 11 and two QTL (Lnqtl1-1 and Lnqtl9-1) associated with average lesion numbers were detected on chromosomes 1 and 9. The QTL Lsqtl9-1 conferring race-specific resistance to 2010-9(G1) at seedling stages showed logarithm of the odds scores of 9.10 and phenotypic variance of 46.19% and might be a major QTL, named Pi-hk2. The line RIL84 with Pi-hk2 derived from a cross between Heikezijing and Suyunuo was selected as Pi-hk2 gene donor for developing fine mapping populations. According to the resistance evaluation of recombinants of three generations (BC1F2, BC1F3, and BC1F4), Pi-hk2 was finally mapped to a 143-kb region between ILP-19 and RM24048, and 18 candidate genes were predicted, including genes that encode pleiotropic drug resistance protein 4 (n = 2), WRKY74 (n = 1), cytochrome b5-like heme/steroid-binding domain containing protein (n = 1), protein kinase (n = 1), and ankyrin repeat family protein (n = 1). These results provide essential information for cloning of Pi-hk2 and its potential utility in breeding resistant rice cultivars by marker-assisted selection.


2013 ◽  
Vol 103 (11) ◽  
pp. 1162-1168 ◽  
Author(s):  
Yunyu Wu ◽  
Yongmei Bao ◽  
Liujie Xie ◽  
Yunyun Su ◽  
Ruizhen Chu ◽  
...  

One Japonica rice landrace, Heikezijing, from the Taihu Lake region of China, exhibits broad-spectrum resistance to rice blast. As characterized in our previous research, a main-effect resistance (R) gene, Pi-hk1, in Heikezijing against five isolates (GD10-279a, JS2004-141-1, JS2004-185, JS90-78, and Hoku1) was roughly mapped on the long arm of chromosome 11. To fine map Pi-hk1, one recombinant inbred line (RIL), RIL72 (F2:8), from the cross between Heikezijing and blast-susceptible variety Suyunuo, was further crossed and backcrossed with Suyunuo to produce a BC1F2 population of 477 individuals. Inoculation experiments with the representative isolate Hoku 1 indicated that RIL72 carries a single dominant R gene for blast resistance. With the help of advanced BC1F3 (915 plants), BC1F4 (4,459 plants), and BC1F5 (2,000 plants) mapping populations, Pi-hk1 was finally mapped to a 107-kb region between molecular markers P3586 and ILP3, and co-segregated with the markers P4098, RM7654, and P4099. By sequence analysis of Heikezijing bacterial artificial chromosome clones covering Pi-hk1 region, 16 predicted genes were identified within this region, including three nucleotide-binding site leucine-rich repeat candidate genes. These results provide essential information for cloning of Pi-hk1 and its application in rice breeding for broad-spectrum blast resistance by marker-assisted selection.


2019 ◽  
Author(s):  
Fabian Giska ◽  
Gregory B. Martin

AbstractPlant immune responses, including the production of reactive oxygen species (ROS), are triggered when pattern recognition receptors (PRR) become activated upon detection of microbe-associated molecular patterns (MAMPs). Receptor-like cytoplasmic kinases are key components of PRR-dependent signaling pathways. In tomato two such kinases, Pti1a and Pti1b, are important positive regulators of the plant immune response. However, it is unknown how these kinases control plant immunity at the molecular level, and how their activity is regulated. To investigate these issues, we used mass spectrometry to search for interactors of Pti1b in Nicotiana benthamiana leaves and identified a protein phosphatase, PP2C6. An in vitro pull-down assay and in vivo split luciferase complementation assay verified this interaction. Pti1b was found to autophosphorylate on threonine-233 and this phosphorylation was abolished in the presence of PP2C6. An arginine-to-cysteine substitution at position 240 in the Arabidopsis MARIS kinase was previously reported to convert it into a constitutive-active form. The analogous substitution in Pti1b made it resistant to PP2C6 phosphatase activity, although it still interacted with PP2C6. Treatment of N. benthamiana leaves with the MAMP flg22 induced threonine phosphorylation of Pti1b. Expression of PP2C6, but not a phosphatase-inactive variant of this protein, in N. benthamiana leaves greatly reduced ROS production in response to treatment with MAMPs flg22 or csp22. The results indicate that PP2C6 acts as a negative regulator by dephosphorylating the Pti1b kinase, thereby interfering with its ability to activate plant immune responses.


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