scholarly journals PacC-dependent adaptation and modulation of host cellular pH controls hemibiotrophic invasive growth and disease development by the rice blast fungus

2020 ◽  
Author(s):  
Xiao-Lin Chen ◽  
Dan He ◽  
Changfa Yin ◽  
Jun Yang ◽  
Jing Sun ◽  
...  

AbstractMany of the world’s most serious crop diseases are caused by hemibiotrophic fungi. These pathogens have evolved the ability to colonize living plant cells, suppressing plant immunity responses, before switching to necrotrophic growth, in which host cells die, providing the energy to fuel sporulation and spread of the fungus. How hemibiotrophic pathogens switch between these two lifestyles remains poorly understood. Here, we report that the devastating rice blast fungus, Magnaporthe oryzae, manipulates host cellular pH to regulate hemibiotrophy. During infection by M. oryzae, host plant cells are alkalinized to pH 7.8 during biotrophic growth, but later acidified to pH 6.5 during necrotrophy. Using a forward genetic screen, we identified alkaline-sensitive mutants of M. oryzae that were blocked in biotrophic proliferation and impaired in induction of host cell acidification and necrotrophy. These mutants defined components of the PacC-dependent ambient pH signal transduction pathway in M. oryzae. We report that PacC exists as a full-length repressor, PacC559, and a truncated transcriptional activator, PacC222, which localize to the fungal nucleus during biotrophic growth and to the cytoplasm during necrotrophy. During biotrophy, PacC222 directly activates genes associated with nutrient acquisition and fungal virulence, while PacC559 represses genes associated with saprophytic mycelial growth and sporulation, which are subsequently de-repressed during necrotrophy. When considered together, our results indicate that temporal regulation of hemibiotrophy by M. oryzae requires PacC-dependent sensing and manipulation of host cellular pH.Author SummaryCrop diseases caused by fungi represent some of the most serious threats to global food security. Many fungal pathogens have evolved the ability to invade living plant tissue and suppress host immunity, before switching to a completely different mode of growth, in which they are able to kill host plant cells. This lifestyle– called hemibiotrophy –is exemplified by the blast fungus, Magnaporthe oryzae, which causes devastating diseases of rice, wheat and many other grasses. We found that during infection by M. oryzae, host cells initially have an alkaline pH, when the fungus is growing in living tissue, but pH rapidly becomes acidic, as host tissue is killed. We identified mutants of the blast fungus that were sensitive to alkaline pH and this enabled us to identify the signal transduction pathway by which the fungus responds to changes in ambient pH. We found that mutants in the pH response pathway were blocked in invasive fungal growth and could not cause acidification of host tissue. Consequently, they are unable to cause blast disease. We characterized the central regulator of this pathway, the PacC transcription factor, which unusually can act as both a repressor and an activator of fungal gene expression. During biotrophic invasive growth, PacC activates many genes previously reported to be required for virulence, including several associated with nutrient acquisition, and at the same time represses genes associated with vegetative growth and sporulation. The PacC signaling pathway is therefore necessary for regulating the switch in fungal lifestyle associated with causing blast disease.

2010 ◽  
Vol 37 (10) ◽  
pp. 913 ◽  
Author(s):  
Pamela H. P. Gan ◽  
Maryam Rafiqi ◽  
Adrienne R. Hardham ◽  
Peter N. Dodds

Plant pathogenic biotrophic fungi are able to grow within living plant tissue due to the action of secreted pathogen proteins known as effectors that alter the response of plant cells to pathogens. The discovery and identification of these proteins has greatly expanded with the sequencing and annotation of fungal pathogen genomes. Studies to characterise effector function have revealed that a subset of these secreted pathogen proteins interact with plant proteins within the host cytoplasm. This review focuses on the effectors of intracellular biotrophic and hemibiotrophic fungal plant pathogens and summarises advances in understanding the roles of these proteins in disease and in elucidating the mechanism of fungal effector uptake into host cells.


Author(s):  
Sergio M. Latorre ◽  
C. Sarai Reyes-Avila ◽  
Angus Malmgren ◽  
Joe Win ◽  
Sophien Kamoun ◽  
...  

AbstractBackgroundUnderstanding the mechanisms and timescales of plant pathogen outbreaks requires a detailed genome-scale analysis of their population history. The fungus Magnaporthe (Syn. Pyricularia) oryzae —the causal agent of blast disease of cereals— is among the most destructive plant pathogens to world agriculture and a major threat to the production of rice, wheat and other cereals. Although M. oryzae is a multihost pathogen that infects more than 50 species of cereals and grasses, all rice-infecting isolates belong to a single genetically defined lineage. Here, we combined multiple genomics datasets to reconstruct the genetic history of the rice-infecting lineage of M. oryzae based on 131 isolates from 21 countries.ResultsThe global population of the rice blast fungus consists of a diverse set of individuals and three well-defined genetic groups. Multiple population genetic tests revealed that the rice-infecting lineage of the blast fungus probably originated from a recombining diverse group in South East Asia followed by three independent clonal expansions that took place over the last ∼200 years. Patterns of allele sharing identified a subpopulation from the recombining diverse group that introgressed with one of the clonal lineages before its global expansion. Remarkably, the four genetic lineages of the rice blast fungus vary in the number and patterns of presence/absence of candidate effector genes. In particular, clonal lineages carry a reduced repertoire of effector genes compared with the diverse group, and specific combinations of effector presence/absence define each of the pandemic clonal lineages.ConclusionsOur analyses reconstruct the genetic history of the rice-infecting lineage of M. oryzae revealing three clonal lineages associated with rice blast pandemics. Each of these lineages displays a specific pattern of presence/absence of effector genes that may have shaped their adaptation to the rice host and their evolutionary history.


2020 ◽  
Vol 6 (1) ◽  
pp. 38 ◽  
Author(s):  
Apinya Longya ◽  
Sucheela Talumphai ◽  
Chatchawan Jantasuriyarat

Rice blast disease is caused by the ascomycete fungus Pyricularia oryzae and is one of the most destructive rice diseases in the world. The objectives of this study were investigating various fungal morphological characteristics and performing a phylogenetic analysis. Inter-simple sequence repeat (ISSR) and sequence-related amplified polymorphism (SRAP) markers were used to examine the genetic variation of 59 rice blast fungus strains, including 57 strains collected from different fields in Thailand and two reference strains, 70-15 and Guy11. All isolates used in this study were determined to be P. oryzae by internal transcribed spacer (ITS) sequence confirmation. A total of 14 ISSR primers and 17 pairs of SRAP primers, which produced clear and polymorphic bands, were selected for assessing genetic diversity. A total of 123 polymorphic bands were generated. The similarity index value for the strains ranged from 0.25 to 0.95. The results showed that the blast fungus population in Thailand has both morphological and genetic variations. A high level of genetic variation, or genome adaptation, is one of the fungal mechanisms that could overcome host resistance to avoid host recognition. Results from this research study could bring substantial benefits and ultimately help to understand the blast fungal pathogen genome and the population structure in Thai blast fungus.


2021 ◽  
Author(s):  
Ammarah Shabbir ◽  
Wajjiha Batool ◽  
Yu Dan ◽  
Lili Lin ◽  
An Anquoli ◽  
...  

Abstract Endo-β-1,4-Xylanases are a group of extracellular enzymes that catalyze the hydrolysis of xylan, a principal constituent of the plant primary cell wall. The contribution of Endo-β-1,4-Xylanase I to both physiology and pathogenesis of the rice blast fungus M. oryzae is unknown. Here, we characterized the biological function of two endoxylanase I (MoXYL1A and MoXYL1B) genes in the development of M. oryzae using targeted gene deletion, biochemical analysis, and fluorescence microscopy. Phenotypic analysis of ∆Moxyl1A strains showed that MoXYL1A is required for the full virulence of M. oryzae but is dispensable for the vegetative growth of the rice blast fungus. MoXYL1B, in contrast, did not have a clear role in the infectious cycle but has a critical function in asexual reproduction of the fungus. The double deletion mutant was severely impaired in pathogenicity and virulence as well as asexual development. We found that MoXYL1A deletion compromised appressorium morphogenesis and function, leading to failure to penetrate host cells. Fluorescently tagged MoXYL1A and MoXYL1B displayed cytoplasmic localization in M. oryzae, while analysis of MoXYL1A-GFP and MoXYL1B-GFP in-planta revealed translocation and accumulation of these effector proteins into host cells. Meanwhile, sequence feature analysis showed that MoXYL1A possesses a transient chloroplast targeting signal peptide, and results from an Agrobacterium infiltration assay confirmed co-localization of MoXYL1A-GFP with ChCPN10C-RFP in the chloroplasts of host cells. MoXYL1B, accumulated to the cytoplasm of the host. Taken together, we conclude that MoXYL1A is a secreted effector protein that likely promotes the virulence of M. oryzae by interfering in the proper functioning of the host chloroplast, while the related xylanase MoXYL1B does not have a major role in virulence of M. oryzae.


2017 ◽  
Vol 61 ◽  
pp. 1-7
Author(s):  
Nguyen Phu Toan ◽  
Pham Thi Thu Ha ◽  
Tran Dang Xuan

Rice blast fungus (Pyricularia grisea) is one of the most problematic pathogen to significantly reduce rice production worldwide. In this study, after being inoculated withP. grisea, changes in phenolic components and antioxidant capacity and correlation with the resistant level against rice blast fungus were investigated. Among screened rice cultivars, AV-3 was the strongest resistant, whereas BII-3 was the most susceptible. It was found that although total contents of phenolics and flavonoids, and antioxidant capacities varied among studied varieties, no significant coefficient with the resistance againstP. griseawas observed. After rice was affected by rice blast fungus, total phenolics and flavonoids were markedly reduced, but in contrast, the DPPH scavenging activities of only the susceptible rice cultivars was reduced. Among the 11 phenolic acids detected, catechol was found only in the tolerant cultivar AV-3, whereas the amount of cinnamic acid was increased after infection. Quantity of vanillin was also promoted, except in the susceptible cultivar BII-3 that was significantly reduced. Findings of this study showed that the resistant level againstP. griseawas proportionally correlated to the antioxidant capacity. Catechol, cinnamic acid, and vanillin may play a role but it needs further elaboration. Observations of this study suggested that the infection of blast disease by reducing amount of phenolics and flavonoids that may weaken the resistance of rice against this detrimental fungus.


2014 ◽  
Vol 27 (10) ◽  
pp. 1027-1034 ◽  
Author(s):  
Naoki Yokotani ◽  
Tomoko Tsuchida-Mayama ◽  
Hiroaki Ichikawa ◽  
Nobutaka Mitsuda ◽  
Masaru Ohme-Takagi ◽  
...  

Plants respond to pathogen attack by transcriptionally regulating defense-related genes via various types of transcription factors. We identified a transcription factor in rice, OsNAC111, belonging to the TERN subgroup of the NAC family that was transcriptionally upregulated after rice blast fungus (Magnaporthe oryzae) inoculation. OsNAC111 was localized in the nucleus of rice cells and had transcriptional activation activity in yeast and rice cells. Transgenic rice plants overexpressing OsNAC111 showed increased resistance to the rice blast fungus. In OsNAC111-overexpressing plants, the expression of several defense-related genes, including pathogenesis-related (PR) genes, was constitutively high compared with the control. These genes all showed blast disease-responsive expression in leaves. Among them, two chitinase genes and one β-1,3-glucanase gene showed reduced expression in transgenic rice plants in which OsNAC111 function was suppressed by a chimeric repressor (OsNAC111-SRDX). OsNAC111 activated transcription from the promoters of the chitinase and β-1,3-glucanase genes in rice cells. In addition, brown pigmentation at the infection sites, a defense response of rice cells to the blast fungus, was lowered in OsNAC111-SRDX plants at the early infection stage. These results indicate that OsNAC111 positively regulates the expression of a specific set of PR genes in the disease response and contributes to disease resistance.


2021 ◽  
Vol 22 (23) ◽  
pp. 13132
Author(s):  
Shen-Hsing Hsu ◽  
Li-Fang Chou ◽  
Chung-Hung Hong ◽  
Ming-Yang Chang ◽  
Chung-Ying Tsai ◽  
...  

Approximately 1 million cases of leptospirosis, an emerging infectious zoonotic disease, are reported each year. Pathogenic Leptospira species express leucine-rich repeat (LRR) proteins that are rarely expressed in non-pathogenic Leptospira species. The LRR domain-containing protein family is vital for the virulence of pathogenic Leptospira species. In this study, the biological mechanisms of an essential LRR domain protein from pathogenic Leptospira were examined. The effects of Leptospira and recombinant LRR20 (rLRR20) on the expression levels of factors involved in signal transduction were examined using microarray, quantitative real-time polymerase chain reaction, and western blotting. The secreted biomarkers were measured using an enzyme-linked immunosorbent assay. rLRR20 colocalized with E-cadherin on the cell surface and activated the downstream transcription factor β-catenin, which subsequently promoted the expression of MMP7, a kidney injury biomarker. Additionally, MMP7 inhibitors were used to demonstrate that the secreted MMP7 degrades surface E-cadherin. This feedback inhibition mechanism downregulated surface E-cadherin expression and inhibited the colonization of Leptospira. The degradation of surface E-cadherin activated the NF-κB signal transduction pathway. Leptospirosis-associated acute kidney injury is associated with the secretion of NGAL, a downstream upregulated biomarker of the NF-κB signal transduction pathway. A working model was proposed to illustrate the crosstalk between E-cadherin/β-catenin and NF-κB signal transduction pathways during Leptospira infection. Thus, rLRR20 of Leptospira induces kidney injury in host cells and inhibits the adhesion and invasion of Leptospira through the upregulation of MMP7 and NGAL.


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