System-Wide Characterization of MoArf GTPase Family Proteins and Adaptor Protein MoGga1 Involved in the Development and Pathogenicity of Magnaporthe oryzae

ABSTRACT ADP ribosylation factor (Arf) small GTPase family members are involved in vesicle trafficking and organelle maintenance in organisms ranging from Saccharomyces cerevisiae to humans. A previous study identified Magnaporthe oryzae Arf6 (MoArf6) as one of the Arf proteins that regulates growth and conidiation in the rice blast fungus M. oryzae, but the remaining family proteins remain unknown. Here, we identified six additional Arf proteins, including MoArf1, MoArl1, MoArl3, MoArl8, MoCin4, and MoSar1, as well as their sole adaptor protein, MoGga1, and determined their shared and specific functions. We showed that the majority of these proteins exhibit positive regulatory functions, most notably, in growth. Importantly, MoArl1, MoCin4, and MoGga1 are involved in pathogenicity through the regulation of host penetration and invasive hyphal growth. MoArl1 and MoCin4 also regulate normal vesicle trafficking, and MoCin4 further controls the formation of the biotrophic interfacial complex (BIC). Moreover, we showed that Golgi-cytoplasm cycling of MoArl1 is required for its function. Finally, we demonstrated that interactions between MoArf1 and MoArl1 with MoGga1 are important for Golgi localization and pathogenicity. Collectively, our findings revealed the shared and specific functions of Arf family members in M. oryzae and shed light on how these proteins function through conserved mechanisms to govern growth, transport, and virulence of the blast fungus. IMPORTANCE Magnaporthe oryzae is the causal agent of rice blast, representing the most devastating diseases of rice worldwide, which results in losses of amounts of rice that could feed more than 60 million people each year. Arf (ADP ribosylation factor) small GTPase family proteins are involved in vesicle trafficking and organelle maintenance in eukaryotic cells. To investigate the function of Arf family proteins in M. oryzae, we systematically characterized all seven Arf proteins and found that they have shared and specific functions in governing the growth, development, and pathogenicity of the blast fungus. We have also identified the pathogenicity-related protein MoGga1 as the common adaptor of MoArf1 and MoArl1. Our findings are important because they provide the first comprehensive characterization of the Arf GTPase family proteins and their adaptor protein MoGga1 functioning in a plant-pathogenic fungus, which could help to reveal new fungicide targets to control this devastating disease.

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Characterization of T-DNA insertion patterns in the genome of rice blast fungus Magnaporthe oryzae

Current Genetics ◽

10.1007/s00294-007-0122-5 ◽

2007 ◽

Vol 51 (4) ◽

pp. 233-243 ◽

Cited By ~ 36

Author(s):

Guihua Li ◽

Zhuangzhi Zhou ◽

Guifu Liu ◽

Fucong Zheng ◽

Chaozu He

Keyword(s):

Magnaporthe Oryzae ◽

Rice Blast ◽

Rice Blast Fungus ◽

Blast Fungus ◽

Dna Insertion

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One of Three Pex11 Family Members Is Required for Peroxisomal Proliferation and Full Virulence of the Rice Blast Fungus Magnaporthe oryzae

PLoS ONE ◽

10.1371/journal.pone.0134249 ◽

2015 ◽

Vol 10 (7) ◽

pp. e0134249 ◽

Cited By ~ 8

Author(s):

Jiaoyu Wang ◽

Ling Li ◽

Zhen Zhang ◽

Haiping Qiu ◽

Dongmei Li ◽

...

Keyword(s):

Magnaporthe Oryzae ◽

Rice Blast ◽

Family Members ◽

Rice Blast Fungus ◽

Blast Fungus

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Genome-wide characterization of methylguanosine-capped and polyadenylated small RNAs in the rice blast fungus Magnaporthe oryzae

Nucleic Acids Research ◽

10.1093/nar/gkq583 ◽

2010 ◽

Vol 38 (21) ◽

pp. 7558-7569 ◽

Cited By ~ 15

Author(s):

Malali Gowda ◽

Cristiano C. Nunes ◽

Joshua Sailsbery ◽

Minfeng Xue ◽

Feng Chen ◽

...

Keyword(s):

Magnaporthe Oryzae ◽

Small Rnas ◽

Rice Blast ◽

Rice Blast Fungus ◽

Blast Fungus ◽

Genome Wide

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Genome-wide Identification and characterization of circular RNAs in the rice blast fungus Magnaporthe oryzae

Scientific Reports ◽

10.1038/s41598-018-25242-w ◽

2018 ◽

Vol 8 (1) ◽

Cited By ~ 3

Author(s):

Jialan Yuan ◽

Zhao Wang ◽

Junjie Xing ◽

Qingyong Yang ◽

Xiao-Lin Chen

Keyword(s):

Magnaporthe Oryzae ◽

Rice Blast ◽

Rice Blast Fungus ◽

Circular Rnas ◽

Blast Fungus ◽

Genome Wide ◽

Identification And Characterization

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The Histone Deacetylases MoRpd3 and MoHst4 Regulate Growth, Conidiation, and Pathogenicity in the Rice Blast Fungus Magnaporthe oryzae

mSphere ◽

10.1128/msphere.00118-21 ◽

2021 ◽

Author(s):

Chaoxiang Lin ◽

Xue Cao ◽

Ziwei Qu ◽

Shulin Zhang ◽

Naweed I. Naqvi ◽

...

Keyword(s):

Magnaporthe Oryzae ◽

Histone Deacetylases ◽

Rice Blast ◽

Pathogenic Fungi ◽

Rice Blast Fungus ◽

Plant Pathogenic Fungi ◽

Content Type ◽

Blast Fungus ◽

Growth Development

HDACs (histone deacetylases) regulate various aspects of growth, development, and pathogenesis in plant-pathogenic fungi. Most members of HDAC classes I to III have been functionally characterized, except for orthologous Rpd3 and Hst4, in the rice blast fungus Magnaporthe oryzae .

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Genetic Variation Bias toward Noncoding Regions and Secreted Proteins in the Rice Blast Fungus Magnaporthe oryzae

mSystems ◽

10.1128/msystems.00346-20 ◽

2020 ◽

Vol 5 (3) ◽

Author(s):

Zhenhui Zhong ◽

Meilian Chen ◽

Lianyu Lin ◽

Ruiqi Chen ◽

Dan Liu ◽

...

Keyword(s):

Genetic Variation ◽

Magnaporthe Oryzae ◽

Experimental Evolution ◽

Rice Blast ◽

Plant Pathogens ◽

Rice Blast Fungus ◽

Content Type ◽

Noncoding Regions ◽

Blast Fungus ◽

Pathogen Populations

ABSTRACT The genomes of plant pathogens are highly variable and plastic. Pathogen gene repertoires change quickly with the plant environment, which results in a rapid loss of plant resistance shortly after the pathogen emerges in the field. Extensive studies have evaluated natural pathogen populations to understand their evolutionary effects; however, the number of studies that have examined the dynamic processes of the mutation and adaptation of plant pathogens to host plants remains limited. Here, we applied experimental evolution and high-throughput pool sequencing to Magnaporthe oryzae, a fungal pathogen that causes massive losses in rice production, to observe the evolution of genome variation. We found that mutations, including single-nucleotide variants (SNVs), insertions and deletions (indels), and transposable element (TE) insertions, accumulated very rapidly throughout the genome of M. oryzae during sequential plant inoculation and preferentially in noncoding regions, while such mutations were not frequently found in coding regions. However, we also observed that new TE insertions accumulated with time and preferentially accumulated at the proximal region of secreted protein (SP) coding genes in M. oryzae populations. Taken together, these results revealed a bias in genetic variation toward noncoding regions and SP genes in M. oryzae and may contribute to the rapid adaptive evolution of the blast fungal effectors under host selection. IMPORTANCE Plants “lose” resistance toward pathogens shortly after their widespread emergence in the field because plant pathogens mutate and adapt rapidly under resistance selection. Thus, the rapid evolution of pathogens is a serious threat to plant health. Extensive studies have evaluated natural pathogen populations to understand their evolutionary effects; however, the study of the dynamic processes of the mutation and adaptation of plant pathogens to host plants remains limited. Here, by performing an experimental evolution study, we found a bias in genetic variation toward noncoding regions and SPs in the rice blast fungus Magnaporthe oryzae, which explains the ability of the rice blast fungus to maintain high virulence variation to overcome rice resistance in the field.

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Molecular characterization of a novel ssRNA ourmia-like virus from the rice blast fungus Magnaporthe oryzae

Archives of Virology ◽

10.1007/s00705-016-3144-9 ◽

2016 ◽

Vol 162 (3) ◽

pp. 891-895 ◽

Cited By ~ 17

Author(s):

Adriana Illana ◽

Marco Marconi ◽

Julio Rodríguez-Romero ◽

Ping Xu ◽

Tamas Dalmay ◽

...

Keyword(s):

Molecular Characterization ◽

Magnaporthe Oryzae ◽

Rice Blast ◽

Rice Blast Fungus ◽

Blast Fungus

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Cellular Dynamics and Genomic Identity of Centromeres in Cereal Blast Fungus

mBio ◽

10.1128/mbio.01581-19 ◽

2019 ◽

Vol 10 (4) ◽

Cited By ~ 9

Author(s):

Vikas Yadav ◽

Fan Yang ◽

Md. Hashim Reza ◽

Sanzhen Liu ◽

Barbara Valent ◽

...

Keyword(s):

Dna Sequence ◽

Chromosome Segregation ◽

Magnaporthe Oryzae ◽

Rice Blast ◽

Metaphase Plate ◽

Blast Disease ◽

Sequence Motifs ◽

Content Type ◽

Kinetochore Assembly ◽

Blast Fungus

ABSTRACT Precise kinetochore-microtubule interactions ensure faithful chromosome segregation in eukaryotes. Centromeres, identified as scaffolding sites for kinetochore assembly, are among the most rapidly evolving chromosomal loci in terms of the DNA sequence and length and organization of intrinsic elements. Neither the centromere structure nor the kinetochore dynamics is well studied in plant-pathogenic fungi. Here, we sought to understand the process of chromosome segregation in the rice blast fungus Magnaporthe oryzae. High-resolution imaging of green fluorescent protein (GFP)-tagged inner kinetochore proteins CenpA and CenpC revealed unusual albeit transient declustering of centromeres just before anaphase separation of chromosomes in M. oryzae. Strikingly, the declustered centromeres positioned randomly at the spindle midzone without an apparent metaphase plate per se. Using CenpA chromatin immunoprecipitation followed by deep sequencing, all seven centromeres in M. oryzae were found to be regional, spanning 57-kb to 109-kb transcriptionally poor regions. Highly AT-rich and heavily methylated DNA sequences were the only common defining features of all the centromeres in rice blast. Lack of centromere-specific DNA sequence motifs or repetitive elements suggests an epigenetic specification of centromere function in M. oryzae. PacBio genome assemblies and synteny analyses facilitated comparison of the centromeric/pericentromeric regions in distinct isolates of rice blast and wheat blast and in Magnaporthiopsis poae. Overall, this study revealed unusual centromere dynamics and precisely identified the centromere loci in the top model fungal pathogens that belong to Magnaporthales and cause severe losses in the global production of food crops and turf grasses. IMPORTANCE Magnaporthe oryzae is an important fungal pathogen that causes a loss of 10% to 30% of the annual rice crop due to the devastating blast disease. In most organisms, kinetochores are clustered together or arranged at the metaphase plate to facilitate synchronized anaphase separation of sister chromatids in mitosis. In this study, we showed that the initially clustered kinetochores separate and position randomly prior to anaphase in M. oryzae. Centromeres in M. oryzae occupy large genomic regions and form on AT-rich DNA without any common sequence motifs. Overall, this study identified atypical kinetochore dynamics and mapped functional centromeres in M. oryzae to define the roles of centromeric and pericentric boundaries in kinetochore assembly on epigenetically specified centromere loci. This study should pave the way for further understanding of the contribution of heterochromatin in genome stability and virulence of the blast fungus and its related species of high economic importance.

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