Transcriptome Profiling of the Rice Blast Fungus <i>Magnaporthe oryzae</i> and Its Host <i>Oryza sativa</i> During Infection

Jeon, Jongbum; Lee, Gir-Won; Kim, Ki-Tae; Park, Sook‐Young; Kim, Seongbeom; Kwon, Seomun; Huh, Aram; Chung, Hyun‐Jung; Lee, Da-Young; Kim, Chi-Yeol; Lee, Yong-Hwan

doi:10.1094/mpmi-07-19-0207-a

Cited by 37 publications

(50 citation statements)

References 20 publications

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“…Although the expression level of EFC genes increased during infection in both plants, the degree of induction in KJ201 appeared much higher than that in MoT isolate (Figure 7). However, additional experiments with more biological repeats and under identical environmental conditions are needed to validate this observation because the transcriptome data for KJ201 were obtained via rice sheath assay to enrich the quantity of fungal RNAs (Jeon et al, 2019), while the data from wheat plants were obtained samples collected in the field (Saunders et al, 2017). We also determined whether the presence of TEs in flanking regions of the EFC genes affect their expression, as some TEs have been suggested to affect the expression of EFC genes in other pathogens (Whisson et al, 2012).…”

Section: Discussionmentioning

confidence: 99%

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Evolution of the Genes Encoding Effector Candidates Within Multiple Pathotypes of Magnaporthe oryzae

Kim

Song

et al. 2019

Front. Microbiol.

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Magnaporthe oryzae infects rice, wheat, and many grass species in the Poaceae family by secreting protein effectors. Here, we analyzed the distribution, sequence variation, and genomic context of effector candidate (EFC) genes in 31 isolates that represent five pathotypes of M. oryzae, three isolates of M. grisea, a sister species of M. oryzae, and one strain each for eight species in the family Magnaporthaceae to investigate how the host range expansion of M. oryzae has likely affected the evolution of effectors. We used the EFC genes of M. oryzae strain 70-15, whose genome has served as a reference for many comparative genomics analyses, to identify their homologs in these strains. We also analyzed the previously characterized avirulence (AVR) genes and single-copy orthologous (SCO) genes in these strains, which showed that the EFC and AVR genes evolved faster than the SCO genes. The EFC and AVR repertoires among M. oryzae pathotypes varied widely probably because adaptation to individual hosts exerted different types of selection pressure. Repetitive DNA elements appeared to have caused the variation of some EFC genes. Lastly, we analyzed expression patterns of the AVR and EFC genes to test the hypothesis that such genes are preferentially expressed during host infection. This comprehensive dataset serves as a foundation for future studies on the genetic basis of the evolution and host specialization in M. oryzae.

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Section: Discussionmentioning

confidence: 99%

“…We analyzed transcriptome data from MoO isolate KJ201 (Jeon et al, 2019) and Bangladesh MoT isolate 12, a strain closely related to BR32 (Saunders et al, 2017). The data for KJ201 covered the mycelial stage in culture and the host infection stage at multiple time points [18, 27, 36, 45, and 72 h post-inoculation (hpi)].…”

Section: Methodsmentioning

confidence: 99%

Evolution of the Genes Encoding Effector Candidates Within Multiple Pathotypes of Magnaporthe oryzae

Kim

Song

et al. 2019

Front. Microbiol.

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“…We analyzed how the MoHTR genes are expressed during vegetative growth and in infected rice sheaths at the pre-penetration (18 hours post inoculation, hpi), biotrophic (27 and 36 hpi), transition (45 hpi), and necrotrophic (72 hpi) stages using available RNA-seq data 17 . Eleven genes were highly expressed during the biotrophic or transition stage, with their log 2 (FPKM+1) being ≥ 4.…”

Section: Resultsmentioning

confidence: 99%

“…We collected 1-kb upstream sequences from the coding region of all rice genes from the Rice Annotation Project Database (RAP-DB) 38 and checked the presence of each EBE. Differentially expressed genes (DEGs) at 36 hpi (biotrophic stage) were identified using transcriptome data generated from infected rice sheaths 17 . Gene ontology (GO) enrichment analysis was performed using RiceNetDB 25 .…”

Section: Methodsmentioning

confidence: 99%

Two nuclear effectors of the rice blast fungus modulate host immunity via transcriptional reprogramming

Kim

Park

et al. 2020

Nat Commun

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Pathogens utilize multiple types of effectors to modulate plant immunity. Although many apoplastic and cytoplasmic effectors have been reported, nuclear effectors have not been well characterized in fungal pathogens. Here, we characterize two nuclear effectors of the rice blast pathogen Magnaporthe oryzae. Both nuclear effectors are secreted via the biotrophic interfacial complex, translocated into the nuclei of initially penetrated and surrounding cells, and reprogram the expression of immunity-associated genes by binding on effector binding elements in rice. Their expression in transgenic rice causes ambivalent immunity: increased susceptibility to M. oryzae and Xanthomonas oryzae pv. oryzae, hemibiotrophic pathogens, but enhanced resistance to Cochliobolus miyabeanus, a necrotrophic pathogen. Our findings help remedy a significant knowledge deficiency in the mechanism of M. oryzae–rice interactions and underscore how effector-mediated manipulation of plant immunity by one pathogen may also affect the disease severity by other pathogens.

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“…Rice blast, caused by M. oryzae, is the most devastating disease of rice and threatens food security worldwide. In M. oryzae-rice interaction, the majority of the effectors are kept transcriptional silencing or expressed relatively low in the vegetative growth stage (Dong et al, 2015, Sharpee et al, 2017, Jeon et al, 2020, but are derepressed during invasive growth stage (Dong et al, 2015, Jeon et al, 2020. During preparing our manuscript, a really good study found that H3K27 dynamics associate with altered transcription of in planta induced genes in M. oryzae (Zhang et al, 2021).…”

Section: Introductionmentioning

confidence: 99%

Polycomb repressive complex 2 coordinates with Sin3 histone deacetylase complex to epigenetically reprogram genome-wide expression ofeffectorsand regulate pathogenicity inMagnaporthe oryzae

Qiu

Shi

et al. 2021

Preprint

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The strict suppression and reprogramming of gene expression are necessary at different development stages and/or in response to environment stimuli in eukaryotes. In Rice Magnaporthe oryzae pathosystem, effectors from pathogen are kept transcriptionally silenced in the vegetative growth stage and are highly expressed during invasive growth stage to adapt to the host environment. However, the mechanism of how such effectors are stably repressed in the vegetative stage and its roles during rice blast infection remain unclear so far. Here, we showed that all subunits of Polycomb Repressive Complex 2 are required for such repression by direct H3K27me3 occupancy and pathogenic process in M. oryzae. Suppression of polycomb-mediated H3K27me3 causes an improper induction of effectors during vegetative growth thus simulating a host environment. Notably, the addition subunit P55 not only acts as the bridge to connect with core subunits to form a complex in M. oryzae, but also recruits Sin3 histone deacetylase complex to prompt H3K27me3 occupancy for stable maintenance of transcriptional silencing of the target genes in the absence of PRC1. In contrast, during invasive growth stage, the repressed state of effectors chromatin can be partially erased during pathogenic development resulting in transcriptional activation of effectors therein. Overall, Polycomb repressive complex 2 coordinates with Sin3 histone deacetylase complex to epigenetically reprogram genome-wide expression of effectors, which act as molecular switch to memorize the host environment from vegetative to invasive growth, thus contributing to the infection of rice blast.

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Transcriptome Profiling of the Rice Blast Fungus Magnaporthe oryzae and Its Host Oryza sativa During Infection

Cited by 37 publications

References 20 publications

Evolution of the Genes Encoding Effector Candidates Within Multiple Pathotypes of Magnaporthe oryzae

Evolution of the Genes Encoding Effector Candidates Within Multiple Pathotypes of Magnaporthe oryzae

Two nuclear effectors of the rice blast fungus modulate host immunity via transcriptional reprogramming

Polycomb repressive complex 2 coordinates with Sin3 histone deacetylase complex to epigenetically reprogram genome-wide expression ofeffectorsand regulate pathogenicity inMagnaporthe oryzae

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