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Global genome and transcriptome analyses of Magnaporthe oryzae epidemic isolate 98-06 uncover novel effectors and pathogenicity-related genes, revealing gene gain and lose dynamics in genome evolution.

Dong Y, Li Y, Zhao M, Jing M, Liu X, Liu M, Guo X, Zhang X, Chen Y, Liu Y, Liu Y, Ye W, Zhang H, Wang Y, Zheng X, Wang P, Zhang Z - PLoS Pathog. (2015)

Bottom Line: A unique 1.4 Mb of genomic sequences was found in isolate 98-06 in comparison to reference strain 70-15.In addition, 134 candidate effectors with various segregation patterns were identified.Characterization of isolate-specific effector candidates Iug6 and Iug9 and PaR candidate Iug18 revealed that they have a role in fungal propagation and pathogenicity.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Nanjing, China; Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, China.

ABSTRACT
Genome dynamics of pathogenic organisms are driven by pathogen and host co-evolution, in which pathogen genomes are shaped to overcome stresses imposed by hosts with various genetic backgrounds through generation of a variety of isolates. This same principle applies to the rice blast pathogen Magnaporthe oryzae and the rice host; however, genetic variations among different isolates of M. oryzae remain largely unknown, particularly at genome and transcriptome levels. Here, we applied genomic and transcriptomic analytical tools to investigate M. oryzae isolate 98-06 that is the most aggressive in infection of susceptible rice cultivars. A unique 1.4 Mb of genomic sequences was found in isolate 98-06 in comparison to reference strain 70-15. Genome-wide expression profiling revealed the presence of two critical expression patterns of M. oryzae based on 64 known pathogenicity-related (PaR) genes. In addition, 134 candidate effectors with various segregation patterns were identified. Five tested proteins could suppress BAX-mediated programmed cell death in Nicotiana benthamiana leaves. Characterization of isolate-specific effector candidates Iug6 and Iug9 and PaR candidate Iug18 revealed that they have a role in fungal propagation and pathogenicity. Moreover, Iug6 and Iug9 are located exclusively in the biotrophic interfacial complex (BIC) and their overexpression leads to suppression of defense-related gene expression in rice, suggesting that they might participate in biotrophy by inhibiting the SA and ET pathways within the host. Thus, our studies identify novel effector and PaR proteins involved in pathogenicity of the highly aggressive M. oryzae field isolate 98-06, and reveal molecular and genomic dynamics in the evolution of M. oryzae and rice host interactions.

No MeSH data available.


Related in: MedlinePlus

Over-expression of IUG6 or IUG9 in Guy11 suppresses defense-related genes in rice.(A) qRT-PCR on IUG6 or IUG9 at different fungal developmental stages in Guy11 overexpression transformants in comparison with mycelium phase of isolate 98–06. RNA was extracted from mycelia and infectious stages (8, 24, and 48 hpi), respectively. (B) Expression of PR1a and Cht1 marker genes in the infected rice is suppressed in the presence of Iug6 or Iug9. RNA samples were collected from rice plants (O. sativa cv CO-39) 0, 24, and 48 h after inoculation with the Guy11, 98–06, or OE strains. The average threshold cycle (Ct) of triplicate reactions was normalized by the stable expressions ACTIN gene in O. sativa. Three independent biological experiments were performed and yielded similar results. Error bars in the figure represent the standard deviation.
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ppat.1004801.g010: Over-expression of IUG6 or IUG9 in Guy11 suppresses defense-related genes in rice.(A) qRT-PCR on IUG6 or IUG9 at different fungal developmental stages in Guy11 overexpression transformants in comparison with mycelium phase of isolate 98–06. RNA was extracted from mycelia and infectious stages (8, 24, and 48 hpi), respectively. (B) Expression of PR1a and Cht1 marker genes in the infected rice is suppressed in the presence of Iug6 or Iug9. RNA samples were collected from rice plants (O. sativa cv CO-39) 0, 24, and 48 h after inoculation with the Guy11, 98–06, or OE strains. The average threshold cycle (Ct) of triplicate reactions was normalized by the stable expressions ACTIN gene in O. sativa. Three independent biological experiments were performed and yielded similar results. Error bars in the figure represent the standard deviation.

Mentions: As Iug6 and Iug9 can suppress the BAX-mediated programmed cell death in tobacco leaves, we investigated whether their expression affects the transcription of the rice defense-related genes. When infected with Guy11 over-expressing IUG6 and IUG9, the pathogenicity of these transformants is not obviously improved, but the expression of PR1a and Cht1 in rice was significantly less than that caused by Guy11 following qRT-PCR analysis (Fig 10B). Similarly, the expression levels of PR1a and Cht1 in rice by infection with isolate 98–06 were also significantly lower than that infected with Guy11 at 24 hpi or 8 hpi, with delayed peak expression. The expression patterns of PR1a and Cht1 in rice when infected with isolates over-expressing IUG6 or IUG9 is similar to that by isolate 98–06, with somewhat lowered peak expression. PR1a and Cht1 are respective SA and ET signaling marker genes. SA is involved in establishing basal defenses, effector-triggered immunity, and systemic acquired resistance in many dicotyledonous species [50,51], as well as in modulating redox balance and protecting rice plants from the oxidative stress caused by M. oryzae [52]. Our above interaction transcriptome analysis also suggested that SA and ET signaling pathways might function positively on rice basal defense against M. oryzae. We hypothesized that Iug6 and Iug9 might target unknown factors in rice, leading to suppression of the SA and ET signaling and promotion of biotrophy.


Global genome and transcriptome analyses of Magnaporthe oryzae epidemic isolate 98-06 uncover novel effectors and pathogenicity-related genes, revealing gene gain and lose dynamics in genome evolution.

Dong Y, Li Y, Zhao M, Jing M, Liu X, Liu M, Guo X, Zhang X, Chen Y, Liu Y, Liu Y, Ye W, Zhang H, Wang Y, Zheng X, Wang P, Zhang Z - PLoS Pathog. (2015)

Over-expression of IUG6 or IUG9 in Guy11 suppresses defense-related genes in rice.(A) qRT-PCR on IUG6 or IUG9 at different fungal developmental stages in Guy11 overexpression transformants in comparison with mycelium phase of isolate 98–06. RNA was extracted from mycelia and infectious stages (8, 24, and 48 hpi), respectively. (B) Expression of PR1a and Cht1 marker genes in the infected rice is suppressed in the presence of Iug6 or Iug9. RNA samples were collected from rice plants (O. sativa cv CO-39) 0, 24, and 48 h after inoculation with the Guy11, 98–06, or OE strains. The average threshold cycle (Ct) of triplicate reactions was normalized by the stable expressions ACTIN gene in O. sativa. Three independent biological experiments were performed and yielded similar results. Error bars in the figure represent the standard deviation.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4383609&req=5

ppat.1004801.g010: Over-expression of IUG6 or IUG9 in Guy11 suppresses defense-related genes in rice.(A) qRT-PCR on IUG6 or IUG9 at different fungal developmental stages in Guy11 overexpression transformants in comparison with mycelium phase of isolate 98–06. RNA was extracted from mycelia and infectious stages (8, 24, and 48 hpi), respectively. (B) Expression of PR1a and Cht1 marker genes in the infected rice is suppressed in the presence of Iug6 or Iug9. RNA samples were collected from rice plants (O. sativa cv CO-39) 0, 24, and 48 h after inoculation with the Guy11, 98–06, or OE strains. The average threshold cycle (Ct) of triplicate reactions was normalized by the stable expressions ACTIN gene in O. sativa. Three independent biological experiments were performed and yielded similar results. Error bars in the figure represent the standard deviation.
Mentions: As Iug6 and Iug9 can suppress the BAX-mediated programmed cell death in tobacco leaves, we investigated whether their expression affects the transcription of the rice defense-related genes. When infected with Guy11 over-expressing IUG6 and IUG9, the pathogenicity of these transformants is not obviously improved, but the expression of PR1a and Cht1 in rice was significantly less than that caused by Guy11 following qRT-PCR analysis (Fig 10B). Similarly, the expression levels of PR1a and Cht1 in rice by infection with isolate 98–06 were also significantly lower than that infected with Guy11 at 24 hpi or 8 hpi, with delayed peak expression. The expression patterns of PR1a and Cht1 in rice when infected with isolates over-expressing IUG6 or IUG9 is similar to that by isolate 98–06, with somewhat lowered peak expression. PR1a and Cht1 are respective SA and ET signaling marker genes. SA is involved in establishing basal defenses, effector-triggered immunity, and systemic acquired resistance in many dicotyledonous species [50,51], as well as in modulating redox balance and protecting rice plants from the oxidative stress caused by M. oryzae [52]. Our above interaction transcriptome analysis also suggested that SA and ET signaling pathways might function positively on rice basal defense against M. oryzae. We hypothesized that Iug6 and Iug9 might target unknown factors in rice, leading to suppression of the SA and ET signaling and promotion of biotrophy.

Bottom Line: A unique 1.4 Mb of genomic sequences was found in isolate 98-06 in comparison to reference strain 70-15.In addition, 134 candidate effectors with various segregation patterns were identified.Characterization of isolate-specific effector candidates Iug6 and Iug9 and PaR candidate Iug18 revealed that they have a role in fungal propagation and pathogenicity.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Pathology, College of Plant Protection, Nanjing Agricultural University, Nanjing, China; Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing, China.

ABSTRACT
Genome dynamics of pathogenic organisms are driven by pathogen and host co-evolution, in which pathogen genomes are shaped to overcome stresses imposed by hosts with various genetic backgrounds through generation of a variety of isolates. This same principle applies to the rice blast pathogen Magnaporthe oryzae and the rice host; however, genetic variations among different isolates of M. oryzae remain largely unknown, particularly at genome and transcriptome levels. Here, we applied genomic and transcriptomic analytical tools to investigate M. oryzae isolate 98-06 that is the most aggressive in infection of susceptible rice cultivars. A unique 1.4 Mb of genomic sequences was found in isolate 98-06 in comparison to reference strain 70-15. Genome-wide expression profiling revealed the presence of two critical expression patterns of M. oryzae based on 64 known pathogenicity-related (PaR) genes. In addition, 134 candidate effectors with various segregation patterns were identified. Five tested proteins could suppress BAX-mediated programmed cell death in Nicotiana benthamiana leaves. Characterization of isolate-specific effector candidates Iug6 and Iug9 and PaR candidate Iug18 revealed that they have a role in fungal propagation and pathogenicity. Moreover, Iug6 and Iug9 are located exclusively in the biotrophic interfacial complex (BIC) and their overexpression leads to suppression of defense-related gene expression in rice, suggesting that they might participate in biotrophy by inhibiting the SA and ET pathways within the host. Thus, our studies identify novel effector and PaR proteins involved in pathogenicity of the highly aggressive M. oryzae field isolate 98-06, and reveal molecular and genomic dynamics in the evolution of M. oryzae and rice host interactions.

No MeSH data available.


Related in: MedlinePlus