Loss of Function of a Proline-Containing Protein Confers Durable Disease Resistance in Rice

Fukuoka, Shuichi; Saka, Norikuni; Koga, Hironori; Ono, Kiyomi; Shimizu, Takehiko; Ebana, Kaworu; Hayashi, Nagao; Takahashi, Akira; Hirochika, Hirohiko; Okuno, Kazutoshi; Yano, Masahiro

doi:10.1126/science.1175550

Cited by 565 publications

(467 citation statements)

References 18 publications

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“…We did not observe the involvement of OsBBI1 in disease resistance against bacterial blight, indicating that OsBBI1-mediated resistance is likely specific to defence against blast fungus, consistent with its induction by BTH and M. oryzae but not by Xoo. In rice, several R genes/loci such as Pi5, Pi9, Pi21, Pi33, Pi39(t), and Pi40(t), have been identified to confer broad-spectrum blast resistance [9,10,[48][49][50][51]. However, molecular mechanisms by which these R genes provide broad-spectrum resistance remain elusive.…”

Section: Discussionmentioning

confidence: 99%

“…This indicates that OsBBI1 may mediate non-race-specific basal resistance against M. oryzae in rice, and is probably involved in an unrecognized PTI network. Some blast resistance QTLs have been identified in rice and some have been characterized [7,10,26]. The OsBBI1 gene (Os06g03580) is located in a region of chromosome 6, in which a number of blast resistance QTLs have been identified [52][53][54][55].…”

Section: Discussionmentioning

confidence: 99%

“…The recognition of M. oryzae-secreted effector protein Avr-Pita by the R protein Pita inside the rice cell could activate innate immune response [8]. Two R genes, Pi9 and Pi21, confer broad-spectrum resistance against multiple races of M. oryzae [9,10]. Rac GTPasemediated events (e.g., generation of ROS), activation of MAP kinase, and other key components, such as RAR1, SGT1, Hsp90, and WRKY45, play important roles in regulating the immune response against M. oryzae [11][12][13][14][15][16][17][18][19][20][21][22][23][24].…”

Section: Introductionmentioning

confidence: 99%

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Rice RING protein OsBBI1 with E3 ligase activity confers broad-spectrum resistance against Magnaporthe oryzae by modifying the cell wall defence

Zhong

et al. 2011

Cell Res

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Emerging evidence suggests that E3 ligases play critical roles in diverse biological processes, including innate immune responses in plants. However, the mechanism of the E3 ligase involvement in plant innate immunity is unclear. We report that a rice gene, OsBBI1, encoding a RING finger protein with E3 ligase activity, mediates broad-spectrum disease resistance. The expression of OsBBI1 was induced by rice blast fungus Magnaporthe oryzae, as well as chemical inducers, benzothiadiazole and salicylic acid. Biochemical analysis revealed that OsBBI1 protein possesses E3 ubiquitin ligase activity in vitro. Genetic analysis revealed that the loss of OsBBI1 function in a Tos17-insertion line increased susceptibility, while the overexpression of OsBBI1 in transgenic plants conferred enhanced resistance to multiple races of M. oryzae. This indicates that OsBBI1 modulates broad-spectrum resistance against the blast fungus. The OsBBI1-overexpressing plants showed higher levels of H 2 O 2 accumulation in cells and higher levels of phenolic compounds and cross-linking of proteins in cell walls at infection sites by M. oryzae compared with wild-type (WT) plants. The cell walls were thicker in the OsBBI1-overexpressing plants and thinner in the mutant plants than in the WT plants. Our results suggest that OsBBI1 modulates broad-spectrum resistance to blast fungus by modifying cell wall defence responses. The functional characterization of OsBBI1 provides insight into the E3 ligase-mediated innate immunity, and a practical tool for constructing broad-spectrum resistance against the most destructive disease in rice.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Rice RING protein OsBBI1 with E3 ligase activity confers broad-spectrum resistance against Magnaporthe oryzae by modifying the cell wall defence

Zhong

et al. 2011

Cell Res

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“…This finding suggested that numerous rare alleles might not be captured in the core collection. In recent decades, many elite genes or alleles have been discovered from landraces and utilized in rice breeding, including the semi-dwarf genes (Monna et al, 2002;Sasaki et al, 2002), resistant/tolerant genes to diseases and pests, and genes for improving grain yield and quality (Fukuoka et al, 2009;Ishimaru et al, 2013). It is likely, therefore, that three minor groups of rice germplasm (aus, aromatic and rayada) that have a limited presence in Chinese germplasm may be important genetic resources for future rice genetics and breeding in China given their unique genetic and phenotypic characteristics (Glaszmann, 1987;Khush, 1997).…”

Section: Diversity and Differentiation Of Chinese Rice Cultivarsmentioning

confidence: 99%

Genetic diversity and classification of Oryza sativa with emphasis on Chinese rice germplasm

et al. 2013

Heredity

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Despite extensive studies on cultivated rice, the genetic structure and subdivision of this crop remain unclear at both global and local scales. Using 84 nuclear simple sequence repeat markers, we genotyped a panel of 153 global rice cultivars covering all previously recognized groups and 826 cultivars representing the diversity of Chinese rice germplasm. On the basis of modelbased grouping, neighbour-joining tree and principal coordinate analysis, we confirmed the widely accepted five major groups of rice cultivars (indica, aus, aromatic, temperate japonica and tropical japonica), and demonstrated that rayada rice was unique in genealogy and should be treated as a new (the sixth) major group of rice germplasm. With reference to the global classification of rice cultivars, we identified three major groups (indica, temperate japonica and tropical japonica) in Chinese rice germplasm and showed that Chinese temperate japonica contained higher diversity than that of global samples, whereas Chinese indica and tropical japonica maintained slightly lower diversity than that present in the global samples. Particularly, we observed that all seasonal, drought-tolerant and endosperm types occurred within each of three major groups of Chinese cultivars, which does not support previous claims that seasonal differentiation exists in Indica and drought-tolerant differentiation is present in Japonica. It is most likely that differentiation of cultivar types arose multiple times stemming from artificial selection for adaptation to local environments.

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“…Some effectors are recognized by intracellular receptors, termed R proteins, to trigger race-specific resistance that contributes to the postinvasive resistance. In the past decades, 21 rice blast R genes have been characterized by molecular cloning, 19 of which encode NBS-LRR proteins, while Pyricularia-Digu2 (Pi-d2) and Pi21 encode a receptor-like kinase protein and a Pro-rich protein, respectively (Fukuoka et al, 2009;Liu et al, 2010Liu et al, , 2013. The Pyricularia-Kanto51-m (Pikm) locus contains two NBS-LRR genes, Pi k-m1-Tsuyuake (Pikm1-TS) and Pikm2-TS, both required to recognize the cognate effector Avr-Pikm to trigger effective resistance to the blast disease (Li et al, 2007;Yoshida et al, 2009).…”

mentioning

confidence: 99%

Multiple Rice MicroRNAs Are Involved in Immunity against the Blast Fungus Magnaporthe oryzae

et al. 2013

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MicroRNAs (miRNAs) are indispensable regulators for development and defense in eukaryotes. However, the miRNA species have not been explored for rice (Oryza sativa) immunity against the blast fungus Magnaporthe oryzae, the most devastating fungal pathogen in rice production worldwide. Here, by deep sequencing small RNA libraries from susceptible and resistant lines in normal conditions and upon M. oryzae infection, we identified a group of known rice miRNAs that were differentially expressed upon M. oryzae infection. They were further classified into three classes based on their expression patterns in the susceptible japonica line Lijiangxin Tuan Hegu and in the resistant line International Rice Blast Line Pyricularia-Kanto51-m-Tsuyuake that contains a single resistance gene locus, Pyricularia-Kanto 51-m (Pikm), within the Lijiangxin Tuan Hegu background. RNA-blot assay of nine of them confirmed sequencing results. Real-time reverse transcription-polymerase chain reaction assay showed that the expression of some target genes was negatively correlated with the expression of miRNAs. Moreover, transgenic rice plants overexpressing miR160a and miR398b displayed enhanced resistance to M. oryzae, as demonstrated by decreased fungal growth, increased hydrogen peroxide accumulation at the infection site, and up-regulated expression of defense-related genes. Taken together, our data indicate that miRNAs are involved in rice immunity against M. oryzae and that overexpression of miR160a or miR398b can enhance rice resistance to the disease.

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Loss of Function of a Proline-Containing Protein Confers Durable Disease Resistance in Rice

Cited by 565 publications

References 18 publications

Rice RING protein OsBBI1 with E3 ligase activity confers broad-spectrum resistance against Magnaporthe oryzae by modifying the cell wall defence

Rice RING protein OsBBI1 with E3 ligase activity confers broad-spectrum resistance against Magnaporthe oryzae by modifying the cell wall defence

Genetic diversity and classification of Oryza sativa with emphasis on Chinese rice germplasm

Multiple Rice MicroRNAs Are Involved in Immunity against the Blast Fungus Magnaporthe oryzae

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