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Natural variation in the expression and catalytic activity of a naringenin 7-O-methyltransferase influences antifungal defenses in diverse rice cultivars.
Plant J 2019PJ

Abstract

Phytoalexins play a pivotal role in plant-pathogen interactions. Whereas leaves of rice (Oryza sativa) cultivar Nipponbare predominantly accumulated the phytoalexin sakuranetin after jasmonic acid induction, only very low amounts accumulated in the Kasalath cultivar. Sakuranetin is synthesized from naringenin by naringenin 7-O-methyltransferase (NOMT). Analysis of chromosome segment substitution lines and backcrossed inbred lines suggested that NOMT is the underlying cause of differential phytoalexin accumulation between Nipponbare and Kasalath. Indeed, both NOMT expression and NOMT enzymatic activity are lower in Kasalath than in Nipponbare. We identified a proline to threonine substitution in Kasalath relative to Nipponbare NOMT as the main cause of the lower enzymatic activity. Expanding this analysis to rice cultivars with varying amounts of sakuranetin collected from around the world showed that NOMT induction is correlated with sakuranetin accumulation. In bioassays with Pyricularia oryzae, Gibberella fujikuroi, Bipolaris oryzae, Burkholderia glumae, Xanthomonas oryzae, Erwinia chyrysanthemi, Pseudomonas syringae, and Acidovorax avenae, naringenin was more effective against bacterial pathogens and sakuranetin was more effective against fungal pathogens. Thus, the relative amounts of naringenin and sakuranetin may provide protection against specific pathogen profiles in different rice-growing environments. In a dendrogram of NOMT genes, those from low sakuranetin-accumulating cultivars formed at least two clusters, only one of which involves the proline to threonine mutation, suggesting that the low sakuranetin chemotype was acquired more than once in cultivated rice. Strains of the wild rice species Oryza rufipogon also exhibited differential sakuranetin accumulation, indicating that this metabolic diversity predates rice domestication.

Authors+Show Affiliations

Graduate School of Sustainability Science, Tottori University, Tottori, 680-8553, Japan.Graduate School of Agriculture, Tottori University, Tottori, 680-8553, Japan.Faculty of Agriculture, Tottori University, Tottori, 680-8553, Japan.Graduate School of Agriculture, Kyoto University, Kitashirakawa Oiwake-Cho, Kyoto, 606-8502, Japan.The United Graduate School of Agricultural Sciences, Tottori University, Tottori, 680-8553, Japan.Faculty of Agriculture, Tottori University, Tottori, 680-8553, Japan.Faculty of Life and Environmental Science, Shimane University, Nishikawatsu 1060, Matsue, 690-8504, Japan.Faculty of Agriculture, Tottori University, Tottori, 680-8553, Japan.Graduate School of Agriculture, Kyoto University, Kitashirakawa Oiwake-Cho, Kyoto, 606-8502, Japan.Boyce Thompson Institute for Plant Research, Ithaca, New York, 14853, USA.Boyce Thompson Institute for Plant Research, Ithaca, New York, 14853, USA.Graduate School of Agriculture, Kyoto University, Kitashirakawa Oiwake-Cho, Kyoto, 606-8502, Japan.Graduate School of Agriculture, Kyoto University, Kitashirakawa Oiwake-Cho, Kyoto, 606-8502, Japan.Faculty of Agriculture, Tottori University, Tottori, 680-8553, Japan.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

31630460

Citation

Murata, Koichi, et al. "Natural Variation in the Expression and Catalytic Activity of a Naringenin 7-O-methyltransferase Influences Antifungal Defenses in Diverse Rice Cultivars." The Plant Journal : for Cell and Molecular Biology, 2019.
Murata K, Kitano T, Yoshimoto R, et al. Natural variation in the expression and catalytic activity of a naringenin 7-O-methyltransferase influences antifungal defenses in diverse rice cultivars. Plant J. 2019.
Murata, K., Kitano, T., Yoshimoto, R., Takata, R., Ube, N., Ueno, K., ... Ishihara, A. (2019). Natural variation in the expression and catalytic activity of a naringenin 7-O-methyltransferase influences antifungal defenses in diverse rice cultivars. The Plant Journal : for Cell and Molecular Biology, doi:10.1111/tpj.14577.
Murata K, et al. Natural Variation in the Expression and Catalytic Activity of a Naringenin 7-O-methyltransferase Influences Antifungal Defenses in Diverse Rice Cultivars. Plant J. 2019 Oct 20; PubMed PMID: 31630460.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Natural variation in the expression and catalytic activity of a naringenin 7-O-methyltransferase influences antifungal defenses in diverse rice cultivars. AU - Murata,Koichi, AU - Kitano,Takashige, AU - Yoshimoto,Riko, AU - Takata,Ryo, AU - Ube,Naoki, AU - Ueno,Kotomi, AU - Ueno,Makoto, AU - Yabuta,Yukinori, AU - Teraishi,Masayoshi, AU - Holland,Cynthia K, AU - Jander,Georg, AU - Okumoto,Yutaka, AU - Mori,Naoki, AU - Ishihara,Atsushi, Y1 - 2019/10/20/ PY - 2019/10/21/pubmed PY - 2019/10/21/medline PY - 2019/10/21/entrez KW - Oryza rufipogon KW - Oryza sativa KW - chemodiversity KW - chemotype KW - naringenin KW - naringenin-7-O-methyltransferase KW - phytoalexin KW - rice KW - sakuranetin JF - The Plant journal : for cell and molecular biology JO - Plant J. N2 - Phytoalexins play a pivotal role in plant-pathogen interactions. Whereas leaves of rice (Oryza sativa) cultivar Nipponbare predominantly accumulated the phytoalexin sakuranetin after jasmonic acid induction, only very low amounts accumulated in the Kasalath cultivar. Sakuranetin is synthesized from naringenin by naringenin 7-O-methyltransferase (NOMT). Analysis of chromosome segment substitution lines and backcrossed inbred lines suggested that NOMT is the underlying cause of differential phytoalexin accumulation between Nipponbare and Kasalath. Indeed, both NOMT expression and NOMT enzymatic activity are lower in Kasalath than in Nipponbare. We identified a proline to threonine substitution in Kasalath relative to Nipponbare NOMT as the main cause of the lower enzymatic activity. Expanding this analysis to rice cultivars with varying amounts of sakuranetin collected from around the world showed that NOMT induction is correlated with sakuranetin accumulation. In bioassays with Pyricularia oryzae, Gibberella fujikuroi, Bipolaris oryzae, Burkholderia glumae, Xanthomonas oryzae, Erwinia chyrysanthemi, Pseudomonas syringae, and Acidovorax avenae, naringenin was more effective against bacterial pathogens and sakuranetin was more effective against fungal pathogens. Thus, the relative amounts of naringenin and sakuranetin may provide protection against specific pathogen profiles in different rice-growing environments. In a dendrogram of NOMT genes, those from low sakuranetin-accumulating cultivars formed at least two clusters, only one of which involves the proline to threonine mutation, suggesting that the low sakuranetin chemotype was acquired more than once in cultivated rice. Strains of the wild rice species Oryza rufipogon also exhibited differential sakuranetin accumulation, indicating that this metabolic diversity predates rice domestication. SN - 1365-313X UR - https://www.unboundmedicine.com/medline/citation/31630460/Natural_variation_in_the_expression_and_catalytic_activity_of_a_naringenin_7-O-methyltransferase_influences_antifungal_defenses_in_diverse_rice_cultivars L2 - https://doi.org/10.1111/tpj.14577 DB - PRIME DP - Unbound Medicine ER -