Natural variation in the expression and catalytic activity of a naringenin 7‐O‐methyltransferase influences antifungal defenses in diverse rice cultivars

Summary 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 synthesiz...

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Published in:	The Plant journal : for cell and molecular biology Vol. 101; no. 5; pp. 1103 - 1117
Main Authors:	Murata, Koichi, Kitano, Takashige, Yoshimoto, Riko, Takata, Ryo, Ube, Naoki, Ueno, Kotomi, Ueno, Makoto, Yabuta, Yukinori, Teraishi, Masayoshi, Holland, Cynthia K., Jander, Georg, Okumoto, Yutaka, Mori, Naoki, Ishihara, Atsushi
Format:	Journal Article
Language:	English
Published:	England Blackwell Publishing Ltd 01-03-2020
Subjects:	Accumulation Antifungal activity Antifungal Agents - pharmacology Ascomycota - drug effects Bioassays Burkholderia - drug effects Catalytic activity chemodiversity chemotype Chromosomes Comamonadaceae - drug effects Cultivars Cultivation Cyclopentanes - metabolism Domestication Enzymatic activity Flavanones - metabolism Flavonoids - metabolism Fungicides Fusarium - drug effects Genetic Variation Grain cultivation Inbreeding Jasmonic acid Methyltransferase Methyltransferases - genetics Methyltransferases - metabolism Mutation Naringenin naringenin‐7‐O‐methyltransferase Oryza - enzymology Oryza - genetics Oryza - immunology Oryza - microbiology Oryza rufipogon Oryza sativa Oxylipins - metabolism Pathogens phytoalexin Phytoalexins Plant Diseases - immunology Plant Diseases - microbiology Proline Rice sakuranetin Substitutes Threonine Xanthomonas - drug effects naringenin Oryza sativa chemotype sakuranetin naringenin-7-O-methyltransferase rice Oryza rufipogon chemodiversity phytoalexin
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Summary:	Summary 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 chrysanthemi, Pseudomonas syringae, and Acidovorax avenae, naringenin was more effective against bacterial pathogens and sakuranetin was more effective against fungal pathogens. Therefore, 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. Significance Statement Although phytoalexin accumulation plays an important role in plant–pathogen interactions, there has been insufficient investigation of within‐species chemodiversity. We found that variation in naringenin O‐methyltransferase, a sakuranetin biosynthetic enzyme, strongly influences the relative abundance of two flavonoid phytoalexins, sakuranetin and its precursor naringenin, in rice. This phytochemical diversity, which is present in both cultivated and wild rice, provides insight into the evolution of plant defenses and may influence susceptibility to bacterial and fungal pathogens.
ISSN:	0960-7412 1365-313X
DOI:	10.1111/tpj.14577