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

Abstract

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.

Tangeretin inhibits fungal ferroptosis to suppress rice blast

“…Of these pathways, most of the enzymes involved in phenylpropanoid biosynthesis (osa00940), which act upstream of the flavonoid pathway, were present in the rice genome. We also identified the enzymes involved in flavonoid biosynthesis (osa00941), catalyzing the production of sakuranetin and apigenin, and their precursor naringenin (Figure S7, pink color highlighted), consistent with the reported isolation of these important flavonoids in rice (Tamogami et al, 1997; Ghasemzadeh et al, 2018; Ma et al, 2019; Murata et al, 2020). That the rice genome harbors orthologous genes for flavonoid biosynthesis (Figure S7, green color highlighted) suggests that the corresponding flavonoids may accumulate in this species, although only a few have been biochemically identified to date.…”

“…However, the use of natural flavonoids to protect crops against pathogenic microorganisms has been limited (Kariu et al, 2017; Paczkowski et al, 2017). Sakuranetin is a major flavonoid phytoalexin identified from rice and displays high antimicrobial activity (Tamogami et al, 1997; Murata et al, 2020). Apigenin is extracted from rice straw (Ma et al, 2019) and red and brown rice bran (Ghasemzadeh et al, 2018) and shows strong antioxidant properties, yet it remains unknown whether it also participates in the rice–pathogen interaction.…”

Molecular dissection of rice phytohormone signaling involved in resistance to a piercing‐sucking herbivore

“…The expression of some characterized genes was tested in JA‐deficient lines and WT plants. The naringenin 7‐O‐methyltransferase ( NOMT ) is a key gene in the biosynthesis of flavonoid phytoalexin sakuranetin (Murata et al ., 2020). NOMT transcripts were strongly upregulated in WT plants at 24 h after BPH treatment (Fig.…”

Defense mechanisms involving secondary metabolism in the grass family

“…59) Here, third leaves from rice cultivars in the WRC were treated with 1 mM jasmonic acid, and the accumulation of sakuranetin was examined. 60) The results indicated that certain cultivars accumulated high concentrations of sakuranetin, while others accumulated naringenin that is the immediate precursor for sakuranetin (Fig. 4).…”