Synergy between virus and three kingdom pathogens, fungus, bacterium and virus is lost in rice mutant lines of OsRDR1/6

Sopan Ganpatrao Wagh; Sachin Ashok Bhor; Akio Miyao; Hirohiko Hirochika; Taiyo Toriba; Hiro-Yuki Hirano; Kappei Kobayashi; Takashi Yaeno; Masamichi Nishiguchi

doi:10.1016/j.plantsci.2024.112244

Synergy between virus and three kingdom pathogens, fungus, bacterium and virus is lost in rice mutant lines of OsRDR1/6

Plant Sci. 2024 Sep 6:349:112244. doi: 10.1016/j.plantsci.2024.112244. Online ahead of print.

Authors

Sopan Ganpatrao Wagh¹, Sachin Ashok Bhor², Akio Miyao³, Hirohiko Hirochika⁴, Taiyo Toriba⁵, Hiro-Yuki Hirano⁶, Kappei Kobayashi⁷, Takashi Yaeno⁷, Masamichi Nishiguchi⁸

Affiliations

¹ The United Graduate School of Agricultural Sciences, Ehime University, Matsuyama, Ehime 790-8566, Japan; Global Change Research Institute of the Czech Academy of Sciences, Brno 60300, Czech Republic. Electronic address: swagh.gene@gmail.com.
² The United Graduate School of Agricultural Sciences, Ehime University, Matsuyama, Ehime 790-8566, Japan.
³ National Institute of Agrobiological Sciences, 2-1-2 Kan-nondai, Tsukuba, Ibaraki 305-8602, Japan; National Agriculture and Food Research Organization (NARO), Tsukuba, Ibaraki 305-8642, Japan.
⁴ National Institute of Agrobiological Sciences, 2-1-2 Kan-nondai, Tsukuba, Ibaraki 305-8602, Japan.
⁵ Department of Biological Sciences, Graduate School of Science, University of Tokyo, Bunkyo-ku, Tokyo 113-8657, Japan; School of Food Industrial Sciences, Miyagi University, 2-2-1 Hatatate, Taihaku-ku, Sendai, Miyagi 982-0215, Japan.
⁶ Department of Biological Sciences, Graduate School of Science, University of Tokyo, Bunkyo-ku, Tokyo 113-8657, Japan.
⁷ The United Graduate School of Agricultural Sciences, Ehime University, Matsuyama, Ehime 790-8566, Japan; Faculty of Agriculture, Ehime University, Matsuyama, Ehime 790-8566, Japan.
⁸ The United Graduate School of Agricultural Sciences, Ehime University, Matsuyama, Ehime 790-8566, Japan; Faculty of Agriculture, Ehime University, Matsuyama, Ehime 790-8566, Japan. Electronic address: mnishigu@agr.ehime-u.ac.jp.

PMID: 39244093
DOI: 10.1016/j.plantsci.2024.112244

Abstract

Co-infection, caused by multiple pathogen attacks on an organism, can lead to disease development or immunity. This complex interaction can be synergetic, co-existing, or antagonistic, ultimately influencing disease severity. The interaction between fungus, bacterium, and virus (three kingdom pathogens) is most prevalent. However, the underlying mechanisms of co-infection need to be explored further. In this study, we investigated the co-infection phenomenon in rice plants exposed to multiple pathogen species, specifically Rice necrosis mosaic virus (RNMV) and rice blast fungus (Magnaporthe oryzae, MO), bacterial leaf blight (Xanthomonas oryzae pv. oryzae, XO) or Cucumber mosaic virus (CMV). Our research showed that RNMV interacts synergistically with MO, XO, or CMV, increasing pathogen growth and lesion size. These findings suggest positive synergy in RNMV co-infections with three kingdom pathogens, increasing accumulation and symptoms. Additionally, to investigate the role of RNAi in pathogen synergism, we analyzed rice mutant lines deficient in RNA-dependent RNA polymerase 1 (OsRDR1) or 6 (OsRDR6). Notably, we observed the loss of synergy in each mutant line, highlighting the crucial role of OsRDR1 and OsRDR6 in maintaining the positive interaction between RNMV and three kingdom pathogens. Hence, our study emphasized the role of the RNA silencing pathway in the intricate landscape of pathogen interactions; the study's outcome could be applied to understand the plant defense response to improve crop yields.

Keywords: Cucumber mosaic virus; Magnaporthe oryzae; RNA dependent RNA polymerase 1/6; Rice necrosis mosaic virus; Synergy; Xanthomonas oryzae pv. oryzae.