RNA N⁶‐methyladenosine modification suppresses replication of rice black streaked dwarf virus and is associated with virus persistence in its insect vector

Abstract

Rice black streaked dwarf virus (RBSDV) (species Rice black streaked dwarf virus, genus Fijivirus, family Reoviridae) is transmitted by the small brown planthopper (SBPH, Laodelphax striatellus) in a persistent propagative manner (Hibino, 1996). Since RBSDV was first identified in Japan in 1952(Kuribayashi & Shinkai, 1952, it has caused serious yield losses of rice and maize in East Asian countries, including several major outbreaks in China, Japan, and South Korea (Hibino, 1996;Wu et al., 2020). In nature, higher population densities of viruliferous SBPHs have largely contributed to RBSDV epidemics in rice and maize fields, especially at early stages of crop development (Chen & Zhang, 2005;Zhang, Wu, et al., 2021). At present, the best economical and effective method for managing RBSDV-induced diseases is controlling vector insects due to the lack of disease-resistant plant varieties. Therefore, understanding the transmission mechanism is crucial for accurate forecasting and disease control.The genome of RBSDV contains 10 double-stranded RNA (dsRNA) segments, S1 to S10, numbered in decreasing order of molecular weight (Milne et al., 2005). Most RBSDV genomic segments contain one open reading frame, but S5, S7, and S9 have two

Functional Characterization of Two RNA Methyltransferase Genes METTL3 and METTL14 Uncovers the Roles of m6A in Mediating Adaptation of Plutella xylostella to Host Plants

“…Coincidentally, both in human HeLa and 293FT cells, knockdown of METTL14 had a greater effect on the decrease in m 6 A levels than METTL3 knockdown [ 38 ]. The average level of m 6 A in an insect vector of rice virus, L. striatellus , decreased when METTL3 and/or METTL14 were knocked down [ 23 ]. Since it has been verified that METTL3 is a catalytically active subunit, and that METTL14 acts as an RNA-binding scaffold in the METTL3–METTL14 complex [ 39 , 40 ], the role of METTL14 in m 6 A modification should be reconsidered.…”

“…m 6 A can regulate the alternative splicing of Sxl (sex-lethal) pre-mRNA and modulate flying behavior in Drosophila melanogaster Meigen [ 20 , 21 ], where the ‘‘reader’’ YT521-B is a major m 6 A effector [ 22 ]. The level of m 6 A in the insect vector Laodelphax striatellus Fallén was found to be negatively correlated with the replication of rice black-streaked dwarf virus (RBSDV) [ 23 ]. In Bemisia tabaci Gennadius, a mutation in the 5′ untranslated region (UTR) of a cytochrome P450 gene CYP4C64 introduces a potential m 6 A site, which confers resistance to the thiamethoxam [ 24 ].…”

m6A‐mediated regulation of crop development and stress responses

“…Accordingly, the m 6 A-mediated stress responses have been extensively studied in ª 2022 The Authors. Plant Biotechnology Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd., 20, 1447-1455 various crops, including tobacco (Nicotiana tabacum) (Li et al, 2018), rice (Cheng et al, 2021;Shi et al, 2019b;Tian et al, 2021;Zhang et al, 2021a), wheat (Sun et al, 2020;Zhang et al, 2021b), sweet sorghum (Zheng et al, 2021), tomato (Yang et al, 2021), apple (Guo et al, 2021;Mao et al, 2021), and pakchoi (Liu et al, 2020).…”

“…Mutation of m 6 A writers in Arabidopsis induces significant changes in the expression of genes responsive to abiotic and biotic stresses, as revealed by transcriptome analysis (Anderson et al ., 2018 ; Bodi et al ., 2012 ; Hu et al ., 2021a ). Accordingly, the m 6 A‐mediated stress responses have been extensively studied in various crops, including tobacco ( Nicotiana tabacum ) (Li et al ., 2018 ), rice (Cheng et al ., 2021 ; Shi et al ., 2019b ; Tian et al ., 2021 ; Zhang et al ., 2021a ), wheat (Sun et al ., 2020 ; Zhang et al ., 2021b ), sweet sorghum (Zheng et al ., 2021 ), tomato (Yang et al ., 2021 ), apple (Guo et al ., 2021 ; Mao et al ., 2021 ), and pak‐choi (Liu et al ., 2020 ).…”

“…In rice, the infection of rice stripe virus or rice black‐stripe dwarf virus (RBSDV) causes a dramatical increase in overall m 6 A methylation level, accompanied by the changed transcription in genes encoding m 6 A machineries, implying that m 6 A modification might be involved in the defence response against virus infection (Zhang et al ., 2021a ). In addition, when the m 6 A methyltransferase genes LsMETTL3 and LsMETTL14 from small brown planthopper (SBPH), the insect vector of RBSDV, were silenced, the titre of RBSDV in the midgut cells of SBPHs increased significantly, suggesting a negative correlation between the overall m 6 A levels and the virus replication (Tian et al ., 2021 ). In watermelon, the infection by cucumber green mottle mosaic virus (CGMMV) leads to the decrease in global m 6 A level and the increase in expression of m 6 A demethylase gene ClALKBH4B (He et al ., 2021 ).…”