Summary Phytohormone, particularly jasmonate (JA) and salicylate (SA) signaling, plays a central role in plant responses to herbivore and pathogen attack. Generally, SA mediates resistance responses against biotrophic pathogens and phloem‐feeding insects, while JA mediates responses against necrotrophic pathogens and chewing insects. The phytohormonal responses mediating rice resistance to a piercing‐sucking herbivore, the brown planthopper (BPH), remains unknown. Here, we combined transcriptome analysis, hormone measurements, genetic analysis and a field study to address this issue. Infestation by BPH adult females resulted in significant transcriptional reprograming. The upregulated genes were enriched in the JA signaling pathway. Consistently, the concentrations of JAs, but not SA, were dramatically increased in response to BPH attack. Two JA‐deficient lines (AOC and MYC2 knockout) and two SA‐deficient lines (nahG overexpression and NPR1 knockout) were constructed. BPH performed better on JA‐deficient lines than on wild‐type (WT) plants, but similarly on SA‐deficient and WT plants. During BPH attack, the accumulation of defensive secondary metabolites was attenuated in JA‐deficient lines compared with WT plants. Moreover, MYC2 mutants were more susceptible to planthoppers than WT plants in nature. This study reveals that JA signaling functions in rice defense against BPH.

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Rice black-streaked dwarf virus (RBSDV), a Fijivirus, causes maize rough dwarf disease and rice black-streaked dwarf disease in the summer maize-growing regions of the Yellow and Huai rivers, respectively, in China. Nevertheless, the diversification and selection of the entire genome from S1 to S10 have not been illuminated. Molecular variation, evolution, conserved regions, and other genomic properties were analyzed in 21 RBSDV isolates from maize (Zea mays L.) and rice (Oryza sativa) hosts sampled from nine geographic locations in China. Low codon adaptation index values ranging from 0.1878 to 0.2918 indicated a low degree of codon-usage bias and low potential expression for all 13 RBSDV open reading frames (ORFs). ORF9-2 showed a stronger effect of codon usage bias than did other ORFs, as the majority of points for this ORF lay close to the standard curve in the Nc plot (the effective number of codons [Nc] versus the frequency of G+C at synonymous third-base positions [GC3]). A 9-bp deletion mutation was detected in the RBSDV genome in the 3′ UTR of S8. Nucleotide diversity analysis indicated that the structural proteins of RBSDV, such as S2 and S4, were all more conserved than nonstructural proteins such as S9. Nucleotide diversity (π) was highest among S9 sequences (0.0656), and was significantly higher than among S4 sequences (0.0225, P < 0.01). The number of conserved regions among the 10 segments varied substantially. The highest number of conserved regions (5) was found in S5, whereas no conserved regions were identified in S9. Nucleotide diversity and the number of conserved regions were independent of the lengths of segments. Nucleotide diversity was also not correlated with the number of conserved regions in segments. Ten recombination events in 21 isolates were found in seven segments with breakpoint positions in UTRs, intergenic spacer regions, and gene coding regions. The number of recombination events was also independent of the lengths of segments. RBSDV isolates from China could be phylogenetically classified into two groups using either 10 segment sequences or the concatenated sequence of S1 through S10, regardless of host or geographical location. The phylogenetic tree generated from pairwise nucleotide identities of individual RBSDV segments such as S9 and S3, with nucleotide identity values of 93.74% and 95.86%, respectively, is similar to the tree constructed from the concatenated sequences of the entire RBSDV genome. The 13 RBSDV ORFs were under negative and purifying selection (Ka/Ks < 1). ORF5-2 was under the greatest selection pressure; however, ORF2, which encodes the core protein of RBSDV, was under the lowest selection pressure.

Rice black-streaked dwarf virus (RBSDV) and Southern rice black-streaked dwarf virus (SRBSDV) cause maize rough dwarf disease (MRDD) and rice black-streaked dwarf disease (RBSDD) in China. RBSDV segment 8 (S8) contains the only deletion mutation in the genomes of these viruses, which are both members of the genus Fijivirus. To illuminate the molecular differences between the RBSDV and SRBSDV genomes and better understand the evolution of these viruses, and to determine which virus is specifically associated with MRDD and RBSDD in each region, S8 was analyzed in 66 virus isolates collected from 10 geographic locations in China and 14 S8 sequences obtained from the National Center for Biotechnology Information GenBank. Phylogenetic analysis showed that the pathogen associated with MRDD and RBSDD in the Yellow and Huai River valleys was RBSDV, whereas the pathogen associated with these diseases in Sanya was SRBSDV. Codon usage bias in S8 differed significantly between RBSDV and SRBSDV, as indicated by effective number of codons used by a gene (Nc) and GC values, Nc plots, and variation explained by the first axis in correspondence analysis. The nucleotide identities among these 66 RBSDV and SRBSDV isolates ranged from 66.2 to 68.2%, and were considerably lower than the nucleotide identities within RBSDV (from 94.1 to 99.9%) or SRBSDV (from 93.9 to 100%) isolates. Most S8 polymorphisms were identified in the region from 1,000 to 1,200 bp in RBSDV and in the region from 500 to 700 bp in SRBSDV. The difference in the lengths of RBSDV (1,936 bp) and SRBSDV (1,928 bp) was due to an 8-bp deletion in the 3′-untranslated region of SRBSDV. Six recombination events were detected in S8 in RBSDV and two recombination events were detected in S8 in SRBSDV. Recombination breakpoints were found within the region containing the deletion mutation in nine isolates. However, no recombination events were detected between RBSDV and SRBSDV. Both of these viruses were under negative and purifying selection, although the ratio of nonsynonymous mutations to synonymous mutations (Ka/Ks) for RBSDV S8 (0.0530) was not significantly lower than that of SRBSDV S8 (0.0823, P = 0.1550). We found that SRBSDV was more highly genetically differentiated (product of effective population size and the migration rate among populations < 1; values for the among-populations component of genetic variation or normalized variation > 0.33; and P values of the sequence statistic, the rank statistic, and the nearest-neighbor statistic < 0.01) than RBSDV. However, gene flow between RBSDV and SRBSDV was not frequent.

Plant defense against herbivores is costly and often associated with growth repression. The phytohormone jasmonate (JA) plays a central role in prioritizing defense over growth during herbivore attack, but the underlying mechanisms remain unclear. When brown planthoppers (BPH, Nilaparavata lugens) attack rice (Oryza sativa), growth is dramatically suppressed. BPH infestation also increases inactive gibberellin (GA) levels and transcripts of GA 2-oxidase (GA2ox) genes, two (GA2ox3 and GA2ox7) of which encode enzymes that catalyze the conversion of bioactive GAs to inactive GAs in vitro and in vivo. Mutation of these GA2oxs diminishes BPH-elicited growth restriction without affecting BPH resistance. Phytohormone profiling and transcriptome analyses revealed that GA2ox-mediated GA catabolism was enhanced by JA signaling. The transcript levels of GA2ox3 and GA2ox7 were significantly attenuated under BPH attack in JA biosynthesis (allene oxide cyclase, aoc) or signaling-deficient (myc2) mutants. In contrast, GA2ox3 and GA2ox7 expression was increased in MYC2 overexpression lines. MYC2 directly binds to the G-boxes in the promoters of both GA2ox genes to regulate their expression. We conclude that JA signaling simultaneously activates defense responses and GA catabolism to rapidly optimize resource allocation in attacked plants and provides a mechanism for phytohormone crosstalk.