Rice (Oryza sativa) is one of the most important food crops, and approximately half of the world population is wholly dependent upon it as a staple crop for nutrition and caloric intake, contributing more than one-fifth of the calories consumed by humans. Owing to the rapid population growth, the current crop yield stability requires an attenuation of the reduction in yield and quality losses caused by environmental stress, owing to shifts in pathogens and other factors (Bailey-Serres et al., 2019; Buresh et al., 2021). Plant pathogens, including viruses, bacteria, fungi, and so forth, cause a total yield loss of ~30% in staple food crops worldwide (Wang P. et al., 2022).

Rice black-streaked dwarf virus (RBSDV) belongs to the genus Fijivirus in the family Spinareoviridae and was first reported in Japan in the early 1950s. It is transmitted by small brown planthoppers (SBPH, Laodelphax striatellus Fallén) in a persistent, circulative, and propagative manner. RBSDV naturally infects various Poaceae crops, including rice, maize, wheat, barley, and Alopecurus aequalis Sobal (Hibino, 1996; Zhang et al., 2001). The first major outbreaks of the disease caused by RBSDV in Japan were recorded in maize from 1957 to 1961 (Hibino, 1996).

Several outbreaks of rice black-streaked dwarf virus disease (RBSDVD) across different rice cultivars were reported in Japan (1965–1967), China (1963; 1965–1967), and Korea (1975–1976) (Hibino, 1996), resulting in severe yield losses in rice production (Ruan et al., 1984; Hibino, 1996). After disappearing for some years, RBSDVD reemerged in China between 1991 and 2002, and outbreaks have been recorded in japonica rice in several provinces in China since 2008 (Wu et al., 2020). The disease incidence (DI) of RBSDVD in rice also increased in Jeonra provinces in Korea around 2005 (Lee et al., 2005) and in Saitama Prefecture in Japan after 2010 (Matsukura et al., 2019). Up to 64,640 ha of the late japonica rice crop were affected by RBSDVD with estimated losses of 120,000 tons of grain per year from 1995 to 2007 in Zhejiang province, China (Wang et al., 2009). Since 2006, RBSDVD has been widespread in Jiangsu, Zhejiang, and Shandong provinces; outbreaks and serious epidemics were recorded during 2013–2014 in China (Ren et al., 2016). Approximately 25 and 35.6% of the planted area in Kaifeng were affected by RBSDVD in 2013 and 2014, respectively, resulting in rice yield losses of up to 200,000 kg (Ren et al., 2016).

Although severe yield losses had been observed in rice after RBSDV infection, it is not clear how yield was affected by the virus invasion, and little is known about the yield components associated with the disease. RBSDV-infected rice plants have been identified, showing pronounced stunting, darkening of leaves, twisting of leaf tips, splitting of the leaf margin, and waxy white-to-black galls along the veins on the underside of leaf blades and the outer surface of sheaths and columns (Ruan et al., 1984; Hibino, 1996). However, none of these are key components for rice yield, which is largely determined by some correlated traits such as panicle number, grain number per panicle, grain weight, and so forth (Song et al., 2022). The grain number per panicle can also be attributed to the spikelet number and seed-setting rate (SSR) of the spikelets. The development processes of these traits are regulated by genes or quantitative trait loci (QTL) involved in different pathways and networks (Xing and Zhang, 2010). In addition, these traits are usually inversely related in rice (Wang B. et al., 2018). Evaluation of the effect of RBSDV on different yield components is beneficial not only for disease control but also for revealing the mechanisms of rice responses to virus invasion.

The cultivation and application of resistance rice with high yield and good quality is an ongoing trend (Wing et al., 2018). However, genetic immunity to disease often comes with an unintended reduction in growth and yield (Ning et al., 2017). Quite a few reports have focused on RBSDVD resistance in germplasm screening and revealed a low percentage of resistant materials among the temperate sources of japonica germplasm. Only several aus, indica, and tropical japonica subspecies displayed higher levels of resistance (Pan et al., 2009; Wang et al., 2010; Zhang et al., 2016). Most of these resistance materials are local germplasms with relatively low yield and quality and have not been used successfully in rice resistance breeding. Therefore, it is necessary to evaluate the effect of resistance materials or genes on rice yield and quality.

Recently, our laboratory identified an RBSDVD-resistant rice variety, W44, and isolated a resistant gene, OsAP47 (Wang Z. et al., 2022). With these results, an RBSDVD-resistant cultivar, ZJ201, was produced (unpublished data). Together with several susceptible rice cultivars, in this study, we aimed to assess the effect of RBSDVD on rice production and evaluate the yield-related traits of rice cultivars with different levels of resistance. The results may help in understanding the mechanisms of rice responses to RBSDV invasion and the utilization of resistance QTL or genes in rice breeding.

To reduce the impact of RBSDVD in regions with epidemics, various measures were produced, which were primarily aimed at interrupting the cycle of virus transmission by the vector SBPHs. These measures included covering rice seedling nurseries with insect-proof nets or applying pesticides to control the insects (Wu et al., 2020). However, these management practices tend to waste natural resources or cause environmental pollution, thereby posing challenges. Identifying natural resistance resources and breeding resistant varieties is considered the most economical and effective approach to control this disease.

According to a 3-year evaluation, three varieties were identified with consistent DI of < 10%, and all originated from Southeast Asia (Wang et al., 2014). Four rice varieties with stable levels of RBSDV resistance were discovered in the rice diversity panel 1 cultivars (Feng et al., 2019). Recently, our laboratory identified a highly RBSDVD-resistant variety, W44, through an extensive evaluation of a diverse international rice panel and isolated a resistance gene, OsAP47 (Wang Z. et al., 2022). To utilize these resistance germplasms in rice resistance breeding, our laboratory bred a new line, ZJ201, based on the resistant cultivar W44, and introduced OsAP47 into a new genetic background. In this study, seven rice cultivars were evaluated, and ZJ201 displayed the highest level of resistance against RBSDVD, as indicated by DI (Figure 3).

As expected, yields of all rice cultivars declined after RBSDV infection, with losses of up to 90.1% in AY, implying significant risks associated with the use of these popular rice varieties at present. ZJ201 displayed minimal reduction, and the difference in AY did not reach a significant level. These results confirmed that breeding resistant rice cultivars could minimize the yield losses caused by RBSDVD. The significant correlations detected between DI and yield reduction suggest that DI could serve as a good indicator for RBSDVD resistance levels and yield potentials.

The interaction between viruses and host plants adversely affects host morphology and physiology, leading to a decline in production. Rice yield is a complex trait determined by various components, primarily including the number of panicles per plant, the number of grains per panicle, and grain weight (Xing and Zhang, 2010). These components were regulated by different genes or QTLs (Li et al., 2000; Hittalmani et al., 2003; Wang et al., 2011; Huang et al., 2013; Tan et al., 2013; Yano et al., 2016), implying their involvement in diverse pathways. However, little is known about which pathway is affected by RBSDV invasion. Among the yield components detected in this study, most of them were reduced, such as PL, SPP, RGPP, and TGW, compared to mock plants after RBSDV infection, suggesting that these components were significantly affected by RBSDV.

Two yield components, SSR and PPSM, did not show a reduction in all rice cultivars after RBSDV infection. SSR significantly declined at levels of P < 0.01 in H5, NJ5055, NJ9108, and WYJ27 and of P < 0.05 in SX867. However, in XD3, despite both SPP and RGPP being significantly affected by RBSDVD, the changes in SSR between mock and inoculated plants did not reach a significant level (Figure 6B). The other component, PPSM, was significantly reduced in NJ5055 but dramatically increased in SX867, and no remarkable differences were detected in ZJ201, H5, NJ9108, XD3, and WYJ27 (Figure 6D). These results suggested that the yield losses produced by RBSDVD were mainly due to the reduction in PL, SPP, RGPP, and TGW but not SSR and PPSM. Similar results were observed in wheat, where the yield component most severely affected by barley yellow dwarf virus infection was the number of kernels per spike, followed by kernel weight, while the tiller number was generally not altered by the infection (Hoffman and Kolb, 1998). These results provided important clues for understanding the mechanisms of RBSDV invasion and its effects on rice after infection.

Active immune response in crops fighting pathogens may result in yield penalties (Wang J. et al., 2018). A genome-wide association study was conducted to assess the association between rice blast disease resistance and yield-related components; the analysis results showed that shorter plants were significantly associated with resistance to blast. Additionally, rice genomes with resistance genes were linked to lighter seed weights, while susceptible alleles were associated with heavier seed weights (Wang et al., 2015). In this study, we evaluated the rice line ZJ201, which carries the RBSDVD resistance gene OsAP47. The results indicated that ZJ201 did not have a notable negative effect on the main yield-contributing characters, for instance, SPP, RGPP, SSR, TGW, and PPSM, thereby producing a higher yield. These observations could facilitate the application of OsAP47 to avoid yield losses caused by RBSDVD. In the future, quality traits will be evaluated for different rice cultivars after RBSDV infection, and ZJ201 will be assessed for its utilization in rice resistance breeding.

Rice yield could be significantly reduced by RBSDV infection, mainly by affecting PL, SPP, RGPP, and TGW. Among these, RGPP contributed the most to yield losses. Resistant rice lines could avoid yield losses by maintaining the normal development of these traits. ZJ201 could be promoted for planting in areas severely affected by RBSDVD or used as a resistance intermediate material in rice breeding.

The original contributions presented in the study are included in the article/Supplementary material, further inquiries can be directed to the corresponding authors.

YS: Data curation, Writing – original draft, Investigation. DJ: Resources, Writing – original draft. JZ: Data curation, Writing – original draft. LD: Investigation, Writing – original draft. CL: Methodology, Writing – original draft. YL: Resources, Writing – original draft. FL: Conceptualization, Data curation, Investigation, Project administration, Supervision, Writing – original draft, Writing – review & editing. TZ: Conceptualization, Funding acquisition, Project administration, Supervision, Writing – review & editing.