The phytohormone jasmonic acid is involved in rice resistance to Southern rice black-streaked dwarf virus

Abstract

Viruses are significant pathogens causing severe plant infections and crop losses globally. The resistance mechanisms of rice to viral diseases, particularly Southern rice black-streaked dwarf virus (SRBSDV), remain poorly understood. In this study, we assessed SRBSDV susceptibility in 20 Xian/indica (XI) and 20 Geng/japonica (GJ) rice varieties. XI-1B accessions in the Xian subgroup displayed higher resistance than GJ accessions. Comparative transcriptome analysis revealed changes in processes like oxidoreductase activity, jasmonic acid (JA) metabolism, and stress response. JA sensitivity assays further linked antiviral defense to the JA pathway. These findings highlight a JA-mediated resistance mechanism in rice and offer insights for breeding SRBSDV-resistant varieties.

Headnote

ARTICLE INFO

Article history:

Received 27 May 2024

Revised 5 July 2024

Accepted 29 August 2024

Available online 7 September 2024

Keywords:

Oryza sativa (rice)

Jasmonic acid

Southern rice black-streaked dwarf virus (SRBSDV)

Variety resistance

Defense response

ABSTRACT

Viruses are significant pathogens causing severe plant infections and crop losses globally. The resistance mechanisms of rice to viral diseases, particularly Southern rice black-streaked dwarf virus (SRBSDV), remain poorly understood. In this study, we assessed SRBSDV susceptibility in 20 Xian/indica (XI) and 20 Geng/japonica (GJ) rice varieties. XI-1B accessions in the Xian subgroup displayed higher resistance than GJ accessions. Comparative transcriptome analysis revealed changes in processes like oxidoreductase activity, jasmonic acid (JA) metabolism, and stress response. JA sensitivity assays further linked antiviral defense to the JA pathway. These findings highlight a JA-mediated resistance mechanism in rice and offer insights for breeding SRBSDV-resistant varieties.

1. Introduction

Rice yields in China and Asia are impaired by several viruses, including Southern rice black-streaked dwarf virus (SRBSDV) [1-5]. Southern rice black streaked dwarf virus belongs to a member of the Fijivirus genus in the Reoviridae family. Under natural conditions, SRBSDV is transmitted by white-backed planthopper (WBPH, Sogatella furcifera) in a persistent manner [6,7]. The proviral factors in the host contribute to viral replication or movement and are critical for SRBSDV infection. The current transcriptomic, proteomic, and metabolomic technologies have facilitated in-depth excavation of key genes or proteins involved in SRBSDV interactions with rice and vectors [8-11]. As a result, based on the omics studies, researchers have identified many genes involved in the spread of SRBSDV. The resistance of rice to SRBSDVD is complex and diverse because it is regulated by multiple genes [12,13]. So far, there is no effective method for controlling SRBSDV, except for the application of insecticides [14]. Accordingly, identification of disease-resistance genes and cultivation of disease-resistant varieties is the most economical and effective strategy for the control of viral diseases [15]. To date, only one SRBSDVD resistance gene has been cloned in rice, and the molecular mechanism of disease resistance has not been reported [16].

In response to attack by viruses, plants produce a complicated mixture of phytohormones, which modulate plant immunity to invading pathogens [17]. Jasmonic acid (JA) and its derivatives are lipid-derived hormones, which function in plant growth and adaptation to the environment [18]. In recent years, an increasing number of studies have focused on understanding the mechanisms by which JA regulates plant resistance to viruses. The JA signaling pathway is a complex process that involves the perception of JA, signaling transduction, activation of transcription factors, and regulation of target gene expression. This process relies on the coordinated action of numerous key proteins, including the receptor protein COI1, negative regulators JAZs, and transcription factors such as MYC2. Upon perception of the JA signal, JAZ proteins are recognized by COI1 and degraded via the 26 s proteasome pathway, releasing transcriptional activators such as MYC2, which in turn activate the expression of JA-responsive genes [19]. JA is involved in the defense responses of plants against viral diseases, including rice. Application of exogenous JA increased resistance of rice to rice dwarf virus (RDV) and RBSDV [20,21]. JA can confer rice resistance against a variety of viruses, such as SRBSDV, RBSDV and RSV. JA signaling and RNA silencing pathway synergistically increase the antiviral defense ability of rice [22,23]. The efficiency of these silencing pathways can be increased by JA, which effectively suppresses viral infections in plants. The activation of the JA signaling pathway functions in the inhibition of RBSDV infection by the auxin pathway [21]. JA functions in antiviral immunity. The activation of JA signaling pathway in rice plants increases their defense responses against viral infections, providing a potential target for the development of resistant rice varieties. Understanding the molecular mechanisms underlying the relationship between JA and rice variety resistance is essential for developing strategies to improve disease resistance in crops.

2. Materials and methods

2.1. Plant materials and growth conditions

A set of 1956 rice accessions from 3K rice germplasm resources [24] were identified by natural inoculation in the field in an area in Kaifeng, Henan province severely affected by RBSDVD. To further test the resistance difference of XI and С] rice varieties to SRBSDV infection, we artificially inoculated 40 representative accessions (20 XI and 20 GJ) with viral infection under natural conditions. The 40 rice varieties in the experiment were listed in Table S2. SRBSDV-infected plants were maintained in our laboratory. The plants were grown in the greenhouse at 28-30 °C with a 12 h/12 h light/dark cycle.

2.2. Insect vector and virus inoculation assays

The inoculation of plants with SRBSDV using WBPHs was performed as previously described [9,10]. To obtain virus-free WBPHs, adult insects were allowed to feed and lay eggs on each plant in glass beakers for 3 d. The eggs were then grown to first- or second-instar virus-free nymphs of WBPHs after 8-10 d. To acquire SRBSDV, these nymphs were fed on SRBSDV-infected rice plants for 3-5 d. They were then transferred to healthy rice seedlings and left for about 10 d to allow viral circulation in the insects. WBPHs infected with SRBSDV or virus-free insects were transferred to 10-d-old (3- to 4-leaf stage) rice seedling, allowed to feed for 3-5 d, and removed. The virus-infected rice seedlings were transferred to the field. For SRBSDV inoculation assays, each independent experiment contained 20-30 seedlings. The inoculated plants were monitored for viral symptoms at about 20 to 30 d post inoculation (dpi). Rice plants with differences from normal plants and phenotypes consistent with the symptoms of SRBSDV (dwarfism, darkened leaves) were judged to be infected with SRBSDV. Infection with SRBSDV in these inoculated plants was confirmed by RTPCR. After 30 dpi, disease symptoms and morbidity were recorded. Virus-infected plant leaves were collected for RNA extraction and transcriptome analysis.

2.3. RT-qPCR experiments for detecting virus content

Total RNA was isolated from mock and SRBSDV-infected plants using TRIzol reagent (Invitrogen, Carlsbad, CA, USA) according to the manufacturer's protocol. 1-2 pg total RNA was mixed with 4·EDNA wiper mix to remove genomic DNA at 42 °C for 2 min and then reverse transcribed to cDNA adding HiScript III qRT Super Mix (Vazyme). There were three biological repeats for each mock and SRBSDV-infected sample. Quantitative real time (qRT)-PCR assay was conducted using ChamQ SYBR qPCR Master Mix (Without ROX) by the ABI7900HT Sequence Detection System (Applied Biosystems, Carlsbad, CA, USA). OsUBQ5 (AK061988) acts as an internal reference. The expression level was analyzed by the 244 method [25,26]. RT-qPCR was repeated at least three times. Table S1 lists the RT-qPCR primers used.

2.4. Transcriptome analysis SRBSDV-infected rice samples

Control and SRBSDV-infected rice samples were collected at 30 dpi, quick-frozen in liquid nitrogen and ground into fine powder, and RNA was extracted. Three to five leaves of different seedlings were used as a biological replicate, and each treatment used three biological replicates. The number and purity of RNA were evaluated, and the addition of adapters, size selection and RNA sequencing were performed by Hangzhou Lianchuan (Hangzhou, Zhejiang, China). RNA sequencing was performed with the illumina HiSegTM 2000 platform (Hangzhou, Zhejiang, China). The sequencing reads were mapped to the rice genome by Bowtie software (the MSUrice genome Annotation Project database version 7.0).

2.5. Root growth inhibition assays

In the JA sensitivity experiment, the seeds germinated at 37 "C, and then the germinated seeds of each rice variety were moved into a dark 96-well plate of rice nutrient solution containing 0.5 pmol L-! MeJA under 8 h light/16 h dark at 30 °C for 7 d. The primary root lengths of seedlings were measured and the phenotypes were photographed. In each treatment, at least 12-15 seedlings per rice variety were treated and measured. The relative root length was used to evaluate the sensitivity to JA.

3. Results

3.1. Resistance evaluation of rice accessions to SRBSDV

By our previous viral inoculation experiments, we identified 20 resistant and 20 susceptible rice varieties. In order to further clarify the resistance difference of XI and GJ rice varieties to SRBSDV infection, we artificially inoculated the 40 representative varieties (20 XI and 20 GJ) with viral infection under natural conditions (Table S2). SRBSDV-infected plants showed dwarfing at 30 d after inoculation. Among the 20 XI varieties, the disease incidence in 7 varieties was less than 50%, accounting for 35% of the test samples. However, the incidence of most GJ varieties was more than 70%, with 5 sensitive varieties reaching 100%, accounting for 25% of the test samples. In contrast, only one XI variety, LAKHA KUAR, was found to be with a 100% incidence rate. The incidence in XI accessions was about 60%, and the incidence of GJ accessions was about 80%. By contrast, the incidence of XI accessions varieties was lower than that of GJ accessions after inoculation with SRBSDV (Fig. 1). More XI-1B than GJ accessions were highly resistant to SRBSDV.

3.2. Viral accumulation in rice accessions

In the previous field natural disease experiment, ZH5 was found to be a high-resistant variety of RBSDV. The incidence of artificial infection in the laboratory is higher than that in the field. We comprehensively analyzed the resistance and susceptibility of each variety based on the results of the two experiments. Varieties with incidence less than or close to ZH5 were classified as resistant varieties. Susceptible varieties were defined as two incidence rates higher than 90%. To further test the viral content in different rice varieties to SRBSDV infection, we measured the expression level of SRBSDV gene by RT-qPCR. First, we screened 8 resistant varieties (ZH5, CEMPO, IR-1813, PR-106, C-166, BR-52, Hua 564 and BODA) and 7 sensitive varieties (LAKHA, OWARI, YONG AN, Laohongdao, ESCARLATE, IRAT and 62,667 with disease incidence of 100%) (Fig. 2; Table S2). The viral accumulation of 15 varieties was quantified using three SRBSDV genomic RNA segments 52, S4 and 56. ZH5 with the middle degree of disease was selected as the control. Compared to the control variety ZH5, the susceptible varieties exhibited significantly higher viral content, while the resistant varieties generally showed lower viral level (Fig. 3). The XI variety CEMPO displayed both the lowest incidence rate and viral accumulation level after SRBSDV inoculation. The RT-qPCR assays indicated that the expression trend of SRBSDV S2, S4 and S6 genes was basically consistent with the incidence in rice different varieties. Viral accumulation was lower in XI than in GJ accessions.

3.3. Transcriptomic analysis suggests that rice variety resistance is closely related to JA pathway

To explore the molecular mechanism of different rice varieties in response to SRBSDV infection, we performed a genome-wide transcriptomic analysis, of the resistant accession CEMPO, C-166 (XI-3) and the highly susceptible accession YONG AN, ESCARLATE (GJ-tmp) after SRBSDV infection. Two-week-old rice seedlings were inoculated with SRBSDV by WBPHs for 3 d. About 30 d after inoculation, the mock and SRBSDV-infected rice leaves were collected with three biological replicates for RNA-seq. In order to reduce the likelihood of false positives, we used a P-value less than 0.05 as the cutoff criterion. We identified 1682 genes as significantly upregulated and 1944 genes were significantly downregulated in the resistant variety CEMPO. The resistant variety C-166 had 1564 genes significantly upregulated and 1982 genes significantly downregulated. We identified DEGs in total, with 7325 (4464 upand 2861 downregulated) in the susceptible variety YONG AN, and 6191 (3199 up- and 2992 downregulated) in the susceptible variety ESCARLATE (Fig. 4). This indicates that after SRBSDV infection, different varieties activate related genes to counteract the viral infection.

We further analyzed the DEGs between two resistant and susceptible varieties. Venn diagram analysis showed that 184 genes were highly overlapped in the upregulated genes of two resistant varieties CEMPO and C-166 (Fig. 4A; Table S3). Gene ontology (GO) analysis was used to classify the biological process of the 184 genes and found that they were mainly involved in the following biological processes: oxido-reductase process, JA metabolic process, response to stress and so on (Fig. 4A). Meanwhile, the downregulated DEGs of 392 genes were highly overlapped in two resistant varieties CEMPO and C-166 (Fig. 4B). GO analysis indicated that these genes were enriched with flavonoid biosythetic process, transmembrane transport, metal ion transport (Fig. 4B). The overlapped upregulated genes of two resistant varieties were involved in defense response and were linked to plant hormone JA. In addition, venn diagram analysis showed that 2047 genes were overlapped in the upregulated genes of two susceptible varieties YONG AN and ESCARLATE (Fig. 4C). The common upregulated genes were significantly enriched in JA response, defense response, and transmembrane transport process (Fig. 4C). The downregulated DEGs of 1472 genes were overlapped in two susceptible varieties (Fig. 4D). GO analysis showed that these genes were enriched to receptor kinase signaling pathway, metabolic process (Fig. 4D). These data imply that rice variety resistance may be associated With JA pathway, powerfully hinting at a role for JA-mediated antiviral immunity in different rice varieties.

3.4. The activation of JA pathway influences resistance of rice to SRBSDV infection

To study the association between the JA pathway and the expression reprogram of different XI and GJ varieties to viral infection, we performed the hierarchical clustering method to group them into four clusters according to their expression profiles. We found that the genes in both resistant varieties were significantly activated in Cluster 4 (responses to JA, stress responses, phosphatidic acid metabolic processes, etc.), but were not activated in susceptible varieties upon SRBSDV infection (Fig. 5A). After SRBSDV infection, genes related to heat response and fatty acid biosynthesis were significantly up-regulated in susceptible varieties, while genes related to hormone-related defense pathways were less. JA plays an active role in rice defense against SRBSDV [27-29]. To confirm the association of variety resistance with JA pathway, we used RT-qPCR to determine the expression levels of the JA-related genes (OsLOX2, OsJAZ6, OsJAZ12, and OsJAmyb) in two resistant and susceptible varieties challenged by SRBSDV. The expression levels of JA-related genes were significantly higher in resistant varieties than those in susceptible varieties after SRBSDV infection (Fig. 5B). These results indicate that JA signaling genes normally induced by SRBSDV infection were more inhibited in susceptible than in resistant accessions.

3.5. JA sensitivity analysis shows that susceptible varieties make rice less sensitive to JA treatment

In order to further study the biological significance of JA signaling pathway in different rice varieties to SRBSDV resistance, we conducted JA sensitivity analysis on the above mentioned 15 rice varieties. MeJA treatment inhibits root growth in plants, and the inhibition of root growth is enhanced when the JA signaling pathWay is activated. We then examined the JA sensitivity by exogenous application of 0.5 pmol L-! MeJA (methyl jasmonate) to rice in hydroponic culture in the dark. Compared with the control, MejJA treatment significantly inhibited the growth of root lengths. However, the effect of root length inhibition of 8 resistant varieties was more obvious than that of 7 susceptible varieties (Fig. 6). Especially, the degree of inhibition of root length of LAKHA and IRAT (32% and 35%, respectively) in susceptible varieties were less reduced than CEMPO and Hua 564 in resistant varieties (68% and 71%, respectively) (Fig. 6A, B). The relative root length also showed that resistant varieties were more inhibited than susceptible varieties after MeJA treatment (Fig. 6C). The above results indicated that 8 resistant varieties were more sensitive to JA treatment than 7 susceptible varieties. These results imply that after SRBSDV infection, the activation of JA signaling pathway in resistant varieties was stronger than that in susceptible varieties, thus increasing the resistance of rice to SRBSDV infection.

4. Discussion

Plant viral diseases have caused significant yield losses in crops. In the case of rice, viruses such as SRBSDV have been particularly damaging. Most of the currently cultivated rice varieties are highly susceptible to SRBSDV [13]. Acquiring reliable and highly resistant germplasms is a critical step in the effective breeding of resistant rice. Despite significant efforts in screening for resistant germplasms over the past few decades, the number of reliable resistant rice accessions identified remains limited. Currently, there are few rice varieties resistant to SRBSDV, and there is no direct resistance gene for SRBSDV. Here, we evaluated the resistance of 40 accessions from XI and GJ subgroups to SRBSDV infection (Fig. 1). The resistance evaluation of rice accessions to SRBSDV showed significant variation in viral resistance among different varieties. Among the 20 XI varieties, 7 varieties had a disease incidence of less than 50%, while most GJ varieties had an incidence rate of more than 70% (Fig. 2). Our results revealed that most XI accessions exhibited higher resistance to SRBSDV compared to GJ accessions. The results were consistent with those of an earlier study that GJ varieties are more susceptible to RBSDV than XI and other subgroups [18]. Moreover, we found that most of the XI-1B accessions were more resistant to SRBSDV than the accessions in the other four XI subgroups, implying that there were also differences in resistance to RBSDV among the subgroups with close phylogenetic relationship. Our analysis of viral accumulation in different rice varieties further supports this observation (Fig. 3).

Rice resistance to SRBSDVD is a complex trait that is regulated by a multitude of genetic factors, including both virus resistancerelated genes and insect resistance-related genes. This intricate genetic regulation makes the breeding of rice for resistance to SRBSDVD more challenging compared to other disease resistance breeding programs. Understanding the genetic basis of viral disease resistance is crucial for effective rice breeding. The transcriptomic analysis revealed that the resistance of rice varieties to SRBSDV is closely related to the JA pathway. JA participates in a variety of plant biological processes and plays a pivotal role in plant defense [18]. In SRBSDV-infected rice, viral protein and OsNF-YA weakened JA-mediated antiviral defense [8,29]. WBPHs infestation down-regulates the expression of JA pathway genes, while up-regulates the expression of SA pathway-related genes. However, when WBPHs infected with SRBSDV, the expression of JA pathway gene OsAOS2 was significantly down-regulated compared to WBPHs infestation alone [30]. This suggests that JA pathways can be influenced by viral infection and insect feeding. In the process of virus infecting plants, plant hosts have evolved complex defense systems. JA is an important hormone in plant antiviral immunity. More and more studies have shown that viruses promote their own infection by destroying the JA pathway of plants during infection. In the process of plant disease resistance, one of the results of JA recognition and subsequent signal cascade reaction was the expression of pathogenesis-related genes [38], which induced the initial immune response to viral infection. A strong link between JA-mediated signaling and RNA silencing was recently demonstrated, accumulating JA promotes rice antiviral defense through inducing AGO18 expression [26]. JA can also synergize with SA to enhance the antiviral ability of rice. It was found that OsNPR1 activates the expression of JA-responsive genes by forming a complex with OsMYC2, thereby enhancing the host's antiviral ability [15]. In addition, a large number of studies have shown that JA is involved in plant growth and development, such as root growth, leaf senescence and reproductive development [31,32]. After MeJA treatment, root length was measured to reflect the sensitivity of different varieties to the JA pathway. MeJA treatment inhibits root growth in plants, the stronger the sensitivity means the higher the level of JA signaling pathway. Our previous studies have found that JA is closely related to rice disease resistance [9,11,29,33,34].

Upon infection with SRBSDV, we observed substantial disparities in the activation of genes involved in the defense response between resistant and susceptible rice varieties, particularly the JA pathway (Fig. 5). Venn diagram analysis revealed that a subset of genes was highly overlapping. GO enrichment of these genes in the JA metabolic process is particularly intriguing, as it suggests a potential role for the JA pathway in the resistance of rice to SRBSDV infection (Fig. 4). The activation of the JA pathway is intricately linked to the resistance of rice viral infection [22]. We employed hierarchical clustering to categorize rice varieties into clusters based on their expression profiles in response to SRBSDV infection. Our findings revealed that the genes in both resistant varieties, were prominently activated in Cluster 4, which is associated with responses to JA pathway. In contrast, the susceptible variety mainly showed activation in Cluster 1, which is linked to responses to heat and fatty acid biosynthesis (Fig. 5A). These results suggest that the resistant varieties used JA-mediated defense mechanisms to enhance their resistance to SRBSDV. Our JA sensitivity analysis provided additional evidence for the role of the JA pathway in rice resistance to SRBSDV. The susceptible varieties showed less sensitivity to JA treatment, indicating that their JA signaling pathway may be less responsive or impaired, which could contribute to their increased susceptibility to SRBSDV (Fig. 6). Understanding the molecular mechanisms underlying the JA-mediated antiviral immunity in rice can lead to the development of new strategies for disease control, such as the application of JA-related compounds or the manipulation of JA signaling pathways in rice plants. Despite the progress made in understanding the role of JA in plant antiviral defense, there are still many unanswered questions. Future research should focus on elucidating the molecular basis of JA-mediated antiviral defense and developing strategies to enhance plant resistance to viruses through manipulation of JA signaling. This will not only advance our knowledge of plant-virus interactions but also provide practical solutions for the control of plant viral diseases.

In conclusion, our study demonstrates that the resistance of rice varieties to SRBSDV is closely associated with the JA pathway. The activation of JA signaling genes and the subsequent regulation of defense responses appear to be key factors in the increased resistance of XI varieties to SRBSDV.

CRediT authorship contribution statement

Chaorui Huang: Writing - original draft, Investigation, Data curation. Qing Liu: Investigation, Data curation. Qingling Qi: Investigation, Data curation. Chenfei Gao: Investigation. Lulu Li: Investigation. Yanjun Li: Investigation. Jianping Chen: Supervision, Funding acquisition. Zongtao Sun: Writing - review & editing, Visualization, Supervision, Funding acquisition. Jianlong Xu: Writing - review & editing, Project administration, Conceptualization. Hehong Zhang: Writing - review & editing, Writing - original draft, Supervision, Project administration, Funding acquisition, Conceptualization.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

This work was funded by the National Key Research and Development Plan of China (2023YFD1400300), National Natural Science Foundation of China (U23A6006, 32270149, 32272555), Zhejiang Provincial Natural Science Foundation (LZ22C140001), and the Ningbo Major Research and Development Plan Project (20237124).

Footnote

* Corresponding authors.

E-mail addresses: [email protected] (J. Xu), [email protected] (H. Zhang).

1 These authors contributed equally to this work.

References

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Appendix A. Supplementary data

Supplementary data for this article can be found online at https://doi.org/10.1016/j.cj.2024.08.002.