Plant viruses are a group of intracellular pathogens that persistently threaten global food security. Significant advances in plant virology have been achieved by Chinese scientists over the last 20 years, including basic research and technologies for preventing and controlling plant viral diseases. Here, we review these milestones and advances, including the identification of new crop-infecting viruses, dissection of pathogenic mechanisms of multiple viruses, examination of multilayered interactions among viruses, their host plants, and virus-transmitting arthropod vectors, and in-depth interrogation of plant-encoded resistance and susceptibility determinants. Notably, various plant virus-based vectors have also been successfully developed for gene function studies and target gene expression in plants. We also recommend future plant virology studies in China.

Fleshy fruits become more susceptible to pathogen infection when they ripen; for example, changes in cell wall properties related to softening make it easier for pathogens to infect fruits. The need for high-quality fruit has driven extensive research on improving pathogen resistance in important fruit crops such as tomato (Solanum lycopersicum). In this review, we summarize current progress in understanding how changes in fruit properties during ripening affect infection by pathogens. These changes affect physical barriers that limit pathogen entry, such as the fruit epidermis and its cuticle, along with other defenses that limit pathogen growth, such as preformed and induced defense compounds. The plant immune system also protects ripening fruit by recognizing pathogens and initiating defense responses involving reactive oxygen species production, mitogen-activated protein kinase signaling cascades, and jasmonic acid, salicylic acid, ethylene, and abscisic acid signaling. These phytohormones regulate an intricate web of transcription factors (TFs) that activate resistance mechanisms, including the expression of pathogenesis-related genes. In tomato, ripening regulators, such as RIPENING INHIBITOR and NON_RIPENING, not only regulate ripening but also influence fruit defenses against pathogens. Moreover, members of the ETHYLENE RESPONSE FACTOR (ERF) family play pivotal and distinct roles in ripening and defense, with different members being regulated by different phytohormones. We also discuss the interaction of ripening-related and defense-related TFs with the Mediator transcription complex. As the ripening processes in climacteric and non-climacteric fruits share many similarities, these processes have broad applications across fruiting crops. Further research on the individual contributions of ERFs and other TFs will inform efforts to diminish disease susceptibility in ripe fruit, satisfy the growing demand for high-quality fruit and decrease food waste and related economic losses.

Plants have evolved complex physical and chemical defense systems that allow them to withstand herbivory infestation. Composed of a complex mixture of very-long-chain fatty acids (VLCFAs) and their derivatives, cuticular wax constitutes the first physical line of defense against herbivores. Here, we report the function of Glossy 8 (ZmGL8), which encodes a 3-ketoacyl reductase belonging to the fatty acid elongase complex, in orchestrating wax production and jasmonic acid (JA)-mediated defenses against herbivores in maize (Zea mays). The mutation of GL8 enhanced chemical defenses by activating the JA-dependent pathway. We observed a trade-off between wax accumulation and JA levels across maize glossy mutants and 24 globally collected maize inbred lines. In addition, we demonstrated that mutants defective in cuticular wax biosynthesis in Arabidopsis thaliana and maize exhibit enhanced chemical defenses. Comprehensive transcriptomic and lipidomic analyses indicated that the gl8 mutant confers chemical resistance to herbivores by remodeling VLCFA-related lipid metabolism and subsequent JA biosynthesis and signaling. These results suggest that VLCFA-related lipid metabolism has a critical role in regulating the trade-offs between cuticular wax and JA-mediated chemical defenses.

NONEXPRESSER OF PATHOGENESIS-RELATED GENES 1 (NPR1), the receptor for salicylic acid (SA), plays a central role in the SA-mediated basal antiviral responses. Recent studies have shown that two different plant RNA viruses encode proteins that suppress such antiviral responses by inhibiting its SUMOylation and inducing its degradation, respectively. However, it is unclear whether targeting NPR1 is a general phenomenon in viruses and whether viruses have novel strategies to inhibit NPR1. In the present study, we report that two different positive-sense single-stranded RNA (+ssRNA) viruses, namely, alfalfa mosaic virus (AMV) and potato virus X (PVX); one negative-sense single-stranded RNA (−ssRNA) virus (calla lily chlorotic spot virus, CCSV); and one single-stranded DNA virus (beet severe curly-top virus, BSCTV) that also encode one or more proteins that interact with NPR1. In addition, we found that the AMV-encoded coat protein (CP) can induce NPR1 degradation by recruiting S-phase kinase-associated protein 1 (Skp1), a key component of the Skp1/cullin1/F-box (SCF) E3 ligase. In contrast, the BSCTV-encoded V2 protein inhibits NPR1 function, probably by affecting its nucleocytoplasmic distribution via the nuclear export factor ALY. Taken together, these data suggest that NPR1 is one of the central hubs in the molecular arms race between plants and viruses and that different viruses have independently evolved different strategies to target NPR1 and disrupt its function.

Calcium ions (Ca²⁺) are crucial intracellular second messengers in eukaryotic cells. Upon pathogen perception, plants generate a transient and rapid increase in cytoplasmic Ca²⁺ levels, which is subsequently decoded by Ca²⁺ sensors and effectors to activate downstream immune responses. The elevation of cytosolic Ca²⁺ is commonly attributed to Ca²⁺ influx mediated by plasma membrane-localized Ca²⁺–permeable channels. However, the contribution of Ca²⁺ release triggered by intracellular Ca²⁺-permeable channels in shaping Ca²⁺ signaling associated with plant immunity remains poorly understood. This review discusses recent advances in understanding the mechanism underlying the shaping of Ca²⁺ signatures upon the activation of immune receptors, with particular emphasis on the identification of intracellular immune receptors as non-canonical Ca²⁺-permeable channels. We also discuss the involvement of Ca²⁺ release from the endoplasmic reticulum in generating Ca²⁺ signaling during plant immunity.

Pathogens generate and secrete effector proteins to the host plant cells during pathogenesis to promote virulence and colonization. If the plant carries resistance (R) proteins that recognize pathogen effectors, effector‐triggered immunity (ETI) is activated, resulting in a robust immune response and hypersensitive response (HR). The bipartite effector AvrRps4 from Pseudomonas syringae pv. pisi has been well studied in terms of avirulence function. In planta , AvrRps4 is processed into two parts. The C‐terminal fragment of AvrRps4 (AvrRps4^C) induces HR in turnip and is recognized by the paired resistance proteins AtRRS1/AtRPS4 in Arabidopsis. Here, we show that AvrRps4^C targets a group of Arabidopsis WRKY, including WRKY46, WRKY53, WRKY54, and WRKY70, to induce its virulence function. Indeed, AvrRps4^C suppresses the general binding and transcriptional activities of immune‐positive regulator WRKY54 and WRKY54‐mediated resistance. AvrRps4^C interferes with WRKY54's binding activity to target gene SARD1 in vitro, suggesting WRKY54 is sequestered from the SARD1 promoter by AvrRps4^C. Through the interaction of AvrRps4^C with four WRKYs, AvrRps4 enhances the formation of homo‐/ heterotypic complexes of four WRKYs and sequesters them in the cytoplasm, thus inhibiting their function in plant immunity. Together, our results provide a detailed virulence mechanism of AvrRps4 through its C‐terminus.

During their co-evolution with herbivorous insects, plants have developed multiple defense strategies that resist pests, such as releasing a blend of herbivory-induced plant volatiles (HIPVs) that repel pests or recruit their natural enemies. However, the responses of insects to HIPVs in maize (Zea mays L.) are not well understood. Here, we demonstrate that the Asian corn borer (ACB, Ostrinia furnacalis), a major insect pest of maize, shows a preference for maize pre-infested with ACB larvae rather than being repelled by these plants. Through combined transcriptomic and metabolomics analysis of ACB-infested maize seedlings, we identified two substances that explain this behavior: (E)-4,8-dimethylnona-1,3,7-triene (DMNT) and (3E,7E)-4,8,12-trimethyltrideca-1,3,7,11-tetraene (TMTT). DMNT and TMTT attracted ACB larvae, and knocking out the maize genes responsible for their biosynthesis via gene editing impaired this attraction. External supplementation with DMNT/TMTT hampered the larvae's ability to locate pre-infested maize. These findings uncover a novel role for DMNT and TMTT in driving the behavior of ACB. Genetic modification of maize to make it less detectable by ACB might be an effective strategy for developing maize germplasm resistant to ACB and for managing this pest effectively in the field.

Plants need to fine-tune defense responses to maintain a robust but flexible host barrier to various pathogens. Helix-loop-helix/basic helix-loop-helix (HLH/bHLH) complexes play important roles in fine-tuning plant development. However, the function of these genes in plant immunity and how they are regulated remain obscure. Here, we identified an atypical bHLH transcription factor, Oryza sativa (Os)HLH46, that interacts with rice receptor-like cytoplasmic kinase (RLCK) Os BRASSINOSTEROID-SIGNALING KINASE1-2 (OsBSK1-2), which plays a key role in rice blast resistance. OsBSK1-2 stabilized OsHLH46 both in vivo and in vitro. In addition, OsHLH46 positively regulates rice blast resistance, which depends on OsBSK1-2. OsHLH46 has no transcriptional activation activity and interacts with a typical bHLH protein, OsbHLH6, which negatively regulates rice blast resistance. OsbHLH6 binds to the promoter of OsWRKY45 and inhibits its expression, while OsHLH46 suppresses the function of OsbHLH6 by blocking its DNA binding and transcriptional inhibition of OsWRKY45. Consistent with these findings, OsWRKY45 was up-regulated in OsHLH46-overexpressing plants. In addition, the oshlh46 mutant overexpressing OsbHLH6 is more susceptible to Magnaporthe oryzae than is the wild type, suggesting that OsHLH46 suppresses OsbHLH6-mediated rice blast resistance. Our results not only demonstrated that OsBSK1-2 regulates rice blast resistance via the OsHLH46/OsbHLH6 complex, but also uncovered a new mechanism for plants to fine-tune plant immunity by regulating the HLH/bHLH complex via RLCKs.

Plant viruses cause substantial agricultural devastation and economic losses worldwide. Plant nucleotide-binding domain leucine-rich repeat receptors (NLRs) play a pivotal role in detecting viral infection and activating robust immune responses. Recent advances, including the elucidation of the interaction mechanisms between NLRs and pathogen effectors, the discovery of helper NLRs, and the resolution of the ZAR1 resistosome structure, have significantly deepened our understanding of NLR-mediated immune responses, marking a new era in NLR research. In this scenario, significant progress has been made in the study of NLR-mediated antiviral immunity. This review comprehensively summarizes the progress made in plant antiviral NLR research over the past decades, with a focus on NLR recognition of viral pathogen effectors, NLR activation and regulation, downstream immune signaling, and the engineering of NLRs.

Systemin, the first peptide hormone identified in plants, was initially isolated from tomato (Solanum lycopersicum) leaves. Systemin mediates local and systemic wound-induced defense responses in plants, conferring resistance to necrotrophic fungi and herbivorous insects. Systemin is recognized by the leucine-rich-repeat receptor-like kinase (LRR-RLK) receptor SYSTEMIN RECEPTOR1 (SYR1), but how the systemin recognition signal is transduced to intracellular signaling pathways to trigger defense responses is poorly understood. Here, we demonstrate that SERK family LRR-RLKs function as co-receptors for SYR1 to mediate systemin signal transduction in tomato. By using chemical genetic approaches coupled with engineered receptors, we revealed that the association of the cytoplasmic kinase domains of SYR1 with SERKs leads to their mutual trans-phosphorylation and the activation of SYR1, which in turn induces a wide range of defense responses. Systemin stimulates the association between SYR1 and all tomato SERKs (SlSERK1, SlSERK3A, and SlSERK3B). The resulting SYR1-SlSERK heteromeric complexes trigger the phosphorylation of TOMATO PROTEIN KINASE 1B (TPK1b), a receptor-like cytoplasmic kinase that positively regulates systemin responses. Additionally, upon association with SYR1, SlSERKs are cleaved by the Pseudomonas syringae effector HopB1, further supporting the finding that SlSERKs are activated by systemin-bound SYR1. Finally, genetic analysis using Slserk mutants showed that SlSERKs are essential for systemin-mediated defense responses. Collectively, these findings demonstrate that the systemin-mediated association of SYR1 and SlSERKs activates defense responses against herbivorous insects.

Late blight pathogen Phytophthora infestans secretes numerous effectors to suppress plant immunity. However, little is known about their underlying biochemical mechanisms. Here we report that, in the host Nicotiana benthamiana, P. infestans core RXLR effector Pi17063 suppresses plant immunity by targeting the host plasma membrane and NbRab-G3 proteins, small GTPases of the Ras-related brain (Rab) family. Pi17063 functions as their specific GTPase-activating protein (GAP), driving them to the cytoplasm-localized guanosine diphosphate (GDP)-bound inactive state. Mutant analysis of the conserved Pi17063 arginine residues showed the essential role of its GAP activity for virulence contribution. All four NbRab-G3 subfamily members are positive immune regulators, and NbRab-G3c mutants lost the ability to switch between active and inactive states and showed compromised immune function. Consistent with this, both silencing and overexpression of an endogenous GAP, NbGYP, inhibited NbRab-G3c-mediated plant immunity. Our results revealed positive immune roles of host NbRab-G3 GTPases, the importance of their state balance, and the biochemical mechanism by which their functions are suppressed by a P. infestans effector, providing insights into understanding eukaryotic effector-mediated plant susceptibility.

Rice black-streaked dwarf virus (RBSDV) is a major viral pathogen threatening rice production worldwide. However, the molecular mechanisms underlying the arms race between RBSDV and its host remain largely elusive. Here, we demonstrate that RBSDV infection, or the expression of viral RNA-silencing suppressor protein P6, promotes the ubiquitination and degradation of rice small ubiquitin-like modifiers (SUMO) conjugating enzyme 1b (OsSCE1b). OsSCE1b catalyzes the SUMOylation of OsPelota, a protein involved in plant antiviral RNA decay. Furthermore, RBSDV P6 enhances the interaction between rice ubiquitin E3 ligases SINAT3/4/5 and OsSCE1b in the cytoplasm, leading to increased ubiquitination and degradation of OsSCE1b. Rice plants overexpressing OsSCE1b exhibited reduced susceptibility to RBSDV infection. Conversely, OsSCE1b knockdown and knockout lines, as well as OsPelota knockout lines, were more susceptible, indicating that both OsSCE1b and OsPelota negatively regulate RBSDV infection. Additionally, our findings show that OsSCE1b-catalyzed SUMOylated OsPelota interacts with the Hsp70 subfamily B suppressor OsHBS1, forming a complex that degrades RBSDV genomic RNAs containing one or more GA₆ motifs. Taken together, our data demonstrate that OsSCE1b negatively regulates RBSDV infection by promoting OsPelota SUMOylation and activating the antiviral RNA decay activity of the OsPelota–OsHBS1 complex. Conversely, RBSDV P6 promotes viral infection by enhancing OsSCE1b ubiquitination and degradation, thereby suppressing OsPelota SUMOylation and the rice antiviral RNA decay defense response.

Transcription activator-like effectors (TALEs) mimic eukaryotic transcriptional activators and translocate into host plant cells via the bacterial type III secretion system (T3SS) during pathogenic interactions. They play a crucial role in disease development by regulating host genes. Despite this, the regulatory mechanisms by which TALEs control OsWRKY transcription factors (TFs) remain poorly understood. In this study, we show that two TALEs from Xanthomonas oryzae pv. oryzae (Xoo) individually modulate two OsWRKY TFs, resulting in increased susceptibility and reduced host defense. Specifically, Xoo1219 and Xoo2145 activate the expression of OsWRKY104 and OsWRKY55, respectively, through direct interactions. OsWRKY104 increases the susceptibility to Xoo by activating OsSWEET11 and OsSWEET14, while OsWRKY55 suppresses host defense against Xoo by directly regulating OsWRKY62. These findings suggest that TALEs hijack the host's OsWRKY TFs to create a favorable environment for bacterial survival.