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Plant viruses typically rely on insect vectors for transmission between plants, with insect salivary proteins playing critical roles in this process. In this study, we demonstrate how Laodelphax striatellus salivary carbonic anhydrase (LssaCA) promotes rice stripe virus (RSV) infection in plants. We discovered that LssaCA directly binds to RSV nucleocapsid protein (NP) in insect salivary glands. This LssaCA-NP complex interacts with a rice thaumatin-like protein (OsTLP) that possesses endo-β-1,3-glucanase activity potentially degrading callose. Upon binding, the LssaCA-NP complex significantly enhances OsTLP enzymatic activity. We further clarify that both L. striatellus feeding and RSV infection induce callose deposition. The tripartite LssaCA-NP-OsTLP interaction enhances callose degradation, thereby facilitating RSV infection via its insect vector. This study provides new insights into complex virus-insect-plant tripartite interactions mediated by insect salivary proteins, with broad implications for numerous plant viruses transmitted by insect vectors.

Pandemics of vector-borne human and plant diseases often depend on the behaviors of their arthropod vectors. Arboviruses, including many bunyaviruses, manipulate vector behavior to accelerate their own transmission to vertebrates, birds, insects, and plants. However, the molecular mechanism underlying this manipulation remains elusive. Here, we report that the non-structural protein NSs of Tomato spotted wilt orthotospovirus, a prototype of the Tospoviridae family and the Orthotospovirus genus, is a key viral factor that indirectly modifies vector preference and increases vector performance. NSs suppresses the biosynthesis of plant volatile monoterpenes, which serve as repellents of the vector western flower thrips (WFT, Frankliniella occidentalis). NSs directly interacts with MYC2, the jasmonate (JA) signaling master regulator and its two close homologs MYC3 and MYC4, to disable JA-mediated activation of terpene synthase genes. The dysfunction of the MYCs subsequently attenuates host defenses, increases the attraction of thrips, and improves thrips fitness. Moreover, MYC2 associated with NSs of Tomato zonate spot orthotospovirus, another Euro/Asian-type orthotospovirus, suggesting that MYC2 is an evolutionarily conserved target of Orthotospovirus species for suppression of terpene-based resistance to promote vector performance. These findings elucidate the molecular mechanism through which an orthotospovirus indirectly manipulates vector behaviors and therefore facilitates pathogen transmission. Our results provide insights into the molecular mechanisms by which Orthotospovirus NSs counteracts plant immunity for pathogen transmission.

Rice (Oryza sativa), the staple food for almost half of the world's population, prefers ammonium (NH4 +) as the major nitrogen resource, and while NH4 + has profound effects on rice growth and yields, the underlying regulatory mechanisms remain largely unknown. Brassinosteroids (BRs) are a class of steroidal hormones playing key roles in plant growth and development. In this study, we show that NH4 + promotes BR biosynthesis through miR444 to regulate rice root growth. miR444 targeted five homologous MADS-box transcription repressors potentially forming homologous or heterogeneous complexes in rice. miR444 positively regulated BR biosynthesis through its MADS-box targets, which directly repress the transcription of BR-deficient dwarf 1 (OsBRD1), a key BR biosynthetic gene. NH4 + induced the miR444-OsBRD1 signaling cascade in roots, thereby increasing the amount of BRs, whose biosynthesis and signaling were required for NH4 +-dependent root elongation inhibition. Consistently, miR444-overexpressing rice roots were hypersensitive to NH4 + depending on BR biosynthesis, and overexpression of miR444's target, OsMADS57, resulted in rice hyposensitivity to NH4 + in root elongation, which was associated with a reduction of BR content. In summary, our findings reveal a cross talk mechanism between NH4 + and BR in which NH4 + activates miR444-OsBRD1, an undescribed BR biosynthesis-promoting signaling cascade, to increase BR content, inhibiting root elongation in rice.

Nucleotide-binding leucine-rich repeat receptors (NLRs) function as core components of innate immunity in both plants and animals. In animals, NLR activation initiates caspase-mediated immune signaling. In contrast, plants lack caspases but instead contain metacaspases (MCAs/MCs), yet their role in antiviral immunity and whether they interface with NLR signaling remain largely unexplored. Here, we demonstrate that cleavage of the conserved immune regulator Bcl-2-associated athanogene 3 (BAG3) by metacaspase 4 (MCAIIa/MC4) induces cell death and activates antiviral immunity in plants. Upon Begomovirus infection, MC4 cleaves BAG3 to release its N-terminal functional domain (BAG3-N) from autoinhibition. BAG3-N assembles into oligomers and induces cell death, effectively inhibiting viral replication. This signaling also interfaces with NLR networks in certain plant species. Viral replication-associated proteins (Reps) counteract this defense response by binding to BAG3-N, highlighting an evolutionary arms race between plants and viruses. Evolutionary analyses reveal that a lysine substitution at position 50 of BAG3 confers its ability to induce cell death in angiosperms. These findings identify BAG3 as a conserved immune regulator linking metacaspase activation to antiviral defense, providing a mechanistic basis for engineering crops with enhanced resistance to insect-borne viruses. This study identifies BAG3 as a conserved immune regulator in plants and demonstrates that its cleavage by metacaspase 4 triggers cell death and antiviral defense, offering a potential strategy for engineering virus-resistant crops.

We previously observed decreased expression of rice OsmiR159a.1 on infection with the bacterial blight‐causing pathogen Xanthomonas oryzae pv. oryzae (Xoo), and identified the OsLRR_RLK (leucine‐rich repeat_ receptor like kinase) gene as an authentic target of OsmiR159a.1. Here, we found that a Tos17 insertion mutant of LRR_RLK displayed increasing temporal resistance to Xoo, whereas the LRR_RLK overexpression lines were susceptible to the pathogen early on in the infection, indicating that LRR_RLK encodes a repressor of rice resistance to Xoo infection, and it was renamed as RIR1 (Rice Immunity Repressor 1). RIR1 overexpression plants were more susceptible to Xoo at late growth stage, suggesting that RIR1 mRNA levels are negatively correlated with the resistance of rice against Xoo. We discovered that OsmiR159a.1 repression in Xoo‐infected plants was largely dependent on the pathogen's type III secretion system. Co‐immunoprecipitation, bimolecular fluoresence complementation, and pull‐down assays indicated that RIR1 interacted with the NADH‐ubiquinone oxidoreductase (NUO) 51‐kDa subunit of the mitochondrial complex I through its kinase domain. Notably, impairment of RIR1 or overexpression of NUO resulted in reactive oxygen species accumulation and enhanced expression of pathogen‐resistance genes, including jasmonic acid pathway genes. We propose that pathogens may inhibit OsmiR159 to interfere with the RIR1–NUO interaction, and subsequently depression of rice immune signalling pathways. The resistance genes manipulated by Xoo can be a probe to explore the regulatory network during host–pathogen interactions. Xanthomonas oryzae may use type III effectors to inhibit OsmiR159 and release its target rice gene RIR1 expression, then promote RIR1–NUO interaction that leads to depression of rice immune signalling pathways.

Tiller angle of cereal crops is a key agronomic trait that contributes to grain production. An understanding of how tiller angle is controlled is helpful for achieving ideal plant architecture to improve grain yield. Phytochrome-interacting factors (PIFs) are known to regulate seed germination, seedling skotomorphogenesis, shade avoidance, and flowering in Arabidopsis thaliana. Here, we report that OsPIL15 is, indeed, a rice PIF that negatively regulates tiller angle. Dominant-negative OsPIL15 plants displayed a larger tiller angle, which was associated with reduced shoot gravitropism. Phytochrome B (phyB) is the main photoreceptor perceiving the low red:far-red ratio of shade light. Compared with wild-type rice plants, loss-offunction phyB plants and OsPIL15-overexpressing plants showed smaller tiller angles and enhanced shoot gravitropism. In addition, more OsPIL15 protein accumulated in phyB plants than in wild-type plants. Light regulates the level of the OsPIL15 protein negatively, depending on phyB partially. We propose that OsPIL15 integrates light and gravity signals to regulate tiller angle in rice.

Insect vitellogenin (Vg) has been considered to be synthesized in the fat body. Here, we found that abundant Vg protein is synthesized in Laodelphax striatellus hemocytes as well. We also determined that only the hemocyte-produced Vg binds to Rice stripe virus (RSV) in vivo. Examination of the subunit composition of L. striatellus Vg (LsVg) revealed that LsVg was processed differently after its expression in different tissues. The LsVg subunit able to bind to RSV exist stably only in hemocytes, while fat body-produced LsVg lacks the RSV-interacting subunit. Nymph and male L. striatellus individuals also synthesize Vg but only in hemocytes, and the proteins co-localize with RSV. We observed that knockdown of LsVg transcripts by RNA interference decreased the RSV titer in the hemolymph, and thus interfered with systemic virus infection. Our results reveal the sex-independent expression and tissue-specific processing of LsVg and also unprecedentedly connect the function of this protein in mediating virus transmission to its particular molecular forms existing in tissues previously known as non-Vg producing.

Most plant viruses are transmitted by hemipteroid insects. Some viruses can be transmitted from female parent to offspring usually through eggs, but the mechanism of this transovarial transmission remains unclear. Rice stripe virus (RSV), a Tenuivirus, transmitted mainly by the small brown planthopper (Laodelphax striatellus), is also spread to the offspring through the eggs. Here, we used the RSV-planthopper system as a model to investigate the mechanism of transovarial transmission and demonstrated the central role of vitellogenin (Vg) of L. striatellus in the process of virus transmission into the eggs. Our data showed Vg can bind to pc3 in vivo and in vitro and colocalize in the germarium. RSV filamentous ribonucleoprotein particles (RNPs) only accumulated in the terminal filaments and pedicel areas prior to Vg expression and was not present in the germarium until Vg was expressed, where RSV RNPs and Vg had colocalized. Observations by immunoelectron microscopy (IEM) also indicated that these two proteins colocalized in nurse cells. Knockdown of Vg expression due to RNA interference resulted in inhibition of the invasion of ovarioles by RSV. Together, the data obtained indicated that RSV RNPs may enter the nurse cell of the germarium via endocytosis through binding with Vg. Finally, the virus enters the oocytes through nutritive cords, using the same route as for Vg transport. Our results show that the Vg of L. striatellus played a critical role in transovarial transmission of RSV and shows how viruses can use existing transovarial transportation systems in insect vectors for their own purposes.

Plant endophytic bacteria colonize the internal tissues of plants and interact with plants closely. The past two decades have witnessed the increasing application of next-generation 16S rRNA gene sequencing in the investigation of bacterial communities. However, deciphering plant endo-bacterial communities by this method is difficult because of the co-amplification of massive plant organellar DNAs with bacterial 16S. Here, we designed polymerase chain reaction (PCR) primer sets, including 799F/1107R, 322F/796R, and 322F-Dr/796Rs (primer pair 322F/796R with a penultimate-base substitution in 322F), that can specifically amplify bacterial 16S from plant total DNAs. We computationally and experimentally evaluated the specificity, coverage, and accuracy of the newly designed primer sets. Both 799F/1107R and 322F-Dr/796Rs produced plant DNA-free 16S amplicon libraries or reduced plant DNA contamination to lower than 5% for the plant materials with extremely-low-abundance bacterial communities. The primer set 322F-A/796R was used through absolute quantitative PCR to quantitate the population size of rice leaf or root endo-bacteriome, which revealed 10 6 –10 7 and 10 9 –10 10 bacteria per gram fresh weight, respectively. These 16S primer sets and amplification methods enable the simple and inexpensive next-generation sequencing and quantification of plant endo-bacteriome, which will significantly advance studies on the plant-related microbiome.

Background Rice cultivation relies on planting grains harboring beneficial microbiota. However, the origination, distribution, and transmission dynamics of grain-borne bacteria remain unclear. Results Using rice grain as a model system, this study investigates the primary sources, major niches in seeds, and the dynamics of community acquisition, maintenance, and transmission between generations of grain-borne bacteria. Quantitative PCR and 16S rRNA gene sequencing demonstrate rice grains acquiring bacteria primarily from the external environment during panicle heading and flowering. These bacteria concentrate between the caryopsis and glumes, establishing sizable communities in developing seeds. The dominant taxa included Pantoea , Pseudomonas , and Sphingomonas . Throughout seed development and storage, community structure remains consistent while abundance fluctuates within one order of magnitude. Upon germination under axenic conditions, seed bacteria successfully colonize shoots and roots of offspring seedlings. However, bacteria transmitted solely through internal routes fail to form comparably large communities. Analysis of taxonomic composition uncovers dramatic reshaping from seeds to seedlings, potentially reflecting functional adaptation. Conclusions We clarify seed-borne bacterial origination, acquisition timing, seed colonization, intergenerational transmission, and seedling diversification. Our findings provide novel insights into rice seed bacterial dynamics critical for microbiome management. 9FJ-hzomPrM-V3Zi4Nmp4K Video Abstract