Wangsheng Zhu

Rice is a staple crop for more than half of the world’s population, and its sustainable production is vital to ensure global food security. However, rice is susceptible to several devastating fungal diseases¹, including blast disease caused by Magnaporthe oryzae, sheath blight by Rhizoctonia solani, false smut by Ustilaginoidea virens, brown spot by Bipolaris oryzae, bakanae by Fusarium fujikuroi and head blight by Fusarium graminearum. The mechanisms underlying the susceptibility to these fungal diseases remain unclear. Here we report that the β subunit of SnRK1, SnRK1β1A, confers broad-spectrum susceptibility to these fungal diseases. Our findings show that diverse rice fungal pathogens have convergently evolved an effector-like protein, Gas2, which interacts with SnRK1β1A to prevent its ubiquitination-mediated degradation and promotes its nuclear translocation. SnRK1β1A is markedly induced on fungal infection, promoting susceptibility by inhibiting SnRK1α1, an α subunit of SnRK1 known to positively regulate broad-spectrum resistance in rice². Notably, rice lines with disrupted SnRK1β1A are resistant to several fungal diseases without compromising growth and yield in the field under normal farming conditions. This study demonstrates that broad-spectrum disease resistance in crops can be achieved by disrupting inducible susceptibility genes whose encoded proteins are targeted by effectors conserved across several pathogens.

Background: Fumonisin B1 (FB1) is a toxic secondary metabolite produced by Fusarium species that commonly contaminates cereal crops, posing serious threats to crop productivity and food safety. In plants, FB1 inhibits ceramide synthase, disrupts sphingolipid metabolism, and induces growth inhibition and programmed cell death. Despite the agricultural importance of fumonisin contamination, genetic strategies to enhance FB1 tolerance or detoxification capacity in crops remain limited, largely due to an incomplete understanding of the underlying genetic determinants. Methods: To identify genetic determinants associated with FB1 tolerance, we exploited natural variation in Arabidopsis thaliana and conducted a genome-wide association study (GWAS). Candidate genes were further examined using gene expression analyses and functional characterization of overexpression and SALK mutant lines. Results: GWAS revealed a significant association locus on chromosome 1 linked to FB1 tolerance. Two adjacent genes within this locus, AT1G14750 and AT1G14755, were identified as positive regulators of FB1 tolerance. Both genes were rapidly induced upon FB1 exposure. Functional analyses demonstrated that overexpression of either gene significantly enhanced tolerance to FB1-induced damage, whereas SALK mutant lines displayed increased sensitivity, manifested by enhanced growth inhibition and necrosis. Conclusions: Our study identifies AT1G14750 and AT1G14755 as previously uncharacterized components of FB1 tolerance in Arabidopsis. These findings provide new insights into the genetic architecture of plant response to mycotoxin stress and establish a foundation for further studies on the molecular mechanisms underlying FB1 tolerance.

Rhizoctonia solani , a globally distributed phytopathogen, causes banded leaf and sheath blight (BLSB) in maize and sheath blight in rice, severely threatening crop productivity. Here, this work identifies ZmRRS1 (Resistance to Rhizoctonia solani 1), which encodes maize malate dehydrogenase, as a key positive regulator of BLSB resistance in the field through a genome‐wide association study. ZmRRS1 knockout lines exhibit increased susceptibility to BLSB, whereas overexpression of ZmRRS1 and its homologs confer enhanced resistance to R. solani in both maize and rice. Using heterozygote inbred families (HIF), this work uncovers that the presence and absence of a 831‐bp transposable element (TE) element is the causal polymorphism that determines the differential expression pattern of the two ZmRRS1 alleles in response to R. solani . Furthermore, the absence of the TE increases the binding of the ZmWRKY44 transcription factor to the W‐box motif in the promoter of ZmRRS1 , thereby enhancing BLSB resistance. Transcriptomic analysis reveals that ZmRRS1 potentiates reactive oxygen species (ROS)‐mediated immunity against BLSB. Notably, the overexpression of ZmRRS1 does not incur agronomic penalties under normal growth conditions. Collectively, this work identifies ZmRRS1 as a positive regulator of BLSB resistance, offering valuable genetic resources for breeding BLSB‐resistant maize and rice varieties.

Pathogens deploy effectors to suppress host immune responses and enable successful colonization in plants. While apoplastic effectors have major roles in pathogenicity, whether and how they directly attack extracellular immune receptors remains unclear. Here we identify an apoplastic effector FgLPMO9A from the fungal pathogen Fusarium graminearum that directly inhibits maize immune receptor ZmLecRK1-mediated resistance. FgLPMO9A belongs to the polysaccharide monooxygenase family, which depolymerizes polysaccharides. Deletion of FgLPMO9A attenuates F. graminearum virulence on maize, but this defect is fully rescued in the zmlecrk1 mutants. FgLPMO9A interacts with the extracellular S-domain of ZmLecRK1 and disrupts N-glycosylation at the N341 site, thereby promoting ZmLecRK1 degradation via the NBR1-mediated autophagy pathway. Notably, the ZmLecRK1 variant with the N341Q substitution confers enhanced resistance to F. graminearum in maize. We demonstrate that F. graminearum dampens maize immunity by deploying an apoplastic effector to induce extracellular immune receptor degradation.

Growth and defence are inversely correlated processes requiring balance for optimal fitness. While each is well studied, their regulatory trade-offs are less understood. Using DANGEROUS MIX ( DM ) autoimmune plants with stunted growth in Arabidopsis thaliana , we investigated the balancing act. Transcriptome analysis of three DM cases and pathogen-treated seedlings identified two major modules representing defence and growth. These core modules, comprising 4,712 genes (∼17% of the transcriptome), were sufficient for projecting the trade-off across immune transcriptome meta-datasets. Removing all three ADR1s , the helper NLRs, reversed the expression patterns of both modules and shifted the trade-off balance. ADR1s had a stronger impact on growth-associated RLK genes than on defence genes. Autoimmune plants also showed greater chromatin accessibility changes in growth loci than in defence loci. Our findings suggest an unexpected mechanism where immune signalling, partly mediated by ADR1s , actively suppresses growth genes, providing a strategy to regulate the growth-defence trade-off.

Summary: Rice is a staple crop for over half of the world’s population, and its sustainable production is vital to ensure global food security. However, rice is highly susceptible to several devastating fungal diseases ¹ , including blast disease caused by Magnaporthe oryzae , sheath blight by Rhizoctonia solani , false smut by Ustilaginoidea virens , brown spot by Bipolaris oryzae , bakanae by Fusarium fujikuroi , and head blight by F. graminearum . The mechanisms underlying the susceptibility of rice to these fungal diseases remain unclear. Here, we report that the β subunit of SnRK1, SnRK1β1A, confers broad-spectrum susceptibility to these fungal diseases. Our findings reveal that diverse rice fungal pathogens have convergently evolved an effector, Gas2, which interacts with SnRK1β1A to prevent its ubiquitination-mediated degradation and promotes its nuclear translocation. While SnRK1 β 1A is expressed at low levels in healthy plants, its expression is markedly induced upon fungal infections, facilitating susceptibility by inhibiting SnRK1α1, the α subunit of SnRK1, whose overexpression has been shown to enhance broad-spectrum resistance in rice ² . Notably, rice lines with disrupted SnRK1 β 1A are resistant to multiple fungal diseases without compromising growth and yield in the field. Together, this study demonstrates that broad-spectrum disease resistance in crops can be achieved by disrupting inducible susceptibility genes whose encoded proteins are targeted by effectors conserved in multiple pathogens.

The origin of genes from non-coding sequences is a long-term and fundamental biological question. However, how de novo genes originate and integrate into the existing pathways to regulate phenotypic variations is largely unknown. Here, we selected seven genes from 782 de novo genes for functional exploration based on transcriptional and translational evidence. Subsequently, we revealed that SWK, a de novo gene that originated from a non-coding sequence in Arabidopsis thaliana, plays a role in seed germination under osmotic stress. SWK is primarily expressed in dry seed, imbibing seed and silique. SWK can be fully translated into an 8 kDa protein, which is mainly located in the nucleus. Intriguingly, SWK was integrated into an extant pathway of hydrogen peroxide content (folate synthesis pathway) via the upstream gene cytHPPK/DHPS, an Arabidopsis-specific gene that originated from the duplication of mitHPPK/DHPS, and downstream gene GSTF9, to improve seed germination in osmotic stress. In addition, we demonstrated that the presence of SWK may be associated with drought tolerance in natural populations of Arabidopsis. Overall, our study highlights how a de novo gene originated and integrated into the existing pathways to regulate stress adaptation.