Tingting Zhao

Key message Our study revealed that SlTCP16 can transcriptional activation and interaction with Sl4CL3, thereby enhancing the tomato’s resistance to Pst DC3000. This resistance is associated with an increased accumulation of lignin. Abstract Lignin deposition serves as a critical physical barrier against bacterial pathogens. However, the precise regulatory networks orchestrating this defense response in tomato remain incompletely understood. We identify the transcription factor SlTCP16 as a novel positive regulator of tomato immunity against Pseudomonas syringae pv. tomato (Pst DC3000). We show that Pst DC3000 infection strongly induces SlTCP16 expression. Functionally, SlTCP16 overexpression significantly reduced reactive oxygen species (ROS) accumulation and bolstered disease resistance, while SlTCP16 knockout mutants showed the opposite performance. Mechanistically, we uncover a dual regulatory mode, SlTCP16 not only directly activates the transcription of the lignin biosynthetic gene Sl4CL3 by binding to its promoter but also physically interacts with the Sl4CL3 protein. Sl4CL3 acts downstream of SlTCP16, and overexpression of Sl4CL3 enhanced disease resistance in the sltcp16 mutant. Collectively, our data suggest that SlTCP16 contributes to disease resistance by regulating Sl4CL3 through transcriptional activation and protein-protein interaction. This regulatory module is associated with increased lignin accumulation.

Tomato leaf mold caused by Cladosporium fulvum ( C. fulvum ) is a devastating disease in tomato cultivation and production. The Cf gene confers resistance to C. fulvum . In our previous study, several JAZ family genes were found to be differentially expressed between resistant ( Cf‐19‐ mediated) and susceptible materials, especially SlJAZ3 , whose expression was significantly upregulated during the Cf‐19 ‐mediated resistance response process. To explore the regulatory function of JAZ genes in this disease resistance system, this study focused on SlJAZ3 and found that both SlJAZ3 and its interacting protein SlJAZ2 can positively regulate the resistance response mediated by Cf‐19 . In addition, SlMYC2 , as a positive regulator of the resistance response, can interact with SlJAZ2 (or SlJAZ3) and activate the expression of SlPR2 . Notably, SlJAZ3 (or SlJAZ2) competitively binds to SlJAZ2 (or SlJAZ3), reducing its binding to SlMYC2, which helps to restore the transcriptional activation of the downstream defense gene SlPR2 . Our findings reveal that the SlJAZ2/SlJAZ3 dimer regulates downstream signal transduction. This study has improved our understanding of Cf ‐mediated resistance and plant immune mechanisms, laying the foundation for the molecular improvement of tomato disease resistance and endows new significance to the formation of the JAZ‐JAZ dimer.

Bacterial leaf spot disease is among the most common diseases affecting tomato production. It is caused by Pseudomonas syringae pv. tomato (Pst) and severely affects tomato plant growth, development, and yield. In this study, we identified a fructose‐1,6‐diphosphate aldolase gene, SlFBA3 , whose expression was significantly increased in the tomato pathway for resistance to Pst. Overexpression of SlFBA3 enhanced tomato plant resistance, whereas knockout of SlFBA3 reduced the resistance of tomato plants. Further analysis revealed that SlSGR is an interacting protein of SlFBA3. Functional analysis showed that overexpression of SlSGR inhibited the resistance of tomato to Pst, whereas knockout of SlSGR increased resistance. Mechanistically, upon flg22 and csp22 elicitation, SlFBA3 can enhance the early immune signalling pathway, while SlSGR inhibits this response. Notably, we found that SlFBA3 can partially antagonize the function of SlSGR, thereby weakening the negative regulatory role of SlSGR in the disease response. In addition, we discovered that the positive regulatory factor SlARF6A of this disease‐resistant response can target and regulate the transcriptional activation activity of SlFBA3 . In conclusion, we revealed that the SlARF6A–SlFBA3/SlSGR module plays an important role in the resistance response of tomato to Pst, providing a new research direction for disease resistance breeding in tomato.

Seed size affects seed vigor, seedling establishment, and seed utilization in tomato. Yet the genetic basis of this trait remains poorly defined in tomato itself. Here, we describe a stable small–seed mutant, T31, isolated from an ethyl methanesulfonate (EMS)–mutagenized population of the elite inbred line DL5. Relative to the wild type, T31 showed a 24% reduction in seed width, whereas vegetative growth and major fruit traits were largely unchanged. Throughout this study, ‘seed size’ refers to seed width, which was used as the principal index of seed size because tomato seeds are oblate. Genetic analysis of six populations (P₁, P₂, F₁, F₂, BC₁, and BC₂) indicated that the phenotype is controlled by a single recessive locus, designated ssm. Bulked segregant analysis sequencing (BSA–seq) placed ssm within a 1.77 –Mb interval on chromosome 4. KASP–based fine mapping reduced this interval to 390 kb and identified six EMS–type SNPs. Only one of these SNPs was located in an exon of Solyc04g073950.2, where it caused a Pro337Ser substitution. This gene encodes a VQ motif–containing protein and was designated SlVQ10. To test gene function, we generated CRISPR/Cas9 knockout lines in the DL5 background. Two independent homozygous knockout lines reproduced the small–seed phenotype. Seed size was reduced by 31–33%, and thousand–seed weight decreased by 33–35%. Histological analysis further showed reduced seed–coat cell expansion in the mutants. Together, the genetic and genome–editing data support SlVQ10 as the gene underlying ssm and indicate that it promotes seed size in tomato.

Key message The Cf-19 gene, which controls tomato leaf mold, was finely mapped to a 130.13-kb region on chromosome 1, strongly suggesting that Solyc01g006550 may be the target gene Cf-19. Abstract Tomato leaf mold, caused by Cladosporium fulvum (C. fulvum), is a devastating disease affecting tomato production. Natural resistance to this disease is mediated by Cf family genes, with different Cf genes confer resistance to different physiological races of the C. fulvum. As these physiological races continue to evolve, the number of effective resistance genes available for breeding is becoming increasingly limited. Cf-19 is considered a highly effective resistance gene against tomato leaf mold disease, but it has not been successfully cloned yet. In our previous research, we mapped Cf-19 in the 2.14 Mb region of chromosome 1 and predicted seven candidate genes. Due to the large interval, the possibility of some candidate genes cannot be ruled out. In this study, we constructed an F₂ population for fine mapping using CGN18423 (disease resistant) and MoneyMaker (disease susceptible) as parental lines. We localized Cf-19 to a 130.13-kb region on chromosome 1 that contained 12 candidate genes. Through functional annotation, protein domain and expression analysis, Solyc01g006550 (annotated as a receptor-like protein Cf-9 homolog) was proposed as a candidate gene. Functional validation revealed that Solyc01g006550 overexpression increased resistance to C. fulvum, whereas Solyc01g006550 knockout reduced resistance. Subcellular localization indicates that the gene is located on the cell membrane. In conclusion, our data collectively suggest that Solyc01g006550 may be the gene Cf-19.

Previously, research has primarily focused on how the environment affects fruit quality, but there is a lack of studies investigating the impact of different growth stages on fruit quality. In this study, a total of 192 differentially abundant metabolites and 5546 differentially expressed genes were categorized into eight modules exhibiting distinct trends, along with an additional module that remained unchanged throughout all growth stages. These modules elucidate the primary metabolic alterations and transcriptional regulatory networks underlying quality variations in tomato fruits at the mature stage across different growth stages (Spike1–Spike3). Furthermore, an investigation was conducted on the module that remained constant throughout the growth stages. It was observed that the soluble sugar content remained stable across the different growth stages, whereas the levels of total phenols and flavonoids exhibited significant variation. Additionally, the principal metabolites influencing tomato flavor—namely aspartic acid, glutamic acid, glucose, fructose, citric acid, α-linolenic acid, and linoleic acid—did not demonstrate significant changes in content. The findings of this study provide novel insights into the formation of tomato quality and establish a theoretical foundation for the cultivation of long-season tomatoes with stable fruit quality.

Tomato (Solanum lycopersicum L.) is valued for its versatile consumption and rich nutrients. Current research on functional metabolite distribution in tomatoes mostly focuses on a few varieties, limiting comprehensive understanding across different colored types. This study investigated metabolic characteristics and functional metabolite distribution in colored tomatoes via metabolomic analysis and functional metabolite quantification across diverse germplasm resources. Metabolomic analysis identified 910 metabolites from four colored cherry tomato varieties. Significantly differential metabolite analysis revealed most were flavonoids (27 in total) and alkaloids (14 in total). Additionally, KEGG enrichment analysis identified 4 significantly enriched pathways, mainly related to amino acid biosynthesis, degradation, and metabolism. Quantification across 113 tomato germplasm resources revealed that red tomatoes had higher lycopene; brown tomatoes were rich in lycopene, chlorophyll, and β-carotene; green tomatoes contained higher chlorophyll, saponin, vitamin E, and naringenin. This study provides an important reference for consumers to select colored tomatoes and for breeders to conduct targeted genetic improvement.

Studies on how SlPR5 genes are involved in Pst DC3000 disease resistance response are lacking. Here, 27 members of the tomato SlPR5 gene family were identified and analyzed. Analysis of conserved structural domains and promoter structure revealed that SlPR5 family members are structurally conserved and contain a variety of antidisease and antistress response elements. We screened out SlPR5-3, which was significantly upregulated, through an analysis of the expression pattern of Pst DC3000 in tomato after inoculation. We generated SlPR5-3 mutants via CRISPR/Cas9 gene editing and SlPR5-3-overexpressing tomato plants to elucidate the function of this gene. The results showed that the SlPR5-3 overexpression lines had reduced lesions, significantly lower pathogen counts, and significantly higher activity indexes of defense-related enzymes, while the mutant lines showed the opposite, indicating that the SlPR5-3 gene positively regulates the immune response against Pst DC3000 in tomato. In this study, we systematically mined and analyzed the tomato SlPR5 family genes, screened out the important genes in this family for the regulation of Pst DC3000 disease resistance, and verified the disease resistance regulatory function of SlPR5-3, laying the foundation for the theoretical study of tomato Pst DC3000 disease resistance and providing a new molecular target for the future breeding of tomato disease resistance.