Integrated transcriptome and metabolome analysis of resistant and susceptible tomato cultivars in response to tomato mottle mosaic virus and functional characterization of snakin-2 in viral defense.
Assays demonstrated that SlSN2 overexpression suppressed ToMMV accumulation and infection, likely via enhanced lignin biosynthesis, suggesting a potential role for SlSN2 in contributing to ToMMV resistance, independent of the known Tm‑2² pathway.
Abstract
Tomato mottle mosaic virus (ToMMV) is an emerging tobamovirus causing severe losses in tomato production. To elucidate host resistance mechanisms, we compared two tomato cultivars with contrasting responses to ToMMV using integrated transcriptomic, metabolomic, and functional analyses. The resistant line (R) carried resistance gene Tm‑2² at extremely low levels, while the susceptible line (S) did not; both lines highly expressed susceptibility gene tm-2. R plants exhibited minimal viral accumulation and maintained chlorophyll levels, whereas S plants showed high viral load and chlorophyll degradation. Multi-omics revealed that in S, ToMMV primarily disrupted chlorophyll biosynthesis and photosynthesis, while activating multiple defense pathways, including plant-pathogen interaction, phenylpropanoid/flavonoid biosynthesis, and MAPK signaling. In R, a broader activation of plant-pathogen interaction and phosphatidylinositol signaling pathways was observed, alongside early upregulation of SlSN2. The abundance of phenolic acids, notably caffeic acid, ferulic acid, and sinapic acid, was significantly higher in R than in S. Integrated transcriptomic and metabolomic analyses showed that both differential genes and metabolites were co-enriched in the phenylpropanoid biosynthesis pathway. Functional assays demonstrated that SlSN2 overexpression suppressed ToMMV accumulation and infection, likely via enhanced lignin biosynthesis. These findings suggest a potential role for SlSN2 in contributing to ToMMV resistance, independent of the known Tm‑2² pathway. This work identifies SlSN2 as a candidate factor for further evaluation in the prevention of ToMMV.
Tomato is a globally important crop that is frequently affected by stress linked to viral infection and drought, both of which significantly reduce yield and quality. Cucumber mosaic virus (CMV) is a major pathogen that induces severe disease symptoms, while drought limits plant growth and productivity in general. Calcium signaling through cyclic nucleotide-gated channels (CNGCs) plays a critical role in plant responses to both biotic and abiotic stresses. However, it remains unclear how the tomato SlCNGC18, a homolog of Arabidopsis thaliana CNGC4 (DND2), regulates viral resistance and drought tolerance in Micro-Tom plants. Using CRISPR/Cas9 gene editing, we generated loss-of-function slcngc18 mutants in tomato (cv. Micro-Tom) and assessed their responses to CMV infection. Drought-related responses were further evaluated using the slcngc18-2 mutant. The mutants showed enhanced resistance to CMV, with more than a threefold reduction in viral accumulation and milder disease symptoms. This resistance was accompanied by a twofold increase in salicylic acid (SA) levels and induction of the defense gene SlPR1, which showed more than sevenfold upregulation. Consistently, SlPBS3 was also upregulated, suggesting its contribution to increased SA levels. Moreover, under drought conditions, slcngc18-2 plants showed approximately sevenfold higher survival rates and reduced water loss compared with wild-type plants. Physiological analyses revealed altered stomatal traits, characterized by smaller stomata with increased stomatal density, along with enhanced abscisic acid (ABA) signaling despite no change in ABA levels. Furthermore, transcriptome profiling indicated downregulation of genes involved in calcium transport and phenylalanine ammonia-lyase. Our results indicate that SlCNGC18 functions as a negative regulator of CMV resistance and drought tolerance-related responses in Micro-Tom. The slcngc18 mutants exhibited elevated SA levels together with enhanced ABA signaling-related gene expression, supporting SlCNGC18 as a promising target for breeding tomato cultivars with improved resilience to multiple stresses. Overall, this study provides new insight into the potential involvement of calcium channel-mediated signaling in hormonal and immune responses during crop stress adaptation.
Minsu Park, Minsun Oh, Yujin Kweon et al.· BMC Plant Biology· 0 citations
The combined transcriptome and metabolome analysis revealed that plant hormone signal transduction, phenylpropanoid biosynthesis, and flavonoid biosynthesis were significantly enriched in resistant rice varieties, providing valuable information on the molecular mechanisms by which rice defends against U. virens infection.
Rong-Tao Fu, Huan Li, Xi Luo et al.· BMC Plant Biology· 0 citations
Results suggest that the stronger resistance to P. nicotianae by X7 is associated with rapid coordination of defense-related transcription, phenylpropanoid and flavonoid metabolism, hormone signaling, and suppression of photosynthesis and primary metabolism.
Guo Li, Chang-Jiang Zhang, Bei Yu et al.· Plant physiology and biochem...· 0 citations
Bacterial wilt caused by Ralstonia solanacearum severely limits tobacco production, yet the molecular basis of resistance to vascular wilt diseases remains poorly understood. We integrated field phenotyping, pathogen isolation, and transcriptomic analyses across different disease stages to investigate root responses of the resistant tobacco cultivar Yunyan 87 at healthy, moderately infected, and severely infected stages. Disease progression was accompanied by marked root biomass loss, with fresh and dry weights reduced by approximately 60% and 70%, respectively. Transcriptomic analyses identified 994 up-regulated and 1,151 down-regulated genes at the moderate stage, and 2,158 up-regulated and 2,284 down-regulated genes at the severe stage. WGCNA identified a disease severity-associated regulatory module. Functional enrichment analyses showed that moderate infection activated stress perception and redox homeostasis, whereas severe infection strongly suppressed translation and ribosome biogenesis. Dynamic expression pattern analysis further revealed coordinated activation of phenylpropanoid metabolism and lignin biosynthesis, and synergistic induction of MAPK, salicylic acid (SA), jasmonic acid (JA), and ethylene (ET) signaling pathways, followed by progressive metabolic repression. Key transcription factor families, including WRKY, MYC2, and ERF, exhibited distinct stage-dependent expression patterns. Collectively, our results demonstrate a disease-stage-associated transcriptional reprogramming strategy that balances defense activation and metabolic restraint during bacterial wilt progression, providing valuable regulatory networks and candidate genes for breeding tobacco cultivars with enhanced resistance.
Chunmei Lai, Xiao-Shan Xiao, Jiahao Cai et al.· Plant Disease· 0 citations
Although tomato mosaic virus (ToMV) is an economically important tobamovirus, the physiological and molecular events occurring during the asymptomatic phase of infection remain poorly understood. In this study, we investigated the early responses of Nicotiana tabacum cv. Samsun to ToMV infection using an integrated physiological, biochemical, photosynthetic, and molecular approach. Viral accumulation was quantified via RT-PCR. Oxidative stress markers, antioxidant systems, photosynthetic performance, and gene expression were analyzed at 7 days post inoculation (DPI), before visible symptoms developed. Although infected plants remained symptomless, ToMV was detected in 80% of inoculated plants. Early infection induced oxidative stress, evidenced by increased malondialdehyde content, reduced free amino acid levels, and enhanced activities of superoxide dismutase and peroxidase. Total glutathione, phenolic compounds, and phenylpropanoids remained unchanged, whereas flavonoid content decreased significantly. ToMV infection also impaired the photosynthetic apparatus, resulting in reduced chlorophyll and carotenoid contents, decreased electron transport efficiency, and increased energy dissipation within photosystem II. Gene expression analysis revealed significant upregulation of defense- and stress-related genes (WRKY1, HSP70, GR, and DHAR), as well as chloroplast-associated genes (psaA and rbcL). Correlation analyses demonstrated coordinated relationships among viral accumulation, oxidative stress, antioxidant responses, and photosynthetic performance. These findings provide new insights into the asymptomatic phase of ToMV infection and identify potential early markers of host responses to viral infection.
Wojciech Makowski, I. Mažeikienė, Łucja Kmita et al.· International Journal of Mol...· 0 citations
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