Genomic insights and antiviral immunity mediated by Serratia marcescens (NMS01) reveal the potential to manage Orthotospovirus arachinecrosis (groundnut bud necrosis virus) in cowpea and tomato

Leaf and bud necrosis in tomato, caused by groundnut bud necrosis virus (GBNV, Orthotospovirus arachinecrosis ), is a serious yield limiting disease. This study evaluated the antiviral potential of Serratia marcescens NMS01 in cowpea (assay host) and tomato plants. Tomato seedlings subjected to biohardening, followed by foliar application of S. marcescens NMS01 (1.5%), showed delayed symptom onset and a significant reduction in disease incidence. Virus titer analysis using DAC-ELISA showed a substantial decrease in viral load in treated plants (0.32–0.96 OD) compared to the untreated control (3.26 OD). qPCR results further, confirmed a lower viral copy number in the treated plants (1.5 × 10 5 ) relative to untreated control (2.4 × 10 6 ). This antiviral activity was supported by the upregulation of key defense genes ( MAPKK1, WRKY33B, and PR1 ) in NMS01 treated plants, as revealed by gene expression analysis. Genome analysis confirmed the absence of human pathogenic genes in S. marcescens NMS01, underscoring its safety and suitability as a biocontrol. AntiSMASH predictions identified genes involved in the production of NRPS derived metabolites, including prodigiosin, thiopeptide, and hserlactone, which are known to have antimicrobial and immunomodulatory properties. Pan-genome analysis revealed that NMS01 harbors 4,023 core genes, 352 dispensable genes, and 664 unique genes, including MAMP genes. Under field conditions, the treated plants exhibited improved growth (133.7 cm height, 26.57 flowers/plant) and lower disease incidence (12.3%) compared to untreated controls (104.73 cm, 11.17 flowers, 30.1% disease incidence). These findings established S. marcescens NMS01 as a promising biocontrol agent for managing GBNV and enhancing tomato productivity. • Serratia marcescens NMS01 significantly reduced GBNV symptoms and viral titer in both cowpea (assay host) and tomato plants, with DAC-ELISA, OD values 0.32–0.96 in treated plants compared to 3.26 in the untreated control. • qPCR analysis showed a marked decrease in N gene copy number in treated tomato plants (1.5 × 10 5 ) compared to untreated controls (2.4 × 10 6 ), confirming the antiviral effect. • Gene expression profiling revealed upregulation of key defense genes ( MAPKK1, WRKY33B, and PR1 ) in NMS01 treated tomato plants, indicating activation of systemic resistance. • Whole genome sequencing confirmed the absence of human pathogenic genes in NMS01, while antiSMASH analysis identified biosynthetic clusters for antiviral and antimicrobial metabolites such as prodigiosin, thiopeptide, and hserlactone. • Field trials revealed that NMS01 treated tomato plants had increased height (133.7 cm), more flowers (26.57 per plant), and lower disease incidence (12.3%) compared to untreated controls (104.73 cm, 11.17 flowers, 30.1% incidence), highlighting its effectiveness in crop protection.