Systematic analysis of lectin gene family reveals dynamic modes of paralogue evolution and immune regulatory functions in tomato

Lectins are a structurally diverse class of carbohydrate-binding proteins implicated in plant development and stress responses. In this study, we present a comprehensive structural, evolutionary, and functional analysis of the lectin gene family in tomato (Solanum lycopersicum cv. Heinz). We identified 247 lectin genes across eight major families, exhibiting diverse domain architectures, including merolectins, hololectins, and chimerolectins. Gene ontology enrichment, tissue-specific expression profiling, and stress-responsive transcriptomics highlighted key roles of lectin genes in development and pathogen defense. Comparative genomic analyses across five Solanum species and ancestral outgroups (Vitis vinifera and Amborella trichopoda) revealed both conserved and lineage-specific expansions driven by whole-genome and small-scale duplications. Evolutionary modeling indicated that most lectin gene duplications are under purifying selection, with some genes exhibit signatures of adaptive evolution. Expression and co-expression variance among duplicated paralogues revealed three distinct evolutionary fates -balance, dominance, and divergence. Notably, small-scale duplications frequently led to functional divergence, whereas whole-genome duplicates largely retained ancestral expression patterns. Functional validation through virus-induced gene silencing (VIGS) of two GNA chimerolectins, Solyc04g077390 and Solyc07g063700, revealed their role as negative regulators of immunity. Silencing these genes enhanced resistance to Ralstonia solanacearum, reduced bacterial colonization, and triggered stronger induction of defense-related genes. Together, these findings highlight the structural innovation, evolutionary dynamics, and immune regulatory roles of lectin genes in tomato, and identifies promising targets for breeding disease-resistant cultivars in Solanum lycopersicum and related crops.