Resistant cotton maintains vascular health via an integrative defence network against Verticillium dahliae

BACKGROUND AND AIMS: Verticillium dahliae, an obligate vascular pathogen that colonizes xylem vessels to cause wilt, poses a severe threat to global cotton production. Understanding the vascular immunity is crucial for durable resistance. This study focuses on vascular immunity by comprehensively comparing the histological, physiological and molecular responses to V. dahliae infection between a resistant cotton cultivar (Gossypium hirsutum ZZM2) and a susceptible cultivar (JM11). METHODS: Histopathological analysis quantified xylem-specific colonization patterns and pit membrane integrity. Physiological stability was assessed via electrolyte leakage and malondialdehyde levels. Reactive oxygen species localization, callose deposition and spatiotemporal activation of salicylic acid/jasmonic acid signalling genes were evaluated for host immunity response. KEY RESULTS: At 16 days post-inoculation, susceptible JM11 exhibited severe wilting (62 % disease index) with widespread xylem vessel colonization (51.7 % colonization rate), pit membrane degradation and vascular collapse. Crucially, pathogen-induced pit membrane rupture enabled radial hyphal spread. In contrast, resistant ZZM2 showed mild symptoms (26 % disease index), with colonization restricted to 28.7 % of vessels, where intact pit membranes physically blocked radial invasion. Notably, ZZM2 showed vascular parenchyma-specific tannin accumulation and elevated root lignin content, directly contributing to its superior resistance against V. dahliae. Mechanistically, ZZM2 preserved vascular integrity via: (1) maintenance of xylem wall and pit membrane integrity to inhibit lateral hyphal spread; (2) early reactive oxygen species bursts localized to xylem cell walls and hyphae coupled with efficient deposition of lignin, tannin and callose in roots; and (3) activation of the salicylic acid/jasmonic acid pathway. CONCLUSIONS: Preservation of xylem integrity through pit membrane-mediated containment, lignin/tannin acumulation, reactive oxygen species-callose defence reinforcement and coordinated salicylic acid/jasmonic acid signalling activation constitutes the core vascular immunity network for cotton resistance. These findings advance the mechanistic understanding of cotton resistance and establish a crucial foundation for breeding durably resistant cultivars.