An ultrastructural study of root invasion in three vascular wilt diseases

Abstract

Transmission electron-microscopy was used to study root invasion in resistant and susceptible cultivars of tomato infected with Fusarium oxysporum f. sp. lycopersici or Verticillium albo-atrum and pea infected with F. oxysporum f. sp. pisi. There were many similarities in invasion by all pathogens of root epidermis and cortex in resistant and susceptible cultivars. Hyphae of tomato pathogens adhered to host root cell walls of susceptible cultivars but remained separated by extracellular electron-opaque material; hyphae of F. oxysporum f. sp. pisi on pea roots were embedded in a mucilaginous sheath. Both forms of adhesion were associated with a localized disruption of adjacent host wall structure. Initial penetration was by intercellular hyphae; subsequent intercellular colonization frequently resulted in the formation of wall appositions and papillae within epidermal and cortical cells. Penetration of host walls was achieved by constricted hyphae and localized wall degradation; continued deposition of material occurred around penetration hyphae with consequent formation of elongated penetration papillae. These were lignified, resistant to enzymic and chemical degradation and apparently effective in preventing further hyphal growth, although the frequency of their formation was similar in both resistant and susceptible cultivars. Papillae did not form in the moribund cells often seen even before penetration by F. oxysporum ff. sp.; in contrast V. albo-atrum was occasionally present within apparently healthy cells surrounded by invaginated host plasmalemma. A differential expression of varietal resistance occurred at the endodermis of both plant species. Accumulation of electron-opaque material in tomato endodermal cells and deposition of suberin and autofluorescent material in pea appeared to limit colonization of the stele. Pathogens circumvented this putative line of resistance either by intercellular growth between endodermal cells or by longitudinal growth from the root tip, which is devoid of mature endodermis. The diffuse and extensive intercellular wall structure of root tip cells is particularly amenable to initial colonization from which longitudinal growth allows entry into immature unlignified xylem elements and subsequently into mature vessels; hyphae were never seen to enter vessels from mature stelar cells.