First Extensive Microscopic Study of Butternut Defense Mechanisms Following Inoculation with the Canker Pathogen Ophiognomonia clavigignenti-juglandacearum Reveals Compartmentalization of Tissue Damage

Abstract

Ophiognomonia clavigignenti-juglandacearum endangers the survival of butternut (Juglans cinerea) throughout its native range. While screening for disease resistance, we found that artificial inoculations of 48 butternut seedlings with O. clavigignenti-juglandacearum induced the expression of external symptoms, but only after a period of dormancy. Before dormancy, compartmentalized tissues such as necrophylactic periderms (NPs) and xylem reaction zones (RZs) contributed to limiting pathogen invasion. Phenols were regularly detected in RZs, often in continuity with NPs during wound closure, and confocal microscopy revealed their presence in parenchyma cells, vessel plugs and cell walls. Vessels were blocked with tyloses and gels, particularly those present in RZs. Suberin was also detected in cells formed over the affected xylem by the callus at the inoculation point, in a few tylosis walls, and in longitudinal tubes that formed near NPs. Following dormancy, in all inoculated seedlings but one, defensive barriers were breached by O. clavigignenti-juglandacearum and then additional ones were produced in response to this new invasion. The results of this histopathological study indicate that trees inoculated in selection programs to test butternut canker resistance should go through at least one period of dormancy and that asymptomatic individuals should be dissected to better assess how they defend themselves against O. clavigignenti-juglandacearum.

Induced ligno-suberin vascular coating and tyramine-derived hydroxycinnamic acid amides restrict Ralstonia solanacearum colonization in resistant tomato roots

“…To prevent the spread of pathogenic propagules, the xylem vasculature of resistant plants undergoes intense structural and metabolic modifications. Resistant plants form vertical barriers such as tyloses and gels inside the vessel lumen, which in some plant-pathogen interactions effectively slow down vertical progression of the pathogen, or even confine it to the infection site, preventing systemic infection (VanderMolen et al ., 1987; Rioux et al ., 2018). Further, resistant plants also reinforce the walls of xylem vessels, pit membranes and surrounding xylem parenchyma cells in response to pathogens (Street et al ., 1986; Benhamou, 1995).…”

Seasonal and long-term consequences of esca on grapevine stem xylem integrity

“…Tyloses could have different impacts, both positive and negative, during wilt disease pathogenesis: (i) tyloses contribute to pathogen resistance as they aim to seal off vessel lumens and impede pathogens spread throughout the host (CODIT model, Shigo, 1984). This is the case regarding the susceptibility of different species or varieties to specific pathogens (Jacobi and MacDonald, 1980; Ouellette et al ., 1999; Clérivet et al ., 2000; Et-Touil et al ., 2005; Venturas et al ., 2014; Park and Juzwik 2014; Rioux et al ., 2018), in particular to Phaeomoniella chlamydospora , one of the pathogen associated with esca (Pouzoulet et al ., 2017; 2020). (ii) In other studies, it has been shown that tyloses can exacerbate symptoms (Talboys, 1972): they cause a reduction in stem hydraulic conductivity, sometimes associated with a reduction in stomatal conductance in leaves and, in the most severe cases, wilting (Parke et al ., 2007; Beier et al ., 2017; Lachenbruch and Zhao, 2019, Mensah et al ., 2020 during fungi development; Sun et al ., 2013; Deyett et al ., 2019 during Pierce’s disease).…”

“…Because tyloses can potentially interfere with the hydraulic functioning of the plant, they could exacerbate disease symptoms (Talboys, 1972). Tyloses are usually observed in close proximity to pathogens, as shown in artificial inoculation studies (Czemmel et al ., 2015; Rioux et al ., 2018, among others). However, pathogens frequently proliferate in perennial organs without physically reaching the leaves, thus leaf symptoms are often induced at a distance (Beckmann and Roberts, 1995).…”

Induced defense strategies of plants against Ralstonia solanacearum

“…In addition to R. solanacearum, Fusarium oxysporum f. sp. cubense (VanderMolen et al, 1987), Ophiognomonia clavigignenti-juglandacearum (Rioux et al, 2018), Fusarium oxysporum f. sp. vasinfectum (Shi et al, 1991), Fusarium oxysporum f. sp.…”