Four bottlenecks restrict colonization and invasion by the pathogen Ralstonia solanacearum in resistant tomato

Abstract

Ralstonia solanacearum is a bacterial vascular pathogen causing devastating bacterial wilt. In the field, resistance against this pathogen is quantitative and is available for breeders only in tomato and eggplant. To understand the basis of resistance to R. solanacearum in tomato, we investigated the spatio-temporal dynamics of bacterial colonization using non-invasive live monitoring techniques coupled to grafting of susceptible and resistant varieties. We found four ‘bottlenecks’ that limit the bacterium in resistant tomato: root colonization, vertical movement from roots to shoots, circular vascular bundle invasion, and radial apoplastic spread in the cortex. Radial invasion of cortical extracellular spaces occurred mostly at late disease stages but was observed throughout plant infection. This study shows that resistance is expressed in both root and shoot tissues, and highlights the importance of structural constraints to bacterial spread as a resistance mechanism. It also shows that R. solanacearum is not only a vascular pathogen but spreads out of the xylem, occupying the plant apoplast niche. Our work will help elucidate the complex genetic determinants of resistance, setting the foundations to decipher the molecular mechanisms that limit pathogen colonization, which may provide new precision tools to fight bacterial wilt in the field.

Revisiting the source of wilt symptoms: X-ray microcomputed tomography provides direct evidence thatRalstoniabiomass clogs xylem vessels

“…When viewed from the side, it was clear that the white occlusions were continuous within the tapered xylem vessels. This suggested that the occlusions were a dense gel formed by bacterial biofilms seen in our and others’ previous microscopic analyses of Ralstonia -infected stems (Vasse et al 1995; Caldwell et al 2017; Planas-Marquès et al 2020).…”

Convergent Rewiring of the Virulence Regulatory Network Promotes Adaptation of Ralstonia solanacearum on Resistant Tomato

“…2013 ). Hawaii 7996 resistance to the RSSC is expressed in both root and shoot tissues ( Planas-Marquès et al. 2020 ).…”

“…Resistance of Hawaii 7996 to bacterial wilt relies on polygenic traits ( Thoquet et al 1996 ; Carmeille et al. 2006 ) and is expressed in both root and shoot tissues ( Planas-Marquès et al. 2020 ).…”

Blocking intruders: inducible physico-chemical barriers against plant vascular wilt pathogens

“…If a pathogen manages to reach the xylem, this transport system becomes an excellent channel of inoculum dissemination throughout the plant. As a consequence, plants have evolved effective structural defense mechanisms to prevent vessel colonization or movement between vessels once vascular colonization has occurred ( Beckman and Roberts, 1995 ) Timely formation of these physico-chemical vascular barriers early upon pathogen perception can lead to confinement of the vascular pathogen at the infected vessel, avoiding the spread of wilt diseases ( Robb et al , 2007 ; Zaini et al , 2018 ; Planas-Marquès et al , 2019 ).…”