Transfer of tomato immune receptor Ve1 confers Ave1‐dependent Verticillium resistance in tobacco and cotton

Abstract

SummaryVerticillium wilts caused by soilborne fungal species of the Verticillium genus are economically important plant diseases that affect a wide range of host plants and are notoriously difficult to combat. Perception of pathogen(‐induced) ligands by plant immune receptors is a key component of plant innate immunity. In tomato, race‐specific resistance to Verticillium wilt is governed by the cell surface‐localized immune receptor Ve1 through recognition of the effector protein Ave1 that is secreted by race 1 strains of Verticillium spp. It was previously demonstrated that transgenic expression of tomato Ve1 in the model plant Arabidopsis thaliana leads to Verticillium wilt resistance. Here, we investigated whether tomato Ve1 can confer Verticillium resistance when expressed in the crop species tobacco (Nicotiana tabcum) and cotton (Gossypium hirsutum). We show that transgenic tobacco and cotton plants constitutively expressing tomato Ve1 exhibit enhanced resistance against Verticillium wilt in an Ave1‐dependent manner. Thus, we demonstrate that the functionality of tomato Ve1 in Verticillium wilt resistance through recognition of the Verticillium effector Ave1 is retained after transfer to tobacco and cotton, implying that the Ve1‐mediated immune signalling pathway is evolutionary conserved across these plant species. Moreover, our results suggest that transfer of tomato Ve1 across sexually incompatible plant species can be exploited in breeding programmes to engineer Verticillium wilt resistance.

Verticillium dahliae strains that infect the same host plant display highly divergent effector catalogs

“…Simian 3), tomato ( Solanum lycopersicum cv. Moneymaker), Nicotiana benthamiana and Arabidopsis thaliana (Col-0) plants using the root-dipping inoculation method as previously described (Fradin et al, 2009; Song et al, 2017). Briefly, two-week-old (Arabidopsis, tomato, cotton, sunflower) or three-week-old ( N. benthamiana ) seedlings were carefully uprooted and the roots were rinsed in water.…”

GbSOBIR1 confers Verticillium wilt resistance by phosphorylating the transcriptional factor GbbHLH171 in Gossypium barbadense

“…Leaves of Inoculated plants were classified according to the disease symptoms, Lv0: healthy leaves, Lv1: leaves showing some necrosis or chlorosis, Lv2: leaves showing severe necrosis or chlorosis, Lv3: dead/shed leaves. The in planta V. dahliae biomass quantification in Arabidopsis and cotton was carried out according to (Fradin et al, 2011) and (Song et al, 2018), respectively.…”

“…Ve1 is activated by Ave1, an effector of Verticillium race 1 strains, and induces a hypersensitive response (HR) in tobacco leaves (de Jonge et al, 2012). It also confers resistance to race 1 V. dahliae when expressed in tobacco and cotton (Song et al, 2018).…”

Host‐induced gene silencing of a regulator of G protein signalling gene (VdRGS1) confers resistance to Verticillium wilt in cotton

“…To alleviate the negative impact of wilt disease, a continuous search for alternative control strategies is required. In the past 10 years, heterologous expression of foreign genes and the silencing of endogenous genes known as ‘susceptible genes’ have been used to improve crop resistance (Gao et al ., ; Song et al ., ). In recent years, an alternative technique called host‐induced gene silencing (HIGS), or host‐delivered RNAi, has been shown to successfully lead to the expression of antisense or hairpin RNAi constructs, or other forms of short interfering RNA molecules, to directly silence a gene of interest and, therefore, engineer plants that are resistant to plant viruses, insects and bacterial and fungal pathogens (Baum et al ., ; Cheng et al ., ; Waterhouse and Fusaro, ; Zhang et al ., ).…”

“…To alleviate the negative impact of wilt disease, a continuous search for alternative control strategies is required. In the past 10 years, heterologous expression of foreign genes and the silencing of endogenous genes known as 'susceptible genes' have been used to improve crop resistance Song et al, 2017).…”