Intra-strain Elicitation and Suppression of Plant Immunity by Ralstonia solanacearum Type-III Effectors in Nicotiana benthamiana

Abstract

Effector proteins delivered inside plant cells are powerful weapons for bacterial pathogens, but this exposes the pathogen to potential recognition by the plant immune system. Therefore, the effector repertoire of a given pathogen must be balanced for a successful infection. Ralstonia solanacearum is an aggressive pathogen with a large repertoire of secreted effectors. One of these effectors, RipE1, is conserved in most R . solanacearum strains sequenced to date. In this work, we found that RipE1 triggers immunity in N . benthamiana , which requires the immune regulator SGT1, but not EDS1 or NRCs. Interestingly, RipE1-triggered immunity induces the accumulation of salicylic acid (SA) and the overexpression of several genes encoding phenylalanine-ammonia lyases (PALs), suggesting that the unconventional PAL-mediated pathway is responsible for the observed SA biosynthesis. Surprisingly, RipE1 recognition also induces the expression of jasmonic acid (JA)-responsive genes and JA biosynthesis, suggesting that both SA and JA may act cooperatively in response to RipE1. We further found that RipE1 expression leads to the accumulation of glutathione in plant cells, which precedes the activation of immune responses. R . solanacearum secretes another effector, RipAY, which is known to inhibit immune responses by degrading cellular glutathione. Accordingly, RipAY inhibits RipE1-triggered immune responses. This work shows a strategy employed by R . solanacearum to counteract the perception of its effector proteins by plant immune system.

A bacterial effector protein prevents MAPK-mediated phosphorylation of SGT1 to suppress plant immunity

“…We have recently shown that RipE1-triggered immunity requires SGT1 [33]. In this work, we show that SGT1 phosphorylation contributes to RipE1-triggered cell death (S10 Fig), and, accordingly, RipAC inhibits RipE1-triggered cell death (Fig 3).…”

“…To maintain pathogenicity, bacterial pathogens need to adapt to new recognition events by losing these recognized effectors or evolving additional effectors that suppress ETI. This pathoadaptation becomes evident in the case of RipE1: a R. solanacearum GMI1000 derivative strain carrying mutations in popP1 and avrA is pathogenic in N. benthamiana [48], despite secreting RipE1, which activates ETI in this plant species [33]. This suggests that R. solanacearum has evolved T3Es that suppress immunity triggered by RipE1 (and potentially other T3Es).…”

Host adaptation and microbial competition drive Ralstonia solanacearum phylotype I evolution in the Republic of Korea

“…These families were chosen because they were reported to trigger programmed cell death when overexpressed in Nicotiana spp. [20–22, 24]. Alleles were classified into groups on the basis of shared amino acid sequence identity; patterns of diversity broadly reflected the phylogenetic groupings in the non-recombinant core genome tree for South Korean phylotype I strains ().…”

“…solanacearum phylotype II BS048 effector recognition identified RipAA, RipE1 and RipH2 as cell death inducers in Nicotiana spp., tomato and lettuce, respectively [20]. The phylotype I GMI1000 RipE1 allele also triggers hypersensitive response in N. benthamiana [21, 22]. RipA family AWR motif-containing effectors are strong inducers of cell death in Nicotiana spp.…”

Insights into the Root Invasion by the Plant Pathogenic Bacterium Ralstonia solanacearum

“…At the same time, and as a result of the arms race between hosts and pathogens, T3Es can also be detected in some plant species by intracellular receptors containing nucleotide-binding and leucine-rich repeat domains (NLRs), resulting in the activation of immune responses that effectively hinder pathogen proliferation as part of the so-called effector-triggered immunity (ETI) [28]. Several T3Es from R. solanacearum have been reported to elicit immune responses in different host plants [29][30][31][32][33][34][35][36][37]. While in some cases T3E recognition leads to an incompatible interaction and the subsequent restriction of host range [31], in other cases these immune responses are further suppressed by other T3Es in the same strain [37], reflecting the bacterial adaptation to T3Es recognition.…”