Inventory and functional analysis of the large Hrp regulon in <i>Ralstonia solanacearum</i>: identification of novel effector proteins translocated to plant host cells through the type III secretion system

Cunnac, Sébastien; Occhialini, Alessandra; Barberis, Patrick; Boucher, Christian; Genin, Stéphane

doi:10.1111/j.1365-2958.2004.04118.x

Cited by 200 publications

(260 citation statements)

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“…To investigate the function of the GALA LRR family of T3SS effectors (14), a yeast two-hybrid (Y2H) screen was carried out with GALA6 on an Arabidopsis cDNA library (Arabidopsis Col-0 whole plants, 6.4 ϫ 10 6 yeast colonies screened; Clontech, Mountain View, CA). This initial screen enabled us to identify the Arabidopsis SKP1-like ASK1 as a potential GALA6 interactor.…”

Section: R Solanacearum Encodes For Type III Effectors Containing F-boxmentioning

confidence: 99%

“…Several effectors are part of multigene families. Among these, we identified a group of seven genes that have homologies with plant-specific leucine-rich repeats (LRR) (14). These T3SS effectors were named ''GALA'' proteins after a conserved GAxALA sequence in their LRR (14).…”

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“…We have shown that the plant pathogen R. solanacearum encodes a large repertoire (up to 80 candidates) of putative T3SS effectors (13)(14)(15). Several effectors are part of multigene families.…”

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confidence: 99%

“…These T3SS effectors were named ''GALA'' proteins after a conserved GAxALA sequence in their LRR (14). GALA6 has been shown to be translocated into plant cells (14), and the first 50 aa of the six other GALA proteins show the characteristic features of T3SS substrates (14,16).…”

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Ralstonia solanacearum requires F-box-like domain-containing type III effectors to promote disease on several host plants

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Peeters

Lechner

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

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The phytopathogenic bacterium Ralstonia solanacearum encodes a family of seven type III secretion system (T3SS) effectors that contain both a leucine-rich repeat and an F-box domain. This structure is reminiscent of a class of typical eukaryotic proteins called F-box proteins. The latter, together with Skp1 and Cullin1 subunits, constitute the SCF-type E3 ubiquitin ligase complex and control specific protein ubiquitinylation. In the eukaryotic cell, depending on the nature of the polyubiquitin chain, the ubiquitintagged proteins either see their properties modified or are doomed for degradation by the 26S proteasome. This pathway is essential to many developmental processes in plants, ranging from hormone signaling and flower development to stress responses. Here, we show that these previously undescribed T3SS effectors are putative bacterial F-box proteins capable of interacting with a subset of the 19 different Arabidopsis Skp1-like proteins like bona fide Arabidopsis F-box proteins. A R. solanacearum strain in which all of the seven GALA effector genes have been deleted or mutated was no longer pathogenic on Arabidopsis and less virulent on tomato. Furthermore, we found that GALA7 is a host-specificity factor, required for disease on Medicago truncatula plants. Our results indicate that the GALA T3SS effectors are essential to R. solanacearum to control disease. Because the F-box domain is essential to the virulence function of GALA7, we hypothesize that these effectors act by hijacking their host SCF-type E3 ubiquitin ligases to interfere with their host ubiquitin͞proteasome pathway to promote disease.plant pathogen ͉ SCF complex ͉ type III secretion system ͉ virulence

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Section: R Solanacearum Encodes For Type III Effectors Containing F-boxmentioning

confidence: 99%

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confidence: 99%

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Ralstonia solanacearum requires F-box-like domain-containing type III effectors to promote disease on several host plants

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Lechner

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

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“…The T3SS translocates some 70 bacterial effector proteins directly into the host cells (Occhialini et al, 2005;Poueymiro & Genin, 2009) to suppress host defence responses and facilitate bacterial multiplication during the first stages of infection (Poueymiro & Genin, 2009). In R. solanacearum, transcription of the T3SS and its associated effectors is strictly dependent on the transcriptional regulator HrpB (Cunnac et al, 2004;Genin et al, 1992;Mukaihara et al, 2004;Occhialini et al, 2005). Regulation of hrpB expression exemplifies exquisitely the coordinated action of both host and environmentally derived signalling.…”

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A luminescent reporter evidences active expression of Ralstonia solanacearum type III secretion system genes throughout plant infection

et al. 2012

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Although much is known about the signals that trigger transcription of virulence genes in plant pathogens, their prevalence and timing during infection are still unknown. In this work, we address these questions by analysing expression of the main pathogenicity determinants in the bacterial pathogen Ralstonia solanacearum. We set up a quantitative, non-invasive luminescent reporter to monitor in planta transcription from single promoters in the bacterial chromosome. We show that the new reporter provides a real-time measure of promoter output in vivo -either after re-isolation of pathogens from infected plants or directly in situ -and confirm that the promoter controlling exopolysaccharide (EPS) synthesis is active in bacteria growing in the xylem. We also provide evidence that hrpB, the master regulator of type III secretion system (T3SS) genes, is transcribed in symptomatic plants. Quantitative RT-PCR assays demonstrate that hrpB and type III effector transcripts are abundant at late stages of plant infection, suggesting that their function is required throughout disease. Our results challenge the widespread view in R. solanacearum pathogenicity that the T3SS, and thus injection of effector proteins, is only active to manipulate plant defences at the first stages of infection, and that its expression is turned down when bacteria reach high cell densities and EPS synthesis starts. INTRODUCTIONDuring infection, pathogens deploy a tightly regulated genetic program to overcome the host natural defences and mobilize metabolic resources to their benefit (Grant et al., 2006;Mudgett, 2005). This program, leading to the appearance of disease symptoms, is still unknown for most pathosystems, although many genes involved in infection have been described and their expression measured in culture.Ralstonia solanacearum is an excellent model to study gene regulation, as the pathways controlling its pathogenicity genes have been characterized in detail (Schell, 2000). This soil-borne b-proteobacterium is the causative agent of bacterial wilt on a wide range of plant hosts, including economically important species such as tomato, potato, peanut and eggplant (Hayward, 2000). R. solanacearum invades plants through root wounds and rapidly colonises the xylem vessels, where it multiplies extensively and produces large amounts of exopolysaccharide (EPS) (Kao et al., 1992;Vasse et al., 2000). EPS accumulation in the vascular system and the ensuing collapse of the water flow causes the wilting symptoms and eventually plant death.Coevolution with its various hosts has led to the emergence of a large number of virulence-promoting genes in R. solanacearum (Poueymiro & Genin, 2009;Schell, 2000). The main pathogenicity determinant is the type III secretion system (T3SS), encoded by the hrp cluster and conserved in most Gram-negative pathogens (van Gijsegem et al., 1995). The T3SS translocates some 70 bacterial effector proteins directly into the host cells (Occhialini et al., 2005;Poueymiro & Genin, 2009) to suppress host defence respons...

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Effectors of Bacterial Pathogens: Modes of Action and Plant Targets

Feng

Zhou

2012

Molecular Plant Immunity

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Inventory and functional analysis of the large Hrp regulon in Ralstonia solanacearum: identification of novel effector proteins translocated to plant host cells through the type III secretion system

Cited by 200 publications

References 56 publications

Ralstonia solanacearum requires F-box-like domain-containing type III effectors to promote disease on several host plants

Ralstonia solanacearum requires F-box-like domain-containing type III effectors to promote disease on several host plants

A luminescent reporter evidences active expression of Ralstonia solanacearum type III secretion system genes throughout plant infection

Effectors of Bacterial Pathogens: Modes of Action and Plant Targets

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