Modular Study of the Type III Effector Repertoire in Pseudomonas syringae pv. tomato DC3000 Reveals a Matrix of Effector Interplay in Pathogenesis

Wei, Hengling; Zhang, Wei; Collmer, Alan

doi:10.1016/j.celrep.2018.04.037

Cited by 84 publications

(87 citation statements)

References 30 publications

(67 reference statements)

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“…It has been reported that P. syringae pv. tomato DC3000 possesses several type III effectors that can suppress HopQ1‐triggered HR cell death (Wei et al , ; Zembek et al , ). GMI1000 might possess effectors that suppress RipB‐triggered ETI responses.…”

Section: Discussionmentioning

confidence: 99%

The type III effector RipB from Ralstonia solanacearum RS1000 acts as a major avirulence factor in Nicotiana benthamiana and other Nicotiana species

Nakano

Mukaihara

2019

Molecular Plant Pathology

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Summary Ralstonia solanacearum is the causal agent of bacterial wilt in solanaceous crops. This pathogen injects approximately 70 effector proteins into plant cells via the Hrp type III secretion system in an early stage of infection. To identify an as‐yet‐unidentified avirulence factor possessed by the Japanese tobacco‐avirulent strain RS1000, we transiently expressed RS1000 effectors in Nicotiana benthamiana leaves and monitored their ability to induce effector‐triggered immunity (ETI). The expression of RipB strongly induced the production of reactive oxygen species and the expressions of defence‐related genes in N. benthamiana . The ripB mutant of RS1002, a nalixidic acid‐resistant derivative of RS1000, caused wilting symptoms in N. benthamiana . A pathogenicity test using R. solanacearum mutants revealed that the two already known avirulence factors RipP1 and RipAA contribute in part to the avirulence of RS1002 in N. benthamiana . The Japanese tobacco‐virulent strain BK1002 contains mutations in ripB and expresses a C‐terminal‐truncated RipB that lost the ability to induce ETI in N. benthamiana , indicating a fine‐tuning of the pathogen effector repertoire to evade plant recognition. RipB shares homology with Xanthomonas XopQ, which is recognized by the resistance protein Roq1. The RipB‐induced resistance against R. solanacearum was abolished in Roq1 ‐silenced plants. These findings indicate that RipB acts as a major avirulence factor in N. benthamiana and that Roq1 is involved in the recognition of RipB.

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Section: Discussionmentioning

confidence: 99%

The type III effector RipB from Ralstonia solanacearum RS1000 acts as a major avirulence factor in Nicotiana benthamiana and other Nicotiana species

Nakano

Mukaihara

2019

Molecular Plant Pathology

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“…Similarly, Arabidopsis accession Col-0 (Col) is resistant to Pst bacteria translocating AvrRpt2, recognized by the CNL RPS2 (Bent et al, 1994;Mindrinos et al, 1994), but resistance is impaired in lines lacking EDS1 and the defense-associated hormone salicylic acid (SA; Venugopal et al, 2009;Vlot et al, 2009;Cui et al, 2017). However, Pst assumingly translocates up to 29 different effectors into host plants (Wei et al, 2015;Wei et al, 2018), and infection assays fail to detect weak recognition events in interactions termed 'compatible'. Indeed, basal resistance is also impaired in lines lacking RAR1 or SGT1 (required for maturation and accumulation of NLRs (Kadota et al, 2010;Zhang et al, 2010)), supporting the occurrence of weak recognition in the Pst DC3000 -Col interaction.…”

Section: Introductionmentioning

confidence: 99%

An EDS1-SAG101 complex functions in TNL-mediated immunity in Solanaceae

Ordon

Kretschmer

Guérois

et al. 2019

Preprint

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EDS1 (Enhanced disease susceptibility 1) forms mutually exclusive heterodimers with its interaction partners PAD4 (Phytoalexin-deficient 4) and SAG101 (Sensecence-associated gene 101). Collectively, these complexes are required for resistance responses mediated by nucleotide-binding leucine-rich repeat-type immune receptors (NLRs) possessing an N-terminal Toll-interleukin-1 receptor-like domain (TNLs). Here, immune functions of EDS1 complexes were comparatively analyzed in a mixed species approach relying on Nicotiana benthamiana (Nb), Solanum lycopersicum (Sl) and Arabidopsis thaliana (At). Genomes of most Solanaceae plants including Nb and Sl encode for two SAG101 isoforms, which engage into distinct complexes with EDS1. By a combination of genome editing and transient complementation, we show that one of these EDS1-SAG101 complexes, and not an EDS1-PAD4 complex as previously described in At, is necessary and sufficient for all tested TNL-mediated immune responses in Nb. Intriguingly, not this EDS1-SAG101 module, but mainly Solanaceae EDS1-PAD4 execute immune functions when transferred to At, and TNL functions are not restored in Nb mutant lines by expression of At EDS1 complexes. We conclude that EDS1 complexes do not represent a complete functional module, but co-evolve with additional factors, most likely protein interaction partners, for their function in TNL signaling networks of individual species. In agreement, we identify a large surface on SlEDS1 complexes required for immune activities, which may function in partner recruitment. We highlight important differences in TNL signaling networks between At and Nb, and genetic resources in the Nb system will be instrumental for future elucidation of EDS1 molecular functions. regions with insertions. Sequence conservation was calculated using the rate4site algorithm (Pupko et al., 2002) and mapped at the surface of structural models using pymol (The PyMOL Molecular Graphics System, Version 2.0 Schrödinger, LLC). Structural models and analysis thereof are provided in Appendix S1. N., Metz, M., Holub, E., Staskawicz, B.J., Daniels, M.J., and Parker, J.E. (1998). Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R genemediated signaling pathways in Arabidopsis. . Dissecting virulence function from recognition: cell death suppression in Nicotiana benthamiana by XopQ/HopQ1-family effectors relies on EDS1dependent immunity. Plant J 91, 430-442. References Aarts,

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“…The genome of DC3000, which is a widely-used strain of Pst , is 6.5 Mb and encodes 5,763 ORFs (Buell et al ., 2003). In addition to 36 type III effectors (T3Es), which contribute to Pst virulence, DC3000 also produces a phytotoxin, coronatine (COR) that induces chlorosis and functions as a jasmonic acid-isoleucine mimic to promote colonization of plants by opening stomata and altering defense signaling pathways (Worley et al ., 2013; Sakatos et al ., 2018; Wei et al ., 2018). By deleting 28 well-expressed T3Es and then reintroducing combinations of multiple effectors back into DC3000, eight effectors were found to be required for near wild-type Pst growth in Nicotiana benthamiana (Cunnac et al ., 2011).…”

Section: Introductionmentioning

confidence: 99%

Natural variation for unusual host responses and flagellin-mediated immunity againstPseudomonas syringaein genetically diverse tomato accessions

Roberts

Mainiero

Powell

et al. 2019

Preprint

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The interaction between tomato and Pseudomonas syringae pv. tomato (Pst) is a well-developed model for investigating the molecular basis of the plant immune system. There is extensive natural variation in Solanum lycopersicum (tomato) but it has not been fully leveraged to enhance our understanding of the tomato-Pst pathosystem. We screened 216 genetically diverse accessions of cultivated tomato and a wild tomato species for natural variation in their response to three strains of Pst. The screen uncovered a broad range of previously unseen host symptoms in response to Pst, and one of these, stem galls, was found to be simply inherited. The screen also identified tomato accessions that showed enhanced responses to flagellin in bacterial population assays and in reactive oxygen species assays upon exposure to flagellin-derived peptides, flg22 and flgII-28. Reporter genes confirmed that the host responses were due primarily to pattern recognition receptor-immunity. This study revealed extensive natural variation in tomato for susceptibility and resistance to Pst and will enable elucidation of the molecular mechanisms underlying these host responses.Key Words: Bacterial speck disease, flagellin, natural variation, NLR-triggered immunity, patterntriggered immunity, plant immunity, PRR-triggered immunity Abramovitch RB, Janjusevic R, Stebbins CE, Martin GB. 2006. Type III effector AvrPtoB requires intrinsic E3 ubiquitin ligase activity to suppress plant cell death and immunity. Proc Natl Acad Sci USA 103: 2851-2856. Abramovitch RB, Kim Y-J, Chen S, Dickman MB, Martin GB. 2003. Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death. EMBO J 22: 60-69. Arredondo CR, Davis RM. 2000. First report of Pseudomonas syringae pv. tomato race 1 on tomato in California. Plant Disease 84: 371. Bao Z, Meng F, Strickler SR, Dunham DM, Munkvold KR, Martin GB. 2015. Identification of a candidate gene in Solanum habrochaites for resistance to a race 1 strain of Pseudomonas syringae pv. tomato. The Plant Genome 8: 10.3835/plantgenome2015.3802.0006. Buell CR, Joardar V, Lindeberg M, Selengut J, Paulsen IT, Gwinn ML, Dodson RJ, Deboy RT, Durkin AS, Kolonay JF, et al. 2003. The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000.

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Modular Study of the Type III Effector Repertoire in Pseudomonas syringae pv. tomato DC3000 Reveals a Matrix of Effector Interplay in Pathogenesis

Cited by 84 publications

References 30 publications

The type III effector RipB from Ralstonia solanacearum RS1000 acts as a major avirulence factor in Nicotiana benthamiana and other Nicotiana species

The type III effector RipB from Ralstonia solanacearum RS1000 acts as a major avirulence factor in Nicotiana benthamiana and other Nicotiana species

An EDS1-SAG101 complex functions in TNL-mediated immunity in Solanaceae

Natural variation for unusual host responses and flagellin-mediated immunity againstPseudomonas syringaein genetically diverse tomato accessions

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