Tomato 14-3-3 Proteins Are Required for <i>Xv3</i> Disease Resistance and Interact with a Subset of <i>Xanthomonas euvesicatoria</i> Effectors

Dubrow, Zoe; Sunitha, Sukumaran; Kim, Jung‐Gun; Aakre, Chris D; Girija, Anil Madhusoodana; Sobol, Guy; Teper, Doron; Chen, Yun-Chu; Ozbaki-Yagan, Nejla; Vance, Hillary; Sessa, Guido; Mudgett, Mary Beth

doi:10.1094/mpmi-02-18-0048-r

Cited by 22 publications

(19 citation statements)

References 49 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…To determine the biological significance of Me10's interaction with TFT7, we first examined if aphid feeding regulates TFT7 expression. Earlier studies showed that TFT7 is a positive regulator of tomato defense signaling (Oh et al ., ) and that its mRNA abundance increases upon pathogen infection (Dubrow et al ., ). We evaluated the temporal expression pattern of TFT7 mRNA in leaves of susceptible tomato plants at multiple time points after potato aphid infestation using reverse transcription real‐time qPCR.…”

Section: Resultsmentioning

confidence: 99%

“…This suggests that binding of these aphid effectors to TFT7 may be isoform specific. Isoform‐specific interactions have been previously reported for members of 14‐3‐3 proteins with their clients (Bridges & Moorhead, ), as well with pathogen effector proteins (Kim et al ., ; Teper et al ., ; Dubrow et al ., ). BiFC microscopy studies with Me10 and TFT7 suggest that formation of an Me10–TFT7 complex occurs within the plant cytoplasm.…”

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Aphid effector Me10 interacts with tomato TFT7, a 14‐3‐3 isoform involved in aphid resistance

Chaudhary

Peng

et al. 2018

New Phytologist

Self Cite

View full text Add to dashboard Cite

We demonstrated previously that expression of Macrosiphum euphorbiae salivary protein Me10 enhanced aphid reproduction on its host tomato (Solanum lycopersicum). However, the mechanism of action of Me10 remained elusive.To confirm the secretion of Me10 by the aphid into plant tissues, we produced Me10 polyclonal antibodies. To identify the plant targets of Me10, we developed a tomato immune induced complementary DNA yeast two-hybrid library and screened it with Me10 as bait. Immunoprecipitation and bimolecular fluorescence complementation (BiFC) assays were performed to validate one of the interactions in planta, and virus-induced gene silencing was used for functional characterization in tomato.We demonstrated that Me10 is secreted into the plant tissues and interacts with tomato 14-3-3 isoform 7 (TFT7) in yeast. Immunoprecipitation assays confirmed that Me10 and its homologue in Aphis gossypii, Ag10k, interact with TFT7 in planta. Further, BiFC revealed that Me10 interaction with TFT7 occurs in the plant cell cytoplasm. While silencing of TFT7 in tomato leaves did not affect tomato susceptibility to M. euphorbiae, it enhanced longevity and fecundity of A. gossypii, the non-host aphid.Our results suggest the model whereby TFT7 plays a role in aphid resistance in tomato and effectors of the Me10/Ag10k family interfere with TFT7 function during aphid infestation.

show abstract

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Aphid effector Me10 interacts with tomato TFT7, a 14‐3‐3 isoform involved in aphid resistance

Chaudhary

Peng

et al. 2018

New Phytologist

Self Cite

View full text Add to dashboard Cite

show abstract

“…Phosphorylation of Tir and CagA are required for the binding of host adaptor proteins for bacterial adhesion (Nougayrede et al, 2003; Higashi et al, 2004). The plant pathogen effectors HopQ1, XopN, and XopE2 are phosphorylated in plants, which results in their associations with host 14-3-3 proteins and phosphorylated residues are required for effector virulence (Taylor et al, 2012; Li et al, 2013; Dubrow et al, 2018). In our study, the phosphorylation of AvrPtoB is required for the effector-mediated inhibition of NPR1/FLS2 accumulation and FLS2-BAK1 complex formation.…”

Section: Discussionmentioning

confidence: 99%

Identification of a plant kinase that phosphorylates the bacterial effector AvrPtoB

Coaker

2020

Preprint

View full text Add to dashboard Cite

9A critical component controlling bacterial virulence is the delivery of pathogen effectors into 10 plant cells during infection. Effectors alter host metabolism and immunity for pathogen benefit. 11 Multiple effectors are phosphorylated by host kinases, and this posttranslational modification is 12 important for their activity. We sought to identify host kinases involved in effector 13 phosphorylation. Multiple effector phosphorylated residues matched the proposed consensus 14 phosphorylation motif of the plant calcium-dependent protein kinase (CDPK) and Snf1-related 15 kinase (SnRK) superfamily. The conserved Pseudomonas effector AvrPtoB acts as an E3 16 ubiquitin ligase and promotes bacterial virulence. We identified a member of the Arabidopsis 17 SnRK family, SnRK2.8, that associated with AvrPtoB in yeast and in planta. SnRK2.8 was 18 required for AvrPtoB virulence functions, including facilitating bacterial colonization, 19 suppression of callose deposition, and targeting the plant defense regulator NPR1 and flagellin 20 receptor FLS2. Mass spectrometry revealed AvrPtoB was phosphorylated at multiple serine 21 residues in planta, with S258 phosphorylation reduced in the snrk2.8 knockout. AvrPtoB 22 phospho-null mutants exhibited compromised virulence functions and were unable to suppress 23 NPR1 accumulation, FLS2 accumulation, or inhibit FLS2-BAK1 complex formation upon 24 flagellin perception. These data identify a conserved plant kinase utilized by a pathogen effector 25 to promote disease.26 27 Plants are exposed to diverse pathogens and rely on both passive and active defenses in order to 29 restrict infection. Passive plant defenses include a waxy cuticle, pre-formed antimicrobial 30 compounds, and the cell wall (Gu et al., 2017). Inducible defenses are often triggered by 31 membrane-localized pattern recognition receptors (PRRs) as well as intracellular nucleotide-32 binding site leucine-rich repeat proteins (NLRs) (Boutrot and Zipfel, 2017; Lolle et al., 2020). 33 Common plant immune responses after active pathogen perception include the production of 34 reactive oxygen species (ROS), callose deposition, activation of mitogen-activated protein 35 kinases, and global transcriptional reprogramming towards defense (Bigeard et al., 2015; Peng et 36 al., 2018). 37 To colonize their hosts, pathogens rely on the ability to secrete effector proteins. Characterized 38 effectors act to suppress plant immune responses, alter host developmental processes, and affect 39 host metabolism to promote pathogen infection (Toruño et al., 2015). Bacterial pathogens have 40 the most well-characterized effector repertoires. For example, the Pseudomonas syringae 41 effectors AvrPto and HopAO1 directly interact with the cytoplasmic domains of the PRRs 42 FLAGELLIN-SENSING 2 (FLS2) and ELONGATION FACTOR-Tu RECEPTOR (EFR), and 43 inhibit PRR kinase activity (Xiang et al., 2008; Macho et al., 2014). Effectors are also capable of 44 manipulating plant hormone processes. The P. syringae effector HopX1 and its Ralstonia 45 solanac...

show abstract

“…The XopQ protein is highly conserved in Xanthomonads (Hajri et al, 2009, Moreira et al, 2010, Jalan et al, 2013, Potnis et al, 2011), and has been shown to require its biochemical activity for complete virulence in rice (Gupta et al, 2015). XopQ also has motifs for binding to 14-3-3 proteins (Dubrow et al, 2018, Deb et al, 2019). The 14-3-3 proteins are eukaryotic adapter proteins which play key roles in multiple cellular events in plants (Cotelle and Leonhardt, 2015, Cotelle et al, 2000).…”

Section: Introductionmentioning

confidence: 99%

“…A number of studies have shown the role of the 14-3-3 proteins in modulation of PTI and ETI (Lozano-Duran and Robatzek, 2015), by the binding of host 14-3-3 proteins with the type III effectors of the pathogen (Dubrow et al, 2018). The ability of X. oryzae pv.…”

Section: Introductionmentioning

confidence: 99%

Interaction of theXanthomonaseffectors XopQ and XopX results in induction of rice immune responses

Deb

Ghosh

Patel

et al. 2020

Preprint

View full text Add to dashboard Cite

SummaryXanthomonas oryzae pv. oryzae uses several type III secretion system (T3SS) effectors, namely XopN, XopQ, XopX, and XopZ, to suppress rice immune responses that are induced following treatment with cell wall degrading enzymes. Here we show that the T3SS secreted effector XopX interacts with two of the eight rice 14-3-3 proteins. Mutants of XopX that are defective in 14-3-3 binding are also defective in suppression of immune responses, suggesting that interaction with 14-3-3 proteins is required for suppression of host innate immunity. However, Agrobacterium mediated delivery of both XopX and XopQ into rice cells results in induction of rice immune responses. These immune responses are not observed when either protein is individually delivered into rice cells. XopQ-XopX induced rice immune responses are not observed in a XopX mutant that is defective in 14-3-3 binding. Yeast two-hybrid and BiFC assays indicate that XopQ and XopX interact with each other. In a screen for Xanthomonas effectors which can suppress XopQ-XopX induced rice immune responses, five effectors were identified, namely XopU, XopV, XopP, XopG and AvrBs2, which were able to do so. These results suggest a complex interplay of Xanthomonas T3SS effectors in suppression of pathogen triggered immunity and effector triggered immunity to promote virulence on rice.Significance statementThis work studies the role of the type III effector XopX in the suppression and induction of rice immune responses, by differential interaction with the 14-3-3 proteins, or with the type III effector XopQ respectively. We have also identified a subset of type III effectors which can suppress this form of immune responses.

show abstract

Tomato 14-3-3 Proteins Are Required for Xv3 Disease Resistance and Interact with a Subset of Xanthomonas euvesicatoria Effectors

Cited by 22 publications

References 49 publications

Aphid effector Me10 interacts with tomato TFT7, a 14‐3‐3 isoform involved in aphid resistance

Aphid effector Me10 interacts with tomato TFT7, a 14‐3‐3 isoform involved in aphid resistance

Identification of a plant kinase that phosphorylates the bacterial effector AvrPtoB

Interaction of theXanthomonaseffectors XopQ and XopX results in induction of rice immune responses

Contact Info

Product

Resources

About