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• W2580697086 abstract "•The transcriptional regulator TCP14 represses JA response to promote disease resistance•The Pseudomonas syringae type III effector HopBB1 interacts with TCP14•HopBB1 activates TCP14-repressed JA response genes and promotes bacterial virulence•HopBB1 targets TCP14 for SCFCOI1-dependent degradation by connecting it to JAZ3 Independently evolved pathogen effectors from three branches of life (ascomycete, eubacteria, and oomycete) converge onto the Arabidopsis TCP14 transcription factor to manipulate host defense. However, the mechanistic basis for defense control via TCP14 regulation is unknown. We demonstrate that TCP14 regulates the plant immune system by transcriptionally repressing a subset of the jasmonic acid (JA) hormone signaling outputs. A previously unstudied Pseudomonas syringae (Psy) type III effector, HopBB1, interacts with TCP14 and targets it to the SCFCOI1 degradation complex by connecting it to the JA signaling repressor JAZ3. Consequently, HopBB1 de-represses the TCP14-regulated subset of JA response genes and promotes pathogen virulence. Thus, HopBB1 fine-tunes host phytohormone crosstalk by precisely manipulating part of the JA regulon to avoid pleiotropic host responses while promoting pathogen proliferation. Independently evolved pathogen effectors from three branches of life (ascomycete, eubacteria, and oomycete) converge onto the Arabidopsis TCP14 transcription factor to manipulate host defense. However, the mechanistic basis for defense control via TCP14 regulation is unknown. We demonstrate that TCP14 regulates the plant immune system by transcriptionally repressing a subset of the jasmonic acid (JA) hormone signaling outputs. A previously unstudied Pseudomonas syringae (Psy) type III effector, HopBB1, interacts with TCP14 and targets it to the SCFCOI1 degradation complex by connecting it to the JA signaling repressor JAZ3. Consequently, HopBB1 de-represses the TCP14-regulated subset of JA response genes and promotes pathogen virulence. Thus, HopBB1 fine-tunes host phytohormone crosstalk by precisely manipulating part of the JA regulon to avoid pleiotropic host responses while promoting pathogen proliferation. A robust immune system defends plants against most microbes. Plants deploy surface-localized pattern recognition receptors to detect conserved microbe-associated molecular patterns (MAMPs), which leads to the activation of MAMP-triggered immunity (MTI). To counteract MTI, pathogenic microbes deploy virulence factors, often termed effector proteins, into plant cells, where they interact with host factors to subvert defense responses or to alter nutrition distribution. To counteract effector protein action, plants evolved a large, polymorphic family of intra-cellular receptors with a nucleotide-binding domain and leucine-rich repeats, termed NLRs. Plant NLR receptors are analogous to animal NLR innate immune receptors. NLR receptors in both kingdoms are activated either by direct interactions with ligands, including effector proteins, or by recognition of effector-modified host cellular machines that are the nominal effector targets or decoys of those targets (Bentham et al., 2016Bentham A. Burdett H. Anderson P.A. Williams S.J. Kobe B. Animal NLRs provide structural insights into plant NLR function.Ann. Bot. (Lond.). 2016; (Published online August 25, 2016)https://doi.org/10.1093/aob/mcw171Crossref PubMed Scopus (63) Google Scholar, Jones and Dangl, 2006Jones J.D. Dangl J.L. The plant immune system.Nature. 2006; 444: 323-329Crossref PubMed Scopus (8280) Google Scholar, van der Hoorn and Kamoun, 2008van der Hoorn R.A. Kamoun S. From Guard to Decoy: a new model for perception of plant pathogen effectors.Plant Cell. 2008; 20: 2009-2017Crossref PubMed Scopus (487) Google Scholar). NLR activation initiates effector-triggered immunity (ETI). Deciphering the mechanisms by which effector repertoires from divergent pathogens act will provide a more comprehensive view of the host cellular machinery responsible for plant immune system function. Interactome studies revealed that candidate effector repertoires from three evolutionarily diverse pathogens—P. syringae (Psy; eubacteria), H. arabidopsidis (Hpa; oomycete), and Golovinomyces orontii (Go; ascomycete)—converge onto a limited set of interconnected Arabidopsis proteins (Dreze et al., 2011Dreze M. Carvunis A.-R. Charloteaux B. Galli M. Pevzner S.J. Tasan M. Ahn Y.-Y. Balumuri P. Barabási A.-L. Bautista V. Arabidopsis Interactome Mapping ConsortiumEvidence for network evolution in an Arabidopsis interactome map.Science. 2011; 333: 601-607Crossref PubMed Google Scholar, Mukhtar et al., 2011Mukhtar M.S. Carvunis A.R. Dreze M. Epple P. Steinbrenner J. Moore J. Tasan M. Galli M. Hao T. Nishimura M.T. et al.European Union Effectoromics ConsortiumIndependently evolved virulence effectors converge onto hubs in a plant immune system network.Science. 2011; 333: 596-601Crossref PubMed Scopus (596) Google Scholar, Weßling et al., 2014Weßling R. Epple P. Altmann S. He Y. Yang L. Henz S.R. McDonald N. Wiley K. Bader K.C. Gläßer C. et al.Convergent targeting of a common host protein-network by pathogen effectors from three kingdoms of life.Cell Host Microbe. 2014; 16: 364-375Abstract Full Text Full Text PDF PubMed Scopus (240) Google Scholar). TCP14, a transcription factor belonging to the conserved TCP (teosinte branched1, CYCLOIDEA, PROLIFERATING CELL FACTORS 1 and 2) family, is one of the convergent host targets. The reference Arabidopsis Col-0 genome encodes 24 TCP family members that share a basic helix-loop-helix (bHLH) domain (the TCP domain) and are versatile regulators of plant development and hormone signaling (Lopez et al., 2015Lopez J.A. Sun Y. Blair P.B. Mukhtar M.S. TCP three-way handshake: linking developmental processes with plant immunity.Trends Plant Sci. 2015; 20: 238-245Abstract Full Text Full Text PDF PubMed Scopus (73) Google Scholar). TCP14 physically interacts with SRFR1 and contributes to effector-triggered immunity (Kim et al., 2014Kim S.H. Son G.H. Bhattacharjee S. Kim H.J. Nam J.C. Nguyen P.D.T. Hong J.C. Gassmann W. The Arabidopsis immune adaptor SRFR1 interacts with TCP transcription factors that redundantly contribute to effector-triggered immunity.Plant J. 2014; 78: 978-989Crossref PubMed Scopus (84) Google Scholar). In various tissues, TCP14 promotes cytokinin and gibberellic acid growth hormone responses (Kieffer et al., 2011Kieffer M. Master V. Waites R. Davies B. TCP14 and TCP15 affect internode length and leaf shape in Arabidopsis.Plant J. 2011; 68: 147-158Crossref PubMed Scopus (202) Google Scholar, Resentini et al., 2015Resentini F. Felipo-Benavent A. Colombo L. Blázquez M.A. Alabadí D. Masiero S. TCP14 and TCP15 mediate the promotion of seed germination by gibberellins in Arabidopsis thaliana.Mol. Plant. 2015; 8: 482-485Abstract Full Text Full Text PDF PubMed Scopus (106) Google Scholar, Steiner et al., 2012Steiner E. Efroni I. Gopalraj M. Saathoff K. Tseng T.S. Kieffer M. Eshed Y. Olszewski N. Weiss D. The Arabidopsis O-linked N-acetylglucosamine transferase SPINDLY interacts with class I TCPs to facilitate cytokinin responses in leaves and flowers.Plant Cell. 2012; 24: 96-108Crossref PubMed Scopus (121) Google Scholar). TCP14 is localized to sub-nuclear foci and its co-expression resulted in the re-localization of 22/33 tested nuclear-localized effectors from the three pathogens noted above (Weßling et al., 2014Weßling R. Epple P. Altmann S. He Y. Yang L. Henz S.R. McDonald N. Wiley K. Bader K.C. Gläßer C. et al.Convergent targeting of a common host protein-network by pathogen effectors from three kingdoms of life.Cell Host Microbe. 2014; 16: 364-375Abstract Full Text Full Text PDF PubMed Scopus (240) Google Scholar). Additionally, the phytoplasma SAP11 effector associates with other members of the TCP family to repress JA biosynthesis, which ultimately enhances the feeding behavior of its insect vector, the leaf hopper (Sugio et al., 2011Sugio A. Kingdom H.N. MacLean A.M. Grieve V.M. Hogenhout S.A. Phytoplasma protein effector SAP11 enhances insect vector reproduction by manipulating plant development and defense hormone biosynthesis.Proc. Natl. Acad. Sci. USA. 2011; 108: E1254-E1263Crossref PubMed Scopus (289) Google Scholar). Plant cells integrate growth and division cues with defense cues via phytohormone signaling interactions (Belkhadir et al., 2014Belkhadir Y. Yang L. Hetzel J. Dangl J.L. Chory J. The growth-defense pivot: crisis management in plants mediated by LRR-RK surface receptors.Trends Biochem. Sci. 2014; 39: 447-456Abstract Full Text Full Text PDF PubMed Scopus (100) Google Scholar, Robert-Seilaniantz et al., 2011Robert-Seilaniantz A. Grant M. Jones J.D. Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism.Annu. Rev. Phytopathol. 2011; 49: 317-343Crossref PubMed Scopus (1265) Google Scholar). The antagonistic regulatory relationship between the defense hormones jasmonic acid (JA) and salicylic acid (SA) endows a plant with the flexibility to prioritize defense responses against pathogens with diverse lifestyles (Robert-Seilaniantz et al., 2011Robert-Seilaniantz A. Grant M. Jones J.D. Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism.Annu. Rev. Phytopathol. 2011; 49: 317-343Crossref PubMed Scopus (1265) Google Scholar). In Arabidopsis, activation of SA-dependent responses limits the growth of biotrophic or hemibiotrophic pathogens. On the other hand, JA-dependent responses limit the growth of necrotrophic pathogens and herbivorous insects. Hence, biotrophic or hemibiotrophic pathogens inhibited by SA-mediated immune responses will benefit from activation of JA-dependent responses (Browse, 2009Browse J. Jasmonate passes muster: a receptor and targets for the defense hormone.Annu. Rev. Plant Biol. 2009; 60: 183-205Crossref PubMed Scopus (700) Google Scholar, He et al., 2004He P. Chintamanani S. Chen Z. Zhu L. Kunkel B.N. Alfano J.R. Tang X. Zhou J.M. Activation of a COI1-dependent pathway in Arabidopsis by Pseudomonas syringae type III effectors and coronatine.Plant J. 2004; 37: 589-602Crossref PubMed Scopus (122) Google Scholar, Zheng et al., 2012Zheng X.Y. Spivey N.W. Zeng W. Liu P.P. Fu Z.Q. Klessig D.F. He S.Y. Dong X. Coronatine promotes Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation.Cell Host Microbe. 2012; 11: 587-596Abstract Full Text Full Text PDF PubMed Scopus (386) Google Scholar). Host cellular machines regulating the SA-JA balance are therefore attractive targets for effectors that mimic the action of either hormone, misdirect the defense response, and thus facilitate pathogen or pest proliferation (Kazan and Lyons, 2014Kazan K. Lyons R. Intervention of phytohormone pathways by pathogen effectors.Plant Cell. 2014; 26: 2285-2309Crossref PubMed Scopus (304) Google Scholar). The transcriptional outputs of JA response are repressed by a group of JASMONATE ZIM DOMAIN (JAZ) proteins through their association with transcription factors (Chini et al., 2007Chini A. Fonseca S. Fernández G. Adie B. Chico J.M. Lorenzo O. García-Casado G. López-Vidriero I. Lozano F.M. Ponce M.R. et al.The JAZ family of repressors is the missing link in jasmonate signalling.Nature. 2007; 448: 666-671Crossref PubMed Scopus (1617) Google Scholar, Zhang et al., 2015Zhang F. Yao J. Ke J. Zhang L. Lam V.Q. Xin X.F. Zhou X.E. Chen J. Brunzelle J. Griffin P.R. et al.Structural basis of JAZ repression of MYC transcription factors in jasmonate signalling.Nature. 2015; 525: 269-273Crossref PubMed Scopus (183) Google Scholar). Three MYC transcription factors (MYC2, MYC3, and MYC4) repressed by JAZ proteins are positive regulators of JA-mediated responses in Arabidopsis (Kazan and Manners, 2013Kazan K. Manners J.M. MYC2: the master in action.Mol. Plant. 2013; 6: 686-703Abstract Full Text Full Text PDF PubMed Scopus (558) Google Scholar). JAZ proteins directly or indirectly recruit a transcription co-repressor complex containing Topless (TPL) and histone deacetylase to repress MYC activity (Pauwels et al., 2010Pauwels L. Barbero G.F. Geerinck J. Tilleman S. Grunewald W. Pérez A.C. Chico J.M. Bossche R.V. Sewell J. Gil E. et al.NINJA connects the co-repressor TOPLESS to jasmonate signalling.Nature. 2010; 464: 788-791Crossref PubMed Scopus (675) Google Scholar). JA biosynthesis is induced during normal development or following either MAMP treatment or Pseudomonas syringae infection (Lewis et al., 2015Lewis L.A. Polanski K. de Torres-Zabala M. Jayaraman S. Bowden L. Moore J. Penfold C.A. Jenkins D.J. Hill C. Baxter L. et al.Transcriptional dynamics driving MAMP-triggered immunity and pathogen effector-mediated immunosuppression in Arabidopsis leaves following infection with pseudomonas syringae pv tomato DC3000.Plant Cell. 2015; 27: 3038-3064Crossref PubMed Scopus (99) Google Scholar, Schmelz et al., 2003Schmelz E.A. Engelberth J. Alborn H.T. O’Donnell P. Sammons M. Toshima H. Tumlinson 3rd, J.H. Simultaneous analysis of phytohormones, phytotoxins, and volatile organic compounds in plants.Proc. Natl. Acad. Sci. USA. 2003; 100: 10552-10557Crossref PubMed Scopus (262) Google Scholar). JAZ proteins bind isoleucine-conjugated JA, which facilitates their physical interaction with the CORONATINE-INSENSITIVE 1 (COI1) F-box component of a Skip-cullin-F-box (SCF)-type E3 ubiquitin ligase (Sheard et al., 2010Sheard L.B. Tan X. Mao H. Withers J. Ben-Nissan G. Hinds T.R. Kobayashi Y. Hsu F.F. Sharon M. Browse J. et al.Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor.Nature. 2010; 468: 400-405Crossref PubMed Scopus (946) Google Scholar). This results in proteasome-mediated degradation of JAZ proteins and allows MYC-dependent activation of JA response genes (Thines et al., 2007Thines B. Katsir L. Melotto M. Niu Y. Mandaokar A. Liu G. Nomura K. He S.Y. Howe G.A. Browse J. JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling.Nature. 2007; 448: 661-665Crossref PubMed Scopus (1693) Google Scholar, Wasternack and Hause, 2013Wasternack C. Hause B. Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany.Ann. Bot. (Lond.). 2013; 111: 1021-1058Crossref PubMed Scopus (1549) Google Scholar). The MYC regulon controls a pleiotropic physiological and developmental response including the repression of SA-dependent transcriptional output (Kazan and Manners, 2013Kazan K. Manners J.M. MYC2: the master in action.Mol. Plant. 2013; 6: 686-703Abstract Full Text Full Text PDF PubMed Scopus (558) Google Scholar). At least two Psy type III effectors, HopX1 and HopZ1a, and the phytotoxin coronatine can activate the JA pathway. Coronatine is a structural mimic of JA-Ile (Katsir et al., 2008Katsir L. Schilmiller A.L. Staswick P.E. He S.Y. Howe G.A. COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine.Proc. Natl. Acad. Sci. USA. 2008; 105: 7100-7105Crossref PubMed Scopus (592) Google Scholar). HopX1 is a cysteine protease that eliminates JAZ proteins by cleaving their central ZIM domain (Gimenez-Ibanez et al., 2014Gimenez-Ibanez S. Boter M. Fernández-Barbero G. Chini A. Rathjen J.P. Solano R. The bacterial effector HopX1 targets JAZ transcriptional repressors to activate jasmonate signaling and promote infection in Arabidopsis.PLoS Biol. 2014; 12: e1001792Crossref PubMed Scopus (173) Google Scholar). HopZ1a is an acetyltransferase that acetylates soybean and Arabidopsis JAZ proteins, promoting COI1-dependent JAZ turnover (Jiang et al., 2013Jiang S. Yao J. Ma K.W. Zhou H. Song J. He S.Y. Ma W. Bacterial effector activates jasmonate signaling by directly targeting JAZ transcriptional repressors.PLoS Pathog. 2013; 9: e1003715Crossref PubMed Scopus (159) Google Scholar). Both HopX1 and HopZ1a were identified from Psy strains deficient in coronatine biosynthesis, and each can rescue the growth defects of a Psy mutant unable to synthesize coronatine (Gimenez-Ibanez et al., 2014Gimenez-Ibanez S. Boter M. Fernández-Barbero G. Chini A. Rathjen J.P. Solano R. The bacterial effector HopX1 targets JAZ transcriptional repressors to activate jasmonate signaling and promote infection in Arabidopsis.PLoS Biol. 2014; 12: e1001792Crossref PubMed Scopus (173) Google Scholar, Jiang et al., 2013Jiang S. Yao J. Ma K.W. Zhou H. Song J. He S.Y. Ma W. Bacterial effector activates jasmonate signaling by directly targeting JAZ transcriptional repressors.PLoS Pathog. 2013; 9: e1003715Crossref PubMed Scopus (159) Google Scholar). Effects of HopX1 or HopZ1a action on the global, JA-activated transcriptional landscape have not been defined, though each causes de-repression of a few tested JA response genes (Gimenez-Ibanez et al., 2014Gimenez-Ibanez S. Boter M. Fernández-Barbero G. Chini A. Rathjen J.P. Solano R. The bacterial effector HopX1 targets JAZ transcriptional repressors to activate jasmonate signaling and promote infection in Arabidopsis.PLoS Biol. 2014; 12: e1001792Crossref PubMed Scopus (173) Google Scholar, Jiang et al., 2013Jiang S. Yao J. Ma K.W. Zhou H. Song J. He S.Y. Ma W. Bacterial effector activates jasmonate signaling by directly targeting JAZ transcriptional repressors.PLoS Pathog. 2013; 9: e1003715Crossref PubMed Scopus (159) Google Scholar). Here, we provide a mechanistic model for how one of the many TCP14-targeting effectors suppresses defense by manipulating the host defense hormone network to promote Psy virulence. Our data demonstrate that the previously unstudied bacterial type III effector, HopBB1, alters subsets of targets from two heretofore unlinked transcriptional regulons, TCP14 and MYC, to de-repress a subset of JA responses and promote virulence while avoiding pleiotropic effects associated with full misregulation of either regulon. We showed that a tcp14 mutant enhanced susceptibility to the avirulent Emwa1 isolate of the oomycete pathogen, Hpa (Mukhtar et al., 2011Mukhtar M.S. Carvunis A.R. Dreze M. Epple P. Steinbrenner J. Moore J. Tasan M. Galli M. Hao T. Nishimura M.T. et al.European Union Effectoromics ConsortiumIndependently evolved virulence effectors converge onto hubs in a plant immune system network.Science. 2011; 333: 596-601Crossref PubMed Scopus (596) Google Scholar, Weßling et al., 2014Weßling R. Epple P. Altmann S. He Y. Yang L. Henz S.R. McDonald N. Wiley K. Bader K.C. Gläßer C. et al.Convergent targeting of a common host protein-network by pathogen effectors from three kingdoms of life.Cell Host Microbe. 2014; 16: 364-375Abstract Full Text Full Text PDF PubMed Scopus (240) Google Scholar). We confirmed and extended this result using a second tcp14 allele and transgenic Arabidopsis overexpressing YFP-TCP14 from the UBQ promoter (Figures 1A and 1B). These plants were modestly smaller than wild-type plants at the same developmental stage (Figures 1A and S1A) and displayed enhanced disease resistance when challenged with the virulent Hpa isolate Noco2 (Figure 1B). We examined the in planta growth of P. syringae pv. tomato strain DC3000 (Pto DC3000, hereafter DC3000) and a coronatine-deficient mutant, Pto DC3000 cor− (hereafter DC3000 cor−), on tcp14 mutants and TCP14 overexpression lines. Plants overexpressing TCP14 displayed enhanced resistance to DC3000 at the same levels as coi1 mutants (Figure 1C). The growth of DC3000 cor− was the same on Col-0 and plants overexpressing TCP14 (Figure 1C). tcp14 mutants were unaltered in their response to DC3000 but rescued the growth defects of DC3000 cor− (Figure 1C). These disease phenotypes suggest that TCP14 regulates immune system output by suppressing the JA response. To test the hypothesis that TCP14 is a negative regulator of the JA pathway, we defined a comprehensive set of marker genes for the JA and SA responses (Figures S1B–S1F; Table S1) and analyzed the transcriptomes of Col-0, tcp14 mutants, and transgenic plants overexpressing TCP14 in 2-week-old seedlings; the time point when altered infection phenotypes were observed. A total of 203 genes were differentially expressed in TCP14-overexpressing seedlings compared to Col-0 (Figure 1D; Table S2). Genes downregulated by TCP14 overexpression were significantly enriched for genes that are activated by JA treatment (26/102; p = 2.19e-19, hypergeometric test; cluster 1, Figures 1D and 1E). Indeed, many of these downregulated genes were also weakly expressed in the coi1-16 mutant (Figure 1D; Table S2). In contrast, only 6 of the 101 genes that were upregulated in the UBQ::YFP-TCP14-3 line are markers of the SA response (Figure 1D), suggesting that TCP14-driven repression of the JA pathway was not a consequence of activated SA response. No global transcriptome changes were observed in tcp14 mutants relative to Col-0 in non-infected plants (Table S2). However, some JA-responsive genes, including VSP2 and those required for anthocyanin biosynthesis, were upregulated in the mutants (Figure 1F). We also examined transcriptional alterations in these plants 24 hr after infection with DC3000 cor−. When compared to infected Col-0, both coi1-16 and the UBQ::YFP-TCP14-4 line showed weaker activation of JA-responsive genes (Figures 1G and 1H; Table S2). Although the suppression of the JA response is an obvious transcriptional alteration in either wild-type or infected UBQ::YFP-TCP14 plants (Figures 1D and 1H), TCP14 may also participate in the regulation of other sectors of the plant immune system. Indeed, the enhanced disease phenotype in UBQ::YFP-TCP14 also correlates with suppression of ABA-responsive genes and responses related to ABA signaling (Figure 1I, Table S2). Moreover, TCP14-overexpressing lines displayed enhanced activation of SA-responsive genes after infection (Figure 1I; Table S2), consistent with their enhanced resistance to both DC3000 and Hpa isolate Noco2 (Figures 1B and 1C). However, only 43 genes were differentially expressed in the infected tcp14-6 mutant relative to wild-type plants (Figure 1G; Table S2). We do not know if the effects of tcp14 mutation would be more dramatic at different time points in the response. Overall, this transcriptional profile supports the conclusion that TCP14 contributes to plant immunity as a negative regulator of subsets of the JA response. To demonstrate how effectors modulate TCP14 function, we focused first on an uncharacterized TCP14-interacting Psy type III effector, HopBB1 (Mukhtar et al., 2011Mukhtar M.S. Carvunis A.R. Dreze M. Epple P. Steinbrenner J. Moore J. Tasan M. Galli M. Hao T. Nishimura M.T. et al.European Union Effectoromics ConsortiumIndependently evolved virulence effectors converge onto hubs in a plant immune system network.Science. 2011; 333: 596-601Crossref PubMed Scopus (596) Google Scholar). In yeast, HopBB1 selectively interacts with a subset of 24 Arabidopsis TCP family members (Figure S2A). We validated the interactions between HopBB1 and TCP14 in planta by inoculating YFP-TCP14 overexpressing Arabidopsis with DC3000 cor− expressing HopBB1-HA at native levels. We observed that HopBB1-HA was co-immunoprecipitated with YFP-TCP14 (Figure 2A), demonstrating that these two proteins associate in vivo during Psy infection. We used random mutagenesis to isolate a HopBB1 mutant, HopBB1G126D that lost interaction with TCP14 in yeast-two-hybridization (Y2H) and failed to associate with TCP14 in planta (Figures 2A, 2B, and S2B). HopBB1111-283 that contains G126, but has no annotated function, was sufficient for association with TCP14 (Figure 2C). TCP14180-489 downstream of the conserved TCP DNA binding domain was sufficient for interaction with HopBB1 in yeast and in planta (Figures 2D, 2E, and S2C). TCP14180-216 co-immunoprecipitated with HopBB1 (Figure 2E). We replaced every six amino acids in this region with a structurally flexible sequence (NAAIRS; Wilson et al., 1985Wilson I.A. Haft D.H. Getzoff E.D. Tainer J.A. Lerner R.A. Brenner S. Identical short peptide sequences in unrelated proteins can have different conformations: a testing ground for theories of immune recognition.Proc. Natl. Acad. Sci. USA. 1985; 82: 5255-5259Crossref PubMed Scopus (133) Google Scholar), and revealed that the TCP14 sequence motif 204-RSAAST-209 is necessary for interaction between full length TCP14 and HopBB1 (Figures 2F, 2G, and S2D). Collectively, these data are consistent with the hypothesis that HopBB1 associates with TCP14 in vivo. We tested the hypothesis that HopBB1 targets TCP14 to manipulate plant JA response. Following delivery of native levels via type III secretion, HopBB1, but not HopBB1G126D, partially rescued the growth defects of DC3000 cor− on Col-0 plants (Figures 3A and S3A). Growth promotion of DC3000 cor− contributed by HopBB1 was suppressed by overexpression of TCP14 and in coi1 (Figure 3A). These observations indicate that HopBB1 partially complements the defects of coronatine deficiency, that this can be modulated by TCP14, and that it requires COI1. We then investigated the effect of HopBB1 on the transcriptome of wild-type plants 24 hr after the infection. As expected, the transcriptome of plants infected with DC3000 was significantly different from those sprayed with either a mock or DC3000 cor− (EV) (Figures 3B and 3C). The set of 697 genes that were more strongly induced by DC3000 than by DC3000 cor− (EV) was enriched in biological processes related to JA and ABA responses (Table S3). Remarkably, infection with DC3000 cor− (HopBB1) resulted in a global transcriptional signature that resembled infection with DC3000 (Figure 3C), supporting our conclusion that HopBB1 can rescue the impaired ability of DC3000 cor− to establish infection. A total of 129 of the 672 (19%) JA-responsive genes were expressed to higher levels in plants infected with DC3000 or DC3000 cor− (HopBB1) than in plants with DC3000 cor− (EV) treatment. Although the transcriptional changes induced by DC3000 cor− (HopBB1G126D) qualitatively resembled those induced by DC3000 (Figure 3C), these JA-responsive genes were less activated (p value = 2.2e−16, Student’s t test), indicating that interaction with TCP14 is required for the full virulence function of HopBB1 (Figure 3D). To exclude the possibility that the transcriptome change induced by bacteria-delivered HopBB1 may be confounded by other effectors that may influence JA signaling, we defined the transcriptome of transgenic plants expressing only HopBB1. As expected if HopBB1 potentiates JA responses, these plants were hypersensitive to JA-mediated inhibition of root elongation (Figure S3C). In addition, DC3000 cor− is more virulent on HopBB1 transgenic plants than on wild-type Col-0, demonstrating that heterologous HopBB1 complements this strain’s coronatine deficiency (Figure 3F), analogous to tcp14 (Figure 1C). We compared the transcriptome of HopBB1-expressing plants to Col-0 at steady state and identified 628 differentially expressed genes (593 upregulated and 35 downregulated) (Table S3). Many of our JA response marker genes (93/672; p = 3.41e−47; hypergeometric test) were upregulated in the HopBB1 expressing plants (Table S3), and the average expression of all 672 JA-responsive genes was higher in these transgenic plants (Figure 3G). JA response genes were enriched in the overlap between HopBB1-upregulated and TCP14-suppressed genes: out of the 102 genes that were downregulated by steady-state TCP14 overexpression (Figure 1D; Table S4), 12 were upregulated in HopBB1 transgenic plants and 10 of these are JA markers (p = 2.26e−17; hypergeometric test) (Table S4). Genes specific to BTH/SA response were also enriched in the HopBB1 upregulated genes (139/2,096; p = 2.53e−33; hypergeometric test). However, genes that are typically associated with SA-mediated defense responses (e.g., PR-1, PR-5, ICS1, and WRKYs) were not differentially expressed, suggesting that the SA response activated in HopBB1-expressing plants is likely to be insufficient for robust defense. As expected, the JA response genes defined in our study were enriched for MYC2 binding motifs in their promoters (Figure S3D). In fact, these genes were enriched for co-occurrence of MYC2 and TCP binding sites (Franco-Zorrilla et al., 2014Franco-Zorrilla J.M. López-Vidriero I. Carrasco J.L. Godoy M. Vera P. Solano R. DNA-binding specificities of plant transcription factors and their potential to define target genes.Proc. Natl. Acad. Sci. USA. 2014; 111: 2367-2372Crossref PubMed Scopus (435) Google Scholar, Kosugi and Ohashi, 2002Kosugi S. Ohashi Y. DNA binding and dimerization specificity and potential targets for the TCP protein family.Plant J. 2002; 30: 337-348Crossref PubMed Scopus (303) Google Scholar). Out of the 88 JA response genes that contain consensus MYC and TCP motifs in their promoters, 22 (25%) were also upregulated by HopBB1 expression (Figure S3E). Interestingly, neither constitutive nor conditional overexpression of HopBB1 caused the chlorotic leaf phenotype observed previously after either coronatine treatment or HopX1 expression (Figure S3F; Gimenez-Ibanez et al., 2014Gimenez-Ibanez S. Boter M. Fernández-Barbero G. Chini A. Rathjen J.P. Solano R. The bacterial effector HopX1 targets JAZ transcriptional repressors to activate jasmonate signaling and promote infection in Arabidopsis.PLoS Biol. 2014; 12: e1001792Crossref PubMed Scopus (173) Google Scholar, Kloek et al., 2001Kloek A.P. Verbsky M.L. Sharma S.B. Schoelz J.E. Vogel J. Klessig D.F. Kunkel B.N. Resistance to Pseudomonas syringae conferred by an Arabidopsis thaliana coronatine-insensitive (coi1) mutation occurs through two distinct mechanisms.Plant J. 2001; 26: 509-522Crossref PubMed Google Scholar). Consistent with this observation, the expression of MYC-dependent and JA-responsive photosynthetic genes (Qi et al., 2015Qi T. Wang J. Huang H. Liu B." @default.
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