{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,2]],"date-time":"2026-10-02T04:19:34Z","timestamp":1790914774372,"version":"4.1.0"},"reference-count":60,"publisher":"Springer Science and Business Media LLC","issue":"6","license":[{"start":{"date-parts":[[2023,4,17]],"date-time":"2023-04-17T00:00:00Z","timestamp":1681689600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2023,4,17]],"date-time":"2023-04-17T00:00:00Z","timestamp":1681689600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001869","name":"Academia Sinica, Taiwan","doi-asserted-by":"publisher","award":["AS\u2010IA\u2010107\u2010L01"],"award-info":[{"award-number":["AS\u2010IA\u2010107\u2010L01"]}],"id":[{"id":"10.13039\/501100001869","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100020595","name":"National Science and Technology Council of Taiwan","doi-asserted-by":"crossref","award":["NSTC 110\u20102311\u2010B\u2010001\u2010032\u2010MY3"],"award-info":[{"award-number":["NSTC 110\u20102311\u2010B\u2010001\u2010032\u2010MY3"]}],"id":[{"id":"10.13039\/100020595","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["EMBO Rep"],"published-print":{"date-parts":[[2023,6,5]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>\n                    Type VI secretion systems (T6SSs) can deliver diverse toxic effectors into eukaryotic and bacterial cells. Although much is known about the regulation and assembly of T6SS, the translocation mechanism of effectors into the periplasm and\/or cytoplasm of target cells remains elusive. Here, we use the\n                    <jats:italic>Agrobacterium tumefaciens<\/jats:italic>\n                    DNase effector Tde1 to unravel the mechanism of translocation from attacker to prey. We demonstrate that Tde1 binds to its adaptor Tap1 through the N\u2010terminus, which harbors continuous copies of GxxxG motifs resembling the glycine zipper structure found in proteins involved in the membrane channel formation. Amino acid substitutions on G\n                    <jats:sup>39<\/jats:sup>\n                    xxxG\n                    <jats:sup>43<\/jats:sup>\n                    motif do not affect Tde1\u2013Tap1 interaction and secretion but abolish its membrane permeability and translocation of its fluorescent fusion protein into prey cells. The data suggest that G\n                    <jats:sup>39<\/jats:sup>\n                    xxxG\n                    <jats:sup>43<\/jats:sup>\n                    governs the delivery of Tde1 into target cells by permeabilizing the cytoplasmic membrane. Considering the widespread presence of GxxxG motifs in bacterial effectors and pore\u2010forming toxins, we propose that glycine zipper\u2010mediated permeabilization is a conserved mechanism used by bacterial effectors for translocation across target cell membranes.\n                  <\/jats:p>","DOI":"10.15252\/embr.202356849","type":"journal-article","created":{"date-parts":[[2023,4,17]],"date-time":"2023-04-17T04:56:53Z","timestamp":1681707413000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":15,"title":["A glycine zipper motif is required for the translocation of a T6SS toxic effector into target cells"],"prefix":"10.1038","volume":"24","author":[{"given":"Jemal","family":"Ali","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5932-9597","authenticated-orcid":false,"given":"Manda","family":"Yu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Li\u2010Kang","family":"Sung","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1421-4419","authenticated-orcid":false,"given":"Yee\u2010Wai","family":"Cheung","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3630-8683","authenticated-orcid":false,"given":"Erh\u2010Min","family":"Lai","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2023,4,17]]},"reference":[{"key":"BFEMBR202356849_CR1","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.62816","volume":"9","author":"S Ahmad","year":"2020","unstructured":"Ahmad S, Tsang KK, Sachar K, Quentin D, Tashin TM, Bullen NP, Raunser S, McArthur AG, Prehna G, Whitney JC (2020) Structural basis for effector transmembrane domain recognition by type VI secretion system chaperones. Elife 9: e62816","journal-title":"Elife"},{"key":"BFEMBR202356849_CR2","volume":"45","author":"J Ali","year":"2022","unstructured":"Ali J, Lai EM (2022) Distinct TssA proteins converge in coordinating tail biogenesis of the type VI secretion systems. Bioessays 45: e2200219","journal-title":"Bioessays"},{"key":"BFEMBR202356849_CR3","doi-asserted-by":"crossref","DOI":"10.1128\/mbio.03396-21","volume":"13","author":"I Atanaskovic","year":"2022","unstructured":"Atanaskovic I, Sharp C, Press C, Kaminska R, Kleanthous C (2022) Bacterial competition systems share a domain required for inner membrane transport of the Bacteriocin Pyocin G from Pseudomonas aeruginosa. mBio 13: e0339621","journal-title":"mBio"},{"key":"BFEMBR202356849_CR4","doi-asserted-by":"crossref","DOI":"10.1038\/msb4100050","volume":"2","author":"T Baba","year":"2006","unstructured":"Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H (2006) Construction of Escherichia coli K\u201012 in\u2010frame, single\u2010gene knockout mutants: the Keio collection. Mol Syst Biol 2: 2006.0008","journal-title":"Mol Syst Biol"},{"key":"BFEMBR202356849_CR5","doi-asserted-by":"crossref","first-page":"182","DOI":"10.1038\/nature10846","volume":"483","author":"M Basler","year":"2012","unstructured":"Basler M, Pilhofer M, Henderson GP, Jensen GJ, Mekalanos JJ (2012) Type VI secretion requires a dynamic contractile phage tail\u2010like structure. Nature 483: 182\u2013186","journal-title":"Nature"},{"key":"BFEMBR202356849_CR6","volume":"11","author":"HM Behrens","year":"2020","unstructured":"Behrens HM, Lowe ED, Gault J, Housden NG, Kaminska R, Weber TM, Thompson CMA, Mislin GLA, Schalk IJ, Walker D et\u00a0al (2020) Pyocin S5 import into Pseudomonas aeruginosa reveals a generic mode of Bacteriocin transport. mBio 11: e03230\u201019","journal-title":"mBio"},{"key":"BFEMBR202356849_CR7","doi-asserted-by":"crossref","first-page":"E3931","DOI":"10.1073\/pnas.1600428113","volume":"113","author":"DD Bondage","year":"2016","unstructured":"Bondage DD, Lin JS, Ma LS, Kuo CH, Lai EM (2016) VgrG C terminus confers the type VI effector transport specificity and is required for binding with PAAR and adaptor\u2010effector complex. Proc Natl Acad Sci U S A 113: E3931\u2013E3940","journal-title":"Proc Natl Acad Sci U S A"},{"key":"BFEMBR202356849_CR8","doi-asserted-by":"crossref","first-page":"7044","DOI":"10.1016\/S0021-9258(18)53143-4","volume":"268","author":"P Casteels","year":"1993","unstructured":"Casteels P, Ampe C, Jacobs F, Tempst P (1993) Functional and chemical characterization of Hymenoptaecin, an antibacterial polypeptide that is infection\u2010inducible in the honeybee (Apis mellifera). J Biol Chem 268: 7044\u20137054","journal-title":"J Biol Chem"},{"key":"BFEMBR202356849_CR9","doi-asserted-by":"crossref","first-page":"1404","DOI":"10.1038\/s41564-018-0260-1","volume":"3","author":"Y Cherrak","year":"2018","unstructured":"Cherrak Y, Rapisarda C, Pellarin R, Bouvier G, Bardiaux B, Allain F, Malosse C, Rey M, Chamot\u2010Rooke J, Cascales E et\u00a0al (2018) Biogenesis and structure of a type VI secretion baseplate. Nat Microbiol 3: 1404\u20131416","journal-title":"Nat Microbiol"},{"key":"BFEMBR202356849_CR10","doi-asserted-by":"publisher","DOI":"10.1128\/microbiolspec.PSIB-0031-2019","author":"Y Cherrak","year":"2019","unstructured":"Cherrak Y, Flaugnatti N, Durand E, Journet L, Cascales E (2019) Structure and activity of the type VI secretion system. Microbiol Spectr 7 https:\/\/doi.org\/10.1128\/microbiolspec.PSIB\u20100031\u20102019","journal-title":"Microbiol Spectr"},{"key":"BFEMBR202356849_CR11","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1186\/s12915-021-01221-y","volume":"20","author":"L Chou","year":"2022","unstructured":"Chou L, Lin YC, Haryono M, Santos MNM, Cho ST, Weisberg AJ, Wu CF, Chang JH, Lai EM, Kuo CH (2022) Modular evolution of secretion systems and virulence plasmids in a bacterial species complex. BMC Biol 20: 16","journal-title":"BMC Biol"},{"key":"BFEMBR202356849_CR12","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1007\/s10930-019-09862-3","volume":"38","author":"PJ Christie","year":"2019","unstructured":"Christie PJ (2019) The rich tapestry of bacterial protein translocation systems. Protein J 38: 389\u2013408","journal-title":"Protein J"},{"key":"BFEMBR202356849_CR13","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1016\/j.tim.2015.10.005","volume":"24","author":"FR Cianfanelli","year":"2016","unstructured":"Cianfanelli FR, Monlezun L, Coulthurst SJ (2016) Aim, load, fire: the type VI secretion system, a bacterial Nanoweapon. Trends Microbiol 24: 51\u201362","journal-title":"Trends Microbiol"},{"key":"BFEMBR202356849_CR14","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1038\/nrmicro3456","volume":"13","author":"TR Costa","year":"2015","unstructured":"Costa TR, Felisberto\u2010Rodrigues C, Meir A, Prevost MS, Redzej A, Trokter M, Waksman G (2015) Secretion systems in gram\u2010negative bacteria: structural and mechanistic insights. Nat Rev Microbiol 13: 343\u2013359","journal-title":"Nat Rev Microbiol"},{"key":"BFEMBR202356849_CR15","doi-asserted-by":"crossref","first-page":"503","DOI":"10.1099\/mic.0.000789","volume":"165","author":"S Coulthurst","year":"2019","unstructured":"Coulthurst S (2019) The type VI secretion system: a versatile bacterial weapon. Microbiology 165: 503\u2013515","journal-title":"Microbiology"},{"key":"BFEMBR202356849_CR16","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1111\/mmi.12918","volume":"96","author":"N Cumby","year":"2015","unstructured":"Cumby N, Reimer K, Mengin\u2010Lecreulx D, Davidson AR, Maxwell KL (2015) The phage tail tape measure protein, an inner membrane protein and a periplasmic chaperone play connected roles in the genome injection process of E. coli phage HK97. Mol Microbiol 96: 437\u2013447","journal-title":"Mol Microbiol"},{"key":"BFEMBR202356849_CR17","doi-asserted-by":"crossref","DOI":"10.3389\/fmicb.2021.754486","volume":"12","author":"S Czolkoss","year":"2021","unstructured":"Czolkoss S, Safronov X, Rexroth S, Knoke LR, Aktas M, Narberhaus F (2021) Agrobacterium tumefaciens type IV and type VI secretion systems reside in detergent\u2010resistant membranes. Front Microbiol 12: 754486","journal-title":"Front Microbiol"},{"key":"BFEMBR202356849_CR18","doi-asserted-by":"crossref","first-page":"555","DOI":"10.1038\/nature14667","volume":"523","author":"E Durand","year":"2015","unstructured":"Durand E, Nguyen VS, Zoued A, Logger L, Pehau\u2010Arnaudet G, Aschtgen MS, Spinelli S, Desmyter A, Bardiaux B, Dujeancourt A et\u00a0al (2015) Biogenesis and structure of a type VI secretion membrane core complex. Nature 523: 555\u2013560","journal-title":"Nature"},{"key":"BFEMBR202356849_CR19","doi-asserted-by":"crossref","first-page":"2250","DOI":"10.1016\/j.bpj.2009.08.006","volume":"97","author":"RF Epand","year":"2009","unstructured":"Epand RF, Sarig H, Mor A, Epand RM (2009) Cell\u2010wall interactions and the selective bacteriostatic activity of a miniature oligo\u2010acyl\u2010lysyl. Biophys J 97: 2250\u20132257","journal-title":"Biophys J"},{"key":"BFEMBR202356849_CR20","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1186\/1750-1326-6-61","volume":"6","author":"V Fonte","year":"2011","unstructured":"Fonte V, Dostal V, Roberts CM, Gonzales P, Lacor PN, Velasco PT, Magrane J, Dingwell N, Fan EY, Silverman MA et\u00a0al (2011) A glycine zipper motif mediates the formation of toxic beta\u2010amyloid oligomers in vitro and in vivo. Mol Neurodegener 6: 61","journal-title":"Mol Neurodegener"},{"key":"BFEMBR202356849_CR21","doi-asserted-by":"crossref","first-page":"1085","DOI":"10.1038\/s41467-020-14951-4","volume":"11","author":"CM Fridman","year":"2020","unstructured":"Fridman CM, Keppel K, Gerlic M, Bosis E, Salomon D (2020) A comparative genomics methodology reveals a widespread family of membrane\u2010disrupting T6SS effectors. Nat Commun 11: 1085","journal-title":"Nat Commun"},{"key":"BFEMBR202356849_CR22","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.24869","volume":"6","author":"L Garcia\u2010Bayona","year":"2017","unstructured":"Garcia\u2010Bayona L, Guo MS, Laub MT (2017) Contact\u2010dependent killing by Caulobacter crescentus via cell surface\u2010associated, glycine zipper proteins. Elife 6: e24869","journal-title":"Elife"},{"key":"BFEMBR202356849_CR23","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1002\/pro.3235","volume":"27","author":"TD Goddard","year":"2018","unstructured":"Goddard TD, Huang CC, Meng EC, Pettersen EF, Couch GS, Morris JH, Ferrin TE (2018) UCSF ChimeraX: meeting modern challenges in visualization and analysis. Protein Sci 27: 14\u201325","journal-title":"Protein Sci"},{"key":"BFEMBR202356849_CR24","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1016\/j.mib.2015.11.006","volume":"29","author":"A Hachani","year":"2016","unstructured":"Hachani A, Wood TE, Filloux A (2016) Type VI secretion and anti\u2010host effectors. Curr Opin Microbiol 29: 81\u201393","journal-title":"Curr Opin Microbiol"},{"key":"BFEMBR202356849_CR25","doi-asserted-by":"crossref","DOI":"10.1128\/mBio.01115-21","volume":"12","author":"SJ Hersch","year":"2021","unstructured":"Hersch SJ, Lam L, Dong TG (2021) Engineered type six secretion systems deliver active exogenous effectors and Cre recombinase. mBio 12: e0111521","journal-title":"mBio"},{"key":"BFEMBR202356849_CR26","doi-asserted-by":"crossref","first-page":"9427","DOI":"10.1073\/pnas.1711219114","volume":"114","author":"BT Ho","year":"2017","unstructured":"Ho BT, Fu Y, Dong TG, Mekalanos JJ (2017) Vibrio cholerae type 6 secretion system effector trafficking in target bacterial cells. Proc Natl Acad Sci U S A 114: 9427\u20139432","journal-title":"Proc Natl Acad Sci U S A"},{"key":"BFEMBR202356849_CR27","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1111\/mmi.14648","volume":"115","author":"D Jurenas","year":"2021","unstructured":"Jurenas D, Journet L (2021) Activity, delivery, and diversity of type VI secretion effectors. Mol Microbiol 115: 383\u2013394","journal-title":"Mol Microbiol"},{"key":"BFEMBR202356849_CR28","first-page":"969","volume":"60","author":"CI Kado","year":"1970","unstructured":"Kado CI, Heskett MG (1970) Selective media for isolation of Agrobacterium, Carynebacterium, Erwinia, Pseudomonas, and Xanthomonas. Phytopathology 60: 969\u2013976","journal-title":"Phytopathology"},{"key":"BFEMBR202356849_CR29","doi-asserted-by":"crossref","first-page":"845","DOI":"10.1038\/nprot.2015.053","volume":"10","author":"LA Kelley","year":"2015","unstructured":"Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJ (2015) The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 10: 845\u2013858","journal-title":"Nat Protoc"},{"key":"BFEMBR202356849_CR30","doi-asserted-by":"crossref","first-page":"5988","DOI":"10.1073\/pnas.0308694101","volume":"101","author":"S Kim","year":"2004","unstructured":"Kim S, Chamberlain AK, Bowie JU (2004) Membrane channel structure of helicobacter pylori vacuolating toxin: role of multiple GXXXG motifs in cylindrical channels. Proc Natl Acad Sci U S A 101: 5988\u20135991","journal-title":"Proc Natl Acad Sci U S A"},{"key":"BFEMBR202356849_CR31","doi-asserted-by":"crossref","first-page":"14278","DOI":"10.1073\/pnas.0501234102","volume":"102","author":"S Kim","year":"2005","unstructured":"Kim S, Jeon TJ, Oberai A, Yang D, Schmidt JJ, Bowie JU (2005) Transmembrane glycine zippers: physiological and pathological roles in membrane proteins. Proc Natl Acad Sci U S A 102: 14278\u201314283","journal-title":"Proc Natl Acad Sci U S A"},{"key":"BFEMBR202356849_CR32","doi-asserted-by":"crossref","first-page":"440","DOI":"10.1038\/s41564-018-0113-y","volume":"3","author":"KD LaCourse","year":"2018","unstructured":"LaCourse KD, Peterson SB, Kulasekara HD, Radey MC, Kim J, Mougous JD (2018) Conditional toxicity and synergy drive diversity among antibacterial effectors. Nat Microbiol 3: 440\u2013446","journal-title":"Nat Microbiol"},{"key":"BFEMBR202356849_CR33","doi-asserted-by":"crossref","first-page":"254","DOI":"10.3389\/fcimb.2017.00254","volume":"7","author":"YW Lien","year":"2017","unstructured":"Lien YW, Lai EM (2017) Type VI secretion effectors: methodologies and biology. Front Cell Infect Microbiol 7: 254","journal-title":"Front Cell Infect Microbiol"},{"key":"BFEMBR202356849_CR34","volume":"8","author":"JS Lin","year":"2013","unstructured":"Lin JS, Ma LS, Lai EM (2013) Systematic dissection of the Agrobacterium type VI secretion system reveals machinery and secreted components for subcomplex formation. PLoS One 8: e67647","journal-title":"PLoS One"},{"key":"BFEMBR202356849_CR35","doi-asserted-by":"crossref","first-page":"3354","DOI":"10.1016\/j.febslet.2010.06.021","volume":"584","author":"H Ling","year":"2010","unstructured":"Ling H, Saeidi N, Rasouliha BH, Chang MW (2010) A predicted S\u2010type pyocin shows a bactericidal activity against clinical Pseudomonas aeruginosa isolates through membrane damage. FEBS Lett 584: 3354\u20133358","journal-title":"FEBS Lett"},{"key":"BFEMBR202356849_CR36","doi-asserted-by":"crossref","first-page":"D265","DOI":"10.1093\/nar\/gkz991","volume":"48","author":"S Lu","year":"2020","unstructured":"Lu S, Wang J, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Marchler GH, Song JS et\u00a0al (2020) CDD\/SPARCLE: the conserved domain database in 2020. Nucleic Acids Res 48: D265\u2013D268","journal-title":"Nucleic Acids Res"},{"key":"BFEMBR202356849_CR38","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1016\/j.chom.2014.06.002","volume":"16","author":"LS Ma","year":"2014","unstructured":"Ma LS, Hachani A, Lin JS, Filloux A, Lai EM (2014) Agrobacterium tumefaciens deploys a superfamily of type VI secretion DNase effectors as weapons for interbacterial competition in planta. Cell Host Microbe 16: 94\u2013104","journal-title":"Cell Host Microbe"},{"key":"BFEMBR202356849_CR39","doi-asserted-by":"crossref","first-page":"5484","DOI":"10.1038\/s41467-019-13439-0","volume":"10","author":"G Mariano","year":"2019","unstructured":"Mariano G, Trunk K, Williams DJ, Monlezun L, Strahl H, Pitt SJ, Coulthurst SJ (2019) A family of type VI secretion system effector proteins that form ion\u2010selective pores. Nat Commun 10: 5484","journal-title":"Nat Commun"},{"key":"BFEMBR202356849_CR40","doi-asserted-by":"crossref","first-page":"12101","DOI":"10.1074\/jbc.M212595200","volume":"278","author":"MS McClain","year":"2003","unstructured":"McClain MS, Iwamoto H, Cao P, Vinion\u2010Dubiel AD, Li Y, Szabo G, Shao Z, Cover TL (2003) Essential role of a GXXXG motif for membrane channel formation by Helicobacter pylori vacuolating toxin. J Biol Chem 278: 12101\u201312108","journal-title":"J Biol Chem"},{"key":"BFEMBR202356849_CR41","doi-asserted-by":"crossref","DOI":"10.1371\/journal.ppat.1003752","volume":"9","author":"ST Miyata","year":"2013","unstructured":"Miyata ST, Unterweger D, Rudko SP, Pukatzki S (2013) Dual expression profile of type VI secretion system immunity genes protects pandemic Vibrio cholerae. PLoS Pathog 9: e1003752","journal-title":"PLoS Pathog"},{"key":"BFEMBR202356849_CR43","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1111\/mmi.14599","volume":"115","author":"T Palmer","year":"2020","unstructured":"Palmer T, Finney AJ, Saha CK, Atkinson GC, Sargent F (2020) A holin\/peptidoglycan hydrolase\u2010dependent protein secretion system. Mol Microbiol 115: 345\u2013355","journal-title":"Mol Microbiol"},{"key":"BFEMBR202356849_CR44","doi-asserted-by":"crossref","first-page":"381","DOI":"10.1093\/protein\/12.5.381","volume":"12","author":"C Pasquier","year":"1999","unstructured":"Pasquier C, Promponas VJ, Palaios GA, Hamodrakas JS, Hamodrakas SJ (1999) A novel method for predicting transmembrane segments in proteins based on a statistical analysis of the SwissProt database: the PRED\u2010TMR algorithm. Protein Eng 12: 381\u2013385","journal-title":"Protein Eng"},{"key":"BFEMBR202356849_CR45","doi-asserted-by":"crossref","first-page":"1865","DOI":"10.1038\/s41467-020-15774-z","volume":"11","author":"TT Pei","year":"2020","unstructured":"Pei TT, Li H, Liang X, Wang ZH, Liu G, Wu LL, Kim H, Xie Z, Yu M, Lin S et\u00a0al (2020) Intramolecular chaperone\u2010mediated secretion of an Rhs effector toxin by a type VI secretion system. Nat Commun 11: 1865","journal-title":"Nat Commun"},{"key":"BFEMBR202356849_CR46","doi-asserted-by":"crossref","first-page":"1142","DOI":"10.1038\/s41564-018-0238-z","volume":"3","author":"D Quentin","year":"2018","unstructured":"Quentin D, Ahmad S, Shanthamoorthy P, Mougous JD, Whitney JC, Raunser S (2018) Mechanism of loading and translocation of type VI secretion system effector Tse6. Nat Microbiol 3: 1142\u20131152","journal-title":"Nat Microbiol"},{"key":"BFEMBR202356849_CR47","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1128\/jb.157.1.165-170.1984","volume":"157","author":"CA Roessner","year":"1984","unstructured":"Roessner CA, Ihler GM (1984) Proteinase sensitivity of bacteriophage lambda tail proteins gpJ and pH in complexes with the lambda receptor. J Bacteriol 157: 165\u2013170","journal-title":"J Bacteriol"},{"key":"BFEMBR202356849_CR48","doi-asserted-by":"crossref","first-page":"386","DOI":"10.1016\/S0021-9258(17)42484-7","volume":"261","author":"CA Roessner","year":"1986","unstructured":"Roessner CA, Ihler GM (1986) Formation of transmembrane channels in liposomes during injection of lambda DNA. J Biol Chem 261: 386\u2013390","journal-title":"J Biol Chem"},{"key":"BFEMBR202356849_CR49","doi-asserted-by":"crossref","first-page":"497","DOI":"10.1146\/annurev-micro-020518-115638","volume":"74","author":"ZC Ruhe","year":"2020","unstructured":"Ruhe ZC, Low DA, Hayes CS (2020) Polymorphic toxins and their immunity proteins: diversity, evolution, and mechanisms of delivery. Annu Rev Microbiol 74: 497\u2013520","journal-title":"Annu Rev Microbiol"},{"key":"BFEMBR202356849_CR50","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1038\/nrmicro3185","volume":"12","author":"AB Russell","year":"2014","unstructured":"Russell AB, Peterson SB, Mougous JD (2014) Type VI secretion system effectors: poisons with a purpose. Nat Rev Microbiol 12: 137\u2013148","journal-title":"Nat Rev Microbiol"},{"key":"BFEMBR202356849_CR51","doi-asserted-by":"crossref","first-page":"408","DOI":"10.1007\/s12602-017-9345-z","volume":"10","author":"KD Saint Jean","year":"2018","unstructured":"Saint Jean KD, Henderson KD, Chrom CL, Abiuso LE, Renn LM, Caputo GA (2018) Effects of hydrophobic amino acid substitutions on antimicrobial peptide behavior. Probiotics Antimicrob Proteins 10: 408\u2013419","journal-title":"Probiotics Antimicrob Proteins"},{"key":"BFEMBR202356849_CR54","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1016\/j.cell.2016.08.023","volume":"167","author":"A Vettiger","year":"2016","unstructured":"Vettiger A, Basler M (2016) Type VI secretion system substrates are transferred and reused among sister cells. Cell 167: 99\u2013110.e12","journal-title":"Cell"},{"key":"BFEMBR202356849_CR55","doi-asserted-by":"crossref","first-page":"621","DOI":"10.1146\/annurev-micro-020518-115420","volume":"73","author":"J Wang","year":"2019","unstructured":"Wang J, Brodmann M, Basler M (2019) Assembly and subcellular localization of bacterial type VI secretion systems. Annu Rev Microbiol 73: 621\u2013638","journal-title":"Annu Rev Microbiol"},{"key":"BFEMBR202356849_CR56","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0228941","volume":"15","author":"S Wettstadt","year":"2020","unstructured":"Wettstadt S, Filloux A (2020) Manipulating the type VI secretion system spike to shuttle passenger proteins. PLoS One 15: e0228941","journal-title":"PLoS One"},{"key":"BFEMBR202356849_CR57","doi-asserted-by":"crossref","first-page":"291","DOI":"10.3389\/fcimb.2020.00291","volume":"10","author":"S Wettstadt","year":"2020","unstructured":"Wettstadt S, Lai EM, Filloux A (2020) Solving the puzzle: connecting a heterologous Agrobacterium tumefaciens T6SS effector to a Pseudomonas aeruginosa spike complex. Front Cell Infect Microbiol 10: 291","journal-title":"Front Cell Infect Microbiol"},{"key":"BFEMBR202356849_CR58","doi-asserted-by":"crossref","first-page":"2841","DOI":"10.1128\/JB.01775-07","volume":"190","author":"HY Wu","year":"2008","unstructured":"Wu HY, Chung PC, Shih HW, Wen SR, Lai EM (2008) Secretome analysis uncovers an hcp\u2010family protein secreted via a type VI secretion system in Agrobacterium tumefaciens. J Bacteriol 190: 2841\u20132850","journal-title":"J Bacteriol"},{"key":"BFEMBR202356849_CR59","doi-asserted-by":"crossref","first-page":"961","DOI":"10.1094\/MPMI-01-19-0021-R","volume":"32","author":"CF Wu","year":"2019","unstructured":"Wu CF, Santos MNM, Cho ST, Chang HH, Tsai YM, Smith DA, Kuo CH, Chang JH, Lai EM (2019) Plant\u2010pathogenic Agrobacterium tumefaciens strains have diverse type VI effector\u2010immunity pairs and vary in in\u2010planta competitiveness. Mol Plant Microbe Interact 32: 961\u2013971","journal-title":"Mol Plant Microbe Interact"},{"key":"BFEMBR202356849_CR60","volume":"21","author":"CF Wu","year":"2020","unstructured":"Wu CF, Lien YW, Bondage D, Lin JS, Pilhofer M, Shih YL, Chang JH, Lai EM (2020) Effector loading onto the VgrG carrier activates type VI secretion system assembly. Embo Rep 21: e47961","journal-title":"Embo Rep"},{"key":"BFEMBR202356849_CR61","volume":"12","author":"CF Wu","year":"2021","unstructured":"Wu CF, Weisberg AJ, Davis EW 2nd, Chou L, Khan S, Lai EM, Kuo CH, Chang JH (2021) Diversification of the type VI secretion system in agrobacteria. mBio 12: e0192721","journal-title":"mBio"},{"key":"BFEMBR202356849_CR62","volume":"203","author":"M Yu","year":"2020","unstructured":"Yu M, Wang YC, Huang CJ, Ma LS, Lai EM (2020) Agrobacterium tumefaciens deploys a versatile antibacterial strategy to increase its competitiveness. J Bacteriol 203: e00490\u201020","journal-title":"J Bacteriol"},{"key":"BFEMBR202356849_CR63","doi-asserted-by":"crossref","DOI":"10.1186\/1745-6150-7-18","volume":"7","author":"D Zhang","year":"2012","unstructured":"Zhang D, de Souza RF, Anantharaman V, Iyer LM, Aravind L (2012) Polymorphic toxin systems: comprehensive characterization of trafficking modes, processing, mechanisms of action, immunity and ecology using comparative genomics. Biol Direct 7: 18","journal-title":"Biol Direct"},{"key":"BFEMBR202356849_CR64","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1038\/nature17182","volume":"531","author":"A Zoued","year":"2016","unstructured":"Zoued A, Durand E, Brunet YR, Spinelli S, Douzi B, Guzzo M, Flaugnatti N, Legrand P, Journet L, Fronzes R et\u00a0al (2016) Priming and polymerization of a bacterial contractile tail structure. Nature 531: 59\u201363","journal-title":"Nature"}],"container-title":["EMBO Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.15252\/embr.202356849.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.15252\/embr.202356849\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.embopress.org\/doi\/pdf\/10.15252\/embr.202356849","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.15252\/embr.202356849.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,5,18]],"date-time":"2026-05-18T14:13:02Z","timestamp":1779113582000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.15252\/embr.202356849"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,4,17]]},"references-count":60,"journal-issue":{"issue":"6","published-print":{"date-parts":[[2023,6,5]]}},"alternative-id":["BFEMBR202356849"],"URL":"https:\/\/doi.org\/10.15252\/embr.202356849","relation":{},"ISSN":["1469-221X","1469-3178"],"issn-type":[{"value":"1469-221X","type":"print"},{"value":"1469-3178","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,4,17]]},"assertion":[{"value":"18 January 2023","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"13 March 2023","order":2,"name":"revised","label":"Revised","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"22 March 2023","order":3,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"17 April 2023","order":4,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}}],"article-number":"EMBR202356849"}}