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-====== AvrBs3 ======
-Author: [[https://www.researchgate.net/profile/Nay_Dia2|Nay C. Dia]]\\
-Internal reviewer: Jens Boch\\
-Expert reviewer: FIXME
-Class: AvrBs3\\
-Family: Transcription Activator-Like (TAL) Effectors, TALEs (previously: AvrBs3/PthA)\\
-Prototype: AvrBs3 (//Xanthomonas euvesicatoria// pv. //euvesicatoria//, ex //Xanthomonas campestris// pv. //vesicatoria//; strain 71-21)\\
-RefSeq ID: [[https://www.ncbi.nlm.nih.gov/protein/P14727.2|P14727.2]] (1164 aa)\\
-D structure: [[https://www.rcsb.org/structure/2KQ5|2KQ5]] (Murakami //et al.//, 2010); [[https://www.rcsb.org/structure/3V6P|3V6P]], [[https://www.rcsb.org/structure/3V6T| 3V6T ]] (Deng //et al.//, 2012a); [[https://www.rcsb.org/structure/4GJP|4GJP]], [[https://www.rcsb.org/structure/4GJR|4GJR]] (Deng //et al.//, 2012b); [[https://www.rcsb.org/structure/4HPZ|4HPZ]] (Gao //et al.//, 2012) ; [[https://www.rcsb.org/structure/3UGM|3UGM]] (Mak //et al.//, 2012); [[https://www.rcsb.org/structure/4GG4|4GG4]] (Yin //et al.//, 2012); [[https://www.rcsb.org/structure/2YPF|2YPF ]] (Stella //et al//., 2013); [[https://www.rcsb.org/structure/4OSH|4OSH]], [[https://www.rcsb.org/structure/4OSI| 4OSI]], [[https://www.rcsb.org/structure/4OSJ| 4OSJ]], [[https://www.rcsb.org/structure/4OSK| 4OSK]], [[https://www.rcsb.org/structure/4OSL| 4OSL]], [[https://www.rcsb.org/structure/4OSM| 4OSM]], [[https://www.rcsb.org/structure/4OSQ|4OSQ]], [[https://www.rcsb.org/structure/4OSR|4OSR]], [[https://www.rcsb.org/structure/4OSS|4OSS]], [[https://www.rcsb.org/structure/4OST| 4OST]], [[https://www.rcsb.org/structure/4OSV| 4OSV]], [[https://www.rcsb.org/structure/4OSW| 4OSW]], [[https://www.rcsb.org/structure/4OSZ| 4OSZ]], [[https://www.rcsb.org/structure/4OT0| 4OT0]], [[https://www.rcsb.org/structure/4OT3| 4OT3]], [[https://www.rcsb.org/structure/4OTO|4OTO]] (Deng //et al.//, 2014); [[https://www.rcsb.org/structure/6JTQ|6JTQ]], [[https://www.rcsb.org/structure/6JVZ|6JVZ]], [[https://www.rcsb.org/structure/6JW0| 6JW0]], [[https://www.rcsb.org/structure/6JW1|6JW1]], [[https://www.rcsb.org/structure/6JW2|6JW2]], [[https://www.rcsb.org/structure/6JW3|6JW3]], [[https://www.rcsb.org/structure/6JW4|6JW4]], [[https://www.rcsb.org/structure/6JW5|6JW5]] (Liu & Yi, unpublished)
-===== Biological function =====
-=== How discovered? ===
-The gene //avrBs3 //was cloned in 1989 and was the first gene described of the TAL effector (TALE) family (Minsavage //et al//., 1990). Different resistant and susceptible cultivars of peppers were inoculated with //Xcv// strains 71-21 and 82-8 (Bonas //et al//., 1989). The pepper cultivar ECW-30R carries the resistance gene //Bs3 //and inoculation of these //Xcv// strains provoked a hypersensitive response (HR) (Bonas //et al//., 1989). This indicated that both //Xcv// strains contained //avrBs3//.
-=== (Experimental) evidence for being a T3E ===
-AvrBs3 is secreted and translocated into the plant via the Hrp type III secretion system (Bonas //et al//., 1991; Van den Ackerveken //et al//., 1996; Bonas //et al//., 1999). In contrast to wild-type bacteria, an //Xcv// mutant carrying a deletion in the conserved //hrp// gene //hrcV// did not secrete AvrBs3 indicating that AvrBs3 is transported by the Hrp system (Rossier //et al//., 1999). In its C-terminal domain, AvrBs3 carries an acidic activation domain which is functional in plant cells (Van den Ackerveken //et al//., 1996). Two nuclear localization signals in the C-terminal domain of AvrBs3 facilitate transport into the plant cell nucleus (Van den Ackerveken //et al//., 1996; Szurek //et al//., 2002). These eukaryotic features support the role of AvrBs3 and members of the TALE family within the eukaryotic host cell.
-=== Regulation ===
-Unlike most other type III effectors, expression of //avrBs3// is not dependend on the hrp regulon and the gene does not contain a PIP box in its promoter region. It is expressed constitutively in cells grown in minimal or complex medium and in planta (Knoop //et al//., 1991).
-=== Phenotypes ===
-AvrBs3, as well as other members of the TALE-family, function as specific transcription factors in plant cells. These proteins bind to specific sequences in promoters and induce expression of target genes. The DNA-binding specificity is encoded in the order of individual 34-amino acid repeats which each recognize one DNA base. Different TALEs typically contain different repeats and accordingly bind to different DNA sequences and target different host genes.
-Expression analysis using gene promoter fusion and western blot analysis demonstrated that //avrBs3// was expressed and resulted in a 122 kDa protein (1164 aa) which was detectable using a specific polyclonal antibody (Bonas //et al//., 1989). The AvrBs3 effector protein elicits two different types of responses in resistant or susceptible plants. Differential cDNA analysis from susceptible pepper plants infected with //Xcv// with or without AvrBs3 led to the discovery of //upa// (upregulated by AvrBs3) genes whose expression is induced by AvrBs3. These //upa// genes all share a conserved promoter element, known as the //UPA// box (Kay //et al.//, 2007). //upa20// act as a master regulator of cell enlargement causing the hypertrophy symptoms associated with AvrBs3. Silencing of //upa20// decreased cell hypertrophy in infected plants while the expression of //upa20// led to hypertrophy in uninfected plants (Kay //et al//., 2007). In resistant pepper plants, the promoter of //Bs3// contains a //UPA// box that is bound by AvrBs3 resulting in the transcription of the gene //Bs3//. //Bs3// encodes a protein that is homologous to flavine-dependent mono-oxygenases and its expression causes rapid cell death.
-The central region of the //avrBs3// gene consists of 17.5 nearly identical 102 bp repeats. Each repeat encodes 34 amino acids (Bonas //et al//., 1989). Repeat variable di-residues (RVDs) at positions 12 and 13 determine the specificity of each repeat (Boch //et al//., 2009; Moscou & Bogdanove, 2009). AvrBs3 binds its UPA box with the C-terminal activation domain directed towards the coding sequence of target genes.
-Gene //Bs3// was introduced into the ECW background to generate near-isogenic line resistant ECW-30R (Bonas //et al//., 1989; Bonas //et al//., 1991). ECW-30R was inoculated using different //Xcv// strains. //Xcv// lines 71-21 and 82-8 induces a hypersensitive response HR in ECW-30R, leading to programmed cell death and thus preventing the spread of the pathogen (Bonas //et al//., 1989; Bonas //et al//., 1991). Different //Xcv// strains were inoculated on susceptible (Early Cal Wonder; ECW) pepper plants. Hypertrophy (i.e. enlargement of mesophyll cells) was observed (Bonas //et al//., 1989; Bonas //et al//., 1991; Kay //et al//., 2007; Marois //et al//., 2002). It was also speculated that this hypertrophy facilitated bacterial colonization (Kay //et al//., 2007). //Agrobacterium// strains carrying a vector with //avrBs3// induced pustules 4-5 dpi in //Nicotiana// //clevelandii//, //N.// //benthamiana//, //N.// //tabacum//, and in potato (//Solanum// //tuberosum//), whereas //Agrobacterium// strains carrying an empty vector did not cause any changes in inoculated plants (Marois //et al//., 2002).
-=== Localization ===
-The //avrBs3// gene is localized on pXV11, a self-transmissible plasmid, and was initially isolated from //Xcv// strain 71-21 (Bonas //et al//., 1989). Using complementation of //Xcv// strain 85-10 (virulent on pepper ECW-30R), a 5-kb fragment including //avrBs3// was discovered (Bonas //et al//., 1989).
-=== Enzymatic function ===
-DNA-binding protein. Transcriptional activator.
-=== Interaction partners ===
-Importin alpha (Szurek //et al.//, 2001) interacts with the nuclear localization sequences of AvrBs3. The basal transcription factor IIA, gamma subunit from rice interacts with a region in the C-terminal domain of TALEs (Yuan //et al//., 2016) and similar interactions might be possible for AvrBs3, too. AvrBs3 and the TALE-family of effectors bind to DNA (Kay //et al//., 2007; Römer //et al//., 2007) with their N-terminal domain exhibiting general DNA-binding properties (Gao //et al.//, 2012) and the repeat region facilitating specific interaction to DNA bases (Boch //et al//., 2009; Moscou and Bogdanove, 2009).
-===== Conservation =====
-=== In xanthomonads ===
-Yes in many pathovars, but not necesssarily all strains within a pathovar.
-=== In other plant pathogens/symbionts ===
-Yes: Genes homologous to //avrBs3// of //Xanthomonas// were detected in some strains of //Ralstonia solanacearum// biovars 3, 4 and 5 (Heuer //et al//., 2007), in endofungal strains of //Burkholderia rhizoxinica // (Lacker //et al//., 2011), and in unknown marine organisms. All these related proteins can bind DNA (de Lange //et al//., 2013; de Lange //et al.//, 2014; de Lange //et al//., 2015).
-===== References =====
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-Bonas U, Stall, RE, Staskawicz B (1989). Genetic and structural characterization of the avirulence gene //avrBs3// from //Xanthomonas campestris// pv. //vesicatoria//. Mol. Gen. Genet. 218: 127-136. DOI: [[http://dx.doi.org/10.1007/BF00330575|10.1007/BF00330575]]
-Bonas U, Schulte R, Fenselau S, Minsavage GV, Staskawicz BJ, Stall RE (1991). Isolation of a gene cluster from //Xanthomonas// //campestris// pv. //vesicatoria// that determines pathogenicity and the hypersensitive response on pepper and tomato. Mol. Plant Microbe Interact 4: 81-88. DOI: [[http://dx.doi.org/10.1094/MPMI-4-081|10.1094/MPMI-4-081]]
-Bonas U, Van den Ackerveken G (1999). Gene-for-gene interactions: bacterial avirulence proteins specify plant disease resistance. Curr. Opin. Microbiol. 2: 94-98. DOI: [[https://doi.org/10.1016/S1369-5274(99)80016-2|10.1016/S1369-5274(99)80016-2]]
-de Lange O, Schreiber T, Schandry N, Radeck J, Braun KH, Koszinowski J, Heuer H, Strauß A, Lahaye T (2013). Breaking the DNA-binding code of //Ralstonia solanacearum// TAL effectors provides new possibilities to generate plant resistance genes against bacterial wilt disease. New Phytol. 199: 773-786. DOI: [[https://doi.org/10.1111/nph.12324|10.1111/nph.12324]]
-de Lange O, Wolf C, Dietze J, Elsaesser J, Morbitzer R, Lahaye T (2014). Programmable DNA-binding proteins from Burkholderia provide a fresh perspective on the TALE-like repeat domain. Nuc. Acids Res. 42: 7436-7449. DOI: [[https://doi.org/10.1093/nar/gku329.|10.1093/nar/gku329.]]
-de Lange O, Wolf C, Thiel P, Krüger J, Kleusch C, Kohlbacher O, Lahaye T (2015). DNA-binding proteins from marine bacteria expand the known sequence diversity of TALE-like repeats. Nuc. Acids Res. 43: 10065-10080. DOI: [[https://doi.org/10.1093/nar/gkv1053|10.1093/nar/gkv1053]]
-Deng D, Yan C, Pan X, Mahfouz M, Wang J, Zhu JK, Shi Y, Yan N (2012a). Structural basis for sequence-specific recognition of DNA by TAL effectors. Science 335: 720-723. DOI: [[https://doi.org/10.1126/science.1215670|10.1126/science.1215670]]
-Deng D, Yan C, Wu J, Pan X, Yan N (2014). Revisiting the TALE repeat. Protein Cell 5: 297-306. DOI: [[https://doi.org/10.1007/s13238-014-0035-2|10.1007/s13238-014-0035-2]]
-Deng D, Yin P, Yan C, Pan X, Gong X, Qi S, Xie T, Mahfouz M, Zhu JK, Yan N, Shi Y (2012b). Recognition of methylated DNA by TAL effectors. Cell Res. 22: 1502-1504. DOI: [[https://doi.org/10.1038/cr.2012.127|10.1038/cr.2012.127]]
-Gao H, Wu X, Chai J, Han Z (2012). Crystal structure of a TALE protein reveals an extended N-terminal DNA binding region. Cell Res. 22: 1716-1720. DOI: [[https://doi.org/10.1038/cr.2012.156|10.1038/cr.2012.156]]
-Herbers K, Conrads-Strauch J, Bonas U (1992). Race-specificity of plant resistance to bacterial spot disease determined by repetitive motifs in a bacterial avirulence protein. Nature 356: 172-174. DOI: [[https://doi.org/10.1038/356172a0|10.1038/356172a0]]
-Heuer H, Yin YN, Xue QY, Smalla K, Guo JH (2007). Repeat domain diversity of avrBs3-like genes in //Ralstonia// //solanacearum// strains and association with host preferences in the field. Appl. Environ. Microbiol. 73: 4379-4384. DOI: [[http://dx.doi.org/10.1128/AEM.00367-07|10.1128/AEM.00367-07]]
-Hopkins CM, White FF, Choi SH, Guo A, Leach JE (1992). Identification of a family of avirulence genes from //Xanthomonas// //oryzae// pv. //oryzae//. Mol. Plant Microbe Interact. 5: 451-459. DOI: [[https://doi.org/10.1094/mpmi-5-451|10.1094/mpmi-5-451]]
-Ji ZY, Xiong L, Zou LF, Li YR, Ma WX, Liu L, Zakria M, Ji GH, Chen GY (2014). AvrXa7-Xa7 mediated defense in rice can be suppressed by transcriptional activator-like effectors TAL6 and TAL11a from //Xanthomonas oryzae// pv. //oryzicola//. Mol. Plant Microbe Interact. 27: 983-995. DOI: [[https://doi.org/10.1094/MPMI-09-13-0279-R|10.1094/MPMI-09-13-0279-R]]. **Retraction in: Mol. Plant Microbe Interact. (2014) 27: 1413.** FIXME
-Kay S, Hahn S, Marois E, Hause G, Bonas U (2007). A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Science 318: 648-651. DOI: [[http://dx.doi.org/10.1126/science.1144956|10.1126/science.1144956]]
-Knoop V, Staskawicz B, Bonas U (1991). Expression of the avirulence gene //avrBs3// from //Xanthomonas// //campestris// pv. //vesicatoria// is not under the control of the //hrp// genes and is independent of plant factors. J. Bacteriol. 173: 7142-7150. DOI: [[http://dx.doi.org/10.1128/jb.173.22.7142-7150.1991|10.1128/jb.173.22.7142-7150.1991]]
-Lackner G, Moebius N, Partida-Martinez LP, Boland S, Hertweck C (2011). Evolution of an endofungal lifestyle: Deductions from the //Burkholderia rhizoxinica// genome. BMC Genomics 12: 210. DOI: [[https://doi.org/10.1186/1471-2164-12-210|10.1186/1471-2164-12-210]]
-Mak AN, Bradley P, Cernadas RA, Bogdanove AJ, Stoddard BL (2012). The crystal structure of TAL effector PthXo1 bound to its DNA target. Science 335: 716-719. DOI: [[https://doi.org/10.1126/science.1216211|10.1126/science.1216211]]
-Marois E, Van den Ackerveken G, Bonas U (2002). The //Xanthomonas// type III effector protein AvrBs3 modulates plant gene expression and induces cell hypertrophy in the susceptible host. Mol. Plant Microbe Interact. 15: 637-646. DOI: [[https://doi.org/10.1094/MPMI.2002.15.7.637|10.1094/MPMI.2002.15.7.637]]
-Minsavage GV, Dahlbeck D, Whalen MC, Kearney B, Bonas U, Staskawicz BJ, Stall, RE (1990). Gene-for-gene relationships specifying disease resistance in //Xanthomonas// //campestris// pv. //vesicatoria//-pepper interactions. Mol. Plant Microbe Interact. 3: 41-47. DOI: [[http://dx.doi.org/10.1094/MPMI-3-041|10.1094/MPMI-3-041]]
-Moscou MJ, Bogdanove AJ (2009). A simple cipher governs DNA recognition by TAL effectors. Science 326: 1501. DOI: [[http://dx.doi.org/10.1126/science.1178817|10.1126/science.1178817]]
-Murakami MT, Sforça ML, Neves JL, Paiva JH, Domingues MN, Pereira AL, Zeri AC, Benedetti CE (2010). The repeat domain of the type III effector protein PthA shows a TPR-like structure and undergoes conformational changes upon DNA interaction. Proteins 78: 3386-3395. DOI: [[https://doi.org/10.1002/prot.22846|10.1002/prot.22846]]
-Römer P, Hahn S, Jordan T, Strauss T, Bonas U, Lahaye T (2007). Plant pathogen recognition mediated by promoter activation of the pepper Bs3 resistance gene. Science 318: 645-648. DOI: [[https://doi.org/10.1126/science.1144958|10.1126/science.1144958]]
-Rossier O, Wengelnik K, Hahn K, Bonas U (1999). The //Xanthomonas// Hrp type III system secretes proteins from plant and mammalian bacterial pathogens. Proc. Natl. Acad. Sci. USA 96: 9368-9373. DOI: [[https://doi.org/10.1073/pnas.96.16.9368|10.1073/pnas.96.16.9368]]
-Scheibner F, Marillonnet S, Büttner D (2017). The TAL effector AvrBs3 from //Xanthomonas campestris// pv. //vesicatoria// contains multiple export signals and can enter plant cells in the absence of the type III secretion translocon. Front Microbiol. 8: 2180. DOI: [[https://doi.org/10.3389/fmicb.2017.02180|10.3389/fmicb.2017.02180]] FIXME  Information needs to be added to the profil!
-Stella S, Molina R, Yefimenko I, Prieto J, Silva G, Bertonati C, Juillerat A, Duchateau P, Montoya G (2013). Structure of the AvrBs3–DNA complex provides new insights into the initial thymine-recognition mechanism. Acta Cryst. 69: 1707-1716. DOI: [[http://dx.doi.org/10.1107/S0907444913016429|10.1107/S0907444913016429]]
-Szurek B, Marois E, Bonas U, Van den Ackerveken G (2001). Eukaryotic features of the //Xanthomonas// type III effector AvrBs3: protein domains involved in transcriptional activation and the interaction with nuclear import receptors from pepper. Plant J. 26: 523-534. DOI: [[https://10.1046/j.0960-7412.2001.01046.x|10.1046/j.0960-7412.2001.01046.x]]
-Szurek B, Rossier O, Hause G, Bonas U (2002). Type III-dependent translocation of the //Xanthomonas// AvrBs3 protein into the plant cell. Mol. Microbiol. 46: 13-23. DOI: [[https://doi.org/10.1046/j.1365-2958.2002.03139.x|10.1046/j.1365-2958.2002.03139.x]]
-Van den Ackerveken G, Marois E, Bonas U (1996). Recognition of the bacterial avirulence protein AvrBs3 occurs inside the host plant cell. Cell 87: 1307-1316. DOI: [[https://doi.org/10.1016/S0092-8674(00)81825-5|10.1016/S0092-8674(00)81825-5]]
-Yin P, Deng D, Yan C, Pan X, Xi JJ, Yan N, Shi Y (2012). Specific DNA-RNA hybrid recognition by TAL effectors. Cell Rep. 2: 707-713. DOI: 1[[https://doi.org/0.1016/j.celrep.2012.09.001|0.1016/j.celrep.2012.09.001]]
-===== Further reading =====
-Boch J, Bonas U (2010). //Xanthomonas// AvrBs3 family-type III effectors: discovery and function. Annu. Rev Phytopathol. 48: 419-436. DOI: [[https://doi.org/10.1146/annurev-phyto-080508-081936|10.1146/annurev-phyto-080508-081936]]
-Boch J, Bonas U, Lahaye T (2014). TAL effectors - pathogen strategies and plant resistance engineering. New Phytol. 204: 823-832. DOI: [[https://doi.org/10.1111/nph.13015|10.1111/nph.13015]]
-Bogdanove AJ, Schornack S, Lahaye T (2010). TAL effectors: finding plant genes for disease and defense. Curr. Opin. Plant Biol. 13: 394-401. DOI: [[https://doi.org/10.1016/j.pbi.2010.04.010|10.1016/j.pbi.2010.04.010]]
-Doyle EL, Stoddard BL, Voytas DF, Bogdanove AJ (2013). TAL effectors: highly adaptable phytobacterial virulence factors and readily engineered DNA-targeting proteins. Trends Cell Biol. 23: 390-398. DOI: [[https://doi.org/10.1016/j.tcb.2013.04.003|10.1016/j.tcb.2013.04.003]]
-Hutin M, Pérez-Quintero AL, Lopez C, Szurek B (2015). MorTAL Kombat: the story of defense against TAL effectors through loss-of-susceptibility. Front. Plant Sci. 6: 535. DOI: [[https://doi.org/10.3389/fpls.2015.00535|10.3389/fpls.2015.00535]]. Erratum in: Front Plant Sci. (2015) 6: 647.
-Scholze H, Boch J (2010). TAL effector-DNA specificity. Virulence 1: 428-432. DOI: [[https://doi.org/10.4161/viru.1.5.12863|10.4161/viru.1.5.12863]]
-Scholze H, Boch J (2011). TAL effectors are remote controls for gene activation. Curr. Opin. Microbiol. 14: 47-53. DOI: [[https://doi.org/10.1016/j.mib.2010.12.001|10.1016/j.mib.2010.12.001]]
-Yuan M, Ke Y, Huang R, Ma L, Yang Z, Chu Z, Xiao J, Li X, Wang S (2016). A host basal transcription factor is a key component for infection of rice by TALE-carrying bacteria. Elife 5: DOI: [[https://doi.org/10.7554/eLife.19605|10.7554/eLife.19605]]
-Zhang J, Yin Z, White F (2015). TAL effectors and the executor //R// genes. Front. Plant Sci. 6: 641. DOI: [[https://doi.org/10.3389/fpls.2015.00641|10.3389/fpls.2015.00641]]

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