====== Plant Resistance Genes in Pepper (//Capsicum annuum// L.) against //Xanthomonas// Infection ======
Author: [[https://www.researchgate.net/profile/Dorota_Tekielska|Dorota Tekielska]]\\
Internal reviewer: [[https://www.genetik.uni-hannover.de/boch.html|Jens Boch]]\\
Expert reviewer: **WANTED!**
===== Pathogen: //Xanthomonas euvesicatoria// =====
==== Resistance gene: //Bs1// ====
=== Synonyms ===
//NA//
=== Source ===
//Capsicum annuum// PI163192 (Cook & Guevara, 1984).
=== Status (identified, mapped, cloned, sequenced) ===
Identified. //Bs1// was backcrossed over 7 generations into the commercial pepper cultivar Early Calwonder (ECW) to produce a near-isogenic pepper cultigen (ECW10R) for identification of race 1 and race 2 pathogenic strains (Stall //et al//., 2009). The three resistance genes //Bs1//, //Bs2//, and //Bs3// were transferred to a single plant of ECW and designated ECW123.
=== Molecular markers ===
//NA//
=== Brief description ===
//Bs1// is a dominant resistance which results in a fast hypersensitive response reaction upon recognition of the type III effector AvrBs1 from //Xanthomonas euvesicatoria //pv. //euvesicatoria// (aka //Xanthomonas campestris //pv. //vesicatoria//). The resistance is rapidly overcome in the field by mutation of //avrBs1// in the bacteria making this resistance unsuitable for commercial breeding.
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==== Resistance gene: //Bs2// ====
=== Synonyms ===
//NA//
=== Source ===
//Capsicum chacoense// (Cook & Stall, 1963).
=== Status (identified, mapped, cloned, sequenced) ===
//Bs2// was the first cloned resistance gene in pepper (Tai //et al.//, 1999). //Bs2// was backcrossed over 7 generations into the commercial pepper cultivar Early Calwonder (ECW) to produce a near-isogenic pepper cultigen (ECW20R) (Stall //et al//., 2009). The three resistance genes //Bs1//, //Bs2//, and //Bs3// were transferred to a single plant of ECW and designated ECW123.
=== Molecular markers ===
Markers for breeding of //Bs2// in pepper have been established (Truong //et al//., 2011). An overview of markers for different disease resistances in pepper has been published (Barka & Lee, 2020).
=== Brief description ===
The dominant //Bs2// resistance gene encodes an NB-LRR protein which interacts with the AvrBs2 protein from //Xanthomonas euvesicatoria //pv. //euvesicatoria// (aka //Xanthomonas campestris //pv. //vesicatoria//)and causes a hypersensitive response (Tai //et al//., 1999). Expression of //Bs2// in other solanaceous plants, but not nonsolanaceous plants, also triggers hypersensitive response to AvrBs2. //Bs2// was broadly used in resistance breeding and in 2000 nearly 100% commercial bell peppers contained the //Bs2// resistance. Because pathogen strains with mutations in //avrBs2// emerged, //Bs2// was only effective for commercial control of bacterial spot disease for 5-6 years.
Transgenic tomato (//Solanum lycopersicum//) lines expressing the //Bs2// resistance gene from pepper, a close relative of tomato, demonstrated improved resistance to bacterial spot disease caused by //Xanthomonas// species in replicated multi-year field trials under commercial type growing conditions (Horvath //et al.//, 2012). The presence of the pepper //Bs2// gene in a highly susceptible tomato background reduced disease to extremely low levels (Horvath //et al.//, 2012).
----
==== Resistance gene: //Bs3// ====
=== Synonyms ===
//NA//
=== Source ===
//Capsicum annuum// PI271322 (Kim & Hartmann, 1985).
=== Status (identified, mapped, cloned, sequenced) ===
Cloned and sequenced (Roemer //et al//., 2007). A near-isogenic line containing the //Bs3// (ECW30R) (Stall //et al//., 2009). The three resistance genes //Bs1//, //Bs2//, and //Bs3// were transferred to a single plant of ECW and designated ECW123.
=== Molecular markers ===
//NA//
=== Brief description ===
//Bs3// is a dominant resistance gene and not expressed during normal life of the plant. The TAL effector AvrBs3 from //Xanthomonas euvesicatoria //pv. //euvesicatoria// (aka //Xanthomonas campestris //pv. //vesicatoria//) binds to the promoter of //Bs3// and causes expression which results in programmed cell death (Römer //et al//., 2007). //Bs3// encodes an unusual flavin monooxygenase, but it is unknown whether the Bs3 protein has any enzymatic activity. The //bs3// variant has a deletion in the promoter which prohibits binding of AvrBs3 (Römer //et al//., 2007). Instead, //bs3// is triggered by binding of a variant of AvrBs3 with deletions of several repeats that cause it to recognize the modified sequence in the promoter of //bs3 // (Römer //et al//., 2007). The TALE AvrHah1 from //Xanthomonas gardneri// also elicits the //Bs3// resistance. Commercial pepper lines containing //Bs2// and //Bs3// were used.
----
==== Resistance gene: //Bs4// ====
=== Synonyms ===
//NA//
=== Source ===
//Capsicum pubescens// PI235047 (Stall //et al//., 2009).
=== Status (identified, mapped, cloned, sequenced) ===
Identified in pepper, cloned from tomato (//Bs4//: Schornack //et al//., 2004) and pepper (//Bs4C//; Strauß //et al.//, 2012).
=== Molecular markers ===
//NA//
=== Brief description ===
//Bs4// is a dominant resistance gene. It has not been introgressed into pepper, because //C. annuum// can not be crossed with //C. pubescens. //Transcriptome profiling (RNA-seq) was used to identify a candidate for //Bs4C//, an //R// gene from pepper that mediates recognition of the //Xanthomonas// TAL effector (TALE) AvrBs4 (Strauß //et al.//, 2012). The candidate //Bs4C// gene was found to have an AvrBs4 binding site in its promoter that directs its transcriptional activation. Comparison of //Bs4C// with a nonfunctional allele that is unable to recognize AvrBs4 revealed a 2-bp polymorphism within the TALE binding site of the //Bs4C// promoter (Strauß //et al.//, 2012). Bs4C encodes a structurally unique R protein and Bs4C-like genes that are present in many solanaceous genomes seem to be as tightly regulated as pepper Bs4C (Strauß //et al.//, 2012).
----
==== Resistance gene: //bs5// ====
=== Synonyms ===
//NA//
=== Source ===
//Capsicum annuum// ECW12346 (Jones //et al//., 2002; Vallejos //et al//., 2010).
=== Status (identified, mapped, cloned, sequenced) ===
Identified. //bs5// has been transferred to the pepper cultivar ECW, backcrossed, and designated ECW50R. //bs5// was delimited to a ~535-kb interval on chromosome 3 and 14 candidate resistance genes for //bs5// were identified based on predicted protein coding polymorphisms between ECW and the corresponding resistant parent (Sharma //et al.//, 2023). Cloned and sequenced (Szabo //et al.//, 2023).
=== Molecular markers ===
AFLP and CAPS markers are available (Vallejos //et al//., 2010; Sharma //et al.//, 2023; Szabo //et al.//, 2023).
=== Brief description ===
//bs5// is a recessive resistance which has been mapped, cloned and sequenced. It is a stronger resistance than the other recessive resistance, //bs6//, but both resistances together have an additive effect (Vallejos //et al//., 2010). The protein encoded by the //bs5// resistance allele is shorter by 2-aa as compared to the wild type Bs5 protein (Szabo //et al.//, 2023). The 2-aa deletion occurred in the cysteine-rich transmembrane domain of the tail-anchored protein, Ca_CYSTM1, and found to be responsible for the resistance phenotype. Yet, both protein variants (bs5 and Bs5) were shown to be located in the cell membrane (Szabo //et al.//, 2023). Since type 3 effector entry was shown to be hampered in //bs5// plants compared with the susceptible pepper lines, it was hypothesized that //bs5// plants are resistant against //X. euvesicatoria// due to the lack of entry of bacterial effectors into the host cell (Szabo //et al.//, 2023). Transcriptome profiling suggest a robust defense mechanism in //bs5//-mediated resistance, primarily mediated through PAMP-triggered immunity (Subedi //et al.//, 2024)
----
==== Resistance gene: //bs6// ====
=== Synonyms ===
//NA//
=== Source ===
//Capsicum annuum// ECW12346 (Jones //et al//., 2002; Vallejos //et al//., 2010).
=== Status (identified, mapped, cloned, sequenced) ===
Identified. //bs6// has been transferred to the pepper cultivar ECW, backcrossed, and designated ECW60R. //bs6// was delimited to a ~666-kb interval on chromosome 6 and 8 candidate resistance genes for //bs6// were identified based on predicted protein coding polymorphisms between ECW and the corresponding resistant parent (Sharma //et al.//, 2023).
=== Molecular markers ===
CAPS markers are available (Sharma //et al.//, 2023).
=== Brief description ===
//bs6// is a recessive resistance which has been mapped. It is a weaker resistance than the other recessive resistance, //bs5//, but both resistances together have an additive effect (Vallejos //et al//., 2010).
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==== Resistance gene: //BsT// ====
=== Synonyms ===
//NA//
=== Source ===
//Capsicum pubescens// PI235047A.
=== Status (identified, mapped, cloned, sequenced) ===
Identified.
=== Molecular markers ===
//NA//
=== Brief description ===
The dominant //BsT// resistance gene from //C. pubescens// causes a hypersensitive response upon recognition of the type III effector AvrBsT from //Xanthomonas euvesicatoria //pv. //euvesicatoria// (aka //Xanthomonas campestris //pv. //vesicatoria//)//.// Expression of //avrBsT// in //C. annuum// using //Agrobacterium// causes an HR and infection of papper with //Xcv// strains containing //avrBsT// on a high-copy plasmid causes a spotty hypersensitive reaction (Escolar //et al//., 2001) indicating that //BsT// is also present in //C. annuum//.
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===== Pathogen: //Xanthomonas hortorum// pv. //gardneri// =====
==== Resistance gene: //Bs7// ====
=== Synonyms ===
//NA//
=== Source ===
//Capsicum baccatum// var. //pendulum// (Potnis //et al//., 2012).
=== Status (identified, mapped, cloned, sequenced) ===
Identified.
=== Molecular markers ===
//NA//
=== Brief description ===
//Bs7// is a dominant resistance gene.
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==== Resistance gene: //bs8// ====
=== Synonyms ===
//NA//
=== Source ===
//Capsicum annuum// accession PI 163192 (Sharma //et al//., 2022).
=== Status (identified, mapped, cloned, sequenced) ===
Mapped to a 2.3 Mb interval on the sub-telomeric region of chromosome 11 (Sharma //et al//., 2022). //bs8// has been transferred to the pepper cultivar ECW, backcrossed, and designated ECW80R.
=== Molecular markers ===
Markers from mapping population (Sharma //et al//., 2022)
=== Brief description ===
//bs8// is a recessive resistance which has been mapped. This resistance in ECW80R was determined to be quantitative, recessively inherited, and non-HR causing, and inhibits lesion expansion and chlorosis. Presence of the resistance in NILs decreased the //in planta// bacterial population by 9-fold compared to ECW (Sharma //et al//., 2022).
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===== References =====
Barka GD, Lee J (2020). Molecular marker development and gene cloning for diverse disease resistance in pepper (//Capsicum annuum// L.): current status and prospects. Plant Breed. Biotech. 8: 89-113. DOI: [[https://doi.org/10.9787/PBB.2020.8.2.89|10.9787/PBB.2020.8.2.89]]
Cook AA, Stall RE (1963). Inheritance of resistance in pepper to bacterial spot. Phytopathology 53: 1060-1062.
Escolar L, van den Ackerveken G, Pieplow S, Rossier O, Bonas U (2001). Type III secretion and in planta recognition of the //Xanthomonas// avirulence proteins AvrBs1 and AvrBsT. Mol. Plant Pathol. 2: 287-296. DOI: [[https://doi.org/10.1046/j.1464-6722.2001.00077.x|10.1046/j.1464-6722.2001.00077.x]]
Horvath DM, Stall RE, Jones JB, Pauly MH, Vallad GE, Dahlbeck D, Staskawicz BJ, Scott JW (2012). Transgenic resistance confers effective field level control of bacterial spot disease in tomato. PLoS One 7: e42036. doi: [[https://doi.org/10.1371/journal.pone.0042036|10.1371/journal.pone.0042036]]
Jones JB, Minsavage GV, Roberts PD, Johnson RR, Kousik CS, Subramanian S, Stall RE (2002). A non-hypersensitive resistance in pepper to the bacterial spot pathogen is associated with two recessive genes. Phytopathology 92: 273-277. DOI: [[https://doi.org/10.1094/PHYTO.2002.92.3.273|10.1094/PHYTO.2002.92.3.273]]
Kim BS, Hartmann RW (1985). Inheritance of a gene (//Bs3//) conferring hypersensitive resistance to //Xanthomonas campestris// pv. //vesicatoria// in pepper (//Capsicum annuum//). Plant Dis. 69: 233-235.
Potnis N, Minsavage G, Smith JK, Hurlbert JC, Norman D, Rodrigues R, Stall RE, Jones JB (2012). Avirulence proteins AvrBs7 from //Xanthomonas gardneri// and AvrBs1. 1 from //Xanthomonas euvesicatoria// contribute to a novel gene-for-gene interaction in pepper. Mol. Plant Microbe Interact. 25: 307-320. DOI: [[https://doi.org/10.1094/MPMI-08-11-0205|10.1094/MPMI-08-11-0205]]
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]]
Sharma A, Minsavage GV, Gill U, Hutton S, Jones JB (2022). Identification and mapping of //bs8//, a novel locus conferring resistance to bacterial spot caused by //Xanthomonas gardneri//. Phytopathology 112: 1640-1650. DOI: [[https://doi.org/10.1094/PHYTO-08-21-0339-R|10.1094/PHYTO-08-21-0339-R]]
Stall RE, Jones JB, Minsavage GV (2009). Durability of resistance in tomato and pepper to xanthomonads causing bacterial spot. Ann. Rev. Phytopathol. 47: 265-284. DOI: [[https://doi.org/10.1146/annurev-phyto-080508-081752|10.1146/annurev-phyto-080508-081752]]
Strauß T, van Poecke RM, Strauss A, Römer P, Minsavage GV, Singh S, Wolf C, Strauss A, Kim S, Lee HA, Yeom SI, Parniske M, Stall RE, Jones JB, Choi D, Prins M, Lahaye T (2012). RNA-seq pinpoints a //Xanthomonas// TAL-effector activated resistance gene in a large-crop genome. Proc. Natl. Acad. Sci. U. S. A. 109: 19480-19485. DOI: [[https://doi.org/10.1073/pnas.1212415109|10.1073/pnas.1212415109]]
Subedi A, Minsavage GV, Roberts PD, Goss EM, Sharma A, Jones JB (2024). Insights into //bs5// resistance mechanisms in pepper against //Xanthomonas euvesicatoria// through transcriptome profiling. BMC Genomics 25: 711. DOI: [[https://doi.org/10.1186/s12864-024-10604-8|10.1186/s12864-024-10604-8]]
Szabó Z, Balogh M, Domonkos Á, Csányi M, Kaló P, Kiss GB (2023). The //bs5// allele of the susceptibility gene //Bs5// of pepper (//Capsicum annuum// L.) encoding a natural deletion variant of a CYSTM protein conditions resistance to bacterial spot disease caused by //Xanthomonas// species. Theor. Appl. Genet. 136: 64. DOI: [[https://doi.org/10.1007/s00122-023-04340-y|10.1007/s00122-023-04340-y]]. Correction in Theor. Appl. Genet. 136: 124. DOI: [[https://doi.org/10.1007/s00122-023-04366-2|10.1007/s00122-023-04366-2]]
Tai TH, Dahlbeck D, Clark ET, Gajiwala P, Pasion R, Whalen MC, Stall RE, Staskawicz BJ (1999). Expression of the //Bs2// pepper gene confers resistance to bacterial spot disease in tomato. Proc. Natl. Acad. Sci. USA 96: 14153-14158. DOI: [[https://doi.org/10.1073/pnas.96.24.14153|10.1073/pnas.96.24.14153]]
Truong HTH, Kim KT, Kim S, Cho MC, Kim HR, Woo JG (2011). Development of gene-based markers for the //Bs2// bacterial spot resistance gene for marker-assisted selection in pepper (//Capsicum// spp.). Hort. Environ. Biotechnol. 52: 65-73. DOI: [[https://doi.org/10.1007/s13580-011-0142-4|10.1007/s13580-011-0142-4]]
Vallejos CE, Jones V, Stall RE, Jones JB, Minsavage GV, Schultz DC, Rodrigues R, Olsen LE, Mazourek M (2010). Characterization of two recessive genes controlling resistance to all races of bacterial spot in peppers. Theor. Appl. Genet. 121: 37-46. DOI: [[https://doi.org/10.1007/s00122-010-1289-6|10.1007/s00122-010-1289-6]]
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===== Further reading =====
Bento CS, de Souza AG, Sudré CP, Pimenta S, Rodrigues R (2017). Multiple genetic resistances in //Capsicum// spp. Genet. Mol. Res. 16: gmr16039789. DOI: [[https://doi.org/10.4238/gmr16039789|10.4238/gmr16039789]]
Choi HW, Hwang BK (2015). Molecular and cellular control of cell death and defense signaling in pepper. Planta 241: 1-27. DOI: [[https://doi.org/10.1007/s00425-014-2171-6|10.1007/s00425-014-2171-6]]
Dugassa Barka G, Lee J (2020). Molecular marker development and gene cloning for diverse disease resistance in pepper (//Capsicum annuum// L.): current status and prospects. Plant Breed. Biotech. 8: 89-113. DOI: [[https://doi.org/10.9787/PBB.2020.8.2.89|10.9787/PBB.2020.8.2.89]]
Hibberd AM, Gillespie D (1982). Heritability of field resistance to bacterial leaf spot disease in pepper (//Capsicum annuum// L.). Scientia Hortic. 17: 301-309. DOI: [[https://doi.org/10.1016/0304-4238(82)90110-8|10.1016/0304-4238(82)90110-8]]
Hong JK, Hwang IS, Hwang BK (2017). Functional roles of the pepper leucine-rich repeat protein and its interactions with pathogenesis-related and hypersensitive-induced proteins in plant cell death and immunity. Planta 246: 351-364. DOI: [[https://doi.org/10.1007/s00425-017-2709-5|10.1007/s00425-017-2709-5]]
Kim DS, Choi HW, Hwang BK (2014). Pepper mildew resistance locus O interacts with pepper calmodulin and suppresses //Xanthomonas// AvrBsT-triggered cell death and defense responses. Planta 240: 827-539. DOI: [[https://doi.org/10.1007/s00425-014-2134-y|10.1007/s00425-014-2134-y]]
Leister RT, Dahlbeck D, Day B, Li Y, Chesnokova O, Staskawicz BJ (2005). Molecular genetic evidence for the role of SGT1 in the intramolecular complementation of Bs2 protein activity in //Nicotiana benthamiana//. Plant Cell 17: 1268-1278. DOI: [[https://doi.org/10.1105/tpc.104.029637|10.1105/tpc.104.029637]]
Park CJ, Shin R, Park JM, Lee GJ, You JS, Paek KH (2002). Induction of pepper cDNA encoding a lipid transfer protein during the resistance response to tobacco mosaic virus. Plant Mol. Biol. 48: 243-254. DOI: [[https://doi.org/10.1023/a:1013383329361|10.1023/a:1013383329361]]
Riva EM, Rodrigues R, Pereira MG, Sudré CP, Karasawa M (2004). Inheritance of bacterial spot disease in //Capsicum annuum// L. Crop Breed. Appl. Biotechnol. 4: 490-494. DOI: [[https://doi.org/10.12702/1984-7033.v04n04a18|10.12702/1984-7033.v04n04a18]]
Riva-Souza EM, Rodrigues R, Sudré CP, Pereira MG, Bento CS, de Pina Matta F (2009). Genetic parameters and selection for resistance to bacterial spot in recombinant F6 lines of //Capsicum annuum//. Crop Breed. Appl. Biotechnol. 9: 108-115. PDF: [[http://www.sbmp.org.br/cbab/siscbab/uploads/c8129491-83fe-7669.pdf|www.sbmp.org.br/cbab/siscbab/uploads/c8129491-83fe-7669.pdf]]
Riva-Souza EM, Rodrigues R, Sudré CP, Pereira MG, Viana AP, do Amaral jr. AT (2007). Obtaining pepper F2:3 lines with resistance to the bacterial spot using the pedigree method. Horticultura Brasileira 25: 567-571. PDF: [[https://www.scielo.br/pdf/hb/v25n4/a14v25n4.pdf|www.scielo.br/pdf/hb/v25n4/a14v25n4.pdf]]
Romero AM, Kousik CS, Ritchie DF (2002). Temperature sensitivity of the hypersensitive response of bell pepper to //Xanthomonas axonopodis// pv. //vesicatoria//. Phytopathology 92: 197-203. DOI: [[https://doi.org/10.1094/PHYTO.2002.92.2.197|10.1094/PHYTO.2002.92.2.197]]
Sharma A, Li J, Wente R, Minsavage GV, Gill US, Ortega A, Vallejos CE, Hart JP, Staskawicz BJ, Mazourek MR, Stall RE, Jones JB, Hutton SF (2023). Mapping of the //bs5 //and //bs6// non-race-specific recessive resistances against bacterial spot of pepper. Front. Plant Sci. 14: 1061803. DOI: [[https://doi.org/10.3389/fpls.2023.1061803|10.3389/fpls.2023.1061803]]
Silva LRA, Rodrigues R, Pimenta S, Correa JWS, Araújo MSB, Bento CS, Sudré CP (2017). Inheritance of bacterial spot resistance in //Capsicum annuum// var. //annuum//. Genet. Mol. Res. 16: gmr16029631. DOI: [[https://doi.org/10.4238/gmr16029631|10.4238/gmr16029631]]
Stall RE, Jones JB, Minsavage GV (2009). Durability of resistance in tomato and pepper to xanthomonads causing bacterial spot. Ann. Rev. Phytopathol. 47: 265-284. DOI: [[https://doi.org/10.1146/annurev-phyto-080508-081752|10.1146/annurev-phyto-080508-081752]]
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===== Acknowledgements =====
This fact sheet is based upon work from COST Action CA16107 EuroXanth, supported by COST (European Cooperation in Science and Technology).