Author: Dorota Tekielska
Internal reviewer: Jens Boch
Expert reviewer: WANTED!

NA

Capsicum annuum PI163192 (Cook & Guevara, 1984).

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.

NA

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.

NA

Capsicum chacoense (Cook & Stall, 1963).

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.

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).

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).

NA

Capsicum annuum PI271322 (Kim & Hartmann, 1985).

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.

NA

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.

NA

Capsicum pubescens PI235047 (Stall et al., 2009).

Identified in pepper, cloned from tomato (Bs4: Schornack et al., 2004) and pepper (Bs4C; Strauß et al., 2012).

NA

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).

NA

Capsicum annuum ECW12346 (Jones et al., 2002; Vallejos et al., 2010).

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).

AFLP and CAPS markers are available (Vallejos et al., 2010; Sharma et al., 2023; Szabo et al., 2023).

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).

NA

Capsicum annuum ECW12346 (Jones et al., 2002; Vallejos et al., 2010).

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).

CAPS markers are available (Sharma et al., 2023).

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).

NA

Capsicum pubescens PI235047A.

Identified.

NA

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.

NA

Capsicum baccatum var. pendulum (Potnis et al., 2012).

Identified.

NA

Bs7 is a dominant resistance gene.

NA

Capsicum annuum accession PI 163192 (Sharma et al., 2022).

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.

Markers from mapping population (Sharma et al., 2022)

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).

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: 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: 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: 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: 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: 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: 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: 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: 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: 10.1073/pnas.1212415109

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: 10.1007/s00122-023-04340-y. Correction in Theor. Appl. Genet. 136: 124. doi: 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: 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: 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: 10.1007/s00122-010-1289-6

Bento CS, de Souza AG, Sudré CP, Pimenta S, Rodrigues R (2017). Multiple genetic resistances in Capsicum spp. Genet. Mol. Res. 16: gmr16039789. DOI: 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: 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: 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: 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: 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: 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: 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: 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: 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: 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 F_2:3 lines with resistance to the bacterial spot using the pedigree method. Horticultura Brasileira 25: 567-571. 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: 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: 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: 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: 10.1146/annurev-phyto-080508-081752