Skip to main content
SpringerLink
Log in

The Co-4 locus on chromosome Pv08 contains a unique cluster of 18 COK-4 genes and is regulated by immune response in common bean

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Key message

The common bean locus Co - 4, traditionally referred to as an anthracnose-resistant gene, contains a cluster of predicted receptor-like kinases (COK-4 and CrRLK1-like), and at least two of these kinases are co-regulated with the plant’s basal immunity.

Abstract

Genetic resistance to anthracnose, caused by the fungus Colletotrichum lindemuthianum (Sacc. and Magnus) Briosi and Cavara, is conferred by major loci throughout the Phaseolus vulgaris genome, named Co. The complex Co-4 locus was previously reported to have several copies of the COK-4 gene that is predicted to code for a receptor-like kinase (RLK). In general, plant RLKs are involved in pathogen perception and signal transduction; however, the molecular function of COK-4 remains elusive. Using newly identified molecular markers (PvTA25 and PvSNPCOK-4), the SAS13 marker, COK-4 sequences and phylogeny, and the recently released bean genome sequence, we determined the most probable boundaries of the Co-4 locus: a 325-Kbp region on chromosome Pv08. Out of the 49 predicted transcripts in that region, 24 encode for putative RLKs (including 18 COK-4 copies) with high similarity to members of the Catharanthus roseus RLK1-like (CrRLK1L) protein family from different plant species, including the well-described FERONIA (FER) and ANXUR. We also determined that two RLK-coding genes in the Co-4 locus (COK-4-3 and FER-like) are transcriptionally regulated when bean plants are challenged with the flg22 peptide, a commonly used elicitor of plant immunity, or the bacterium Pseudomonas syringae pv. phaseolicola, the causal agent of halo blight. While COK-4-3 is activated during immune response, FER-like is downregulated suggesting that these genes could play a role in plant responses to biotic stress. These results highlight the importance of dissecting the regulation and molecular function of individual genes within each locus, traditionally referred to as resistance gene based on genetic segregation analysis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Awale HE, Kelly JD (2001) Development of SCAR markers linked to Co-4 2 gene in common bean. Annu Rep Bean Improv Coop 44:119–120

    Google Scholar 

  • Balardin RS, Kelly JD (1998) Interaction between races of Colletotrichum lindemuthianum and gene pool diversity in Phaseolus vulgaris. J Am Soc Hortic Sci 123:1038–1047

    Google Scholar 

  • Björklund ÅK, Ekman D, Light S, Frey-Skött J, Elofsson A (2005) Domain rearrangements in protein evolution. J Mol Biol 353(4):911–923. doi:10.1016/j.jmb.2005.08.067

    Article  PubMed  Google Scholar 

  • Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60:379–406. doi:10.1146/annurev.arplant.57.032905.105346

    Article  CAS  PubMed  Google Scholar 

  • Borges A, Tsai SM, Caldas DGG (2011) Validation of reference genes for RT-qPCR normalization in common bean during biotic and abiotic stresses. Plant Cell Rep 5:827–838. doi:10.1007/s00299-011-1204-x

    Google Scholar 

  • Boycheva S, Daviet L, Wolfender JL, Fitzpatrick TB (2014) The rise of operon-like gene clusters in plants. Trends in Plant Sci 7:447–459. doi:10.1016/j.tplants.2014.01.013

    Article  Google Scholar 

  • Broughton WJ, Hernandez G, Blair M, Beebe S, Gepts P, Vanderleyden J (2003) Beans (Phaseolus spp.)—model food legumes. Plant Soil 252:55–128. doi:10.1023/A:1024146710611

    Article  CAS  Google Scholar 

  • Chinchilla D, Bauer Z, Regenass M, Boller T, Felix G (2006) The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell 18:465–476. doi:10.1105/tpc.105

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nurnberger T, Jones JDG, Felix G, Boller T (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448:497-U412. doi:10.1038/nature05999

    Article  Google Scholar 

  • Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 11(8):539–548. doi:10.1038/nrg2812

    Article  CAS  PubMed  Google Scholar 

  • Ferreira JJ, Campa A, Kelly JD (2013) Organization of genes conferring resistance to anthracnose in common bean. In: Varshney RK, Tuberosa R (eds) Translational genomics for crop breeding, 1st edn. Wiley, Blackwell, pp 151–182

    Chapter  Google Scholar 

  • Fouilloux G (1979) New races of bean anthracnose and consequences on our breeding programs. In: Maraitre H, Meyer JA (eds) Disease of tropical food crops. Université Catholique de Louvain la Neuve, Belgium, pp 221–235

    Google Scholar 

  • Hazen SP, Leroy P, Ward R (2002) AFLP in Triticumaestivum L.: patterns of genetic diversity and genome distribution. Euphytica 125:89–102. doi:10.1023/A:1015760802026

    Article  CAS  Google Scholar 

  • Hou S, Mu R, Ma G, Xu X, Zhang C, Yang Y, Wu D (2011) Pseudomonas syringae pv. phaseolicola effector HopF1 inhibits pathogen-associated molecular pattern-triggered immunity in a RIN4-independent manner in common bean (Phaseolus vulgaris). FEMS Microbiol Lett 323(1):35–43. doi:10.1111/j.1574-6968.2011.02356.x

    Article  CAS  PubMed  Google Scholar 

  • Huang F, Xu G, Chi Y, Liu H, Xue Q, Zhao T, Gai J, Yu D (2014) A soybean MADS-box protein modulates floral organ numbers, petal identity and sterility. BMC Plant Biol 14(1):89. doi:10.1186/1471-2229-14-89

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jones JDG, Dangl JL (2006) The plant immune system. Nature 444(7117):323–329. doi:10.1038/nature05286

    Article  CAS  PubMed  Google Scholar 

  • Katagiri F, Thilmony R, He SY (2002) The Arabidopsis thaliana-Pseudomonas syringae interaction. In: Somerville CR, Meyerowitz EM (eds) The Arabidopsis book. American Society of Plant Biologists, Rockville, pp 1–35. doi:10.1199/tab.0039

    Google Scholar 

  • Keinath NF, Kierszniowska S, Lorek J, Bourdais G, Kessler SA, Shimosato-Asano H, Panstruga R (2010) PAMP (pathogen-associated molecular pattern)-induced changes in plasma membrane compartmentalization reveal novel components of plant immunity. J Biol Chem 285(50):39140–39149. doi:10.1074/jbc.M110.160531

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kelly JD, Vallejo VA (2004) A comprehensive review of the major genes conditioning resistance to anthracnose in common bean. Hortic Sci 39(6):1196–1207

    CAS  Google Scholar 

  • Kessler SA, Shimosato-Asano H, Keinath NF, Wuest SE, Ingram G, Panstruga R, Grossniklaus U (2010) Conserved molecular components for pollen tube reception and fungal invasion. Science 330(6006):968–971. doi:10.1126/science.1195211

    Article  CAS  PubMed  Google Scholar 

  • Kuć J (1982) Induced immunity to plant disease. Bioscience 32(11):854–860. doi:10.2307/1309008

    Article  Google Scholar 

  • Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181. doi:10.1016/0888-7543(87)90010-3

    Article  CAS  PubMed  Google Scholar 

  • Lindner H, Müller LM, Boisson-Dernier A, Grossniklaus U (2012) CrRLK1L receptor-like kinases: not just another brick in the wall. Curr Opin Plant Biol 15(6):659–669. doi:10.1016/j.pbi.2012.07.003

    Article  CAS  PubMed  Google Scholar 

  • Liu BH (1998) Statistical genomics: linkage, mapping and QTL analysis. CRC Press, Cleveland 611

    Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−∆∆CT method. Methods 25(4):402–408. doi:10.1006/meth.2001.1262

    Article  CAS  PubMed  Google Scholar 

  • Long M, VanKuren NW, Chen S, Vibranovski MD (2013) New gene evolution: little did we know. Annu Rev Genet 47:307–333. doi:10.1146/annurev-genet-111212-133301

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lopez-Gomez M, Sandal N, Stougaard J, Boller T (2011) Interplay of flg22-induced defence responses and nodulation in Lotus japonicus. J Exp Bot. doi:10.1093/jxb/err1291

    PubMed Central  PubMed  Google Scholar 

  • Marchler-Bauer A, Zheng C, Chitsaz F, Derbyshire MK, Geer LY, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Lanczycki CJ, Lu F, Shennan Lu, Marchler GH, Song JS, Thanki N, Yamashita RA, Zhang D, Bryant SH (2013) CDD: conserved domains and protein three-dimensional structure. Nucleic Acids Res 41(D1):D384-52. doi:10.1093/nar/gks1243

    Article  Google Scholar 

  • Melotto M, Kelly JD (2001) Fine mapping of the Co-4 locus of common bean reveals a resistance gene candidate, COK-4, that encodes for a protein kinase. Theor Appl Genet 103(4):508–517. doi:10.1007/s001220100609

    Article  CAS  Google Scholar 

  • Melotto M, Balardin RS, Kelly JD (2000) Host-pathogen interaction and variability of Colletotrichum lindemuthianum. In: Prusky D, Freeman S, Dickman MB (eds) Colletotrichum host specificity, pathology, and host-pathogen interaction. APS Press, St Paul, pp 346–361

    Google Scholar 

  • Melotto M, Coelho MF, Pedrosa-Harand A, Kelly JD, Camargo LEA (2004) The anthracnose resistance locus Co-4 of common bean is located on chromosome 3 and contains putative disease resistance-related genes. Theor Appl Genet 109(4):690–699. doi:10.1007/s00122-004-1697-6

    Article  CAS  PubMed  Google Scholar 

  • Michelmore RW, Paran J, Kesseli RV (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregation populations. Proc Natl Acad Sci 88:9828–9832. doi:10.1073/pnas.88.21.9828

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Navarro L, Zipfel C, Rowland O, Keller I, Robatzek S, Boller T, Jones JDG (2004) The transcriptional innate immune response to flg22. Interplay and overlap with Avr gene-dependent defense responses and bacterial pathogenesis. Plant Physiol 135:1113–1128. doi:10.1104/pp.103.036749

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • O’Connell RJ, Thon MR, Hacquard S et al (2012) Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nat Genet 44(9):1060–1065. doi:10.1038/ng.2372

    Article  PubMed  Google Scholar 

  • Oblessuc PR, Borges A, Chowdhury B, Caldas DGG, Tsai SM, Camargo LEA, Melotto M (2012) Dissecting Phaseolus vulgaris innate immune system against Colletotrichum lindemuthianum infection. PLoS ONE 7(8):e43161. doi:10.1371/journal.pone.0043161

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pabón-Mora N, Ambrose BA, Litt A (2012) Poppy APETALA1/FRUITFULL orthologs control flowering time, branching, perianth identity, and fruit development. Plant Physiol 158(4):1685–1704. doi:10.1104/pp.111.192104

    Article  PubMed Central  PubMed  Google Scholar 

  • Queiroz VT, Sousa CS, Costa MR, Sanglad DA, Arruda KMA, Souza TLPO, Ragagnin VA, Barros EG, Moreira MA (2004) Development of SCAR markers linked to common bean anthracnose resistance genes Co-4 and Co-6. Annu Rep Bean Improv Coop 47:249–250

    Google Scholar 

  • Reuter M (2012) Image analysis: dot count. DotCount v1.2. http://reuter.mit.edu/software/dotcount/

  • Richard MMS, Chen NWG, Thareau V, Pflieger S, Blanchet S, Pedrosa-Harand A, Iwata A, Chavarro C, Jackson SA, Geffroy V (2013) The subtelomerickhipu satellite repeat from Phaseolus vulgaris: lessons learned from the genome analysis of the andean genotype G19833. Front Plant Sci 4:109. doi:10.3389/fpls.2013.00109

    Article  PubMed Central  PubMed  Google Scholar 

  • Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3(6):1101–1108. doi:10.1038/nprot.2008.73

    Article  CAS  PubMed  Google Scholar 

  • Schmutz J, McClean PE, Mamidi S et al (2014) A reference genome for common bean and genome-wide analysis of dual domestications. Nat Genet 46:707–713. doi:10.1038/ng.3008

    Article  CAS  PubMed  Google Scholar 

  • Sessa G, Martin GB (2000) Signal recognition and transduction mediated by the tomato Pto kinase: a paradigm of innate immunity in plants. Microb Infec 2(13):1591–1597

    Article  CAS  Google Scholar 

  • Shiu SH, Bleecker AB (2001) Plant receptor-like kinase gene family: diversity, function, and signaling. Sci STKE 113:re22. doi:10.1126/stke.2001.113.re22

    Google Scholar 

  • Silverio L, Vidigal MC, Vidigal Filho PS, Barelli MAA, Thomazella C, Nunes WMC (2002) Genetic resistance to Colletotrichum lindemuthianum race 2047 in G2333. Annu Rep Bean Improv Coop 45:74–75

    Google Scholar 

  • Singh SP, Schwartz HF (2010) Breeding common bean for resistance to diseases: a review. Crop Sci 50(6):2199. doi:10.2135/cropsci2009.03.0163

    Article  Google Scholar 

  • Song WY, Wang GL, Chen L, Kim HS, Pi LY, Gardner J, Wang B, Holsten T, Zhai WX, Zhu LH, Fauquet C, Ronald PC (1995) A receptor kinase-like protein encoded by the rice disease resistance gene Xa21. Science 270:1804–1806. doi:10.1126/science.270.5243.1804

    Article  CAS  PubMed  Google Scholar 

  • Spoel SH, Dong X (2012) How do plants achieve immunity? Defence without specialized immune cells. Nat Rev Immunol 12(2):89–100. doi:10.1038/nri3141

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. doi:10.1093/molbev/msr121

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tatusova TA, Madden TL (1999) BLAST 2 sequences, a new tool for comparing protein and nucleotide sequences. FEMS Microbiol Lett 174:247–250. doi:10.1111/j.1574-6968.1999.tb13575.x

    Article  CAS  PubMed  Google Scholar 

  • Temnykh S, DeClerck G, Lukashova A, Lipovich L, Cartinhour S, McCouch S (2001) Computational and experimental analysis of microsatellites in rice (Oryza sativa L.): frequency, length variation, transposon associations, and genetic marker potential. Genom Res 11:1441–1452. doi:10.1101/gr.184001 PMID:11483586

    Article  CAS  Google Scholar 

  • Thomma BPHJ, Nürnberger T, Joosten MHAJ (2011) Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23(1):4–15. doi:10.1105/tpc.110.082602

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Vanhouten W, MacKenzie S (1999) Construction and characterization of a common bean bacterial artificial chromosome library. Plant Mol Biol 40(6):977–983. doi:10.1023/A:1006234823105

    Article  CAS  PubMed  Google Scholar 

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78. doi:10.1093/jhered/93.1.77

    Article  CAS  PubMed  Google Scholar 

  • Wolf S, Hématy K, Höfte H (2012) Growth control and cell wall signaling in plants. Annu Rev Plant Biol 63:381–407. doi:10.1146/annurev-arplant-042811-105449

    Article  CAS  PubMed  Google Scholar 

  • Young RA, Kelly JD (1996) Characterization of genetic resistance to Colletotrichum lindemuthianum in common bean differential cultivars. Plant Dis 80(6):650–654. doi:10.1590/S1516-89132008000500002

    Article  Google Scholar 

  • Young RA, Melotto M, Nodari RO, Kelly JD (1998) Marker assisted dissection of the oligogenic anthracnose resistance in common bean cultivar G2333. Theor Appl Genet 96:87–94. doi:10.1007/s001220050713

    Article  CAS  Google Scholar 

  • Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JD, Felix G, Boller T (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428:764–767. doi:10.1038/nature02485

    Article  CAS  PubMed  Google Scholar 

  • Zmasek CM, Godzik A (2011) Strong functional patterns in the evolution of eukaryotic genomes revealed by the reconstruction of ancestral protein domain repertoires. Genom Biol 12(1):R4. doi:10.1186/gb-2011-12-1-r4

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Dr. L.E.A. Camargo for hosting CF and MM in his lab during the screening process for AFLP markers; Dr. J.D. Kelly for common bean seeds and the Colletotrichum lindemuthianum isolate; Dr. David Guttman for the Pseudomonas phaseolicola strain. The authors also thank CAPES/Science Without Borders for the post-doctoral fellowship awarded to PRO (award #9773-13-4), and FAPESP for the Undergraduate Research Assistantship to CF (award #01/11218-0). This study was funded by FAPESP—Fundação de Amparo à Pesquisa do Estado de São Paulo, Brazil (Grant #00/09049-2) to MM.

Conflict of interest

The authors declare that they have no conflict of interests.

Ethical standards

All experiments described in this manuscript comply with the current laws of the country in which they were performed.

Author information

Author notes

  1. Camila Francisco

    Present address: Hospital Municipal Universitário de São Bernardo, São Bernardo Do Campo, SP, 09735-260, Brazil

Authors and Affiliations

  1. Department of Plant Sciences, University of California, One Shields Avenue, Davis, CA, 95616, USA

    Paula Rodrigues Oblessuc, Camila Francisco & Maeli Melotto

  2. CAPES foundation, Brazilian Ministry of Education, Brasília, DF, 70040-020, Brazil

    Paula Rodrigues Oblessuc

Authors
  1. Paula Rodrigues Oblessuc
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Camila Francisco
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maeli Melotto
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maeli Melotto.

Additional information

Communicated by D. E. Mather.

Electronic supplementary material

Below is the link to the electronic supplementary material.

122_2015_2500_MOESM1_ESM.pdf

Fig. S1 Phylogenetic analysis of the top 100 protein kinases with the highest similarity to the predicted COK-4_SEL1308 protein. The top 100 hits were obtained from BLASTP analysis (threshold E-value ≤ 1 x 10−20 and identity > 30 %) using COK-4_SEL1308 as query against the common bean proteome database available at Phytozome. The phylogenetic tree was obtained with the maximum parsimony method using the MEGA 5.05 software (Tamura et al. 2011). Bootstrap support values are adjacent to the tree nodes. Co-4 locus-associated kinases formed a single cluster (red box), and kinase/malectin proteins formed another sub-cluster (blue box). (PDF 34 kb)

Supplementary material 2 (DOCX 32 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Oblessuc, P.R., Francisco, C. & Melotto, M. The Co-4 locus on chromosome Pv08 contains a unique cluster of 18 COK-4 genes and is regulated by immune response in common bean. Theor Appl Genet 128, 1193–1208 (2015). https://doi.org/10.1007/s00122-015-2500-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-015-2500-6

Keywords

Search

Navigation