Skip to main content
SpringerLink
Log in

Development of four phylogenetically-arrayed BAC libraries and sequence of the APA locus in Phaseolus vulgaris

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

Abstract

The APA family of seed proteins consists of three subfamilies, in evolutionary order of hypothesized appearance: phytohaemagglutinins (PHA), α-amylase inhibitors (αAI), and arcelins (ARL). The APA family plays a defensive role against mammalian and insect seed predation in common bean (Phaseolus vulgaris L.). The main locus (APA) for this gene family is situated on linkage group B4. In order to elucidate the pattern of duplication and diversification at this locus, we developed a BAC library in each of four different Phaseolus genotypes that represent presumptive steps in the evolutionary diversification of the APA family. Specifically, BAC libraries were established in one P. lunatus (cv. ‘Henderson: PHA+ αAI− ARL−) and three P. vulgaris accessions (presumed ancestral wild G21245 from northern Peru: PHA+ αAI + ARL−; Mesoamerican wild G02771: PHA+ αAI + ARL+; and Mesoamerican breeding line BAT93: PHA+ αAI + ARL−). The libraries were constructed after HindIII digestion of high molecular weight DNA, obtained with a novel nuclei isolation procedure. The frequency of empty or cpDNA-sequence-containing clones in all libraries is low (generally <1%). The Henderson, G21245, and G02771 libraries have a 10× genome coverage, whereas the BAT93 library has a 20× coverage to allow further, more detailed genomic analysis of the bean genome. The complete sequence of a 155 kbp-insert clone of the G02771 library revealed six sequences belonging to the APA gene family, including members of the three subfamilies, as hypothesized. The different subfamilies were interspersed with retrotransposon sequences. In addition, other sequences were identified with similarity to chloroplast DNA, a dehydrin gene, and the Arabidopsis flowering D locus. Linkage between the dehydrin gene and the D1711 RFLP marker identifies a potential syntenic region between parts of common bean linkage group B4 and cowpea linkage group 2

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

Similar content being viewed by others

References

  • Acosta-Gallegos J, Quintero C, Vargas J, Toro O, Tohme J, Cardona C (1998) A new variant of arcelin in wild common bean, Phaseolus vulgaris L., from southern Mexico. Genet Res Crop Evol 45:235–242

    Article  Google Scholar 

  • Aravind L, Iyer LM (2002) The SWIRM domain: a conserved module found in chromosomal proteins points to novel chromatin-modifying activities. Genome Biol 3: research0039.0031–0039.0037

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Chrispeels MJ, Raikhel NV (1991) Lectins, lectin genes, and their role in plant defense. Plant Cell 3:1–9

    Article  PubMed  CAS  Google Scholar 

  • Colucci G, Moore J, Feldman M, Chrispeels M (1999) cDNA cloning of FRIL, a lectin from Dolichos lablab, that preserves hematopoietic progenitors in suspension culture. Proc Nat Acad Sci USA 96:646–650

    Article  PubMed  CAS  Google Scholar 

  • Delgado-Salinas A, Turley T, Richman A, Lavin M (1999) Phylogenetic analysis of the cultivated and wild species of Phaseolus (Fabaceae). Syst Bot 24:438–460

    Article  Google Scholar 

  • Dubcovsky J, Ramakrishna W, SanMiguel PJ, Busso CS, Yan L, Shiloff BA, Bennetzen JL (2001) Comparative sequence analysis of colinear barley and rice bacterial artificial chromosomes. Plant Physiology 125:1342–1353

    Article  PubMed  CAS  Google Scholar 

  • Ewing B, Green P (1998) Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 8:186–194

    PubMed  CAS  Google Scholar 

  • Ewing B, Hillier L, Wendl M, Green P (1998) Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 8:175–185

    PubMed  CAS  Google Scholar 

  • Feinberg AP, Vogelstein B (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132:9–13

    Article  Google Scholar 

  • Feinberg AP, Vogelstein B (1984)A technique for radiolabelling DNA restriction endonuclease fragments to high specific activity (addendum). Anal Biochem 137:266–267

    Article  PubMed  CAS  Google Scholar 

  • Ferrier-Cana E, Macadre C, Sevignac M, David P, Langin T, Geffroy V (2005) Distinct post-transcriptional modifications result into seven alternative transcripts of the CC-NBS-LRR gene JA1tr of Phaseolus vulgaris. Theor Appl Genet 110:895–905

    Article  PubMed  CAS  Google Scholar 

  • Finardi-Filho F, Mirkov T, Chrispeels M (1996) A putative precursor protein in the evolution of the bean α-amylase inhibitor. Phytochemistry 43:57–62

    Article  PubMed  CAS  Google Scholar 

  • Freyre R, Skroch PW, Geffroy V, Adam-Blondon A-F, Shirmohamadali A, Johnson W, Llaca V, Nodari RO, Pereira P, Tsai S-M, Tohme J, Dron M, Nienhuis J, Vallejos CE, Gepts P (1998) Towards an integrated linkage map of common bean. 4. Development of a core map and alignment of RFLP maps. Theor Appl Genet 97:847–856

    Article  CAS  Google Scholar 

  • Freytag GF, Debouck DG (2002) Taxonomy, distribution, and ecology of the genus Phaseolus (Leguminosae—Papilionoideae) in North America, Mexico and Central America, edn. Botanical Research Institute of Texas, Forth Worth, TX

  • Geffroy V, Sévignac M, De Oliveira J, Fouilloux G, Skroch P, Thoquet P, Gepts P, Langin T, Dron M (2000) Inheritance of partial resistance against Colletotrichum lindemuthianum in Phaseolus vulgaris and co-localization of QTL with genes involved in specific resistance. Mol Plant-Microbe Interact 13:287–296

    Article  PubMed  CAS  Google Scholar 

  • Gepts P (1998) Origin and evolution of common bean: past events and recent trends. HortScience 33:1124–1130

    Google Scholar 

  • Gepts P (1999) Development of an integrated genetic linkage map in common bean (Phaseolus vulgaris L.) and its use. In: S. Singh (ed) Bean breeding for the 21st century. Kluwer, Dordrecht, pp 53–91, 389–400

  • Gepts P, Beavis WD, Brummer EC, Shoemaker RC, Stalker HT, Weeden NF, Young ND (2005) Legumes as a model plant family. Genomics for food and feed Report of the Cross-Legume Advances through Genomics Conference. Plant Physiol 137:1228–1235

    Article  PubMed  CAS  Google Scholar 

  • Goossens A, Geremia R, Bauw G, Van Montagu M, Angenon G (1994) Isolation and characterisation of arcelin-5 proteins and cDNAs. Eur J Biochem 225:787–795

    Article  PubMed  CAS  Google Scholar 

  • Gordon D, Abajian C, Green P (1998) Consed: A graphical tool for sequence finishing. Genome Res 8:195–202

    PubMed  CAS  Google Scholar 

  • Gutiérrez Salgado A, Gepts P, Debouck D (1995) Evidence for two gene pools of the lima bean, Phaseolus lunatus L., in the Americas. Genet Res Crop Evol 42:15–22

    Article  Google Scholar 

  • Hall AE (2004) Breeding for adaptation to drought and heat in cowpea. Eur J Agron 21:447–454

    Article  Google Scholar 

  • He Y, Michaels SD, Amasino RM (2003) Regulation of flowering time by histone acetylation in Arabidopsis. Science 302:1751–1754

    Article  PubMed  CAS  Google Scholar 

  • Ho MF, Yin X, Finardi Filho F, Lajolo F, Whitaker JR (1994) Naturally occurring α-amylase inhibitors: structure/function relationships. In: Yada R, Jackman LR, Smith J (eds) Protein structure-function relationships in food Bishopbriggs. Blackie Academic and Professional, Glasgow, pp 89–119

    Google Scholar 

  • Hoffman LM, Donaldson DD (1985) Characterization of two Phaseolus vulgaris phytohemagglutinin genes closely linked on the chromosome. EMBO J 4:883–889

    PubMed  CAS  Google Scholar 

  • Hoffman LM, Ma Y, Barker RF (1982) Molecular cloning of Phaseolus vulgaris lectin mRNA and use of cDNA as a probe to estimate lectin transcript levels in various tissues. Nucl Acids Res 10:7819–7828

    Article  PubMed  CAS  Google Scholar 

  • Ismail AM, Hall AE, Close TJ (1999) Allelic variation of a dehydrin gene cosegregates with chilling tolerance during seedling emergence. Proc Nat Acad Sci USA 96:13566–13570

    Article  PubMed  CAS  Google Scholar 

  • John ME, Long CM (1990) Sequence analysis of arcelin 2, a lectin-like plant protein. Gene 86:171–176

    Article  PubMed  CAS  Google Scholar 

  • Kami J, Becerra Velásquez B, Debouck DG, Gepts P (1995) Identification of presumed ancestral DNA sequences of phaseolin in Phaseolus vulgaris. Proc Nat Acad Sci USA 92:1101–1104

    Article  PubMed  CAS  Google Scholar 

  • Kelly JD, Gepts P, Miklas PN, Coyne DP (2003) Tagging and mapping of genes and QTL and molecular marker-assisted selection for traits of economic importance in bean and cowpea. Field Crops Res 82:135–154

    Article  Google Scholar 

  • Koinange EMK, Singh SP, Gepts P (1996) Genetic control of the domestication syndrome in common-bean. Crop Sci 36:1037–1045

    Article  Google Scholar 

  • Kuehl R (1964) Isolation of plant nuclei. Z Naturforsch, B: Anorg Chem, Org Chem, Biochem Biophys Biol 198:525–534

    Google Scholar 

  • Lioi L, Sparvoli F, Galasso I, Lanave C, Bollini R (2003) Lectin-related resistance factors against bruchids evolved through a number of duplication events. Theor Appl Genet 107:814–822

    Article  PubMed  CAS  Google Scholar 

  • Llaca V, Delgado Salinas A, Gepts P (1994) Chloroplast DNA as an evolutionary marker in the Phaseolus vulgaris complex. Theor Appl Genet 88:646–652

    Article  CAS  Google Scholar 

  • Llaca V, Gepts P (1996) Pulsed field gel electrophoresis analysis of the phaseolin locus region in Phaseolus vulgaris. Genome 39:722–729

    CAS  PubMed  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 109:690–699

    Article  PubMed  CAS  Google Scholar 

  • Minney B, Gatehouse A, Dobie P, Dendy J, Cardona C, Gatehouse A (1990) Biochemical bases of seed resistance to Zabrotes subfasciatus (bean weevil) in Phaseolus vulgaris (common bean)—a mechanism for arcelin toxicity. J Insect Phys 36:757

    Article  CAS  Google Scholar 

  • Mirkov TE, Wahlstrom JM, Hagiwara K, Finardi-Filho F, Kjemtrup S, Chrispeels MJ (1994) Evolutionary relationships among proteins in the phytohemagglutinin-arcelin-alpha-amylase inhibitor family of the common bean and its relatives. Plant Mol Biol 26:1103–1113

    Article  PubMed  CAS  Google Scholar 

  • Moreno J, Chrispeels MJ (1989) A lectin gene encodes the α-amylase inhibitor of the common bean. Proc Natl Acad Sci USA 86:7885–7889

    Article  PubMed  CAS  Google Scholar 

  • Nodari RO, Tsai SM, Gilbertson RL, Gepts P (1993) Towards an integrated linkage map of common bean. II. Development of an RFLP-based linkage map. Theor Appl Genet 85:513–520

    Article  CAS  Google Scholar 

  • Noutsos C, Richly E, Leister D (2005) Generation and evolutionary fate of insertions of organelle DNA in the nuclear genomes of flowering plants. Genome Res 15:616–628

    Article  PubMed  CAS  Google Scholar 

  • Osborn TC, Alexander DC, Sun SSM, Cardona C, Bliss FA (1988) Insecticidal activity and lectin homology of arcelin seed protein. Science 240:207–210

    Article  CAS  Google Scholar 

  • Osborn TC, Blake T, Gepts P, Bliss FA (1986) Bean arcelin. 2. Genetic variation, inheritance and linkage relationships of a novel seed protein of Phaseolus vulgaris. Theor Appl Genet 71:847–855

    Article  CAS  Google Scholar 

  • Ouédraogo JT, Gowda BS, Jean M, Close TJ, Ehlers JD, Hall AE, Gillaspie AG, Roberts PA, Ismail AM, Bruening G, Gepts P, Timko MP, Belzile FJ (2002) An improved genetic linkage map for cowpea (Vigna unguiculata L.) combining AFLP, RFLP, RAPD, biochemical markers, and biological resistance traits. Genome 45:175–188

    Article  PubMed  Google Scholar 

  • Peterson DG, Tomkins JP, Frisch DA, Wing RA, Paterson AH (2000) Construction of plant bacterial artificial chromosome (BAC) libraries: an illustrated guide. J Agric Genomics 5: (http://www.ncgr.org/research/jag)

  • Pueyo JJ, Delgado-Salinas A (1997) Presence of α-amylase inhibitor in some members of the subtribe Phaseolinae (Phaseoleae: Fabaceae). Am J Bot 84:79–84

    CAS  Google Scholar 

  • Pusztai A (1991) Plant lectins. Cambridge University Press, Cambridge, p 263

    Google Scholar 

  • Romero-Andreas J, Yandell BS, Bliss FA (1986) Bean arcelin. 1. Inheritance of a novel seed protein of Phaseolus vulgaris L. and its effect on seed composition. Theor Appl Genet 72:123–128

    Article  Google Scholar 

  • Rougé P, Barre A, Causse H, Chatelain C, Porthe G (1993) Arcelin and alpha-amylase inhibitor from the seeds of common bean (Phaseolus vulgaris L.) are truncated lectins. Biochem Syst Evol 21:696–703

    Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Santimone M, Koukiekolo R, Moreau Y, Le Berre V, Rougé P, Marchis-Mouren G, Desseaux V (2004) Porcine pancreatic α-amylase inhibition by the kidney bean (Phaseolus vulgaris) inhibitor (α-AI1) and the structural changes in the α-amylase inhibitor complex. Biochim Biophys Acta 1696:181–190

    PubMed  CAS  Google Scholar 

  • Sparvoli F, Bollini R (1998) Arcelin in wild bean (Phaseolus vulgaris L.) seeds: sequence of arcelin 6 shows it is a member of the arcelins 1 and 2 subfamily. Genet Res Crop Evol 45:383–388

    Article  Google Scholar 

  • Suzuki K, Ishimoto M, Kikuchi F, Kitamura K (1993) Growth inhibitory effect of an alpha-amylase inhibitor from the wild common bean resistant to the Mexican bean weevil (Zabrotes subfasciatus). Japan J Breed 43:257–265

    CAS  Google Scholar 

  • Suzuki K, Ishimoto M, Kitamura K (1994) cDNA sequence and deduced primary structure of an α-amylase inhibitor from a bruchid resistant wild common bean. Biochim Biophys Acta 1206:289–291

    PubMed  CAS  Google Scholar 

  • Suzuki K, Ishimoto M, Iwanaga M, Kikuchi F, Kitamura K (1995) Inheritance of seed α-amylase inhibitor in the common bean and genetic relationships to arcelin. Theor Appl Genet 90:762–766

    Article  CAS  Google Scholar 

  • Talbot D, Adang M, Slightom J, Hall T.C. (1984) Size and organization of a multigene family encoding phaseolin, the major seed storage protein of Phaseolus vulgaris L Mol. Gen Genet 198:42–49

    Article  CAS  Google Scholar 

  • Toth EC, Vissi E, Kovacs I, Szoke A, Arino J, Gergely P, Dudits D, Dombradi V (2000) Protein phosphatase 2A holoenzyme and its subunits from Medicago sativa. Plant Mol Biol 43:527–536

    Article  PubMed  CAS  Google Scholar 

  • Vallejos CE, Astua-Monge G, Jones V, Plyler T, Sakiyama N, Vanhoutten W, Mackenzie S (2004) Abstract 25003: Genetic and molecular characterization of the I locus of Phaseolus vulgaris. American Society of Plant Biologists Annual Meeting July 24–28, 2004, Lake Buena Vista, FL. http://www.abstracts.aspb.org/pb2004/public/M12/7715.html

  • Vanhouten W, Mackenzie S (1999) Construction and characterization of a common bean bacterial artificial chromosome library. Plant Molec Biol 40:977–983

    Article  CAS  Google Scholar 

  • Voelker T, Sturm A, Chrispeels M (1987) Differences in expression between seed lectin alleles obtained from normal and lectin-deficient beans are maintained in transgenic tobacco. EMBO J 6:3571–3577

    PubMed  CAS  Google Scholar 

  • Young ND, Cannon SB, Sato S, Kim D, Cook DR, Town CD, Roe BA, Tabata S (2005) Sequencing the genespaces of Medicago truncatula and Lotus japonicus. Plant Physiol 137:1174–1181

    Article  PubMed  CAS  Google Scholar 

  • Zhang HB, Zhao X, Ding X, Paterson AH, Wing RA (1995) Preparation of megabase-size DNA from plant nuclei. Plant J 7:175–184

    Article  CAS  Google Scholar 

Download references

Acknowledgments

BAC sequencing was performed at the Purdue Genomics Core Facility by Phillip San Miguel and Paul Parker. The project was supported by the National Research Initiative of the USDA Cooperative State Research, Education and Extension Service, grant number #00–01972.

Author information

Author notes

  1. Valérie Poncet

    Present address: UMR 1097 Diversité et Génomes des Plantes Cultivées, Institut de Recherche pour le Développement, 911 avenue Agropolis, 34394, Montpellier cedex 5, France

  2. Valérie Geffroy

    Present address: Institut de Biotechnologie des Plantes, Bâtiment 630, Université de Paris-Sud, 91405, Orsay Cedex, France

Authors and Affiliations

  1. Department of Plant Sciences, Section of Crop and Ecosystem Sciences, University of California, Mailstop 1, 1 Shields Avenue, Davis, CA, 95616-8780, USA

    James Kami, Valérie Poncet, Valérie Geffroy & Paul Gepts

Authors
  1. James Kami
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Valérie Poncet
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Valérie Geffroy
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Paul Gepts
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Paul Gepts.

Additional information

Communicated by F. J. Muehlbauer

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kami, J., Poncet, V., Geffroy, V. et al. Development of four phylogenetically-arrayed BAC libraries and sequence of the APA locus in Phaseolus vulgaris . Theor Appl Genet 112, 987–998 (2006). https://doi.org/10.1007/s00122-005-0201-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-005-0201-2

Keywords

Search

Navigation