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QUES, a new Phaseolus vulgaris genotype resistant to common bean weevils, contains the Arcelin-8 allele coding for new lectin-related variants

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Abstract

In common bean (Phaseolus vulgaris L.), the most abundant seed proteins are the storage protein phaseolin and the family of closely related APA proteins (arcelin, phytohemagglutinin and α-amylase inhibitor). High variation in APA protein composition has been described and the presence of arcelin (Arc) has been associated with bean resistance against two bruchid beetles, the bean weevil (Acanthoscelides obtectus Say) and the Mexican bean weevil (Zabrotes subfasciatus Bohemian). So far, seven Arc variants have been identified, all in wild accessions, however, only those containing Arc-4 were reported to be resistant to both species. Although many efforts have been made, a successful breeding of this genetic trait into cultivated genotypes has not yet been achieved. Here, we describe a newly collected wild accession (named QUES) and demonstrate its resistance to both A. obtectus and Z. subfasciatus. Immunological and proteomic analyses of QUES seed protein composition indicated the presence of new Arc and arcelin-like (ARL) polypeptides of about 30 and 27 kDa, respectively. Sequencing of cDNAs coding for QUES APA proteins confirmed that this accession contains new APA variants, here referred to as Arc-8 and ARL-8. Moreover, bioinformatic analysis showed the two proteins are closely related to APA components present in the G12949 wild bean accession, which contains the Arc-4 variant. The presence of these new APA components, combined with the observations that they are poorly digested and remain very abundant in A. obtectus feces, so-called frass, suggest that the QUES APA locus is involved in the bruchid resistance. Moreover, molecular analysis indicated a lower complexity of the locus compared to that of G12949, suggesting that QUES should be considered a valuable source of resistance for further breeding purposes.

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Abbreviations

αAI:

α-Amylase inhibitor

AIL:

α-Amylase inhibitor like

APA:

Arcelin/phytohemagglutinin/α-amylase inhibitor

Arc:

Arcelin

ARL:

Arcelin-like

2DE:

Two-dimensional gel electrophoresis

LC–MS/MS:

Liquid-chromatography tandem mass spectrometry

PHA:

Phytohemagglutinin

IS:

Index of susceptibility

References

  • Blair MW, Muñoz C, Buendía HF, Flower J, Bueno JM, Cardona C (2010) Genetic mapping of microsatellite markers around the arcelin bruchid resistance locus in common bean. Theor Appl Genet 121:393–402

    Article  PubMed  CAS  Google Scholar 

  • Bollini R, Chrispeels MJ (1978) Characterization and subcellular localization of vicilin and phytohemagglutinin, the two major reserve proteins of Phaseolus vulgaris L. Planta 142:291–298

    Article  CAS  Google Scholar 

  • Campion B, Perrone D, Galasso I, Bollini R (2009) Common bean (Phaseolus vulgaris L.) lines devoid of major lectin proteins. Plant Breed 128:199–204

    Article  CAS  Google Scholar 

  • Cardona C (2004) Common beans: Latin America. In: Hodges R, Farrell G (eds) Crop post-harvest: science and technology durables, vol 2. Blackwell, Oxford, pp 145–150

    Google Scholar 

  • Cardona C, Kornegay J (1999) Bean germplasm resources for insect resistance. In: Clement S, Quisenberry S (eds) Global plant genetic resources for insect-resistant crops. CRC Press, Boca Raton

    Google Scholar 

  • Cardona C, Posso CE, Kornegay J, Valor J, Serrano M (1989) Antibiosis effects of wild dry bean accessions on the Mexican bean weevil and the bean weevil (Coleoptera: Bruchidae). J Econ Entomol 82:310–315

    Google Scholar 

  • Cardona C, Kornegay J, Posso C, Morales F, Ramirez H (1990) Comparative value of four arcelin variants in the development of dry bean lines resistant to the Mexican bean weevil. Entomol Exp Appl 56:197–206

    Article  Google Scholar 

  • Carlini CR, Grossi-de-Sá MF (2002) Plant toxic proteins with insecticidal properties. a review on their potentialities as bioinsecticides. Toxicon 40:11515–11539

    Article  Google Scholar 

  • Ceriotti A, Vitale A, Bollini R (1989) Lectin-like protein accumulates as fragmentation products in bean seed protein bodies. FEBS Lett 250:157–160

    Article  CAS  Google Scholar 

  • Chen H, Gonzales-Vigil E, Wilkerson CG, Howe GA (2007) Stability of plant defense proteins in the gut of insect herbivores. Plant Physiol 143(4):1954–1967

    Article  PubMed  CAS  Google Scholar 

  • Dendy J, Credland PF (1991) Development, fecundity and egg dispersion of Zabrotes subfasciatus. Entomol Exp Appl 59:9–17

    Article  Google Scholar 

  • Dobie P, Dendy J, Sherman C, Padgham J, Wood A, Gatehouse AMR (1990) New sources of resistance to A. obtectus (Say) and Zabrotes subfasciatus Boheman (Coleoptera: Bruchidae) in mature seeds of five species of Phaseolus. J Stored Prod Res 26(4):177–186

    Article  Google Scholar 

  • Fabre C, Causse H, Mourey L, Koninkx J, Rivière M, Hendriks H, Puzo G, Samama JP, Rougé P (1998) Characterization and sugar-binding properties of arcelin-1, an insecticidal lectin-like protein isolated from kidney bean (Phaseolus vulgaris L. cv. RAZ-2) seeds. Biochem J 329:551–560

    PubMed  CAS  Google Scholar 

  • Fileppi M, Sparvoli F, Bollini R (2002) Major lima bean seed storage proteins are poorly digested by bean weevil larvae. In: International conference on legume genomics and genetics: translation to crop improvement, Minneapolis-St Paul, MN, USA, 2–6 June, p 126

  • Galasso I, Lioi L, Lanave C, Campion B, Bollini R, Sparvoli F (2005) Identification and sequencing of a BAC clone belonging to the Phaseolus vulgaris (L.) insecticidal Arc4 lectin locus. Bean Improvement Cooperative 48, p 40

    Google Scholar 

  • Gatehouse AMR, Dobie P, Hodges RJ, Meik J, Pusztai A, Boulter D (1987) Role of carbohydrates in insect resistance in Phaseolus vulgaris. J Insect Physiol 33(11):843–850

    Article  CAS  Google Scholar 

  • Gepts P, Aragão FJL, de Barros E, Blair MW, Brondani R, Broughton W, Galasso I, Hernández G, Kami J, Lariguet P, McClean P, Melotto M, Miklas P, Pauls P, Pedrosa-Harand A, Porch T, Sánchez F, Sparvoli F, Yu K (2008) Genomics of Phaseolus beans, a major source of dietary protein and micronutrient in the Tropics. In: Moore PH, Ming R (eds) Genomics of tropical crop plants. Springer, Berlin, pp 113–143

    Chapter  Google Scholar 

  • Goossens A, Quintero C, Dillen W, De Rycke R, Valor JF, De Clercq J, Van Montagu M, Cardona C, Angenon G (2000) Analysis of bruchid resistance in the wild common bean accession G02771: no evidence for insecticidal activity of arcelin 5. J Exp Bot 51:1229–1236

    Article  PubMed  CAS  Google Scholar 

  • Grossi de Sa MF, Mirkov TE, Ishimoto M, Colucci G, Bateman KS, Chrispeels MJ (1997) Molecular characterization of a bean alpha-amylase inhibitor that inhibits the alpha-amylase of the Mexican bean weevil Zabrotes subfasciatus. Planta 203:295–303

    Article  PubMed  CAS  Google Scholar 

  • Hartweck LM, Osborn TC (1997) Altering protein composition by genetically removing phaseolin from common bean seeds containing arcelin or phytohemagglutinin. Theor Appl Genet 95:1012–1017

    Article  CAS  Google Scholar 

  • Hartweck LM, Vogelzang RD, Osborn TC (1991) Characterization and comparison of arcelin seed protein variants from common bean. Plant Physiol 97:204–211

    Google Scholar 

  • Heller M, Schlappritzi E, Stalder D, Nuoffer J-M, Haeberli A (2007) Compositional protein analysis of high density lipoproteins in hypercholesterolemia by shotgun LC-MS/MS and probabilistic peptide scoring. Mol Cell Proteomics 6:1059–1072

    Article  PubMed  CAS  Google Scholar 

  • Howe RW, Currie JE (1964) Some laboratory observations on the rates of development, mortality and oviposition of several species of Bruchidae breeding in stored pulses. Bull Entomol Res 55:437–477

    Article  Google Scholar 

  • Ishimoto M, Suzuki K, Iwanaga M, Kikuchi F, Kitamura K (1995) Variation of seed α-amylase inhibitors in the common bean. Theor Appl Genet 90:425–429

    Article  CAS  Google Scholar 

  • Kami J, Poncet V, Geffroy V, Gepts P (2006) Development of four phylogenetically arrayed BAC libraries and sequence of the APA locus in Phaseolus vulgaris. Theor Appl Genet 112:987–998

    Article  PubMed  CAS  Google Scholar 

  • Kornegay J, Cardona C (1991) Inheritance of resistance to A. obtectus in a wild common bean accession crossed to commercial bean cultivars. Euphytica 52:103–111

    Google Scholar 

  • Kornegay J, Cardona C, Posso CE (1993) Inheritance of resistance to Mexican bean weevil in common bean, determined by bioassay and biochemical tests. Crop Sci 33:589–594

    Article  CAS  Google Scholar 

  • Kusolwa PM, Myers JR (2011) Seed storage proteins Arl2 and its variants from the APA locus of wild tepary bean G40199 confers resistance to A. obtectus when expressed in common beans. Afr Crop Sci J 19:255–265

    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 

  • Lioi L, Galasso I, Lanave C, Daminati MG, Bollini R, Sparvoli F (2007) Evolutionary analysis of the APA genes in the Phaseolus genus: wild and cultivated bean species as sources of lectin-related resistance factors? Theor Appl Genet 115:959–970

    Article  PubMed  CAS  Google Scholar 

  • Mbogo PK, Myers JR, Davis J (2009) Transfer of the Arcelin-Phytohemmaglutinin-α Amylase inhibitor seed protein locus from tepary bean (Phaseolus acutifolius A. Gray) to common bean (P. vulgaris L.). Biotechnology 8:285–295

    Article  CAS  Google Scholar 

  • Minney BHP, Gatehouse AMR, Dobie P, Dendy J, Cardona C, Gatehouse JA (1990) Biochemical bases of seed resistance to Zabrotes subfasciatus (bean weevil) in Phaseolus vulgaris (common bean): a mechanism for arcelin toxicity. J Insect Physiol 36:757–767

    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-α-amylase inhibitor family of the common bean and its relatives. Plant Mol Biol 26:1103–1113

    Article  PubMed  CAS  Google Scholar 

  • Myers JR, Davie J, Kean D, Nchimbi-Msolla S, Misangu R (2001) Backcross breeding to introduce Arcelin alleles into improved African bean cultivars. In: Proceedings “Bean seed workshop” Arusha, Tanzania 12–14 Jan. http://sustainableseedsystems.wsu.edu/proceedings/Myers.pdf

  • Nishizawa K, Teraishi M, Utsami S, Ishimoto M (2007) Assessment of the importance of α-amylase inhibitor 2 in bruchid resistance of wild common bean. Theor Appl Genet 114:755–764

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Paes NS, Gerhardt IR, Coutinho MV, Yokoyama M, Santana E, Harris N, Chrispeels MJ, Grossi-de-Sá MF (2000) The effect of arcelin-1on the structure of the midgut of bruchid larvae and immunolocalization of the arcelin protein. J Insect Physiol 46:393–402

    Article  PubMed  CAS  Google Scholar 

  • Santino A, Orchard J, Daminati MG, Cantoni R, Bollini R (1993) Bean (Phaseolus vulgaris L.) lectins and protection of the stored seed. In: Basu J, Kindu M, Chakrabarti P (eds) Lectins: Biology, Biochemistry, Clinical Biochemistry, vol 9. Wiley Eastern Lt., New Delhi, pp 19–26

    Google Scholar 

  • Schoonhoven A, Cardona C, Valor J (1983) Resistance to the bean weevil and the Mexican bean weevil (Coleoptera: Bruchidae) in non-cultivated common bean accessions. J Econ Entomol 76:1255–1259

    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 arcelin 1 and 2 subfamily. Genet Res Crop Evol 45:383–388

    Article  Google Scholar 

  • Sparvoli F, Daminati MG, Bollini R (1994) Biochemical and molecular characterisation of a Phaseolus vulgaris mutant lacking the major lectin-related seed proteins. Ann Rep Bean Improv Coop 37:110

    Google Scholar 

  • Sparvoli F, Lanave C, Satucci A, Bollini R, Lioi L (2001) Lectin and lectin-related proteins in lima bean (Phaseolus lunatus L.) seeds: biochemical and evolutionary studies. Plant Mol Biol 45:587–597

    Article  PubMed  CAS  Google Scholar 

  • Sparvoli F, Galasso I, Lioi L, Campion B, Nielsen E, Hernandez G, Bollini R (2008) Modulation of antinutritional components in common bean (Phaseolus vulgaris L.) seeds. In: IV International conference on legume genomics and genetics, Puerto vallarta, Mexico, 7–12 Dec, p 100

  • Stalder D, Haeberli A, Heller M (2008) Evaluation of reducibility of protein identification results after multidimensional human serum protein separation. Proteomics 8:414–424

    Article  PubMed  CAS  Google Scholar 

  • van Tunen AJ, Koes RE, Spelt CE, van der Krol AR, Stuitje AR, Mol JN (1988) Cloning of the two chalcone flavanone isomerase genes from Petunia hybrida: coordinate, light-regulated and differential expression of flavonoid genes. EMBO 7:1257–1263

    Google Scholar 

  • Velten G, Rott AS, Cardona C, Dorn S (2007) The inhibitory effect of the natural seed storage protein arcelin on the development of A. obtectus. J Stored Prod Res 43:550–557

    Article  CAS  Google Scholar 

  • Young NM, Thibault P, Watson DC, Chrispeels MJ (1999) Post-translational processing of two alpha-amylase inhibitors and an arcelin from the common bean, Phaseolus vulgaris. FEBS Lett 446(1):203–206

    Article  PubMed  CAS  Google Scholar 

  • Zambre M, Goossens A, Cardona C, Van Montagu M, Terryn N, Angenon G (2005) A reproducible genetic transformation system for cultivated Phaseolus acutifolius (tepary bean) and its use to assess the role of arcelins in resistance to the Mexican bean weevil. Theor Appl Genet 110(5):914–924

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

Research was partially supported by MiPAAF with funds released by C.I.P.E (Resolution 17/2003) and by Regione Lombardia/CNR agreement, project 2 to FS; IZ was supported by the National Center of Competence in Research (NCCR), “Plant Survival”. We thank Prof. Marcello Duranti and Dr. Eleonora Cominelli for critical reading of the manuscript and helpful suggestions.

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Authors and Affiliations

  1. Unit of Ecology and Evolution, Department of Biology, University of Fribourg, Fribourg, Switzerland

    Isabelle Zaugg & Sven Bacher

  2. Department of AgriFood Molecular Sciences, State University of Milan, Milan, Italy

    Chiara Magni

  3. Institute of Agricultural Biology and Biotechnology, CNR, Via Bassini 15, 20133, Milan, Italy

    Dario Panzeri, Maria Gloria Daminati, Roberto Bollini & Francesca Sparvoli

  4. LEAE, Institute de Zoologie, University of Neuchâtel, Neuchâtel, Switzerland

    Betty Benrey

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  1. Isabelle Zaugg
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  2. Chiara Magni
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  3. Dario Panzeri
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  4. Maria Gloria Daminati
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  5. Roberto Bollini
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  6. Betty Benrey
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  7. Sven Bacher
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  8. Francesca Sparvoli
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Correspondence to Francesca Sparvoli.

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Communicated by J. Ray.

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Zaugg, I., Magni, C., Panzeri, D. et al. QUES, a new Phaseolus vulgaris genotype resistant to common bean weevils, contains the Arcelin-8 allele coding for new lectin-related variants. Theor Appl Genet 126, 647–661 (2013). https://doi.org/10.1007/s00122-012-2008-2

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