Advertisement

Comparison of Gene Families: Seed Storage and Other Seed Proteins

  • Jaya Joshi
  • Sudhakar Pandurangan
  • Marwan Diapari
  • Frédéric MarsolaisEmail author
Chapter
Part of the Compendium of Plant Genomes book series (CPG)

Abstract

Common bean (Phaseolus vulgaris) is an important source of protein and dietary fiber in human diets. Seed proteins, therefore, determine, at least in part, the nutritional value of common bean. From the very beginning of plant molecular biology, in the 1980s, common bean has been a prominent model plant to study seed storage proteins. The recent availability of several sequences for the common bean genome, coupled with seed transcriptomic and proteomic information, enables a comprehensive, in-depth view of seed protein genes in this organism. Comparisons between these sequences highlight interesting variation in lectin gene composition between the two centers of domestication. Alleles conferring storage protein deficiency may be used to improve the levels of essential sulfur amino acids and therefore protein quality. Some of the seed proteins represent anti-nutritionals, including some lectins, trypsin inhibitors, and lipoxygenases, and represent targets to be potentially removed from the genome. Other proteins have potential as bioproducts due to their biological activity against fungi or insects, including defensin D1 and albumin-1.

Keywords

Seed storage protein Globulin Albumin Lectin Legumin Protein quality Defensin 

Notes

Acknowledgements

This work was supported by a grant from the Ontario Research Fund—Research Excellence program. We thank Gregory Perry, Seth Munholland, William Crosby, and Peter Pauls for sharing the OAC-Rex sequence. We are grateful to Alex Molnar for help with figures.

References

  1. Adachi M, Takenaka Y, Gidamis AB, Mikami B, Utsumi S (2001) Crystal structure of soybean proglycinin A1aB1b homotrimer. J Mol Biol 305:291–305PubMedCrossRefGoogle Scholar
  2. Anthony JL, Vonder Haar RA, Hall TC (1990) Nucleotide sequence of an α-phaseolin gene from Phaseolus vulgaris. Nucleic Acids Res 18:3396PubMedPubMedCentralCrossRefGoogle Scholar
  3. Balsamo GM, Valentim-Neto PA, Mello CS, Arisi ACM (2015) Comparative proteomic analysis of two varieties of genetically modified (GM) Embrapa 5.1 common bean (Phaseolus vulgaris L.) and their non-GM counterparts. J Agric Food Chem 63:10569–10577PubMedCrossRefGoogle Scholar
  4. Barbashov SF, Egorov TA, Kochkina VM (1991) Isolation and characteristics of insulin-binding proteins from soybeans. Bioorg Khim 17:421–423PubMedGoogle Scholar
  5. Bobb AJ, Eiben HG, Bustos MM (1995) PvAlf, an embryo-specific acidic transcriptional activator enhances gene expression from phaseolin and phytohemagglutinin promoters. Plant J 8:331–343PubMedCrossRefGoogle Scholar
  6. Bobb AJ, Chern MS, Bustos MM (1997) Conserved RY-repeats mediate transactivation of seed-specific promoters by the developmental regulator PvALF. Nucleic Acids Res 25:641–647PubMedPubMedCentralCrossRefGoogle Scholar
  7. Bollini R, Allavena A, Vitale A (1985) Genomic analysis of phytohemagglutinin-deficient Phaseolus vulgaris cultivars. Annu Rep Bean Improv Coop 37:82Google Scholar
  8. Bustos MM, Begum D, Kalkan FA, Battraw MJ, Hall TC (1991) Positive and negative cis-acting DNA domains are required for spatial and temporal regulation of gene expression by a seed storage protein promoter. EMBO J 10:1469–1479PubMedPubMedCentralGoogle Scholar
  9. Carranco R, Chandrasekharan MB, Townsend JC, Hall TC (2004) Interaction of PvALF and VP1 B3 domains with the β-phaseolin promoter. Plant Mol Biol 55:221–237PubMedCrossRefGoogle Scholar
  10. Chandrasekharan MB, Bishop KJ, Hall TC (2003) Module-specific regulation of the β-phaseolin promoter during embryogenesis. Plant J 33:853–866PubMedCrossRefGoogle Scholar
  11. Chern MS, Bobb AJ, Bustos MM (1996a) The regulator of MAT2 (ROM2) protein binds to early maturation promoters and represses PvALF-activated transcription. Plant Cell 8:305–321PubMedPubMedCentralCrossRefGoogle Scholar
  12. Chern MS, Eiben HG, Bustos MM (1996b) The developmentally regulated bZIP factor ROM1 modulates transcription from lectin and storage protein genes in bean embryos. Plant J 10:135–148PubMedCrossRefGoogle Scholar
  13. Clemente A, Arques MC, Dalmais M, Le Signor C, Chinoy C, Olias R, Rayner T, Isaac PG, Lawson DM, Bendahmane A, Domoney C (2015) Eliminating anti-nutritional plant food proteins: the case of seed protease inhibitors in pea. PLoS ONE 10:e0134634PubMedPubMedCentralCrossRefGoogle Scholar
  14. Colucci G, Moore JG, Feldman M, Chrispeels MJ (1999) cDNA cloning of FRIL, a lectin from Dolichos lablab, that preserves hematopoietic progenitors in suspension culture. Proc Natl Acad Sci USA 96:646–650PubMedPubMedCentralCrossRefGoogle Scholar
  15. Czubinski J, Barciszewski J, Gilski M, Szpotkowski K, Debski J, Lampart-Szczapa E, Jaskolski M (2015) Structure of γ-conglutin: insight into the quaternary structure of 7S basic globulins from legumes. Acta Cryst D 71:224–238CrossRefGoogle Scholar
  16. De La Fuente M, Borrajo A, Bermúdez J, Lores M, Alonso J, López M, Santalla M, De Ron AM, Zapata C, Alvarez G (2011) 2-DE-based proteomic analysis of common bean (Phaseolus vulgaris L.) seeds. J Proteomics 74:262–267CrossRefGoogle Scholar
  17. De Ron AM, Papa R, Bitocchi E, González AM, Debouck DG, Brick MA, Fourie D, Marsolais F, Beaver J, Geffroy V, McClean P, Santalla M, Lozano R, Yuste-Lisbona FJ, Casquero PA (2015) Common bean. In: De Ron AM (ed) Grain Legumes. Handbook of Plant Breeding, vol 10. Springer, New York, pp 1–36Google Scholar
  18. Delahaie J, Hundertmark M, Bove J, Leprince O, Rogniaux H, Buitink J (2013) LEA polypeptide profiling of recalcitrant and orthodox legume seeds reveals ABI3-regulated LEA protein abundance linked to desiccation tolerance. J Exp Bot 64:4559–4573PubMedPubMedCentralCrossRefGoogle Scholar
  19. Duranti M, Consonni A, Magni C, Sessa F, Scarafoni A (2008) The major proteins of lupin seed: Characterisation and molecular properties for use as functional and nutraceutical ingredients. Trends Food Sci Technol 19:624–633CrossRefGoogle Scholar
  20. Finardi-Filho F, Mirkov TE, Chrispeels MJ (1996) A putative precursor protein in the evolution of the bean α-amylase inhibitor. Phytochemistry 43:57–62PubMedCrossRefGoogle Scholar
  21. Freyre R, Skroch PW, Geffroy V, Adam-Blondon AF, Shirmohamadali A, Johnson WC, Llaca V, Nodari RO, Pereira PA, Tsai SM, Tohme J, Dron M, Nienhuis J, Vallejos CE, Gepts P (1998) Towards an integrated linkage map of common bean. 4. Development of a core linkage map and alignment of RFLP maps. Theor Appl Genet 97:847–856CrossRefGoogle Scholar
  22. Gabriel I, Quillien L, Cassecuelle F, Marget P, Juin H, Lessire M, Sève B, Duc G, Burstin J (2008) Variation in seed protein digestion of different pea (Pisum sativum L.) genotypes by cecectomized broiler chickens: 2. Relation between in vivo protein digestibility and pea seed characteristics, and identification of resistant pea polypeptides. Livest Sci 113:262–273CrossRefGoogle Scholar
  23. Galasso I, Piergiovanni AR, Lioi L, Campion B, Bollini R, Sparvoli F (2009) Genome organization of Bowman-Birk inhibitor in common bean (Phaseolus vulgaris L.). Mol Breeding 23:617–624CrossRefGoogle Scholar
  24. Games PD, dos Santos IS, Mello EO, Diz MSS, Carvalho AO, de Souza-Filho GA, Da Cunha M, Vasconcelos IM, dos S. Ferreira B, Gomes VM (2008) Isolation, characterization and cloning of a cDNA encoding a new antifungal defensin from Phaseolus vulgaris L. seeds. Peptides 29:2090–2100Google Scholar
  25. Gaur V, Qureshi IA, Singh A, Chanana V, Salunke DM (2010) Crystal structure and functional insights of hemopexin fold protein from grass pea. Plant Physiol 152:1842–1850PubMedPubMedCentralCrossRefGoogle Scholar
  26. Gepts P, Bliss FA (1984) Enhanced available methionine concentration associated with higher phaseolin levels in common bean seeds. Theor Appl Genet 69:47–53PubMedCrossRefGoogle Scholar
  27. Gepts P, Bliss FA (1986) Phaseolin variability among wild and cultivated common beans (Phaseolus vulgaris) from Colombia. Econ Bot 40:469–478CrossRefGoogle Scholar
  28. Gepts P, Nodari R, Tsai SM, Koinange EMK, Llaca V, Gilbertson LA, Guzman P (1993) Linkage mapping in common bean. Annu Rep Bean Improv Coop 45:xxiv–xxxviiiGoogle Scholar
  29. Gillman JD, Kim W-S, Krishnan HB (2015) Identification of a new soybean Kunitz trypsin inhibitor mutation and its effect on Bowman—Birk protease inhibitor content in soybean seed. J Agric Food Chem 63:1352–1359PubMedCrossRefGoogle Scholar
  30. González Vélez A, Ferwerda F, Abreu E, Beaver JS (2012) Development of bean lines (Phaseolus vulgaris L.) resistant to BGYMV, BCMNV and bean weevil (Acanthoselides obtectus Say). Annu Rep Bean Improv Coop 55:89–90Google Scholar
  31. Hall TC, Chandrasekharan MB, Li G (1999) Phaseolin: its past, properties, regulation and future. In: Shewry PR, Casey R (eds) Seed Proteins. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 209–240CrossRefGoogle Scholar
  32. Hanada K, Hirano H (2004) Interaction of a 43-kDa receptor-like protein with a 4-kDa hormone-like peptide in soybean. Biochemistry 43:12105–12112PubMedCrossRefGoogle Scholar
  33. Hanada K, Nishiuchi Y, Hirano H (2003) Amino acid residues on the surface of soybean 4-kDa peptide involved in the interaction with its binding protein. Eur J Biochem 270:2583–2592PubMedCrossRefGoogle Scholar
  34. Hartweck LM, Vogelzang RD, Osborn TC (1991) Characterization and comparison of arcelin seed protein variants from common bean. Plant Physiol 97:204–211PubMedPubMedCentralCrossRefGoogle Scholar
  35. Hernández-Ledesma B, Hsieh CC, de Lumen BO (2013) Chemopreventive properties of peptide lunasin: a review. Protein Pept Lett 20:424–432PubMedGoogle Scholar
  36. Higgins TJ, Chandler PM, Randall PJ, Spencer D, Beach LR, Blagrove RJ, Kortt AA, Inglis AS (1986) Gene structure, protein structure, and regulation of the synthesis of a sulfur-rich protein in pea seeds. J Biol Chem 261:11124–11130PubMedGoogle Scholar
  37. Higgins TJV, Beach LR, Spencer D, Chandler PM, Randall PJ, Blagrove RJ, Kortt AA, Guthrie RE (1987) cDNA and protein sequence of a major pea seed albumin (PA 2: Mr ≈ 26 000). Plant Mol Biol 8:37–45PubMedCrossRefGoogle Scholar
  38. Hoffman LM, Donaldson DD (1985) Characterization of two Phaseolus vulgaris phytohemagglutinin genes closely linked on the chromosome. EMBO J 4:883–889PubMedPubMedCentralGoogle Scholar
  39. Ingham DJ, Beer S, Money S, Hansen G (2001) Quantitative real-time PCR assay for determining transgene copy number in transformed plants. Biotechniques 31:132–140PubMedGoogle Scholar
  40. Jofuku KD, Goldberg RB (1989) Kunitz trypsin inhibitor genes are differentially expressed during the soybean life cycle and in transformed tobacco plants. Plant Cell 1:1079–1093PubMedPubMedCentralCrossRefGoogle Scholar
  41. Kami JA, Gepts P (1994) Phaseolin nucleotide sequence diversity in Phaseolus. I. Intraspecific diversity in Phaseolus vulgaris. Genome 37:751–757PubMedCrossRefGoogle Scholar
  42. 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 112:987–998PubMedCrossRefGoogle Scholar
  43. Karaki L, Da Silva P, Rizk F, Chouabe C, Chantret N, Eyraud V, Gressent F, Sivignon C, Rahioui I, Kahn D, Brochier-Armanet C, Rahbé Y, Royer C (2016) Genome-wide analysis identifies gain and loss/change of function within the small multigenic insecticidal albumin 1 family of Medicago truncatula. BMC Plant Biol 16:1–19CrossRefGoogle Scholar
  44. Kawagoe Y, Campbell BR, Murai N (1994) Synergism between CACGTG (G-box) and CACCTG cis-elements is required for activation of the bean seed storage protein β-phaseolin gene. Plant J 5:885–890PubMedCrossRefGoogle Scholar
  45. Lacerda AF, Vasconcelos EAR, Pelegrini PB, Grossi de Sa MF (2014) Antifungal defensins and their role in plant defense. Front Microbiol 5:116PubMedPubMedCentralCrossRefGoogle Scholar
  46. Le Gall M, Quillien L, Seve B, Gueguen J, Lalles JP (2007) Weaned piglets display low gastrointestinal digestion of pea (Pisum sativum L.) lectin and pea albumin 2. J Anim Sci 85:2972–2981PubMedCrossRefGoogle Scholar
  47. Lenis JM, Gillman JD, Lee JD, Shannon JG, Bilyeu KD (2010) Soybean seed lipoxygenase genes: molecular characterization and development of molecular marker assays. Theor Appl Genet 120:1139–1149PubMedCrossRefGoogle Scholar
  48. Li G, Chandler SP, Wolffe AP, Hall TC (1998) Architectural specificity in chromatin structure at the TATA box in vivo: nucleosome displacement upon β-phaseolin gene activation. Proc Natl Acad Sci USA 95:4772–4777PubMedPubMedCentralCrossRefGoogle Scholar
  49. Li G, Bishop KJ, Chandrasekharan MB, Hall TC (1999) β-Phaseolin gene activation is a two-step process: PvALF-facilitated chromatin modification followed by abscisic acid-mediated gene activation. Proc Natl Acad Sci USA 96:7104–7109PubMedPubMedCentralCrossRefGoogle Scholar
  50. Liao D, Pajak A, Karcz SR, Chapman BP, Sharpe AG, Austin RS, Datla R, Dhaubhadel S, Marsolais F (2012) Transcripts of sulphur metabolic genes are co-ordinately regulated in developing seeds of common bean lacking phaseolin and major lectins. J Exp Bot 63:6283–6295PubMedPubMedCentralCrossRefGoogle Scholar
  51. 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 107:814–822PubMedCrossRefGoogle Scholar
  52. Livingstone D, Beilinson V, Kalyaeva M, Schmidt MA, Herman EM, Nielsen NC (2007) Reduction of protease inhibitor activity by expression of a mutant Bowman-Birk gene in soybean seed. Plant Mol Biol 64:397–408PubMedCrossRefGoogle Scholar
  53. López-Pedrouso M, Alonso J, Zapata C (2014a) Evidence for phosphorylation of the major seed storage protein of the common bean and its phosphorylation-dependent degradation during germination. Plant Mol Biol 84:415–428PubMedCrossRefGoogle Scholar
  54. López-Pedrouso M, Bernal J, Franco D, Zapata C (2014b) Evaluating two-dimensional electrophoresis profiles of the protein phaseolin as markers of genetic differentiation and seed protein quality in common bean (Phaseolus vulgaris L.). J Agric Food Chem 62:7200–7208PubMedCrossRefGoogle Scholar
  55. Louis S, Delobel B, Gressent F, Rahioui I, Quillien L, Vallier A, Rahbe Y (2004) Molecular and biological screening for insect-toxic seed albumins from four legume species. Plant Sci 167:705–714CrossRefGoogle Scholar
  56. Lovati MR, Manzoni C, Castiglioni S, Parolari A, Magni C, Duranti M (2012) Lupin seed gamma-conglutin lowers blood glucose in hyperglycaemic rats and increases glucose consumption of HepG2 cells. Br J Nutr 107:67–73PubMedCrossRefGoogle Scholar
  57. Magni C, Sessa F, Accardo E, Vanoni M, Morazzoni P, Scarafoni A, Duranti M (2004) Conglutin γ, a lupin seed protein, binds insulin in vitro and reduces plasma glucose levels of hyperglycemic rats. J Nutr Biochem 15:646–650PubMedCrossRefGoogle Scholar
  58. Majumdar S, Almeida IC, Arigi EA, Choi H, VerBerkmoes NC, Trujillo-Reyes J, Flores-Margez JP, White JC, Peralta-Videa JR, Gardea-Torresdey JL (2015) Environmental effects of nanoceria on seed production of common bean (Phaseolus vulgaris): a proteomic analysis. Environ Sci Technol 49:13283–13293PubMedCrossRefGoogle Scholar
  59. Marsolais F, Pajak A, Yin F, Taylor M, Gabriel M, Merino DM, Ma V, Kameka A, Vijayan P, Pham H, Huang S, Rivoal J, Bett K, Hernández-Sebastià C, Liu Q, Bertrand A, Chapman R (2010) Proteomic analysis of common bean seed with storage protein deficiency reveals up-regulation of sulfur-rich proteins and starch and raffinose metabolic enzymes, and down-regulation of the secretory pathway. J Proteomics 73:1587–1600PubMedCrossRefGoogle Scholar
  60. Mbogo KP, Davis J, Myers JR (2009) Transfer of the arcelin-phytohaemagglutinin-α amylase inhibitor seed protein locus from tepary bean (Phaseolus acutifolius A. Gray) to common bean (P. vulgaris L.). Biotechnology 8:285–295CrossRefGoogle Scholar
  61. McClean P, Myers J (1990) Pedigrees of dry bean cultivars, lines and PIs. Annu Rep Bean Improv Coop 33:xxv–xxxGoogle Scholar
  62. McClean PE, Mamidi S, McConnell M, Chikara S, Lee R (2010) Synteny mapping between common bean and soybean reveals extensive blocks of shared loci. BMC Genom 11:184CrossRefGoogle Scholar
  63. Mensack MM, Fitzgerald VK, Ryan EP, Lewis MR, Thompson HJ, Brick MA (2010) Evaluation of diversity among common beans (Phaseolus vulgaris L.) from two centers of domestication using ‘omics’ technologies. BMC Genom 11:686CrossRefGoogle Scholar
  64. Mirkov TE, Wahlstrom J, 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 26:1103–1113PubMedCrossRefGoogle Scholar
  65. Monaghan EK, Venkatachalam M, Seavy M, Beyer K, Sampson HA, Roux KH, Sathe SK (2008) Enzyme-linked immunosorbent assay (ELISA) for detection of sulfur-rich protein (SRP) in soybeans (Glycine max L.) and certain other edible plant seeds. J Agric Food Chem 56:765–777PubMedCrossRefGoogle Scholar
  66. Montoya CA, Lallès JP, Beebe S, Leterme P (2010) Phaseolin diversity as a possible strategy to improve the nutritional value of common beans (Phaseolus vulgaris). Food Res Int 43:443–449CrossRefGoogle Scholar
  67. Moore JG, Fuchs CA, Hata YS, Hicklin DJ, Colucci G, Chrispeels MJ, Feldman M (2000) A new lectin in red kidney beans called PvFRIL stimulates proliferation of NIH 3T3 cells expressing the Flt3 receptor. Biochim Biophys Acta 1475:216–224PubMedCrossRefGoogle Scholar
  68. Moreno J, Chrispeels MJ (1989) A lectin gene encodes the α-amylase inhibitor of the common bean. Proc Natl Acad Sci USA 86:7885–7889PubMedPubMedCentralCrossRefGoogle Scholar
  69. Muench SP, Rawson S, Eyraud V, Delmas AF, Da Silva P, Phillips C, Trinick J, Harrison MA, Gressent F, Huss M (2014) PA1b inhibitor binding to subunits c and e of the vacuolar ATPase reveals its insecticidal mechanism. J Biol Chem 289:16399–16408PubMedPubMedCentralCrossRefGoogle Scholar
  70. Muhling M, Gilroy J, Croy RRD (1997) Legumin proteins from seeds of Phaseolus vulgaris L. J Plant Physiol 150:489–492CrossRefGoogle Scholar
  71. Natarajan SS, Pastor-Corrales MA, Khan FH, Garrett WM (2013) Proteomic analysis of common bean (Phaseolus vulgaris L.) by two-dimensional gel electrophoresis and mass spectrometry. J Basic Appl Sci 9:424–437Google Scholar
  72. Ng DWK, Hall TC (2008) PvALF and FUS3 activate expression from the phaseolin promoter by different mechanisms. Plant Mol Biol 66:233–244CrossRefGoogle Scholar
  73. Ng DW, Chandrasekharan MB, Hall TC (2006) Ordered histone modifications are associated with transcriptional poising and activation of the phaseolin promoter. Plant Cell 18:119–132PubMedPubMedCentralCrossRefGoogle Scholar
  74. O′Rourke JA, Iniguez LP, Fu F, Bucciarelli B, Miller SS, Jackson SA, McClean PE, Li J, Dai X, Zhao PX, Hernandez G, Vance CP (2014) An RNA-Seq based gene expression atlas of the common bean. BMC Genom 15:866CrossRefGoogle Scholar
  75. Osborn TC, Bliss FA (1985) Effects of genetically removing lectin seed protein on horticultural and seed characteristics of common bean. J Am Soc Hortic Sci 110:484–488Google Scholar
  76. 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 L. Theor Appl Genet 71:847–855PubMedCrossRefGoogle Scholar
  77. Osborn TC, Alexander DC, Sun SSM, Cardona C, Bliss FA (1988) Insecticidal activity and lectin homology of arcelin seed protein. Science 240:207–210CrossRefGoogle Scholar
  78. Osborn TC, Hartweck LM, Harmsen RH, Vogelzang RD, Kmiecik KA, Bliss FA (2003) Registration of Phaseolus vulgaris genetic stocks with altered seed protein compositions. Crop Sci 43:1570–1571CrossRefGoogle Scholar
  79. Pandurangan S, Marsolais F (2017) Analysis of phaseolin copy number by quantitative PCR. Annu Rep Bean Improv Coop 60:107–108Google Scholar
  80. Pandurangan S, Sandercock M, Beyaert R, Conn KL, Hou A, Marsolais F (2015) Differential response to sulfur nutrition of two common bean genotypes differing in storage protein composition. Front Plant Sci 6:92PubMedPubMedCentralCrossRefGoogle Scholar
  81. Pandurangan S, Diapari M, Yin F, Munholland S, Perry G, Chapman BP, Huang S, Sparvoli F, Bollini R, Crosby W, Pauls KP, Marsolais F (2016) Genomic analysis of storage protein deficiency in genetically related lines of common bean (Phaseolus vulgaris). Front Plant Sci 7:389PubMedPubMedCentralCrossRefGoogle Scholar
  82. Parreira JR, Bouraada J, Fitzpatrick MA, Silvestre S, Bernardes da Silva A, Marques da Silva J, Almeida AM, Fevereiro P, Altelaar AFM, Araújo SS (2016) Differential proteomics reveals the hallmarks of seed development in common bean (Phaseolus vulgaris L.). J Proteomics 143:188–198PubMedCrossRefGoogle Scholar
  83. Prescott VE, Campbell PM, Moore A, Mattes J, Rothenberg ME, Foster PS, Higgins TJV, Hogan SP (2005) Transgenic expression of bean α-amylase inhibitor in peas results in altered structure and immunogenicity. J Agric Food Chem 53:9023–9030PubMedCrossRefGoogle Scholar
  84. Reinprecht Y, Luk-Labey SY, Yu K, Poysa VW, Rajcan I, Ablett GR, Peter Pauls K (2011) Molecular basis of seed lipoxygenase null traits in soybean line OX948. Theor Appl Genet 122:1247–1264PubMedCrossRefGoogle Scholar
  85. Schmidt MA, Hymowitz T, Herman EM (2015) Breeding and characterization of soybean Triple Null; a stack of recessive alleles of Kunitz trypsin inhibitor, soybean agglutinin, and P34 allergen nulls. Plant Breed 134:310–315CrossRefGoogle Scholar
  86. Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu S, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du J, Tian Z, Zhu L, Gill N, Joshi T, Libault M, Sethuraman A, Zhang XC, Shinozaki K, Nguyen HT, Wing RA, Cregan P, Specht J, Grimwood J, Rokhsar D, Stacey G, Shoemaker RC, Jackson SA (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183PubMedCrossRefGoogle Scholar
  87. Schmutz J, McClean PE, Mamidi S, Wu GA, Cannon SB, Grimwood J, Jenkins J, Shu S, Song Q, Chavarro C, Torres-Torres M, Geffroy V, Moghaddam SM, Gao D, Abernathy B, Barry K, Blair M, Brick MA, Chovatia M, Gepts P, Goodstein DM, Gonzales M, Hellsten U, Hyten DL, Jia G, Kelly JD, Kudrna D, Lee R, Richard MM, Miklas PN, Osorno JM, Rodrigues J, Thareau V, Urrea CA, Wang M, Yu Y, Zhang M, Wing RA, Cregan PB, Rokhsar DS, Jackson SA (2014) A reference genome for common bean and genome-wide analysis of dual domestications. Nat Genet 46:707–713PubMedCrossRefGoogle Scholar
  88. Severin AJ, Woody JL, Bolon YT, Joseph B, Diers BW, Farmer AD, Muehlbauer GJ, Nelson RT, Grant D, Specht JE, Graham MA, Cannon SB, May GD, Vance CP, Shoemaker RC (2010) RNA-seq atlas of Glycine max: a guide to the soybean transcriptome. BMC Plant Biol 10:160PubMedPubMedCentralCrossRefGoogle Scholar
  89. Singh SP, Gepts P, Debouck DG (1991) Races of common bean (Phaseolus vulgaris, Fabaceae). Econ Bot 45:379–396CrossRefGoogle Scholar
  90. Slightom JL, Sun SM, Hall TC (1983) Complete nucleotide sequence of a French bean storage protein gene: phaseolin. Proc Natl Acad Sci USA 80:1897–1901PubMedPubMedCentralCrossRefGoogle Scholar
  91. Slightom JL, Drong RF, Klassy RC, Hoffman LM (1985) Nucleotide sequences from phaseolin cDNA clones: the major storage proteins from Phaseolus vulgaris are encoded by two unique gene families. Nucleic Acids Res 13:6483–6498PubMedPubMedCentralCrossRefGoogle Scholar
  92. Sparvoli F, Bollini R, Cominelli E (2015) Nutritional value. In: De Ron AM (ed) Grain Legumes. Handbook of Plant Breeding, vol 10. Springer Science+Business Media, New York, pp 291–325Google Scholar
  93. Staswick PE, Hermodson MA, Nielsen NC (1984) Identification of the cystines which link the acidic and basic components of the glycinin subunits. J Biol Chem 259:13431–13435PubMedGoogle Scholar
  94. Sturm A, Van Kuik JA, Vliegenthart JF, Chrispeels MJ (1987) Structure, position, and biosynthesis of the high mannose and the complex oligosaccharide side chains of the bean storage protein phaseolin. J Biol Chem 262:13392–13403PubMedGoogle Scholar
  95. Sundaram S, Kertbundit S, Shakirov EV, Iyer LM, Juricek M, Hall TC (2013) Gene networks and chromatin and transcriptional regulation of the phaseolin promoter in Arabidopsis. Plant Cell 25:2601–2617PubMedPubMedCentralCrossRefGoogle Scholar
  96. Talbot DR, Adang MJ, Slightom JL, Hall TC (1984) Size and organization of a multigene family encoding phaseolin, the major seed storage protein of Phaseolus vulgaris L. Mol Gen Genet 198:42–49CrossRefGoogle Scholar
  97. Tolleter D, Jaquinod M, Mangavel C, Passirani C, Saulnier P, Manon S, Teyssier E, Payet N, Avelange-Macherel M-H, Macherel D (2007) Structure and function of a mitochondrial late embryogenesis abundant protein are revealed by desiccation. Plant Cell 19:1580–1589PubMedPubMedCentralCrossRefGoogle Scholar
  98. Tsubokura Y, Hajika M, Kanamori H, Xia Z, Watanabe S, Kaga A, Katayose Y, Ishimoto M, Harada K (2012) The β-conglycinin deficiency in wild soybean is associated with the tail-to-tail inverted repeat of the α-subunit genes. Plant Mol Biol 78:301–309PubMedCrossRefGoogle Scholar
  99. van der Geest AH, Hall TC (1996) A 68 bp element of the β-phaseolin promoter functions as a seed-specific enhancer. Plant Mol Biol 32:579–588PubMedCrossRefGoogle Scholar
  100. Vigeolas H, Chinoy C, Zuther E, Blessington B, Geigenberger P, Domoney C (2008) Combined metabolomic and genetic approaches reveal a link between the polyamine pathway and albumin 2 in developing pea seeds. Plant Physiol 146:74–82PubMedPubMedCentralCrossRefGoogle Scholar
  101. Vitale A, Bollini R (1995) Legume storage proteins. In: Kigel J, Galili G (eds) Seed Development and Germination. Marcel Dekker, New York, pp 73–102Google Scholar
  102. Vlasova A, Capella-Gutierrez S, Rendon-Anaya M, Hernandez-Onate M, Minoche AE, Erb I, Camara F, Prieto-Barja P, Corvelo A, Sanseverino W, Westergaard G, Dohm JC, Pappas GJ Jr, Saburido-Alvarez S, Kedra D, Gonzalez I, Cozzuto L, Gomez-Garrido J, Aguilar-Moron MA, Andreu N, Aguilar OM, Garcia-Mas J, Zehnsdorf M, Vazquez MP, Delgado-Salinas A, Delaye L, Lowy E, Mentaberry A, Vianello-Brondani RP, Garcia JL, Alioto T, Sanchez F, Himmelbauer H, Santalla M, Notredame C, Gabaldon T, Herrera-Estrella A, Guigo R (2016) Genome and transcriptome analysis of the Mesoamerican common bean and the role of gene duplications in establishing tissue and temporal specialization of genes. Genome Biol 17:32PubMedPubMedCentralCrossRefGoogle Scholar
  103. Voelker TA, Staswick P, Chrispeels MJ (1986) Molecular analysis of two phytohemagglutinin genes and their expression in Phaseolus vulgaris cv. Pinto, a lectin-deficient cultivar of the bean. EMBO J 5:3075–3082PubMedPubMedCentralGoogle Scholar
  104. Voelker TA, Moreno J, Chrispeels MJ (1990) Expression analysis of a pseudogene in transgenic tobacco: a frameshift mutation prevents mRNA accumulation. Plant Cell 2:255–261PubMedPubMedCentralCrossRefGoogle Scholar
  105. Wato S, Kamei K, Arakawa T, Philo JS, Wen J, Hara S, Yamaguchi H (2000) A chimera-like α-amylase inhibitor suggesting the evolution of Phaseolus vulgaris α-amylase inhibitor. J Biochem 128:139–144Google Scholar
  106. Wilson KA, Laskowski M (1973) Isolation of three isoinhibitors of trypsin from garden bean, Phaseolus vulgaris, having either lysine or arginine at the reactive site. J Biol Chem 248:756–762PubMedGoogle Scholar
  107. Wilson KA, Laskowski M (1975) The partial amino acid sequence of trypsin inhibitor II from garden bean, Phaseolus vulgaris, with location of the trypsin and elastase-reactive sites. J Biol Chem 250:4261–4267PubMedGoogle Scholar
  108. Yamauchi F, Sato K, Yamagishi T (1984) Isolation and partial characterization of a salt-extractable globulin from soybean seeds. Agric Biol Chem 48:645–650Google Scholar
  109. Yin F, Pajak A, Chapman R, Sharpe A, Huang S, Marsolais F (2011) Analysis of common bean expressed sequence tags identifies sulfur metabolic pathways active in seed and sulfur-rich proteins highly expressed in the absence of phaseolin and major lectins. BMC Genom 12:268CrossRefGoogle Scholar
  110. Yoshizawa T, Shimizu T, Yamabe M, Taichi M, Nishiuchi Y, Shichijo N, Unzai S, Hirano H, Sato M, Hashimoto H (2011) Crystal structure of basic 7S globulin, a xyloglucan-specific endo-β-1,4-glucanase inhibitor protein-like protein from soybean lacking inhibitory activity against endo-β-glucanase. FEBS J 278:1944–1954PubMedCrossRefGoogle Scholar
  111. Zaugg I, Magni C, Panzeri D, Daminati MG, Bollini R, Benrey B, Bacher S, Sparvoli F (2013) 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 126:647–661PubMedCrossRefGoogle Scholar

Copyright information

© Crown Copyright 2017

Authors and Affiliations

  • Jaya Joshi
    • 1
  • Sudhakar Pandurangan
    • 1
  • Marwan Diapari
    • 2
  • Frédéric Marsolais
    • 1
    Email author
  1. 1.Department of BiologyUniversity of Western Ontario; and Genomics and Biotechnology, London Research and Development Centre, Agriculture and Agri-Food CanadaLondonCanada
  2. 2.Genomics and BiotechnologyLondon Research and Development Centre, Agriculture and Agri-Food CanadaLondonCanada

Personalised recommendations