Seed Storage Proteins of Faba Bean (Vicia faba L): Current Status and Prospects for Genetic Improvement

Journal of Agricultural and Food Chemistry

Volumn 66, Issue 48, 2018, Pages 12617-12626

  Warsame, Ahmed O ^a   O'Sullivan, Donal M ^a   Tosi, Paola ^a  

^a UNIVERSITY OF READING   (United Kingdom)

Author keywords

genetic improvement; legumin and vicilin; storage proteins; sustainability; Vicia faba

Indexed keywords

CROPS; FOOD STORAGE; GENES; SUSTAINABLE DEVELOPMENT;

ANIMAL NUTRITIONS; COMPLEX RELATIONSHIPS; GENETIC IMPROVEMENTS; GENETIC INFORMATION; SEED STORAGE PROTEINS; STORAGE PROTEINS; VICIA FABA; VICILIN;

PROTEINS;

SEED STORAGE PROTEIN;

CHEMISTRY; GENETIC VARIATION; GENETICS; METABOLISM; PLANT SEED; VICIA FABA;

GENETIC VARIATION; SEED STORAGE PROTEINS; SEEDS; VICIA FABA;

EID: 85058062194     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.8b04992     Document Type: Article

References (108)

1. Henchion, M.; Hayes, M.; Mullen, A.; Fenelon, M.; Tiwari, B. Future Protein Supply and Demand: Strategies and Factors Influencing a Sustainable Equilibrium. Foods 2017, 6, 53, 10.3390/foods6070053
2. Young, V. R.; Pellett, P. L. Plant proteins in relation to human protein and amino acid nutrition. Am. J. Clin. Nutr. 1994, 59, 1203S-1212S, 10.1093/ajcn/59.5.1203S
3. Smýkal, P.; Coyne, C. J.; Ambrose, M. J.; Maxted, N.; Schaefer, H.; Blair, M. W.; Berger, J.; Greene, S. L.; Nelson, M. N.; Besharat, N.; Vymyslický, T.; Toker, C.; Saxena, R. K.; Roorkiwal, M.; Pandey, M. K.; Hu, J.; Li, Y. H.; Wang, L. X.; Guo, Y.; Qiu, L. J.; Redden, R. J.; Varshney, R. K. Legume Crops Phylogeny and Genetic Diversity for Science and Breeding. Crit. Rev. Plant Sci. 2015, 34, 43-104, 10.1080/07352689.2014.897904
4. Foyer, C. H.; Lam, H. M.; Nguyen, H. T.; Siddique, K. H.; Varshney, R. K.; Colmer, T. D.; Cowling, W.; Bramley, H.; Mori, T. A.; Hodgson, J. M.; Cooper, J. W.; Miller, A. J.; Kunert, K.; Vorster, J.; Cullis, C.; Ozga, J. A.; Wahlqvist, M. L.; Liang, Y.; Shou, H.; Shi, K.; Yu, J.; Fodor, N.; Kaiser, B. N.; Wong, F. L.; Valliyodan, B.; Considine, M. J. Neglecting legumes has compromised human health and sustainable food production. Nat. Plants 2016, 2, 16112, 10.1038/nplants.2016.112
5. Duc, G. Faba bean (Vicia faba L). Field Crops Res. 1997, 53, 99-109, 10.1016/S0378-4290(97)00025-7
6. Tanno, K.-i.; Willcox, G. The origins of cultivation of Cicer arietinum L. and Vicia faba L.: early finds from Tell el-Kerkh, north-west Syria, late 10th millennium b.p. Veg Hist Archaeobot 2006, 15, 197-204, 10.1007/s00334-005-0027-5
7. Cubero, J. I. On the evolution of Vicia faba L. Theor. Appl. Genet. 1974, 45, 47-51, 10.1007/BF00283475
8. Vilarino, M.; Metayer, J. P.; Crepon, K.; Duc, G. Effects of varying vicine, convicine and tannin contents of faba bean seeds (Vicia faba L.) on nutritional values for broiler chicken. Anim. Feed Sci. Technol. 2009, 150, 114-121, 10.1016/j.anifeedsci.2008.08.001
9. Kaskinen, T.; Lähteenoja, S.; Sokero, M.; Suomela, I. Strategic Business Examples from Finland: The Growth of the Smartup Industry. Factor X: Challenges, Implementation Strategies and Examples for a Sustainable Use of Natural Resources 2018, 32, 325-333, 10.1007/978-3-319-50079-9-22
10. Coda, R.; Varis, J.; Verni, M.; Rizzello, C. G.; Katina, K. Improvement of the protein quality of wheat bread through faba bean sourdough addition. LWT-Food Sci. Technol. 2017, 82, 296-302, 10.1016/j.lwt.2017.04.062
11. Rizzello, C. G.; Verni, M.; Koivula, H.; Montemurro, M.; Seppa, L.; Kemell, M.; Katina, K.; Coda, R.; Gobbetti, M. Influence of fermented faba bean flour on the nutritional, technological and sensory quality of fortified pasta. Food Funct. 2017, 8, 860-871, 10.1039/C6FO01808D
12. VTT. Gluten-free faba bean for bread and pasta. VTT Technical Research Centre of Finland, LTD: 2014; https://www.vttresearch.com/media/news/gluten-free-faba-bean-for-bread-and-pasta (accessed July 25, 2018).
13. Cernay, C.; Pelzer, E.; Makowski, D. A global experimental dataset for assessing grain legume production. Sci. Data 2016, 3, 160084, 10.1038/sdata.2016.84
14. Baddeley, J.; Jones, S.; Topp, C.; Watson, C.; Helming, J.; Stoddard, F. Biological nitrogen fixation (BNF) by legume crops in Europe. Legume Futures Report 1.5; Legume Futures: 2013; www.legumefutures.de (accessed January 4, 2018).
15. Jensen, E. S.; Peoples, M. B.; Hauggaard-Nielsen, H. Faba bean in cropping systems. Field Crop Res. 2010, 115, 203-216, 10.1016/j.fcr.2009.10.008
16. Köpke, U.; Nemecek, T. Ecological services of faba bean. Field Crops Res. 2010, 115, 217-233, 10.1016/j.fcr.2009.10.012
17. Perez-Maldonado, R. A.; Mannion, P. F.; Farrell, D. J. Optimum inclusion of field peas, faba beans, chick peas and sweet lupins in poultry diets. I. Chemical composition and layer experiments. Br. Poult. Sci. 1999, 40, 667-673, 10.1080/00071669987061
18. Koivunen, E.; Tuunainen, P.; Valkonen, E.; Rossow, L.; Valaja, J. Use of faba beans (Vicia faba L.) in diets of laying hens. Agric. Food Sci. 2014, 23, 165-172, 10.23986/afsci.41329
19. Lessire, M.; Gallo, V.; Prato, M.; Akide-Ndunge, O.; Mandili, G.; Marget, P.; Arese, P.; Duc, G. Effects of faba beans with different concentrations of vicine and convicine on egg production, egg quality and red blood cells in laying hens. Animal 2017, 11, 1270-1278, 10.1017/S1751731116002688
20. Kawashima, H.; Bazin, M. J.; Lynch, J. M. A modelling study of world protein supply and nitrogen fertilizer demand in the 21st century. Environ. Conserv. 1997, 24, 50-57, 10.1017/S037689299700009X
21. Speedy, A. W. Overview of world feed protein needs and supply. In Proceedings of the FAO Animal Production and Health (FAO), Protein Sources for the Animal Feed Industry, 2004; FAO: Rome, Italy, 2004.
22. Chiari, N. Food Security. The Challenge of Nutrition in the New Century. Relations. Beyond Anthropocentrism 2017, 5, 145-156, 10.7358/rela-2017-002-chia
23. WHO/FAO/UNU. Protein and amino acid requirements in human nutrition. WHO Technol. Rep. Ser.; World Health Organization: 2007; pp 1-265. and back cover.
24. Balyan, H. S.; Gupta, P. K.; Kumar, S.; Dhariwal, R.; Jaiswal, V.; Tyagi, S.; Agarwal, P.; Gahlaut, V.; Kumari, S. Genetic improvement of grain protein content and other health-related constituents of wheat grain. Plant Breed. 2013, 132, 446-457, 10.1111/pbr.12047
25. de Visser, C. L. M.; Schreuder, R.; Stoddard, F. The EU's dependency on soya bean import for the animal feed industry and potential for EU produced alternatives. OCL: Oilseeds Fats, Crops Lipids 2014, 21, D407, 10.1051/ocl/2014021
26. Statista. Meat consumption and vegetarianism in Europe-Statistics and Facts. https://www.statista.com/topics/3345/meat-consumption-and-vegetarianism-in-europe/ (accessed December 25, 2018).
27. de Boer, J.; Aiking, H. Prospects for pro-environmental protein consumption in Europe: Cultural, culinary, economic and psychological factors. Appetite 2018, 121, 29-40, 10.1016/j.appet.2017.10.042
28. Griffiths, D. W.; Lawes, D. A. Variation in the crude protein content of field beans (Vicia faba L.) in relation to the possible improvement of the protein content of the crop. Euphytica 1978, 27, 487-495, 10.1007/BF00043174
29. Sjödin, J. Protein Quantity and Quality in Vicia Faba. In Faba Bean Improvement: Proceedings of the Faba Bean Conference, Cairo, Egypt, March 7-11, 1981, Hawtin, G., Webb, C., Eds.; Springer Netherlands: Dordrecht, 1982; pp 319-331.
30. Frauen, M.; Röbbelen, G.; Ebmeyer, E. Quantitative Measurement of Quality Determining Constituents in Seeds of Different Inbred Lines from A World Collection of Vicia Faba. In Vicia faba: Agronomy, Physiology and Breeding, Hebblethwaite, P. D., Dawkins, T. C. K., Heath, M. C., Lockwood, G., Eds.; Springer-Science+Business Media, B.V.: Brussels-Luxembourg, 1984; Vol. 10, pp 279-287.
31. Crépon, K.; Marget, P.; Peyronnet, C.; Carrouée, B.; Arese, P.; Duc, G. Nutritional value of faba bean (Vicia faba L.) seeds for feed and food. Field Crops Res. 2010, 115, 329-339, 10.1016/j.fcr.2009.09.016
32. Yu, E.-M.; Zhang, H.-F.; Li, Z.-F.; Wang, G.-J.; Wu, H.-K.; Xie, J.; Yu, D.-G.; Xia, Y.; Zhang, K.; Gong, W.-B. Proteomic signature of muscle fibre hyperplasia in response to faba bean intake in grass carp. Sci. Rep. 2017, 7, 45950, 10.1038/srep45950
33. Makkar, H. P. S.; Becker, K.; Abel, H.; Pawelzik, E. Nutrient contents, rumen protein degradability and antinutritional factors in some colour- and white-flowering cultivars of Vicia faba beans. J. Sci. Food Agric. 1997, 75, 511-520, 10.1002/(SICI)1097-0010(199712)75:4<511::AID-JSFA907>3.0.CO;2-M
34. Rizzello, C. G.; Losito, I.; Facchini, L.; Katina, K.; Palmisano, F.; Gobbetti, M.; Coda, R. Degradation of vicine, convicine and their aglycones during fermentation of faba bean flour. Sci. Rep. 2016, 6, 32452, 10.1038/srep32452
35. Coda, R.; Melama, L.; Rizzello, C. G.; Curiel, J. A.; Sibakov, J.; Holopainen, U.; Pulkkinen, M.; Sozer, N. Effect of air classification and fermentation by Lactobacillus plantarum VTT E-133328 on faba bean (Vicia faba L.) flour nutritional properties. Int. J. Food Microbiol. 2015, 193, 34-42, 10.1016/j.ijfoodmicro.2014.10.012
36. Gallo, V.; Skorokhod, O. A.; Simula, L. F.; Marrocco, T.; Tambini, E.; Schwarzer, E.; Marget, P.; Duc, G.; Arese, P. No red blood cell damage and no hemolysis in G6PD-deficient subjects after ingestion of low vicine/convicine Vicia faba seeds. Blood 2018, 131, 1621-1625, 10.1182/blood-2017-09-806364
37. Khazaei, H.; Purves, R. W.; Song, M.; Stonehouse, R.; Bett, K. E.; Stoddard, F. L.; Vandenberg, A. Development and validation of a robust, breeder-friendly molecular marker for the vc-locus in faba bean. Mol. Breed. 2017, 37, 140, 10.1007/s11032-017-0742-5
38. Webb, A.; Cottage, A.; Wood, T.; Khamassi, K.; Hobbs, D.; Gostkiewicz, K.; White, M.; Khazaei, H.; Ali, M.; Street, D.; Duc, G.; Stoddard, F. L.; Maalouf, F.; Ogbonnaya, F. C.; Link, W.; Thomas, J.; O'Sullivan, D. M. A SNP-based consensus genetic map for synteny-based trait targeting in faba bean (Vicia faba L.). Plant Biotechnol J. 2016, 14, 177-85, 10.1111/pbi.12371
39. O'Sullivan, D. M.; Angra, D. Advances in Faba Bean Genetics and Genomics. Front. Genet. 2016, 7, 150, 10.3389/fgene.2016.00150
40. Duc, G.; Aleksić, J. M.; Marget, P.; Mikic, A.; Paull, J.; Redden, R. J.; Sass, O.; Stoddard, F. L.; Vandenberg, A.; Vishnyakova, M.; Torres, A. M.; Ron, A. M. D. Faba Bean. Grain Legumes 2015, 10, 141-178, 10.1007/978-1-4939-2797-5-5
41. Patil, G.; Mian, R.; Vuong, T.; Pantalone, V.; Song, Q.; Chen, P.; Shannon, G. J.; Carter, T. C.; Nguyen, H. T. Molecular mapping and genomics of soybean seed protein: a review and perspective for the future. Theor. Appl. Genet. 2017, 130, 1975-1991, 10.1007/s00122-017-2955-8
42. Liu, Y.; Wu, X.; Hou, W.; Li, P.; Sha, W.; Tian, Y. Structure and function of seed storage proteins in faba bean (Vicia faba L.). 3 Biotech 2017, 7, 74, 10.1007/s13205-017-0691-z
43. Shewry, P. R.; Casey, R.; Shewry, P. R.; Casey, R. Seed Proteins. Seed Proteins 1999, 1-10, 10.1007/978-94-011-4431-5-1
44. Joshi, J.; Pandurangan, S.; Diapari, M.; Marsolais, F.; Pérez de la Vega, M.; Santalla, M.; Marsolais, F. Comparison of Gene Families: Seed Storage and Other Seed Proteins. The Common Bean Genome 2017, 201-217, 10.1007/978-3-319-63526-2-10
45. Müntz, K.; Horstmann, C.; Schlesier, B.; Shewry, P. R.; Casey, R. Vicia globulins. Seed Proteins 1999, 259-284, 10.1007/978-94-011-4431-5-12
46. Kesari, P.; Sharma, A.; Katiki, M.; Kumar, P.; Gurjar, B. R.; Tomar, S.; Sharma, A. K.; Kumar, P. et al. Structural, Functional and Evolutionary Aspects of Seed Globulins. Protein Pept. Lett. 2017, 24, 267-277, 10.2174/0929866523666161220112641
47. Meng, G. T.; Ma, C. Y. Thermal properties of Phaseolus angularis (red bean) globulin. Food Chem. 2001, 73, 453-460, 10.1016/S0308-8146(00)00329-0
48. Kimura, A.; Fukuda, T.; Zhang, M.; Motoyama, S.; Maruyama, N.; Utsumi, S. Comparison of Physicochemical Properties of 7S and 11S Globulins from Pea, Fava Bean, Cowpea, and French Bean with Those of Soybean-French Bean 7S Globulin Exhibits Excellent Properties. J. Agric. Food Chem. 2008, 56, 10273-10279, 10.1021/jf801721b
49. Heng, L.; van Koningsveld, G. A.; Gruppen, H.; van Boekel, M. A. J. S.; Vincken, J. P.; Roozen, J. P.; Voragen, A. G. J. Protein-flavour interactions in relation to development of novel protein foods. Trends Food Sci. Technol. 2004, 15, 217-224, 10.1016/j.tifs.2003.09.018
50. Baumlein, H.; Wobus, U.; Pustell, J.; Kafatos, F. C. The legumin gene family: structure of a B type gene of Vicia faba and a possible legumin gene specific regulatory element. Nucleic Acids Res. 1986, 14, 2707-2720, 10.1093/nar/14.6.2707
51. Tucci, M.; Capparelli, R.; Costa, A.; Rao, R. Molecular heterogeneity and genetics of Vicia faba seed storage proteins. Theor. Appl. Genet. 1991, 81, 50-58, 10.1007/BF00226111
52. Le Signor, C.; Gallardo, K.; Prosperi, J. M.; Salon, C.; Quillien, L.; Thompson, R.; Duc, G. Genetic diversity for seed protein composition in Medicago truncatula. Plant Genet. Resour. 2005, 3, 59-71, 10.1079/PGR200562
53. O'Kane, F. E.; Happe, R. P.; Vereijken, J. M.; Gruppen, H.; van Boekel, M. A. J. S. Characterization of Pea Vicilin. 1. Denoting Convicilin as the α-Subunit of the Pisum Vicilin Family. J. Agric. Food Chem. 2004, 52, 3141-3148, 10.1021/jf035104i
54. Krishnan, H. B.; Natarajan, S. S.; Oehrle, N. W.; Garrett, W. M.; Darwish, O. Proteomic Analysis of Pigeonpea (Cajanus cajan) Seeds Reveals the Accumulation of Numerous Stress-Related Proteins. J. Agric. Food Chem. 2017, 65, 4572-4581, 10.1021/acs.jafc.7b00998
55. Boehm, J. D.; Nguyen, V.; Tashiro, R. M.; Anderson, D.; Shi, C.; Wu, X.; Woodrow, L.; Yu, K.; Cui, Y.; Li, Z. Genetic mapping and validation of the loci controlling 7S α′ and 11S A-type storage protein subunits in soybean [Glycine max (L.) Merr.]. Theor. Appl. Genet. 2018, 131, 659-671, 10.1007/s00122-017-3027-9
56. Galili, G.; Amir, R. Fortifying plants with the essential amino acids lysine and methionine to improve nutritional quality. Plant Biotechnol. J. 2013, 11, 211-222, 10.1111/pbi.12025
57. Kwanyuen, P.; Pantalone, V. R.; Burton, J. W.; Wilson, R. F. A new approach to genetic alteration of soybean protein composition and quality. J. Am. Oil Chem. Soc. 1997, 74, 983-987, 10.1007/s11746-997-0015-2
58. Jackson, P.; Boulter, D.; Thurman, D. A. A comparison of some properties of vicilin and legumin isolated from seeds of Pisum sativum, Vicia faba and Cicer arietinum. New Phytol. 1969, 68, 25-33, 10.1111/j.1469-8137.1969.tb06416.x
59. De Pace, C.; Delre, V.; Scarascia Mugnozza, G. T.; Maggini, E.; Cremonini, R.; Frediani, M.; Cionini, P. G. Legumin of Vicia faba major: accumulation in developing cotyledons, purification, mRNA characterization and chromosomal location of coding genes. Theor. Appl. Genet. 1991, 83, 17-23, 10.1007/BF00229221
60. Abirached-Darmency, M.; Dessaint, F.; Benlicha, E.; Schneider, C. Biogenesis of protein bodies during vicilin accumulation in Medicago truncatula immature seeds. BMC Res. Notes 2012, 5, 409-409, 10.1186/1756-0500-5-409
61. Gallardo, K.; Le Signor, C.; Vandekerckhove, J.; Thompson, R. D.; Burstin, J. Proteomics of Medicago truncatula seed development establishes the time frame of diverse metabolic processes related to reserve accumulation. Plant Physiol. 2003, 133, 664-682, 10.1104/pp.103.025254
62. Rubio, L. A.; Perez, A.; Ruiz, R.; Guzman, M. A.; Aranda-Olmedo, I.; Clemente, A. Characterization of pea (Pisum sativum) seed protein fractions. J. Sci. Food Agric. 2014, 94, 280-287, 10.1002/jsfa.6250
63. Krishnan, H. B.; Bennett, J. O.; Kim, W.-S.; Krishnan, A. H.; Mawhinney, T. P. Nitrogen Lowers the Sulfur Amino Acid Content of Soybean (Glycine max [L.] Merr.) by Regulating the Accumulation of Bowman-Birk Protease Inhibitor. J. Agric. Food Chem. 2005, 53, 6347-6354, 10.1021/jf050510i
64. Rolletschek, H.; Hosein, F.; Miranda, M.; Heim, U.; Gotz, K. P.; Schlereth, A.; Borisjuk, L.; Saalbach, I.; Wobus, U.; Weber, H. Ectopic expression of an amino acid transporter (VfAAP1) in seeds of Vicia narbonensis and pea increases storage proteins. Plant Physiol. 2005, 137, 1236-1249, 10.1104/pp.104.056523
65. Lafiandra, D.; Polignano, G. B.; Filippetti, A.; Porceddu, E. Genetic variability for protein content and S-aminoacids in broad-beans (Vicia faba L.). Kulturpflanze 1981, 29, 115-127, 10.1007/BF02014742
66. Schumacher, H.; Paulsen, H. M.; Gau, A. E.; Link, W.; Jurgens, H. U.; Sass, O.; Dieterich, R. Seed protein amino acid composition of important local grain legumes Lupinus angustifolius L., Lupinus luteus L., Pisum sativum L. and Vicia faba L. Plant Breed. 2011, 130, 156-164, 10.1111/j.1439-0523.2010.01832.x
67. Fuchs, J.; Schubert, I. Localization of seed protein genes on metaphase chromosomes of Vicia faba via fluorescencein situ hybridization. Chromosome Res. 1995, 3, 94-100, 10.1007/BF00710669
68. Rerie, W. G.; Whitecross, M.; Higgins, T. J. V. Developmental and environmental regulation of pea legumin genes in transgenic tobacco. Mol. Gen. Genet. 1991, 225, 148-157, 10.1007/BF00282653
69. Heim, U.; Schubert, R.; Baumlein, H.; Wobus, U. The legumin gene family: structure and evolutionary implications of Vicia faba B-type genes and pseudogenes. Plant Mol. Biol. 1989, 13, 653-63, 10.1007/BF00016020
70. Weschke, W.; Bassüner, R.; Van Hai, N.; Czihal, A.; Baümlein, H.; Wobus, U. The structure of a Vicia faba vicilin gene. Biochem. Physiol. Pflanz. 1988, 183, 233-242, 10.1016/S0015-3796(88)80107-0
71. Macas, J.; Weschke, W.; Bäumlein, H.; Pich, U.; Houben, A.; Wobus, U.; Schubert, I. Localization of vicilin genes via polymerase chain reaction on microisolated field bean chromosomes. Plant J. 1993, 3, 883-886, 10.1111/j.1365-313X.1993.00883.x
72. Fuchs, J.; Joos, S.; Licheter, P.; Schubert, I. Localization of Vicilin Genes on Field Bean Chromosome II by Fluorescent in situ Hybridization. J. Hered. 1994, 85, 487-488, 10.1093/oxfordjournals.jhered.a111506
73. Le Signor, C.; Aimé, D.; Bordat, A.; Belghazi, M.; Labas, V.; Gouzy, J.; Young, N. D.; Prosperi, J.-M.; Leprince, O.; Thompson, R. D.; Buitink, J.; Burstin, J.; Gallardo, K. Genome-wide association studies with proteomics data reveal genes important for synthesis, transport and packaging of globulins in legume seeds. New Phytol. 2017, 214, 1597-1613, 10.1111/nph.14500
74. Bourgeois, M.; Jacquin, F.; Savois, V.; Sommerer, N.; Labas, V.; Henry, C.; Burstin, J. Dissecting the proteome of pea mature seeds reveals the phenotypic plasticity of seed protein composition. Proteomics 2009, 9, 254-271, 10.1002/pmic.200700903
75. Qi, Z.; Zhang, Z.; Wang, Z.; Yu, J.; Qin, H.; Mao, X.; Jiang, H.; Xin, D.; Yin, Z.; Zhu, R.; Liu, C.; Yu, W.; Hu, Z.; Wu, X.; Liu, J.; Chen, Q. Meta-analysis and transcriptome profiling reveal hub genes for soybean seed storage composition during seed development. Plant, Cell Environ. 2018, 0, 1-19, 10.1111/pce.13175
76. Verdier, J.; Thompson, R. D. Transcriptional regulation of storage protein synthesis during dicotyledon seed filling. Plant Cell Physiol. 2008, 49, 1263-1271, 10.1093/pcp/pcn116
77. Mori, T.; Maruyama, N.; Nishizawa, K.; Higasa, T.; Yagasaki, K.; Ishimoto, M.; Utsumi, S. The composition of newly synthesized proteins in the endoplasmic reticulum determines the transport pathways of soybean seed storage proteins. Plant J. 2004, 40, 238-249, 10.1111/j.1365-313X.2004.02204.x
78. Panitz, R.; Borisjuk, L.; Manteuffel, R.; Wobus, U. Transient expression of storage-protein genes during early embryogenesis of Vicia faba: synthesis and metabolization of vicilin and legumin in the embryo, suspensor and endosperm. Planta 1995, 196, 765-774, 10.1007/BF01106772
79. Wang, X. D.; Song, Y.; Sheahan, M. B.; Garg, M. L.; Rose, R. J. From embryo sac to oil and protein bodies: embryo development in the model legume Medicago truncatula. New Phytol. 2012, 193, 327-338, 10.1111/j.1469-8137.2011.03925.x
80. Zhang, L.; Garneau, M. G.; Majumdar, R.; Grant, J.; Tegeder, M. Improvement of pea biomass and seed productivity by simultaneous increase of phloem and embryo loading with amino acids. Plant J. 2015, 81, 134-146, 10.1111/tpj.12716
81. Golombek, S.; Rolletschek, H.; Wobus, U.; Weber, H. Control of storage protein accumulation during legume seed development. J. Plant Physiol. 2001, 158, 457-464, 10.1078/0176-1617-00357
82. Peng, B.; Kong, H.; Li, Y.; Wang, L.; Zhong, M.; Sun, L.; Gao, G.; Zhang, Q.; Luo, L.; Wang, G.; Xie, W.; Chen, J.; Yao, W.; Peng, Y.; Lei, L.; Lian, X.; Xiao, J.; Xu, C.; Li, X.; He, Y. OsAAP6 functions as an important regulator of grain protein content and nutritional quality in rice. Nat. Commun. 2014, 5, 4847, 10.1038/ncomms5847
83. Ramaekers, L.; Galeano, C. H.; Garzón, N.; Vanderleyden, J.; Blair, M. W. Identifying quantitative trait loci for symbiotic nitrogen fixation capacity and related traits in common bean. Mol. Breed. 2013, 31, 163-180, 10.1007/s11032-012-9780-1
84. Bourion, V.; Rizvi, S. M. H.; Fournier, S.; de Larambergue, H.; Galmiche, F.; Marget, P.; Duc, G.; Burstin, J. Genetic dissection of nitrogen nutrition in pea through a QTL approach of root, nodule, and shoot variability. Theor. Appl. Genet. 2010, 121, 71-86, 10.1007/s00122-010-1292-y
85. Picard, J. Some results dealing with breeding protein content in Vicia faba L. In Protein quality from leguminous crops; ECSC-EEC-EAEC: Brussels-Luxembourg, 1977; Vol. EUR 5686 EN, pp 339-347.
86. Griffiths, D. W. An Assessment of the Potential for Improving the Nutritive Value of Field Beans (Vicia Faba)-A Progress Report. In Vicia faba: Agronomy, Physiology and Breeding, Hebblethwaite, P. D., Dawkins, T. C. K., Heath, M. C., Lockwood, G., Eds.; Springer-Science+Business Media, B.V.: Brussels-Luxembourg, 1984; Vol. 10, pp 271-278.
87. Chen, Y.; Lübberstedt, T. Molecular basis of trait correlations. Trends Plant Sci. 2010, 15, 454-461, 10.1016/j.tplants.2010.05.004
88. Munier-Jolain, N.; Larmure, A.; Salon, C. Determinism of carbon and nitrogen reserve accumulation in legume seeds. C. R. Biol. 2008, 331, 780-787, 10.1016/j.crvi.2008.07.020
89. Egle, K.; Beschow, H.; Merbach, W. Nitrogen allocation in barley: Relationships between amino acid transport and storage protein synthesis during grain filling. Can. J. Plant Sci. 2015, 95, 451-459, 10.4141/cjps2013-324
90. Bogard, M.; Allard, V.; Brancourt-Hulmel, M.; Heumez, E.; Machet, J.-M.; Jeuffroy, M.-H.; Gate, P.; Martre, P.; Le Gouis, J. Deviation from the grain protein concentration-grain yield negative relationship is highly correlated to post-anthesis N uptake in winter wheat. J. Exp. Bot. 2010, 61, 4303-4312, 10.1093/jxb/erq238
91. Taulemesse, F.; Le Gouis, J.; Gouache, D.; Gibon, Y.; Allard, V. Bread Wheat (Triticum aestivum L.) Grain Protein Concentration Is Related to Early Post-Flowering Nitrate Uptake under Putative Control of Plant Satiety Level. PLoS One 2016, 11, e0149668, 10.1371/journal.pone.0149668
92. Poeta, F.; Ochogavia, A. C.; Permingeat, H. R.; Rotundo, J. L. Storage-Associated Genes and Reserves Accumulation in Soybean Cultivars Differing in Physiological Strategies for Attaining High Seed Protein Concentration. Crop Sci. 2017, 57, 427-436, 10.2135/cropsci2016.07.0611
93. Hanafy, M.; Pickardt, T.; Kiesecker, H.; Jacobsen, H.-J. Agrobacterium-mediated transformation of faba bean (Vicia faba L.) using embryo axes. Euphytica 2005, 142, 227-236, 10.1007/s10681-005-1690-4
94. Wang, X.; Jiang, G.-L.; Song, Q.; Cregan, P. B.; Scott, R. A.; Zhang, J.; Yen, Y.; Brown, M. Quantitative trait locus analysis of seed sulfur-containing amino acids in two recombinant inbred line populations of soybean. Euphytica 2015, 201, 293-305, 10.1007/s10681-014-1223-0
95. Warrington, C. V.; Abdel-Haleem, H.; Hyten, D. L.; Cregan, P. B.; Orf, J. H.; Killam, A. S.; Bajjalieh, N.; Li, Z.; Boerma, H. R. QTL for seed protein and amino acids in the Benning x Danbaekkong soybean population. Theor. Appl. Genet. 2015, 128, 839-850, 10.1007/s00122-015-2474-4
96. Martensson, P. Variation in legumin: vicilin ratio between and within cultivars of Vicia faba L. var. minor. In Vicia faba: feeding value, processing and viruses in Proceedings of a seminar in the EEC Programme of Coordination of Research on the Improvement of the Production of Plant Proteins, Cambridge, England, June 27-29, 1979, World crops: production, utilization and description; Martinus Nijhoff: The Hague, The Netherlands, 1980; Vol. 3., pp 159-172.
97. Gatehouse, J. A.; Croy, R. R. D.; McIntosh, R.; Paul, C.; Boulter, D. Quantitative and qualitative variation in the storage proteins of material from the EEC joint field bean test. Vicia faba: feeding value, processing and viruses 1980, 173-188
98. Ma, Y.; Kan, G.; Zhang, X.; Wang, Y.; Zhang, W.; Du, H.; Yu, D. Quantitative Trait Loci (QTL) Mapping for Glycinin and beta-Conglycinin Contents in Soybean (Glycine max L. Merr.). J. Agric. Food Chem. 2016, 64, 3473-3483, 10.1021/acs.jafc.6b00167
99. Sjödin, J. Induced morphological variation in Vicia faba L. Hereditas 1971, 67, 155-179, 10.1111/j.1601-5223.1971.tb02371.x
100. Duc, G. Mutagenesis of faba bean (Vicia faba L.) and the identification of five different genes controlling no nodulation, ineffective nodulation or supernodulation. Euphytica 1995, 83, 147-152, 10.1007/BF01678042
101. Brosnan, J. T.; Brosnan, M. E. The sulfur-containing amino acids: an overview. J. Nutr. 2006, 136, 1636S-1640S, 10.1093/jn/136.6.1636S
102. Utsumi, S.; Yokoyama, Z.-i.; Mori, T. Comparative Studies of Subunit Compositions of Legumins from Various Cultivars of Vicia faba L. Seeds. Agric. Biol. Chem. 1980, 44, 595-601, 10.1080/00021369.1980.10863994
103. Fontes, E. P. B.; Moreira, M. A.; Davies, C. S.; Nielsen, N. C. Urea-elicited changes in relative electrophoretic mobility of certain glycinin and β-conglycinin subunits. Plant Physiol. 1984, 76, 840-842, 10.1104/pp.76.3.840
104. Poysa, V.; Woodrow, L.; Yu, K. Effect of soy protein subunit composition on tofu quality. Food Res. Int. 2006, 39, 309-317, 10.1016/j.foodres.2005.08.003
105. Mertens, C.; Dehon, L.; Bourgeois, A.; Verhaeghe-Cartrysse, C.; Blecker, C. Agronomical factors influencing the legumin/vicilin ratio in pea (Pisum sativum L.) seeds. J. Sci. Food Agric. 2012, 92, 1591-1596, 10.1002/jsfa.4738
106. Ladjal-Ettoumi, Y.; Boudries, H.; Chibane, M.; Romero, A. Pea, Chickpea and Lentil Protein Isolates: Physicochemical Characterization and Emulsifying Properties. Food Biophys. 2016, 11, 43-51, 10.1007/s11483-015-9411-6
107. Duc, G.; Marget, P.; Esnault, R.; Le Guen, J.; Bastianelli, D. Genetic variability for feeding value of faba bean seeds (Vicia faba): Comparative chemical composition of isogenics involving zero-tannin and zero-vicine genes. J. Agric. Sci. 1999, 133, 185-196, 10.1017/S0021859699006905
108. Schumacher, H.; Paulsen, H. M.; Gau, A. E. Phenotypical indicators for the selection of methionine enriched local legumes in plant breeding. Agri. For. Res. 2009, 54 (4), 339-344