Improving pulse crops as a source of protein, starch and micronutrients

Nutrition Bulletin

Volumn 44, Issue 3, 2019, Pages 202-215

  Robinson, G H J ^a   Balk, J ^a,b   Domoney, C ^a  

^a NORWICH RESEARCH PARK   (United Kingdom)

^b UNIVERSITY OF EAST ANGLIA   (United Kingdom)

Author keywords

biofortification; essential amino acids; favism; legume; resistant starch; sustainability

Indexed keywords

EID: 85070986131     PISSN: 14719827     EISSN: 14673010     Source Type: Journal    
DOI: 10.1111/nbu.12399     Document Type: Review

References (117)

1. Amarakoon D, Thavarajah D, McPhee K et al. (2012) Iron-, zinc-, and magnesium-rich field peas (Pisum sativum L.) with naturally low phytic acid: a potential food-based solution to global micronutrient malnutrition. Journal of Food Composition and Analysis 27: 8–13.
2. Amarakoon D, Thavarajah D, Gupta D et al. (2015) Genetic and environmental variation of seed iron and food matrix factors of North-Dakota-grown field peas (Pisum sativum L.). Journal of Food Composition and Analysis 37: 67–74.
3. Ambigaipalan P, Hoover R, Donner E et al. (2011) Structure of faba bean, black bean and pinto bean starches at different levels of granule organization and their physicochemical properties. Food Research International 44: 2962–74.
4. Baloch FS, Karaköy T, Demirbaş A et al. (2014) Variation of some seed mineral contents in open pollinated faba bean (Vicia faba L.) landraces from Turkey. Turkish Journal of Agriculture and Forestry 38: 591–602.
5. Barać MB, Pešić MB, Stanojević SP et al. (2015) Techno-functional properties of pea (Pisum sativum) protein isolates-a review. Acta Periodica Technologica 46: 1–18.
6. Barton L, Thamo T, Engelbrecht D et al. (2014) Does growing grain legumes or applying lime cost effectively lower greenhouse gas emissions from wheat production in a semi-arid climate? Journal of Cleaner Production 83: 194–203.
7. BBC News (2019) Folic acid: Consultation starts on plan to fortify flour. Available at: www.bbc.co.uk/news/health-48608653 (accessed 13 June 2019).
8. Bhattacharyya MK, Smith AM, Ellis THN et al. (1990) The wrinkled-seed character of pea described by Mendel is caused by a transposon-like insertion in a gene encoding starch-branching enzyme. Cell 60: 115–22.
9. Birk Y (1985) The Bowman-Birk inhibitor. Trypsin- and chymotrypsin-inhibitor from soybeans. International Journal of Peptide and Protein Research 25: 113–31.
10. Bogracheva TY, Cairns P, Noel TR et al. (1999) Effect of mutant genes at the r, rb, rug3, rug4, rug5 and lam loci on the granular structure and physico-chemical properties of pea seed starch. Carbohydrate Polymers 39: 303–14.
11. Bourgeois M, Jacquin F, Cassecuelle F et al. (2011) A PQL (protein quantity loci) analysis of mature pea seed proteins identifies loci determining seed protein composition. Proteomics 11: 1581–94.
12. Briat JF, Duc C, Ravet K et al. (2010) Ferritins and iron storage in plants. Biochimica et Biophysica Acta - General Subjects 1800: 806–14.
13. Brighenti F, Casiraghi MC & Baggio C (1998) Resistant starch in the Italian diet. British Journal of Nutrition 80: 333–41.
14. Casey R & Short MN (1981) Variation in amino acid composition of legumin from Pisum. Phytochemistry 20: 21–3.
15. Casey R, Domoney C, Forster C et al. (1998) The effect of modifying carbohydrate metabolism on seed protein gene expression in peas. Journal of Plant Physiology 152: 636–40.
16. Chung KT, Wei CI & Johnson MG (1998) Are tannins a double-edged sword in biology and health? Trends in Food Science and Technology 9: 168–75.
17. Clemente A & Olias R (2017) Beneficial effects of legumes in gut health. Current Opinion in Food Science 14: 32–6.
18. Clemente A, Arques MC, Dalmais M et al. (2015) Eliminating anti-nutritional plant food proteins: the case of seed protease inhibitors in pea. PLoS ONE 10: e0134634.
19. Cooper JW, Wilson MH, Derks MFL et al. (2017) Enhancing faba bean (Vicia faba L.) genome resources. Journal of Experimental Botany 68: 1941–53.
20. Crépon K, Marget P, Peyronnet C et al. (2010) Nutritional value of faba bean (Vicia faba L.) seeds for feed and food. Field Crops Research 115: 329–39.
21. Croy RRD, Hoque MS, Gatehouse JA et al. (1984) The major albumin proteins from pea (Pisum sativum L). Biochemical Journal 218: 795–803.
22. Curatti L & Rubio LM (2014) Challenges to develop nitrogen-fixing cereals by direct nif-gene transfer. Plant Science 225: 130–7.
23. Dahl WJ, Foster LM & Tyler RT (2012) Review of the health benefits of peas (Pisum sativum L.). British Journal of Nutrition 108: 3–10.
24. Demidov D, Horstmann C, Meixner M et al. (2003) Additive effects of the feed-back insensitive bacterial aspartate kinase and the Brazil nut 2S albumin on the methionine content of transgenic narbon bean (Vicia narbonensis L.). Molecular Breeding 11: 187–201.
25. Demirbaş A (2018) Micro and macronutrients diversity in Turkish pea (Pisum sativum) germplasm. International Journal of Agriculture and Biology 20: 701–10.
26. Diapari M, Sindhu A, Warkentin TD et al. (2015) Population structure and marker-trait association studies of iron, zinc and selenium concentrations in seed of field pea (Pisum sativum L.). Molecular Breeding 35: 30.
27. Domoney C, Knox M, Moreau C et al. (2013) Exploiting a fast neutron mutant genetic resource in Pisum sativum (pea) for functional genomics. Functional Plant Biology 40: 1261–70.
28. Duc M, Marget P, Page D et al. (2004) Facile breeding markers to lower contents of vicine and convicine in faba bean seeds and trypsin inhibitors in pea seeds. In: Recent Advances of Research in Antinutritional Factors in Legume Seeds and Oilseeds, (M Muzquiz, GD Hill, C Cuadrado, MM Pedrosa & C Burbano eds), pp. 281–5. Wageningen: Wageningen Academic Publishers.
29. Erbersdobler HF, Barth CA & Jahreis G (2017) Körnerleguminosen in der Humanernährung. Nährstoffgehalt und Proteinqualität von Hülsenfrüchten. Ernährungs-Umschau 64: 134–9.
30. Etemadi F, Barker AV, Hashemi M et al. (2018) Nutrient accumulation in faba bean varieties. Communications in Soil Science and Plant Analysis 49: 2064–73.
31. FAO (Food and Agriculture Organization) (2015) What are pulses?| FAO. Available at: www.fao.org/pulses-2016/news/news-detail/en/c/337107/ (accessed 10 July 2019).
32. FAO (Food and Agriculture Organization) (2019) FAOSTAT. Available at: www.fao.org/faostat/en/#compare (accessed 18 June 2019).
33. Foyer CH, Lam HM, Nguyen HT et al. (2016) Neglecting legumes has compromised human health and sustainable food production. Nature Plants 2: 16112.
34. FSA (Food Standards Agency) (2002) McCance and Widdowson's The Composition of Foods. 6th summary edition. Royal Society of Chemistry: Cambridge.
35. Gali KK, Liu Y, Sindhu A et al. (2018) Construction of high-density linkage maps for mapping quantitative trait loci for multiple traits in field pea (Pisum sativum L.). BMC Plant Biology 18: 172.
36. Galili G & Amir R (2013) Fortifying plants with the essential amino acids lysine and methionine to improve nutritional quality. Plant Biotechnology Journal 11: 211–22.
37. Garg M, Sharma N, Sharma S et al. (2018) Biofortified crops generated by breeding, agronomy, and transgenic approaches are improving lives of millions of people around the world. Frontiers in Nutrition 5: 12.
38. Gasim S, Hamad SAA, Abdelmula A et al. (2015) Yield and quality attributes of faba bean inbred lines grown under marginal environmental conditions of Sudan. Food Science and Nutrition 3: 539–47.
39. Gawłowska M, Święcicki W, Lahuta L et al. (2017) Raffinose family oligosaccharides in seeds of Pisum wild taxa, type lines for seed genes, domesticated and advanced breeding materials. Genetic Resources and Crop Evolution 64: 569–78.
40. Guillamón E, Pedrosa MM, Burbano C et al. (2008) The trypsin inhibitors present in seed of different grain legume species and cultivar. Food Chemistry 107: 68–74.
41. Gunasekera SUAK, Stoddard FL & Marshall DR (1999) Variation in faba bean amylose content. Starch/Staerke 51: 259–62.
42. Gupta RK, Gangoliya SS & Singh NK (2015) Reduction of phytic acid and enhancement of bioavailable micronutrients in food grains. Journal of Food Science and Technology 52: 676–84.
43. Gutiérrez N, Ávila CM, Duc G et al. (2006) CAPs markers to assist selection for low vicine and convicine contents in faba bean (Vicia faba L.). Theoretical and Applied Genetics 114: 59–66.
44. Gutiérrez N, Ávila CM, Moreno MT et al. (2008) Development of SCAR markers linked to zt-2, one of the genes controlling absence of tannins in faba bean. Australian Journal of Agricultural Research 59: 62–8.
45. Hagerman AE, Riedl KM, Jones GA et al. (1998) High Molecular Weight Plant Polyphenolics (Tannins) as Biological Antioxidants. Journal of Agricultural and Food Chemistry 46: 1887–92.
46. Harrison CJ, Hedley CL & Wang TL (1998) Evidence that the rug3 locus of pea (Pisum sativum L.) encodes plastidial phosphoglucomutase confirms that the imported substrate for starch synthesis in pea amyloplasts is glucose-6-phosphate. Plant Journal 13: 753–62.
47. Hughes RK, Desforges N, Selwood C et al. (2001) Genes affecting starch biosynthesis exert pleiotropic effects on the protein content and composition of pea seeds. Journal of the Science of Food and Agriculture 81: 877–82.
48. Hurrell R & Egli I (2010) Iron bioavailability and dietary reference values. American Journal of Clinical Nutrition 91: 1461S–7S.
49. Hylton C & Smith AM (1992) The rb mutation of peas causes structural and regulatory changes in ADP glucose pyrophosphorylase from developing embryos. Plant Physiology 99: 1626–34.
50. Irwin RE, Pentieva K, Cassidy T et al. (2016) The interplay between DNA methylation, folate and neurocognitive development. Epigenomics 8: 863–79.
51. Ivarsson E & Neil M (2018) Variations in nutritional and antinutritional contents among faba bean cultivars and effects on growth performance of weaner pigs. Livestock Science 212: 14–21.
52. Jha AB, Ashokkumar K, Diapari M et al. (2015) Genetic diversity of folate profiles in seeds of common bean, lentil, chickpea and pea. Journal of Food Composition and Analysis 42: 134–40.
53. Johnston KL, Thomas EL, Bell JD et al. (2010) Resistant starch improves insulin sensitivity in metabolic syndrome. Diabetic Medicine 27: 391–7.
54. Kamaljit K, Baljeet S & Amarjeet K (2010) Preparation of bakery products by incorporating pea flour as a functional ingredient. American Journal of Food Technology 5: 130–5.
55. Kennedy AR, Beazer-Barclay Y, Kinzler KW et al. (1996) Suppression of carcinogenesis in the intestines of Min mice by the soybean-derived Bowman-Birk inhibitor. Cancer Research 56: 679–82.
56. Khan MA, Ammar MH, Migdadi HM et al. (2015) Comparative nutritional profiles of various faba bean and chickpea genotypes. International Journal of Agriculture and Biology 17: 449–57.
57. Khazaei H, O'Sullivan DM, Jones H et al. (2015) Flanking SNP markers for vicine–convicine concentration in faba bean (Vicia faba L.). Molecular Breeding 35: 38.
58. Khazaei H, Stoddard FL, Purves RW et al. (2018) A multi-parent faba bean (Vicia faba L.) population for future genomic studies. Plant Genetic Resources: Characterization and Utilization 16: 419–23.
59. Kneen BE, Larue TA, Welch RM et al. (1990) Pleiotropic effects of brz: a mutation in Pisum sativum (L) cv. ‘Sparkle’ conditioning decreased nodulation and increased iron uptake and leaf necrosis. Plant Physiology 93: 717–22.
60. Kozłowska H (2001) Nutrition. In: Carbohydrates in grain legume seeds: improving nutritional quality and agronomic characteristics, (CL Hedley ed.), pp. 61–89. CABI Publishing: Wallingford.
61. Kumar A, Nidhi PN et al. (2014) Nutritional and antinutritional attributes of faba bean (Vicia faba L.) germplasms growing in Bihar, India. Physiology and Molecular Biology of Plants 21: 159–62.
62. Le Gall M, Quillien L, Sève B et al. (2007) Weaned piglets display low gastrointestinal digestion of pea (Pisum sativum L.) lectin and pea albumin 2. Journal of Animal Science 85: 2972–81.
63. Lea E, Worsley A & Crawford D (2005) Australian adult consumers’ beliefs about plant foods: a qualitative study. Health Education and Behavior 32: 795–808.
64. Lessire M, Gallo V, Prato M et al. (2017) Effects of faba beans with different concentrations of vicine and convicine on egg production, egg quality and red blood cells in laying hens. Animal 11: 1270–8.
65. Liu X, Glahn RP, Arganosa GC et al. (2015) Iron bioavailability in low Phytate Pea. Crop Science 55: 320.
66. Lockyer S & Nugent AP (2017) Health effects of resistant starch. Nutrition Bulletin 42: 10–41.
67. Lockyer S, White A & Buttriss JL (2018) Biofortified crops for tackling micronutrient deficiencies – what impact are these having in developing countries and could they be of relevance within Europe? Nutrition Bulletin 43: 319–57.
68. Lombardo S, Pandino G, Pesce GR et al. (2016) Variation in seed mineral elements profile and yield in field bean (Vicia faba L. var. minor) genotypes. Italian Journal of Agronomy 11: 261–7.
69. Lönnerdal B, Bryant A, Liu X et al. (2006) Iron absorption from soybean ferritin in nonanemic women. American Journal of Clinical Nutrition 83: 103–7.
70. Lucas T & Horton R (2019) The 21st-century great food transformation. The Lancet 393: 386–87.
71. Ma Y, Coyne CJ, Grusak MA et al. (2017) Genome-wide SNP identification, linkage map construction and QTL mapping for seed mineral concentrations and contents in pea (Pisum sativum L.). BMC Plant Biology 17: 43.
72. Moore KL, Rodríguez-Ramiro I, Jones ER et al. (2018) The stage of seed development influences iron bioavailability in pea (Pisum sativum L.). Scientific Reports 8: 6865.
73. Multari S, Stewart D & Russell WR (2015) Potential of fava bean as future protein supply to partially replace meat intake in the human diet. Comprehensive Reviews in Food Science and Food Safety 14: 511–22.
74. Müntz K, Horstmann C & Schlesier B (1999) Vicia Globulins. In: Seed Proteins, (PR Shewry & R Casey eds), pp. 259–84. Kluwer Academic Publishers: Dordrecht.
75. Nemecek T, von Richthofen JS, Dubois G et al. (2008) Environmental impacts of introducing grain legumes into European crop rotations. European Journal of Agronomy 28: 380–93.
76. O'Kane FE, Happe RP, Vereijken JM et al. (2004) Heat-induced gelation of pea legumin: comparison with soybean glycinin. Journal of Agricultural and Food Chemistry 52: 5071–8.
77. Oomah BD, Luc G, Leprelle C et al. (2011) Phenolics, phytic acid, and phytase in Canadian-grown low-tannin faba bean (Vicia faba L.) genotypes. Journal of Agricultural and Food Chemistry 59: 3763–71.
78. Perfecto A, Rodriguez-Ramiro I, Rodriguez-Celma J et al. (2018) Pea ferritin stability under gastric pH conditions determines the mechanism of iron uptake in Caco-2 cells. Journal of Nutrition 148: 1229–35.
79. Peterbauer T, Mach L, Mucha J et al. (2002) Functional expression of a cDNA encoding pea (Pisum sativum L.) raffinose synthase, partial purification of the enzyme from maturing seeds, and steady-state kinetic analysis of raffinose synthesis. Planta 215: 839–46.
80. Petropoulou K, Chambers ES, Morrison DJ et al. (2016) Identifying crop variants with high resistant starch content to maintain healthy glucose homeostasis. Nutrition Bulletin 41: 372–7.
81. Petropoulou K, Salt L, Warren F, et al. (2017) A seed trait studied by Gregor Mendel in Pisum sativum L. (pea): potential prevention of type 2 diabetes. In: Legumes for Global Food Security, (A C, JC J-L eds), pp. 129–55. Nova Science Publishers: New York.
82. Petry N, Egli I, Campion B, et al. (2013) Genetic reduction of phytate in common bean (Phaseolus vulgaris L.) seeds increases iron absorption in young women. The Journal of Nutrition 143: 1219–24.
83. PGRO (Processors and Growers Research Organisation) (2018) ‘Blueprint for UK Pulses in a post-Brexit world’ Executive summary. 1–20. Available at: www.pgro.org/downloads/PGROBLUEPRINTFORPULSES.pdf" (accessed 1 August 2019).
84. Poblaciones MJ & Rengel Z (2017) Combined foliar selenium and zinc biofortification in field pea (Pisum sativum): accumulation and bioavailability in raw and cooked grains. Crop and Pasture Science 68: 265–71.
85. Poore J & Nemecek T (2018) Reducing food's environmental impacts through producers and consumers. Science 360: 987–92.
86. PHE (Public Health England) (2018) The Eatwell Guide. Available at: https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/742750/Eatwell_Guide_booklet_2018v4.pdf (accessed 16 July 2019).
87. PHE (Public Health England) (2019) National Diet and Nutrition Survey Years 1-9 2008/2009 – 2016/2017. Available at: https://doi.org/10.5255/ukda-sn-6533-13 (accessed 8 May 2019).
88. Pulses UK (2017) Export Markets - Pulses UK. Available at: http://www.pulsesuk.co.uk/export-markets/ (accessed 11 February 2019).
89. Ramírez-Moreno JM, Salguero Bodes I, Romaskevych O et al. (2015) Broad bean (Vicia faba) consumption and Parkinson's disease: a natural source of L-dopa to consider. Neurologia 30: 375–6.
90. Ratnayake WS, Hoover R & Warkentin T (2002) Pea starch: composition, structure and properties - a review. Starch/Staerke 54: 217–34.
91. Ray H, Bett K, Tar'an B et al. (2014) Mineral micronutrient content of cultivars of field pea, chickpea, common bean, and lentil grown in Saskatchewan, Canada. Crop Science 54: 1698–708.
92. Rayner T, Moreau C, Ambrose M et al. (2017) Genetic variation controlling wrinkled seed phenotypes in Pisum: how lucky was Mendel? International Journal of Molecular Sciences 18: 6.
93. Rehman HM, Cooper JW, Lam HM et al. (2019) Legume biofortification is an underexploited strategy for combatting hidden hunger. Plant, Cell and Environment 42: 52–70.
94. Shen S, Hou H, Ding C et al. (2016) Protein content correlates with starch morphology, composition and physicochemical properties in field peas. Canadian Journal of Plant Science 96: 404–12.
95. Shewry PR & Tatham AS (1999) 2. The characteristics, structures and evolutionary relationships of prolamins. In: Seed Proteins (PR Shewry & R Casey eds), pp. 11–33. Kluwer Academic Publishers: Dordrecht.
96. Shewry PR, Napier JA & Tatham AS (1995) Seed storage proteins: structures and biosynthesis. The Plant Cell 7: 945–56.
97. Shunmugam AS, Bock C, Arganosa G et al. (2014) Accumulation of phosphorus-containing compounds in developing seeds of low-phytate pea (Pisum sativum L.) mutants. Plants 4: 1–26.
98. Sierra I, Vidal-Valverde C & Kozlowska H (1998) Effect of ripening stage on thiamin and riboflavin levels in lupin, pea and faba bean seeds. Zeitschrift für Lebensmitteluntersuchung und -Forschung A 206: 126–9.
99. Silva-Cristobal L, Osorio-Díaz P & Bello-Pérez LA (2007) Digestibilidad del almidón en haba (Vicia faba L.). Agrociencia 41: 845–52.
100. Souza Monteiro DM, Brandt K, Cooper J et al. (2017) Opportunities and Challenges for the Development of Pulses Markets. Executive summary. Available at: www.pgro.org/downloads/Pulse-market-trends.pdf (accessed 1 August 2019)
101. Stagnari F, Maggio A, Galieni A et al. (2017) Multiple benefits of legumes for agriculture sustainability: an overview. Chemical and Biological Technologies in Agriculture 4: 2.
102. Steinfeld H, Gerber P, Wassenaar T et al. (2006) Livestock's Long Shadow: Environmental Issues and Options. Food and Agriculture Organization of the United Nations: Rome.
103. Stevenson EJ, Watson AW, Brunstrom JM et al. (2018) Protein for life: towards a focussed dietary framework for healthy ageing. Nutrition Bulletin 43: 97–102.
104. Tayeh N, Klein A, Le Paslier M-C et al. (2015) Genomic prediction in pea: effect of marker density and training population size and composition on prediction accuracy. Frontiers in Plant Science 6: 941.
105. The Good Food Institute (2018) U.S. Plant Based Market Overview - Research from Nielsen - The Good Food Institute. Available at: www.gfi.org/marketresearch (accessed 16 July 2019).
106. The Vegan Society (2018) Statistics. Available at: www.vegansociety.com/news/media/statistics (accessed 8 May 2019).
107. Tzitzikas EN, Vincken JP, De Groot J et al. (2006) Genetic variation in pea seed globulin composition. Journal of Agricultural and Food Chemistry 54: 425–33.
108. United Nations University (2002) Protein and amino acid requirements in human nutrition. WHO Technical Report Series 935: 1–265.
109. Vaz Patto MC, Amarowicz R, Aryee ANA, et al. (2015) Achievements and challenges in improving the nutritional quality of food legumes. Critical Reviews in Plant Sciences 34: 105–43. https://doi.org/10.1080/07352689.2014.897907
110. Vigeolas H, Chinoy C, Zuther E et al. (2008) Combined metabolomic and genetic approaches reveal a link between the polyamine pathway and albumin 2 in developing pea seeds. Plant Physiology 146: 74–82.
111. Wang X, Warkentin TD, Briggs CJ et al. (1998) Total phenolics and condensed tannins in field pea (Pisum sativum L.) and grass pea (Lathyrus sativus L.). Euphytica 101: 97–102.
112. Warkentin TD, Delgerjav O, Arganosa G et al. (2012) Development and characterization of low-phytate pea. Crop Science 52: 74–8.
113. Warsame AO, O'Sullivan DM & Tosi P (2018) Seed storage proteins of faba bean (Vicia faba L.): current status and prospects for genetic improvement. Journal of Agricultural and Food Chemistry 66: 12617–26.
114. Webb A, Cottage A, Wood T et al. (2016) A SNP-based consensus genetic map for synteny-based trait targeting in faba bean (Vicia faba L.). Plant Biotechnology Journal 14: 177–85.
115. Wessells KR & Brown KH (2012) Estimating the global prevalence of zinc deficiency: results based on zinc availability in national food supplies and the prevalence of stunting. PLoS ONE 7: e50568.
116. White PJ (2016) Selenium accumulation by plants. Annals of Botany 117: 217–35.
117. WHO (World Health Organization) (2015) The Global Prevalence of Anaemia in 2011. World Health Organization: Geneva.