Research progress of RuBisCO, a new plant protein source

  • FENG Wenjuan ,
  • GAO Sicong ,
  • HUANG Wenxuan ,
  • LI Yungao ,
  • HUANG Zhichao ,
  • MIAO Ming
Expand
  • 1(State Key Laboratory of Food Science and Technology, College of Food Science, Jiangnan University, Wuxi 214122, China)
    2(Qinhuangdao Senyuan Investment Group Co. Ltd., Qinhuangdao 066199, China)

Received date: 2023-07-11

  Revised date: 2023-08-24

  Online published: 2024-08-02

Abstract

Ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO) is an essential enzyme that plays a vital role in plants by regulating carbon assimilation rate and the process of photorespiration.It is responsible for about 15% of soluble leaf proteins in C4 plants like maize and sorghum, while making up over 50% of total nitrogen in C3 plants such as wheat, tobacco, and alfalfa.RuBisCO has a molecular weight of approximately 560 kDa and consists of 8 large subunits and 8 small subunits.Its shape can be either spherical or cylindrical, and it can undergo subunit dissociation under specific conditions.However, the current methods for extracting RuBisCO have several issues, including high cost, low efficiency, and complex technology.To address these problems, it is important to ensure strict control over the quality of raw materials, develop extraction and purification methods that are both economically viable and of high quality, and explore the possibility of developing additional by-products.From a physicochemical perspective, RuBisCO exhibits excellent solubility, emulsifying capacity, foaming capacity, and can even form brittle gels at low concentrations, highlighting its significant application potential.In terms of nutritional and functional characteristics, RuBisCO is rich in essential amino acids, and its derived peptides have demonstrated health-promoting functions in laboratory studies.This review provides a comprehensive overview of the sources, structure, extraction process, physicochemical properties, nutritional and functional characteristics of RuBisCO.It also suggests future research directions and discusses the potential applications of RuBisCO.

Cite this article

FENG Wenjuan , GAO Sicong , HUANG Wenxuan , LI Yungao , HUANG Zhichao , MIAO Ming . Research progress of RuBisCO, a new plant protein source[J]. Food and Fermentation Industries, 2024 , 50(13) : 340 -348 . DOI: 10.13995/j.cnki.11-1802/ts.036730

References

[1] HAYER-HARTL M, HARTL F U.Chaperone machineries of RuBisCO-the most abundant enzyme[J].Trends in Biochemical Sciences, 2020, 45(9):748-763.
[2] VON CAEMMERER S.RuBisCO carboxylase/oxygenase:From the enzyme to the globe:A gas exchange perspective[J].Journal of Plant Physiology, 2020, 252:153240.
[3] ZHOU H L, VU G, MCCLEMENTS D J.Formulation and characterization of plant-based egg white analogs using RuBisCO protein[J].Food Chemistry, 2022, 397:133808.
[4] PÉREZ-VILA S, FENELON M A, O'MAHONY J A, et al.Extraction of plant protein from green leaves:Biomass composition and processing considerations[J].Food Hydrocolloids, 2022, 133:107902.
[5] KU M S B, SCHMITT M R, EDWARDS G E.Quantitative determination of RuBP carboxylase-oxygenase protein in leaves of several C3 and C4 plants[J].Journal of Experimental Botany, 1979, 30(1):89-98.
[6] HOJILLA-EVANGELISTA M P, SELLING G W, HATFIELD R, et al.Extraction, composition, and functional properties of dried alfalfa (Medicago sativa L.) leaf protein[J].Journal of the Science of Food and Agriculture, 2017, 97(3):882-888.
[7] WU Z L, SHU T, ZHANG M W, et al.Foam fractionation for effective recovery of leaf protein from alfalfa (Medicago sativa L.) [J].Separation Science and Technology, 2020, 55(7):1388-1397.
[8] MCCREE K J.Maintenance requirements of white clover at high and low growth Rates1[J].Crop Science, 1982, 22(2):345-351.
[9] MØLLER A H, HAMMERSHØJ M, DOS PASSOS N H M, et al.Biorefinery of green Biomass─How to extract and evaluate high quality leaf protein for food?[J].Journal of Agricultural and Food Chemistry, 2021, 69(48):14341-14357.
[10] SHI W Y, LI H B, ZENG X H, et al.The extraction of tobacco protein from discarded tobacco leaf by hollow fiber membrane integrated process[J].Innovative Food Science & Emerging Technologies, 2019, 58:102245.
[11] CAI M, MU L, WANG Z L, et al.Assessment of mulberry leaf as a potential feed supplement for animal feeding in P.R.China[J].Asian-Australasian Journal of Animal Sciences, 2019, 32(8):1145-1152.
[12] CALDERÓN-CHIU C, CALDERÓN-SANTOYO M, HERMAN-LARA E, et al.Jackfruit (Artocarpus heterophyllus Lam) leaf as a new source to obtain protein hydrolysates:Physicochemical characterization, techno-functional properties and antioxidant capacity[J].Food Hydrocolloids, 2021, 112:106319.
[13] ISLAM M M, AKTHER S M, SUJON S A, et al.Effects of vermicompost and PK on growth and protein content of spinach (Spinacia oleracia L.) [J].Bangladesh Journal of Botany, 2020, 49:141-146.
[14] AKYÜZ A, ERSUS S.Optimization of enzyme assisted extraction of protein from the sugar beet (Beta vulgaris L.) leaves for alternative plant protein concentrate production [J].Food Chemistry, 2021, 335:127673.
[15] PEROVĆ J, ŠAPONJAC V T, KOJIĆ J, et al.Chicory (Cichorium intybus L.) as a food ingredient- Nutritional composition, bioactivity, safety, and health claims:A review[J].Food Chemistry, 2021, 336:127676.
[16] YEOH H H, CHEW M Y.Protein content and amino acid composition of cassava leaf[J].Phytochemistry, 1976, 15(11):1597-1599.
[17] ABEROUMAND A.Nutritional evaluation of edible Portulaca oleracia as plant food[J].Food Analytical Methods, 2009, 2(3):204-207.
[18] TAYLOR J, ZHANG K, WANG D.Industrial and Nonfood Applications [M]//TAYLOR J R N, DUODU K G.Sorghum and Millets (Second Edition).Saint Paul, Minnesota:AACC International Press,2019:393-420.
[19] RAHMAN S, VANCE G F, MUNN L C.Salinity induced effects on the nutrient status of soil, corn leaves and kernels[J].Communications in Soil Science and Plant Analysis, 1993, 24(17-18):2251-2269.
[20] BASSI D, MENOSSI M, MATTIELLO L.Nitrogen supply influences photosynthesis establishment along the sugarcane leaf[J].Scientific Reports, 2018, 8(1):2327.
[21] MANGAN J L.2.1 the nitrogenous constituents of fresh forages[J].BSAP Occasional Publication, 1982, 6:25-40.
[22] YU Y F, KLEUTER M, TAGHIAN DINANI S, et al.The role of plant age and leaf position on protein extraction and phenolic compounds removal from tomato (Solanum lycopersicum) leaves using food-grade solvents[J].Food Chemistry, 2023, 406:135072.
[23] KIM H, PARK J, LIM S, et al.Cryo-EM structures of GroEL:ES2 with RuBisCO visualize molecular contacts of encapsulated substrates in a double-cage chaperonin[J].iScience, 2022, 25(1):103704.
[24] GALMÉS J, CAPÓ-BAUÇÀ S, NIINEMETS Ü, et al.Potential improvement of photosynthetic CO2 assimilation in crops by exploiting the natural variation in the temperature response of RuBisCO catalytic traits[J].Current Opinion in Plant Biology, 2019, 49:60-67.
[25] SPREITZER R J.Questions about the complexity of chloroplast ribulose-1, 5-bisphosphate carboxylase/oxygenase[J].Photosynthesis Research, 1999, 60(1):29-42.
[26] ANDERSSON I, BACKLUND A.Structure and function of rubisco[J].Plant Physiology and Biochemistry, 2008, 46(3):275-291.
[27] SPREITZER R J.Genetic dissection of rubisco structure and function[J].Annual Review of Plant Physiology and Plant Molecular Biology, 1993, 44(1):411-434.
[28] DU X J, SUN Y Y, PAN D D, et al.Change of the structure and the digestibility of myofibrillar proteins in Nanjing dry-cured duck during processing[J].Journal of the Science of Food and Agriculture, 2018, 98(8):3140-3147.
[29] GREENFIELD N J.Using circular dichroism spectra to estimate protein secondary structure[J].Nature Protocols, 2006, 1(6):2876-2890.
[30] AMER B, JUUL L, MØLLER A H, et al.Improved solubility of proteins from white and red clover- inhibition of redox enzymes [J].International Journal of Food Science & Technology, 2021, 56(1):302-311.
[31] EDWARDS R H, MILLER R E, DE FREMERY D, et al.Pilot plant production of an edible white fraction leaf protein concentrate from alfalfa[J].Journal of Agricultural and Food Chemistry, 1975, 23(4):620-626.
[32] XU Y, LI Y T, BAO T, et al.A recyclable protein resource derived from cauliflower by-products:Potential biological activities of protein hydrolysates[J].Food Chemistry, 2017, 221:114-122.
[33] DU J, SHI J C, OBADI M, et al.Decolorization of commercial zein via protein precipitation involving organic solvents at low temperatures[J].Colloids and Surfaces A:Physicochemical and Engineering Aspects, 2020, 596:124738.
[34] 金伟丽, 郑国栋, 黎冬明.硅藻土对米渣蛋白脱色工艺的研究[J].粮食与油脂, 2016, 29(3):50-52.
JIN W L, ZHENG G D, LI D M.Study on the diatomite decoloration process of rice residue protein[J].Cereals & Oils, 2016, 29(3):50-52.
[35] 王松, 李成辉, 王洪彩, 等.大豆肽的硅藻土脱色工艺优化[J].中国油脂, 2020, 45(6):41-44.
WANG S, LI C H, WANG H C, et al.Optimization of bleaching of soybean peptide by diatomite[J].China Oils and Fats, 2020, 45(6):41-44.
[36] 许英一, 吴红艳, 王宇, 等.大孔树脂纯化苜蓿叶蛋白肽的工艺优化[J].食品与机械, 2019, 35(5):167-171.
XU Y Y, WU H Y, WANG Y, et al.Optimization on purification technology of alfalfa leaf protein peptide bymacroporous adsoption resin[J].Food & Machinery, 2019, 35(5):167-171.
[37] MA G X, YANG W J, FANG Y, et al.Antioxidant and cytotoxicites of Pleurotus eryngii residue polysaccharides obtained by ultrafiltration[J].LWT, 2016, 73:108-116.
[38] 吴万灵, 韩鲁佳, 王唯涌.苜蓿叶蛋白提取工艺参数优化试验研究[J].中国农业大学学报, 2006, 11(5):65-69.
WU W L, HAN L J, WANG W Y.Experimental study on parameter optimization of extraction process of leaf protein from alfalfa[J].Journal of China Agricultural University, 2006, 11(5):65-69.
[39] 李道娥, 刘向阳, 韩鲁佳, 等.加热法提取叶蛋白的工艺研究[J].农业工程学报, 1998, 14(1):238-242.
LI D E, LIU X Y, HAN L J, et al.Study on the technology of extracting leaf protein by heating[J].Transactions of the Chinese Society of Agricultural Engineering, 1998, 14(1):238-242.
[40] PANDEY V N, SRIVASTAVA A K.A simple, low energy requiring method of coagulating leaf proteins for food use[J].Plant Foods for Human Nutrition, 1993, 43(3):241-245.
[41] 辛小丽. 紫花苜蓿叶蛋白的提取及其功能特性的改善研究[D].西宁:青海师范大学, 2020.
XIN X L.Extraction of alfalfa leaf protein and improvement of its functional properties[D].Xining:Qinghai Normal University, 2020.
[42] 谢正军. 苜蓿叶蛋白和酶法制备抗氧化肽的研究[D].无锡:江南大学, 2009.
XIE Z J.Study on the alfalfa leaf protein and preparation of antioxidant peptides by enzymic hydrolyzing[D].Wuxi:Jiangnan University, 2009.
[43] D'ALVISE N, LESUEUR- L A M B E R T C, FERTIN B, et al.Removal of polyphenols and recovery of proteins from alfalfa white protein concentrate by ultrafiltration and adsorbent resin separations[J].Separation Science and Technology, 2000, 35(15):2453-2472.
[44] MARTIN A H, NIEUWLAND M, DE JONG G A H.Characterization of heat-set gels from RuBisCO in comparison to those from other proteins[J].Journal of Agricultural and Food Chemistry, 2014, 62(44):10783-10791.
[45] 李明. 枸杞叶蛋白提取及应用研究[D].武汉:武汉轻工大学, 2020.
LI M.Study on the extraction and application of Lycium barbarum leaf protein[D].Wuhan:Wuhan Polytechnic University, 2020.
[46] YOUSEFI N, ABBASI S.Food proteins:Solubility & thermal stability improvement techniques[J].Food Chemistry Advances, 2022, 1:100090.
[47] PREVOT-D'ALVISE N, LESUEUR-LAMBERT C, FERTIN-BAZUS A, et al.Continuous enzymatic solubilization of alfalfa proteins in an ultrafiltration reactor[J].Enzyme and Microbial Technology, 2004, 34(5):380-391.
[48] SHEEN S J, SHEEN V L.Functional properties of fraction 1 protein from tobacco leaf[J].Journal of Agricultural and Food Chemistry, 1985, 33(1):79-83.
[49] 莫耽, 黄行健, 段雅庆, 等.辐照对大豆分离蛋白功能特性影响[J].食品科学, 2011, 32(1):52-55.
MO D, HUANG X J, DUAN Y Q, et al.Effect of irradiation on functional properties of soybean protein isolate[J].Food Science, 2011, 32(1):52-55.
[50] TAHERIAN A R, MONDOR M, LAMARCHE F.Enhancing nutritional values and functional properties of yellow pea protein via membrane processing [J].Peas:Cultivation, Varieties and Nutritional Uses, 2012:1-48.
[51] 郭本恒, 骆承庠.乳清蛋白变性的测定方法[J].中国乳品工业, 1994, 22(5):221-224.
GUO B H, LUO C X.Method for determination of denaturation of whey protein[J].China Dairy Industry, 1994, 22(5):221-224.
[52] PELEGRINE D H G, GASPARETTO C A.Whey proteins solubility as function of temperature and pH[J].LWT- Food Science and Technology, 2005, 38(1):77-80.
[53] SHARMA H P, MADAN A, JOSHI D C.Clarifying Agents [M]//MELTON L, SHAHIDI F, VARELIS P.Encyclopedia of Food Chemistry.Oxford;Academic Press,2019:53-60.
[54] LAMSAL B P, KOEGEL R G, GUNASEKARAN S.Some physicochemical and functional properties of alfalfa soluble leaf proteins[J].LWT- Food Science and Technology, 2007, 40(9):1520-1526.
[55] DUCROCQ M, BOIRE A, ANTON M, et al.Rubisco:A promising plant protein to enrich wheat-based food without impairing dough viscoelasticity and protein polymerisation[J].Food Hydrocolloids, 2020, 109:106101.
[56] MARTIN A H, CASTELLANI O, DE JONG G A, et al.Comparison of the functional properties of RuBisCO protein isolate extracted from sugar beet leaves with commercial whey protein and soy protein isolates[J].Journal of the Science of Food and Agriculture, 2019, 99(4):1568-1576.
[57] SPOTTI M J, TARHAN Ö, SCHAFFTER S, et al.Whey protein gelation induced by enzymatic hydrolysis and heat treatment:Comparison of creep and recovery behavior[J].Food Hydrocolloids, 2017, 63:696-704.
[58] BARBEAU W E.Functional properties of leaf proteins:Criteria required in food applications[J].Italian Journal of Food Science, 1990, 2(4):213-225.
[59] FU T J, ABBOTT U R, HATZOS C.Digestibility of food allergens and nonallergenic proteins in simulated gastric fluid and simulated intestinal fluid: A comparative study[J].Journal of Agricultural and Food Chemistry, 2002, 50(24):7154-7160.
[60] KANDEMIR-CAVAS C, PÉREZ-SANCHEZ H, MERT-OZUPEK N, et al.In silico analysis of bioactive peptides in invasive sea grass Halophila stipulacea[J].Cells, 2019, 8(6):557.
[61] SAITO Y, WANEZAKI K, KAWATO A, et al.Antihypertensive effects of peptide in sake and its by-products on spontaneously hypertensive rats[J].Bioscience, Biotechnology, and Biochemistry, 1994, 58(5):812-816.
[62] KOBBI S, BALTI R, BOUGATEF A, et al.Antibacterial activity of novel peptides isolated from protein hydrolysates of RuBisCO purified from green juice alfalfa[J].Journal of Functional Foods, 2015, 18:703-713.
[63] STEFANO E D, AGYEI D, NJOKU E N, et al.Plant RuBisCO:An underutilized protein for food applications[J].Journal of the American Oil Chemists' Society, 2018,95:1063-1074.
Outlines

/