The loss of polyphenol oxidase function is associated with hilum pigmentation and has been selected during pea domestication
Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
35585778
DOI
10.1111/nph.18256
Knihovny.cz E-zdroje
- Klíčová slova
- dormancy, gallocatechin, germination, laccase, legumes, polyphenol oxidase, seed coat, seeds,
- MeSH
- domestikace MeSH
- hrách setý * genetika metabolismus MeSH
- katecholoxidasa * genetika metabolismus MeSH
- pigmentace MeSH
- proteomika MeSH
- semena rostlinná genetika metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- katecholoxidasa * MeSH
Seed coats serve as protective tissue to the enclosed embryo. As well as mechanical there are also chemical defence functions. During domestication, the property of the seed coat was altered including the removal of the seed dormancy. We used a range of genetic, transcriptomic, proteomic and metabolomic approaches to determine the function of the pea seed polyphenol oxidase (PPO) gene. Sequencing analysis revealed one nucleotide insertion or deletion in the PPO gene, with the functional PPO allele found in all wild pea samples, while most cultivated peas have one of the three nonfunctional ppo alleles. PPO functionality cosegregates with hilum pigmentation. PPO gene and protein expression, as well as enzymatic activity, was downregulated in the seed coats of cultivated peas. The functionality of the PPO gene relates to the oxidation and polymerisation of gallocatechin in the seed coat. Additionally, imaging mass spectrometry supports the hypothesis that hilum pigmentation is conditioned by the presence of both phenolic precursors and sufficient PPO activity. Taken together these results indicate that the nonfunctional polyphenol oxidase gene has been selected during pea domestication, possibly due to better seed palatability or seed coat visual appearance.
Agricultural Research Ltd Troubsko 664 41 Czech Republic
Department of Biochemistry Faculty of Sciences Palacky University Olomouc 783 71 Czech Republic
Department of Biochemistry St Petersburg State University St Petersburg 199004 Russia
Department of Bioorganic Chemistry Leibniz Institut für Pflanzenbiochemie Halle 06120 Germany
Department of Botany Faculty of Sciences Palacky University Olomouc 783 71 Czech Republic
Zobrazit více v PubMed
Appelhagen I, Thiedig K, Nordholt N, Schmidt N, Huep G, Sagasser M, Weisshaar B. 2014. Update on transparent testa mutants from Arabidopsis thaliana: characterisation of new alleles from an isogenic collection. Planta 240: 955-970.
Baskin C, Baskin JM. 2014. Seed ecology, biogeography, and evolution of dormancy and germination, 2nd edn. London, UK: Academic Press & Elsevier.
Blaschek L, Pesquet E. 2021. Phenoloxidases in plants-how structural diversity enables functional specificity. Frontiers in Plant Sciences 12: 754601.
Boeckx T, Winters A, Webb KJ, Kingston-Smith AH. 2017. Detection of potential chloroplastic substrates for polyphenol oxidase suggests a role in undamaged leaves. Frontiers in Plant Science 8: 237.
Cai X, Davis EJ, Ballif J, Liang M, Bushman E, Haroldsen V, Torabinejad J, Wu Y. 2006. Mutant identification and characterization of the laccase gene family in Arabidopsis. Journal of Experimental Botany 57: 2563-2569.
Cechová M, Válková M, Hradilová I, Janská A, Soukup A, Smýkal P, Bednář P. 2017. Towards better understanding of pea seed dormancy using laser desorption/ionization mass spectrometry. International Journal of Molecular Sciences 18: 2196.
Constabel CP, Barbehenn R. 2008. Defensive roles of polyphenol oxidase in plants. In: Schaller A, ed. Induced plant resistance to herbivory. Dordrecht, the Netherlands: Springer Science and Business Media, 253-269.
Corso M, Perreau F, Mouille G, Lepiniec L. 2020. Specialized phenolic compounds in seeds: structures, functions, and regulations. Plant Science 296: 110471.
Dalling JW, Davis AS, Schutte BJ, Elizabeth AA. 2011. Seed survival in soil: interacting effects of predation, dormancy and the soil microbial community. Journal of Ecology 99: 89-95.
Debeaujon I, Léon-Kloosterziel KM, Koornneef M. 2000. Influence of the testa on seed dormancy, germination, and longevity in Arabidopsis. Plant Physiology 122: 403-414.
Deng Y, Lu S. 2017. Biosynthesis and regulation of phenylpropanoids in plants. Critical Reviews in Plant Sciences 36: 257-290.
Egley GH, Paul RN, Vaughn KC, Duke SO. 1983. Role of peroxidase in the development of water-impermeable seed coats in Sida spinosa L. Planta 157: 224-232.
Elessawy FM, Vandenberg A, El-Aneed A, Purves RW. 2021. An untargeted metabolomics approach for correlating pulse crop seed coat polyphenol profiles with antioxidant capacity and iron chelation ability. Molecules 26: 3833.
Fei X, Qi Y, Lei Y, Wang S, Hu H, Wei A. 2021. Transcriptome and metabolite analysis reveals key genes for melanin synthesis during the development of Zanthoxylum bungeanum seeds. Industrial Crops and Products 165: 113419.
Fu F, Zhang W, Li YY, Wang HL. 2017. Establishment of the model system between phytochemicals and gene expression profiles in macrosclereid cells of Medicago truncatula. Scientific Reports 7: 2580.
Fuerst EP, Anderson JV, Kennedy AC, Gallagher RS. 2011. Induction of polyphenol oxidase activity in dormant wild oat (Avena fatua) seeds and caryopses: a defense response to seed decay fungi. Weed Science 59: 137-144.
Fuerst EP, Anderson JV, Morris CF. 2006. Polyphenol oxidase in wheat grain: whole kernel and bran assays for total and soluble activity. Cereal Chemistry 83: 10-16.
Fuerst EP, Okubara PA, Anderson JV, Morris CF. 2014. Polyphenol oxidase as a biochemical seed defense mechanism. Frontiers in Plant Science 5: 689.
Fukunaga K, Nur MZ, Inoue T, Taketa S, Ichitani K. 2020. Phylogenetic analysis of the Si7PPO gene in foxtail millet, Setaria italica, provides further evidence for multiple origins of the negative phenol color reaction phenotype. Genes & Genetic Systems 95: 191-199.
Gali KK, Sackville A, Tafesse EG, Lachagari VBR, McPhee K, Hybl M, Mikić A, Smýkal P, McGee R, Burstin J et al. 2019. Genome-wide association mapping for agronomic and seed quality traits of field pea (Pisum sativum L.). Frontiers in Plant Science 10: 1538.
Glagoleva AY, Shoeva OY, Khlestkina EK. 2020. Melanin pigment in plants: current knowledge and future perspectives. Frontiers in Plant Science 11: 770.
Govorov LI. 1928. Pea of Afghanistan (on a problem of the origin of cultivated pea). Bulletin of Applied Botany, Genetics and Plant Breeding 19: 497-522.
Gross BL, Skare KJ, Olsen KM. 2009. Novel Phr1 mutations and the evolution of phenol reaction variation in US weedy rice (Oryza sativa). New Phytologist 184: 842-850.
Hellens RP, Moreau C, Lin-Wang K, Schwinn KE, Thomson SJ, Fiers MWEJ, Frew TJ, Murray SR, Hofer JMI, Jacobs JME et al. 2010. Identification of mendel's white flower character. PLoS ONE 5: e13230.
Hollander JL, Wall SBV, Longland WS. 2012. Olfactory detection of caches containing wildland versus cultivated seeds by granivorous rodents. Western North American Naturalist 72: 339-347.
Hradilová I, Duchoslav M, Brus J, Pechanec V, Hýbl M, Kopecký P, Smržová L, Štefelová N, Vaclávek T, Bariotakis M et al. 2019. Variation in wild pea (Pisum sativum ssp. elatius) seed dormancy and its relationship to the environment and seed coat traits. PeerJ 7: e6263.
Hradilová I, Trněný O, Válková M, Cechová M, Janská A, Prokešová L, Aamir K, Krezdorn N, Rotter B, Winter P et al. 2017. A combined comparative transcriptomic, metabolomic, and anatomical analyses of two key domestication traits: pod dehiscence and seed dormancy in pea (Pisum sp.). Frontiers in Plant Science 8: 542.
Inoue T, Yuo T, Ohta T, Hitomi E, Ichitani K, Kawase M, Taketa S, Fukunaga K. 2015. Multiple origins of the phenol reaction negative phenotype in foxtail millet, Setaria italica (L.) P. Beauv., were caused by independent loss-of-function mutations of the polyphenol oxidase (Si7PPO) gene during domestication. Molecular Genetics and Genomics 290: 1563-1574.
Janská A, Pecková E, Sczepaniak B, Smýkal P, Soukup A. 2019. The role of the testa during the establishment of physical dormancy in the pea seed. Annals of Botany 123: 815-829.
Jha AB, Purves RW, Elessawy FM, Zhang H, Vandenberg A, Warkentin TD. 2019. Polyphenolic profile of seed components of white and purple flower pea lines. Crop Science 59: 2711-2719.
Khazaei H, O'Sullivan DM, Jones H, Pitts N, Sillanpää MJ, Pärssinen P, Manninen O, Stoddard FL. 2015. Flanking SNP markers for vicine-convicine concentration in faba bean (Vicia faba L.). Molecular Breeding 35: 38.
Kreplak J, Madoui M-A, Cápal P, Novák P, Labadie K, Aubert G, Bayer PE, Gali KK, Syme RA, Main D et al. 2019. A reference genome for pea provides insight into legume genome evolution. Nature Genetics 51: 1411-1422.
Kuznetsova A, Brockhoff PB, Christensen RH. 2017. lmertest package: tests in linear mixed effects models. Journal of Statistical Software 82: 1-26.
Labeeuw L, Martone PT, Boucher Y, Case RJ. 2015. Ancient origin of the biosynthesis of lignin precursors. Biology Direct 10: 23.
Lamprecht H. 1948. The variation of linkage and the course of crossing-over. Agri Hortique Genetica 6: 10-48.
Letunic I, Bork P. 2021. Interactive tree of life (iTOL) v.5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Research 49: W293-W296.
Liang M, Davis E, Gardner D, Cai X, Wu Y. 2006. Involvement of AtLAC15 in lignin synthesis in seeds and in root elongation of Arabidopsis. Planta 224: 1185-1196.
Liu X, Bouxin FP, Fan J, Budarin VL, Hu C, Clark JH. 2020. Recent advances in the catalytic depolymerization of lignin towards phenolic chemicals: a review. ChemSusChem 13: 4296.
Lock RH. 1907. On the inheritance of certain invisible characters in peas. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 79: 28-34.
Makasheva RKH. 1979. Flora of cultivated plants. IV. Grain legumes. Part 1. Pea. Leningrad, Russia: Kolos.
Mamontova T, Afonin AM, Ihling C, Soboleva A, Lukasheva E, Sulima AS, Shtark OY, Akhtemova GA, Povydysh MN, Sinz A et al. 2019. Profiling of seed proteome in pea (Pisum sativum L.) lines characterized with high and low responsivity to combined inoculation with nodule bacteria and arbuscular mycorrhizal fungi. Molecules 24: 1603.
Mamontova T, Lukasheva E, Mavropolo-Stolyarenko G, Proksch C, Bilova T, Kim A, Babakov V, Grishina T, Hoehenwarter W, Medvedev S et al. 2018. Proteome map of pea (Pisum sativum L.) embryos containing different amounts of residual chlorophylls. International Journal of Molecular Sciences 19: 4066.
Marbach I, Mayer AM. 1974. Permeability of seed coats to water as related to drying conditions and metabolism of phenolics 1. Plant Physiology 54: 817-820.
Marbach I, Mayer AM. 1975. Changes in catechol oxidase and permeability to water in seed coats of Pisum elatius during seed development and maturation. Plant Physiology 56: 93-96.
Marbach I, Mayer AM. 1978. Formation of catechol oxidase in seed coats of Pisum elatius during seed maturation. Journal of Experimental Botany 29: 69-75.
Marles MAS, Vandenberg A, Bett KE. 2008. Polyphenol oxidase activity and differential accumulation of polyphenolics in seed coats of pinto bean (Phaseolus vulgaris L.) characterize postharvest color changes. Journal of Agricultural and Food Chemistry 56: 7049-7056.
Matamoros MA, Kim A, Peñuelas M, Ihling C, Griesser E, Hoffmann R, Fedorova M, Frolov A, Becana M. 2018. Protein carbonylation and glycation in legume nodules. Plant Physiology 177: 1510-1528.
Mayer AM. 2006. Polyphenol oxidases in plants and fungi: going places? A review. Phytochemistry 67: 2318-2331.
Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, Haeseler A, Lanfear R. 2020. IQ-Tree 2: new models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution 37: 1530-1534.
Mnich E, Bjarnholt N, Eudes A, Harholt J, Holland C, Jørgensen B, Larsen FH, Liu M, Manat R, Meyer AS et al. 2020. Phenolic cross-links: building and de-constructing the plant cell wall. Natural Product Reports 37: 919-961.
Naseer S, Lee Y, Lapierre C, Franke R, Nawrath C, Geldner N. 2012. Casparian strip diffusion barrier in Arabidopsis is made of a lignin polymer without suberin. Proceedings of the National Academy of Sciences, USA 109: 10101-10106.
Paauw M, Koes R, Quattrocchio FM. 2019. Alteration of flavonoid pigmentation patterns during domestication of food crops. Journal of Experimental Botany 70: 3719-3735.
Pang Y, Peel GJ, Sharma SB, Tang Y, Dixon RA. 2008. A transcript profiling approach reveals an epicatechin-specific glucosyltransferase expressed in the seed coat of Medicago truncatula. Proceedings of the National Academy of Sciences, USA 105: 14210-14215.
Paulsen TR, Colville L, Kranner I, Daws MI, Högstedt G, Vandvik V, Thompson K. 2013. Physical dormancy in seeds: a game of hide and seek? New Phytologist 198: 496-503.
Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29: e45.
Pollard AT. 2018. Seeds vs fungi: an enzymatic battle in the soil seedbank. Seed Science Research 28: 197-214.
Pourcel L, Routaboul J-M, Cheynier V, Lepiniec L, Debeaujon I. 2007. Flavonoid oxidation in plants: from biochemical properties to physiological functions. Trends in Plant Science 12: 29-36.
Pourcel L, Routaboul J-M, Kerhoas L, Caboche M, Lepiniec L, Debeaujon I. 2005. TRANSPARENT TESTA10 encodes a laccase-like enzyme involved in oxidative polymerization of flavonoids in Arabidopsis seed coat. Plant Cell 17: 2966-2980.
Quideau S, Deffieux D, Douat-Casassus C, Pouységu L. 2011. Plant polyphenols: chemical properties, biological activities, and synthesis. Angewandte Chemie International Edition 50: 586-621.
Raviv B, Aghajanyan L, Granot G, Makover V, Frenkel O, Gutterman Y, Grafi G. 2017. The dead seed coat functions as a long-term storage for active hydrolytic enzymes. PLoS ONE 12: e0181102.
Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A. 2017. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Molecular Biology and Evolution 34: 3299-3302.
Smýkal P, Hradilová I, Trněný O, Brus J, Rathore A, Bariotakis M, Das RR, Bhattacharyya D, Richards C, Coyne CJ et al. 2017. Genomic diversity and macroecology of the crop wild relatives of domesticated pea. Scientific Reports 7: 17384.
Smýkal P, Vernoud V, Blair MW, Soukup A, Thompson RD. 2014. The role of the testa during development and in establishment of dormancy of the legume seed. Frontiers in Plant Science 5: 351.
Stetter MG, Vidal-Villarejo M, Schmid KJ. 2020. Parallel seed color adaptation during multiple domestication attempts of an ancient new world grain. Molecular Biology and Evolution 37: 1407-1419.
Sullivan ML. 2015. Beyond brown: polyphenol oxidases as enzymes of plant specialized metabolism. Frontiers in Plant Science 5: 783.
Sweeney MT, Thomson MJ, Cho YG, Park YJ, Williamson SH, Bustamante CD, McCouch SR. 2007. Global dissemination of a single mutation conferring white pericarp in rice. PLoS Genetics 3: e133.
Swiecicky W. 2019. The catalogue of Pisum genes. Poznan, Poland: Agencja reklamova Kreatiff, 128.
Taketa S, Matsuki K, Amano S, Saisho D, Himi E, Shitsukawa N, Yuo T, Noda K, Takeda K. 2010. Duplicate polyphenol oxidase genes on barley chromosome 2H and their functional differentiation in the phenol reaction of spikes and grains. Journal of Experimental Botany 61: 3983-3993.
Tran LT, Taylor JS, Constabel CP. 2012. The polyphenol oxidase gene family in land plants: lineage-specific duplication and expansion. BMC Genomics 13: 395.
Trněný O, Brus J, Hradilová I, Rathore A, Das RR, Kopecký P, Coyne CJ, Reeves P, Richards C, Smýkal P. 2018. Molecular evidence for two domestication events in the pea crop. Genes 9: 535.
Troszyńska A, Ciska E. 2002. Phenolic compounds of seed coats of white and coloured varieties of pea (Pisum sativum L.) and their total antioxidant activity. Czech Journal of Food Sciences 20: 15-22.
Turlapati PV, Kim K-W, Davin LB, Lewis NG. 2011. The laccase multigene family in Arabidopsis thaliana: towards addressing the mystery of their gene function(s). Planta 233: 439-470.
Weller JL, Liew LC, Hecht VFG, Rajandran V, Laurie RE, Ridge S, Wenden B, Schoor JKV, Jaminon O, Blassiau C et al. 2012. A conserved molecular basis for photoperiod adaptation in two temperate legumes. Proceedings of the National Academy of Sciences, USA 109: 21158-21163.
Werker E, Marbach I, Mayer AM. 1979. Relation between the anatomy of the testa, water permeability and the presence of phenolics in the genus Pisum. Annals of Botany 43: 765-771.
White OE. 1917. Studies of inheritance in Pisum. II. The present state of knowledge of heredity and variation in peas. Proceedings of the American Philosophical Society 56: 487-588.
Yonekura-Sakakibara K, Yamamura M, Matsuda F, Ono E, Nakabayashi R, Sugawara S, Mori T, Tobimatsu Y, Umezawa T, Saito K. 2021. Seed-coat protective neolignans are produced by the dirigent protein AtDP1 and the laccase AtLAC5 in Arabidopsis. Plant Cell 33: 129-152.
Yu Y, Tang T, Qian Q, Wang Y, Yan M, Zeng D, Han B, Wu C-I, Shi S, Li J. 2008. Independent losses of function in a polyphenol oxidase in rice: differentiation in grain discoloration between subspecies and the role of positive selection under domestication. Plant Cell 20: 2946-2959.
Zablatzká L, Balarynová J, Klčová B, Kopecký P, Smýkal P. 2021. Anatomy and histochemistry of seed coat development of wild (Pisum sativum ssp. elatius M. Bieb.) Asch. et Graebn. and domesticated pea (Pisum sativum ssp. sativum L.). International Journal of Molecular Sciences 22: 4602.
Zhuang Y, Zuo D, Tao Y, Cai H, Li L. 2020. Laccase3-based extracellular domain provides possible positional information for directing Casparian strip formation in Arabidopsis. Proceedings of the National Academy of Sciences, USA 117: 15400-15402.
Phenylpropanoid Content of Chickpea Seed Coats in Relation to Seed Dormancy
Domestication has altered the ABA and gibberellin profiles in developing pea seeds
The giant diploid faba genome unlocks variation in a global protein crop