Phenylpropanoid Content of Chickpea Seed Coats in Relation to Seed Dormancy
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
CZ.02.1.01/0.0/0.0/16_019/0000827
Ministry of Agriculture
PubMed
37514301
PubMed Central
PMC10384132
DOI
10.3390/plants12142687
PII: plants12142687
Knihovny.cz E-zdroje
- Klíčová slova
- chickpea, dormancy, flavonoids, legumes, phenolic acids, seed coat,
- Publikační typ
- časopisecké články MeSH
The physical dormancy of seeds is likely to be mediated by the chemical composition and the thickness of the seed coat. Here, we investigate the link between the content of phenylpropanoids (i.e., phenolics and flavonoids) present in the chickpea seed coat and dormancy. The relationship between selected phenolic and flavonoid metabolites of chickpea seed coats and dormancy level was assessed using wild and cultivated chickpea parental genotypes and a derived population of recombinant inbred lines (RILs). The selected phenolic and flavonoid metabolites were analyzed via the LC-MS/MS method. Significant differences in the concentration of certain phenolic acids were found among cultivated (Cicer arietinum, ICC4958) and wild chickpea (Cicer reticulatum, PI489777) parental genotypes. These differences were observed in the contents of gallic, caffeic, vanillic, syringic, p-coumaric, salicylic, and sinapic acids, as well as salicylic acid-2-O-β-d-glucoside and coniferaldehyde. Additionally, significant differences were observed in the flavonoids myricetin, quercetin, luteolin, naringenin, kaempferol, isoorientin, orientin, and isovitexin. When comparing non-dormant and dormant RILs, significant differences were observed in gallic, 3-hydroxybenzoic, syringic, and sinapic acids, as well as the flavonoids quercitrin, quercetin, naringenin, kaempferol, and morin. Phenolic acids were generally more highly concentrated in the wild parental genotype and dormant RILs. We compared the phenylpropanoid content of chickpea seed coats with related legumes, such as pea, lentil, and faba bean. This information could be useful in chickpea breeding programs to reduce dormancy.
Czech Advanced Technology and Research Institute Palacký University 783 71 Olomouc Czech Republic
Department of Botany Faculty of Science Palacký University 783 71 Olomouc Czech Republic
Department of Plant Biology Mendel University in Brno 613 00 Brno Czech Republic
Zobrazit více v PubMed
Gil J., Cubero J.I. Inheritance of Seed Coat Thickness in Chickpea (Cicer arietinum L.) and its Evolutionary Implications. Plant Breed. 1993;111:257–260. doi: 10.1111/j.1439-0523.1993.tb00639.x. DOI
Merga B., Haji J. Economic importance of chickpea: Production, value, and world trade. Cogent Food Agric. 2019;5:1615718. doi: 10.1080/23311932.2019.1615718. DOI
Redden R.J., Berger J.D. History and origin of chickpea. In: Yadav S.S., Redden R.J., Chen W., Sharma B., editors. Chickpea Breeding and Management. CABI; Wallingford, UK: 2007. pp. 1–13. DOI
Sedláková V., Hanáček P., Grulichová M., Zablatzká L., Smýkal P. Evaluation of Seed Dormancy, One of the Key Domestication Traits in Chickpea. Agronomy. 2021;11:2292. doi: 10.3390/agronomy11112292. DOI
Varma Penmetsa R., Carrasquilla-Garcia N., Bergmann E.M., Vance L., Castro B., Kassa M.T., Sarma B.K., Datta S., Farmer A.D., Baek J., et al. Multiple post-domestication origins of kabuli chickpea through allelic variation in a diversification-associated transcription factor. New Phytol. 2016;211:1440–1451. doi: 10.1111/nph.14010. PubMed DOI
Kudapa H., Garg V., Chitikineni A., Varshney R.K. The RNA-Seq-based high resolution gene expression atlas of chickpea (Cicer arietinum L.) reveals dynamic spatio-temporal changes associated with growth and development: RNA-Seq based chickpea gene expression atlas. Plant Cell Environ. 2018;41:2209–2225. doi: 10.1111/pce.13210. PubMed DOI
Tor-Roca A., Garcia-Aloy M., Mattivi F., Andres-Lacueva C., Urpi-Sarda M. Phytochemicals in Legumes: A Qualitative Reviewed Analysis. J. Agric. Food Chem. 2020;68:13486–13496. doi: 10.1021/acs.jafc.0c04387. PubMed DOI
Singh B., Singh J.P., Kaur A., Singh N. Phenolic composition and antioxidant potential of grain legume seeds: A review. Food Res. Int. 2017;101:1–16. doi: 10.1016/j.foodres.2017.09.026. PubMed DOI
Deng Y., Lu S. Biosynthesis and Regulation of Phenylpropanoids in Plants. Crit. Rev. Plant Sci. 2017;36:257–290. doi: 10.1080/07352689.2017.1402852. DOI
Corso M., Perreau F., Mouille G., Lepiniec L. Specialized phenolic compounds in seeds: Structures, functions, and regulations. Plant Sci. 2020;296:110471. doi: 10.1016/j.plantsci.2020.110471. PubMed DOI
Balarynová J., Klčová B., Sekaninová J., Kobrlová L., Cechová M.Z., Krejčí P., Leonová T., Gorbach D., Ihling C., Smržová L., et al. The loss of polyphenol oxidase function is associated with hilum pigmentation and has been selected during pea domestication. New Phytol. 2022;235:1807–1821. doi: 10.1111/nph.18256. PubMed DOI
Duenas M., Hernandez T., Estrella I. Assessment of in vitro antioxidant capacity of the seed coat and the cotyledon of legumes in relation to their phenolic contents. Food Chem. 2006;98:95–103. doi: 10.1016/j.foodchem.2005.05.052. DOI
Gan R.-Y., Deng Z.-Q., Yan A.-X., Shah N.P., Lui W.-Y., Chan C.-L., Corke H. Pigmented edible bean coats as natural sources of polyphenols with antioxidant and antibacterial effects. LWT. 2016;73:168–177. doi: 10.1016/j.lwt.2016.06.012. DOI
Smýkal P., Nelson M., Berger J., Von Wettberg E. The Impact of Genetic Changes during Crop Domestication. Agronomy. 2018;8:119. doi: 10.3390/agronomy8070119. DOI
Zhou S., Sekizaki H., Yang Z., Sawa S., Pan J. Phenolics in the Seed Coat of Wild Soybean (Glycine soja) and Their Significance for Seed Hardness and Seed Germination. J. Agric. Food Chem. 2010;58:10972–10978. doi: 10.1021/jf102694k. PubMed DOI
Smýkal P., Vernoud V., Blair M.W., Soukup A., Thompson R.D. The role of the testa during development and in establishment of dormancy of the legume seed. Front. Plant Sci. 2014;5:351. doi: 10.3389/fpls.2014.00351. PubMed DOI PMC
Hradilová I., Trněný O., Válková M., Cechová M., Janská A., Prokešová L., Aamir K., Krezdorn N., Rotter B., Winter P., et al. A Combined Comparative Transcriptomic, Metabolomic, and Anatomical Analyses of Two Key Domestication Traits: Pod Dehiscence and Seed Dormancy in Pea (Pisum sp.) Front. Plant Sci. 2017;8:542. doi: 10.3389/fpls.2017.00542. PubMed DOI PMC
Hradilová I., Duchoslav M., Brus J., Pechanec V., Hýbl M., Kopecký P., Smržová L., Štefelová N., Vaclávek T., Bariotakis M., et al. Variation in wild pea (Pisum sativum subsp. elatius) seed dormancy and its relationship to the environment and seed coat traits. PeerJ. 2019;7:e6263. doi: 10.7717/peerj.6263. PubMed DOI PMC
Wyatt J.E. Seed Coat and Water Absorption Properties of Seed of Near-isogenic Snap Bean Lines Differing in Seed Coat Color. J. Am. Soc. Hortic. 1977;102:478–480. doi: 10.21273/JASHS.102.4.478. DOI
Werker E., Marbach I., Mayer A.M. Relation between the Anatomy of the Testa, Water Permeability and the Presence of Phenolics in the Genus Pisum. Ann. Bot. 1979;43:765–771. doi: 10.1093/oxfordjournals.aob.a085691. DOI
Kantar F., Pilbeam C.J., Hebblethwaite P.D. Effect of tannin content of faba bean (Vicia faba) seed on seed vigour, germination and field emergence. Ann. Appl. Biol. 1996;128:85–93. doi: 10.1111/j.1744-7348.1996.tb07092.x. DOI
Moïse J.A., Han S., Gudynaite-Savitch L., Johnson D.A., Miki B.L.A. Seed coats: Structure, development, composition, and biotechnology. In Vitro Cell. Dev. Biol. 2005;41:620–644. doi: 10.1079/IVP2005686. DOI
Marbach I., Mayer A.M. Permeability of Seed Coats to Water as Related to Drying Conditions and Metabolism of Phenolics. Plant Physiol. 1974;54:817–820. doi: 10.1104/pp.54.6.817. PubMed DOI PMC
Caldas G.V., Blair M.W. Inheritance of seed condensed tannins and their relationship with seed-coat color and pattern genes in common bean (Phaseolus vulgaris L.) Theor. Appl. Genet. 2009;119:131–142. doi: 10.1007/s00122-009-1023-4. PubMed DOI
Díaz A.M., Caldas G.V., Blair M.W. Concentrations of condensed tannins and anthocyanins in common bean seed coats. Food Res. Int. 2010;43:595–601. doi: 10.1016/j.foodres.2009.07.014. DOI
Ramsay G. Inheritance and linkage of a gene for testa-imposed seed dormancy in faba bean (Vicia faba L.) Plant Breed. 1997;116:287–289. doi: 10.1111/j.1439-0523.1997.tb00998.x. DOI
Liu W., Peffley E.B., Powell R.J., Auld D.L., Hou A. Association of seedcoat color with seed water uptake, germination, and seed components in guar (Cyamopsis tetragonoloba (L.) Taub) J. Arid Environ. 2007;70:29–38. doi: 10.1016/j.jaridenv.2006.12.011. DOI
Legesse N., Powel A.A. Relationship between the development of seed coat pigmentation, seed coat adherence to the cotyledons and the rate of imbibition during the maturation of grain legumes. Seed Sci. Technol. 1996;24:23–32.
Lepiniec L., Debeaujon I., Routaboul J.-M., Baudry A., Pourcel L., Nesi N., Caboche M. Genetics and biochemistry of seed flavonoids. Ann. Rev. Plant Biol. 2006;57:405–430. doi: 10.1146/annurev.arplant.57.032905.105252. PubMed DOI
Vogt T. Phenylpropanoid Biosynthesis. Mol. Plant. 2010;3:2–20. doi: 10.1093/mp/ssp106. PubMed DOI
Marchiosi R., dos Santos W.D., Constantin R.P., de Lima R.B., Soares A.R., Finger-Teixeira A., Mota T.R., de Oliveira D.M., Foletto-Felipe M.P., Abrahão J., et al. Biosynthesis and metabolic actions of simple phenolic acids in plants. Phytochem. Rev. 2020;19:865–906. doi: 10.1007/s11101-020-09689-2. DOI
Šamec D., Karalija E., Šola I., Bok V.V., Salopek-Sondi B. The Role of Polyphenols in Abiotic Stress Response: The Influence of Molecular Structure. Plants. 2021;10:118. doi: 10.3390/plants10010118. PubMed DOI PMC
Dong N.-Q., Lin H.-X. Contribution of phenylpropanoid metabolism to plant development and plant–environment interactions. J. Integr. Plant Biol. 2020;1:180–209. doi: 10.1111/jipb.13054. PubMed DOI
Shah F.A., Ni J., Chen J., Wang Q., Lie W., Chen X., Tang C., Fu S., Wu L. Proanthocyanidins in seed coat tegmen and endospermic cap inhibit seed germination in Sapium sebiferum. PeerJ. 2018;6:e4690. doi: 10.7717/peerj.4690. PubMed DOI PMC
Appelhagen I., Thiedig K., Nordholt N., Schmidt N., Huep G., Sagasser M., Weisshaar B. Update on transparent testa mutants from Arabidopsis thaliana: Characterisation of new alleles from an isogenic collection. Planta. 2014;240:955–970. doi: 10.1007/s00425-014-2088-0. PubMed DOI
Diederichsen A., Jones-Flory L.L. Accelerated aging tests with seeds of 11 flax (Linum usitatissimum) cultivars. Seed Sci. Technol. 2005;33:419–429. doi: 10.15258/sst.2005.33.2.14. DOI
Zhang X.K., Yang G.T., Chen L., Yin J.M., Tang Z.L., Li J.N. Physiological differences between yellow-seeded and black-seeded rapeseed (Brassica napus L.) with different testa characteristics during artificial ageing. Seed Sci. Technol. 2006;34:373–381. doi: 10.15258/sst.2006.34.2.13. DOI
Li X., Li S., Wang J., Chen G., Tao X., Xu S. Metabolomic Analysis Reveals Domestication-Driven Reshaping of Polyphenolic Antioxidants in Soybean Seeds. Antioxidants. 2023;12:912. doi: 10.3390/antiox12040912. PubMed DOI PMC
Baudry A., Heim M.A., Dubreucq B., Caboche M., Weisshaar B., Lepiniec L. TT2, TT8, and TTG1 synergistically specify the expression of BANYULS and proanthocyanidin biosynthesis in Arabidopsis thaliana. Plant J. 2004;39:366–380. doi: 10.1111/j.1365-313X.2004.02138.x. PubMed DOI
Debeaujon I., Léon-Kloosterziel K.M., Koornneef M. Influence of the Testa on Seed Dormancy, Germination, and Longevity in Arabidopsis. Plant Physiol. 2000;122:403–414. doi: 10.1104/pp.122.2.403. PubMed DOI PMC
Francoz E., Lepiniec L., North H.M. Seed coats as an alternative molecular factory: Thinking outside the box. Plant Reprod. 2018;31:327–342. doi: 10.1007/s00497-018-0345-2. PubMed DOI
Alseekh S., Scossa F., Wen W., Luo J., Yan J., Beleggia R., Klee H.J., Huang S., Papa R., Fernie A.R. Domestication of Crop Metabolomes: Desired and Unintended Consequences. Trends Plant Sci. 2021;26:650–661. doi: 10.1016/j.tplants.2021.02.005. PubMed DOI
Ku Y.S., Contador C.A., Ng M.S., Yu J., Chung G., Lam H.M. The Effects of Domestication on Secondary Metabolite Composition in Legumes. Front. Genet. 2020;11:581357. doi: 10.3389/fgene.2020.581357. PubMed DOI PMC
Paauw M., Koes R., Quattrocchio F.M. Alteration of flavonoid pigmentation patterns during domestication of food crops. J. Exp. Bot. 2019;70:3719–3735. doi: 10.1093/jxb/erz141. PubMed DOI
Troszyńska A., Ciska E. Phenolic compounds of seed coats of white and coloured varieties of pea (Pisum sativum L.) and their total antioxidant activity. Czech J. Food Sci. 2002;20:15–22. doi: 10.17221/3504-CJFS. DOI
Ferraro K., Jin A.L., Nguyen T.D., Reinecke D.M., Ozga J.A., Ro D.K. Characterization of proanthocyanidin metabolism in pea (Pisum sativum) seeds. BMC Plant Biol. 2014;14:238. doi: 10.1186/s12870-014-0238-y. PubMed DOI PMC
Jha A.B., Purves R.W., Elessawy F.M., Zhang H., Vandenberg A., Warkentin T.D. Polyphenolic Profile of Seed Components of White and Purple Flower Pea Lines. Crop Sci. 2019;59:2711–2719. doi: 10.2135/cropsci2019.04.0279. DOI
Segev A., Badani H., Kapulnik Y., Shomer I., Oren-Shamir M., Galili S. Determination of Polyphenols, Flavonoids, and Antioxidant Capacity in Colored Chickpea (Cicer arietinum L.) J. Food Sci. 2010;75:115–119. doi: 10.1111/j.1750-3841.2009.01477.x. PubMed DOI
Xu B.J., Yuan S.H., Chang S.K.C. Comparative Analyses of Phenolic Composition, Antioxidant Capacity, and Color of Cool Season Legumes and Other Selected Food Legumes. J. Food Sci. 2007;72:167–177. doi: 10.1111/j.1750-3841.2006.00261.x. PubMed DOI
Pang Y., Peel G.J., Wright E., Wang Z., Dixon R.A. Early Steps in Proanthocyanidin Biosynthesis in the Model Legume Medicago truncatula. Plant Phys. 2007;145:601–615. doi: 10.1104/pp.107.107326. PubMed DOI PMC
Zhao J., Dixon R.A. MATE Transporters Facilitate Vacuolar Uptake of Epicatechin 3′-O-Glucoside for Proanthocyanidin Biosynthesis in Medicago truncatula and Arabidopsis. Plant Cell. 2009;21:2323–2340. doi: 10.1105/tpc.109.067819. PubMed DOI PMC
Zhao J., Huhman D., Shadle G., He X.Z., Summer L.W., Tang Y., Dixon R.A. MATE2 Mediates Vacuolar Sequestration of Flavonoid Glycosides and Glycoside Malonates in Medicago truncatula. Plant Cell. 2011;23:1536–1555. doi: 10.1105/tpc.110.080804. PubMed DOI PMC
Galussi A.A., Argüello J.A., Moya M.E., Zuriaga F.D., Zimmermann L.R. Seed dormancy mechanism as a factor influencing seed physiological quality in alfalfa (Medicago sativa) cv. Baralfa 85. Seed Sci. Technol. 2013;41:50–59. doi: 10.15258/sst.2013.41.1.05. DOI
Desta K.T., Hur O.S., Lee S., Yoon H., Shin M.J., Yi J., Lee Y., Ro Y.R., Wang X., Choi Y.M. Origin and seed coat color differently affect the concentrations of metabolites and antioxidant activities in soybean (Glycine max (L.) Merrill) seeds. Food Chem. 2022;381:132249. doi: 10.1016/j.foodchem.2022.132249. PubMed DOI
Senda M., Yamaguchi N., Hiraoka M., Kawada S., Iiyoshi R., Yamashita K., Sonoki T., Maeda H., Kawasaki M. Accumulation of proanthocyanidins and/or lignin deposition in buff-pigmented soybean seed coats may lead to frequent defective cracking. Planta. 2017;245:659–670. doi: 10.1007/s00425-016-2638-8. PubMed DOI
Elessawy F.M., Wright D., Vandenberg A., El-Aneed A., Purves R.W. Mass Spectrometry-Based Untargeted Metabolomics Reveals the Importance of Glycosylated Flavones in Patterned Lentil Seed Coats. J. Agric. Food Chem. 2023;71:3541–3549. doi: 10.1021/acs.jafc.2c07844. PubMed DOI PMC
Kaur K., Grewal S.K., Gill P.S., Singh S. Comparison of cultivated and wild chickpea genotypes for nutritional quality and antioxidant potential. J. Food Sci. Technol. 2019;56:1864–1876. doi: 10.1007/s13197-019-03646-4. PubMed DOI PMC
Lamichaney A., Kudekallu S. Differences in seed vigour traits between desi (pigmented) and kabuli (non-pigmented) ecotypes of chickpea (Cicer arietinum) and its association with field emergence. J. Environ. Biol. 2017;38:735–742. doi: 10.22438/jeb/38/5/MRN-340. DOI
Wood J.A., Knights E.J., Choct M. Morphology of Chickpea Seeds (Cicer arietinum L.): Comparison of desi and kabuli Types. Int. J. Plant Sci. 2011;172:632–643. doi: 10.1086/659456. DOI
Aguilera Y., Estrella I., Benitez V., Esteban R.M., Martín-Cabrejas M. Bioactive phenolic compounds and functional properties of dehydrated bean flours. Food Res. Int. 2011;44:774–780. doi: 10.1016/j.foodres.2011.01.004. DOI
Fratianni F., Cardinale F., Cozzolino A., Granese T., Albanese D., Di Matteo M., Zaccardelli M., Coppolo R., Nazzaro F. Polyphenol composition and antioxidant activity of different grass pea (Lathyrus sativus), lentils (Lens culinaris), and chickpea (Cicer arietinum) ecotypes of the Campania region (Southern Italy) J. Funct. Foods. 2014;7:551–557. doi: 10.1016/j.jff.2013.12.030. DOI
Magalhães S.C.Q., Taveira M., Cabrita A.R.J., Fonseca A.J.M., Valentao P., Andrade P.B. European marketable grain legume seeds: Further insight into phenolic compounds profiles. Food Chem. 2017;215:177–184. doi: 10.1016/j.foodchem.2016.07.152. PubMed DOI
Elessawy F.M., Bazghaleh N., Vandenberg A., Purves R.W. Polyphenol profile comparisons of seed coats of five pulse crops using a semi-quantitative liquid chromatography-mass spectrometric method. Phytochem. Anal. 2019;31:458–471. doi: 10.1002/pca.2909. PubMed DOI
Amarowicz R., Pegg R.B. Legumes as a source of natural antioxidants. Eur. J. Lipid Sci. Technol. 2008;110:865–878. doi: 10.1002/ejlt.200800114. DOI
Pathiraja D., Wanasundara J.P.D., Elessawy F.M., Purves R.W., Vandenberg A., Shand P.J. Water-soluble phenolic compounds and their putative antioxidant activities in the seed coats from different lentil (Lens culinaris) genotypes. Food Chem. 2023;407:135145. doi: 10.1016/j.foodchem.2022.135145. PubMed DOI
Quintero-Soto M.F., Saracho-Peña A.G., Chavez-Ontiveros J., Garzon-Tiznado J.A., Pineda-Hidalgo K.V., Delgado-Vargas F., Lopez-Valenzuela J.A. Phenolic profiles and their contribution to the antioxidant activity of selected chickpea genotypes from Mexico and ICRISAT collections. Plant Foods Hum. Nutr. 2018;73:122–129. doi: 10.1007/s11130-018-0661-6. PubMed DOI
Mirali M., Purves R.W., Vandenberg A. Profiling the Phenolic Compounds of the Four Major Seed Coat Types and Their Relation to Color Genes in Lentil. J. Nat. Prod. 2017;80:1310–1317. doi: 10.1021/acs.jnatprod.6b00872. PubMed DOI
Zhu L., Li W., Deng Z., Li H., Zhang B. The Composition and Antioxidant Activity of Bound Phenolics in Three Legumes, and Their Metabolism and Bioaccessibility of Gastrointestinal Tract. Foods. 2020;9:1816. doi: 10.3390/foods9121816. PubMed DOI PMC
Yeo J.D., Shahidi F. Identification and quantification of soluble and insoluble-bound phenolics in lentil hulls using HPLC-ESI-MS/MS and their antioxidant potential. Food Chem. 2020;315:126202. doi: 10.1016/j.foodchem.2020.126202. PubMed DOI
Rivas-San Vincente M., Plasencia J. Salicylic acid beyond defence: Its role in plant growth and development. J. Exp. Bot. 2011;62:3321–3338. doi: 10.1093/jxb/err031. PubMed DOI
Zeljković S.Ć., Komzáková K., Šišková J., Karalija E., Smékalová K., Tarkowski P. Phytochemical variability of selected basil genotypes. Ind. Crop. Prod. 2020;157:112910. doi: 10.1016/j.indcrop.2020.112910. DOI
Zeljković S.Ć., Šišková J., Komzáková K., De Diego N., Kaffková K., Tarkowski P. Phenolic Compounds and Biological Activity of Selected Mentha Species. Plants. 2021;10:550. doi: 10.3390/plants10030550. PubMed DOI PMC