GENES DETERMINING THE SYNTHESIS OF LAVONOID AND MELANIN PIGMENTS IN BARLEY
https://doi.org/10.18699/VJ18.369
Abstract
In addition to the green color caused by chlorophyll, grain and vegetative organs of barley can be colored by compounds of phenolic nature, such as melanins and lavonoids, which include anthocyanins, proanthocyanidins. Due to the wide biological activity of these pigmented compounds and their uncolored precursors in respect to plants and humans, there has recently been an increased interest in studying genes that determine pigmentation in plants. The gene network determining the synthesis of lavonoid pigments is the most studied one. Since the 1970s, structural genes that encode the enzymes of lavonoid metabolism, as well as regulatory genes that determine the tissue-speciic accumulation of these pigments in grain tissues, as well as in vegetative organs have been identiied and localized in the barley genome. The Ant1 and Ant2 genes, determining the accumulation of anthocyanins in grain pericarp, the Ant28 gene controlling the biosynthesis of proanthocyanidins (condensed tannins) in seed coat, as well as the HvMpc2, HvMyc2 and HvWD40 genes responsible for the accumulation of anthocyanins in the aleurone layer of barley grain have been determined. Melanins are less studied pigments of plants. Due to the complex structure and resistance to various solvents, the chemical nature of these pigments has not been established. However, due to the comparative analysis of transcriptomes in the colored and uncolored lemma and grain pericarp of barley near-isogenic lines, it was possible to identify the metabolic pathways underlying the formation of the melanin pigmentation. The proposed article reviews the results of the studies on the genetic control of barley coloration.
About the Authors
O. Yu. ShoevaRussian Federation
Novosibirsk
K. V. Strygina
Russian Federation
Novosibirsk
E. K. Khlestkina
Russian Federation
Novosibirsk, St. Petersburg
References
1. Aastrup S., Outtrup H., Erdal K. Location of the proanthocyanidins in the barley grain. Carlsberg Res. Commun. 1984;49:105-109. DOI 10.1007/BF02913969.
2. Adzhieva V.F., Babak O.G., Shoeva O.Y., Kilchevsky A.V., Khlestkina E.K. Molecular genetic mechanisms of the development of fruit and seed coloration in plants. Russ. J. Genet. Appl. Res. 2016;6(5): 537-552. DOI 10.1134/S2079059716050026.
3. Barley, BinMap 2005. GrainGenes Map Data Report. Available at: http://wheat.pw.usda.gov/cgi-bin/graingenes/report.cgi?class=mapd ata&name=Barley,+BinMap+2005.
4. Biffen R.H. The hybridisation of barleys. J. Agric. Sci. 1907;2(2):183206. DOI 10.1017/S0021859600001271.
5. Bogs J., Downey M.O., Harvey J.S., Ashton A.R., Tanner G.J., Robinson S.P. Proanthocyanidin synthesis and expression of genes encoding leucoanthocyanidin reductase and anthocyanidin reductase in developing grape berries and grapevine leaves. Plant Physiol. 2005; 139(2):652-663. DOI 10.1104/pp.105.064238.
6. Briggs F.N. Linkage relations of factors for resistance to mildew in barley. Genetics. 1945;30(2):115-118.
7. Buckley G.F.H. Inheritance in barley with special reference to the color of caryopsis and lemma. Sci. Agric. 1930;10(7):460-492. DOI 10.4141/sa-1930-0021.
8. Bunea A., Rugină D., Sconţa Z., Pop R.M., Pintea A., Socaciu C., Tăbăran F., Grootaert C., Struijs K., VanCamp J. Anthocyanin determination in blueberry extracts from various cultivars and their antiproliferative and apoptotic properties in B16-F10 metastatic murine melanoma cells. Phytochemistry. 2013;95:436-444. DOI 10.1016/j.phytochem.2013.06.018.
9. Bungartz A., Klaus M., Mathew B., Léon J., Naz A.A. Development of new SNP derived cleaved amplified polymorphic sequence marker set and its successful utilization in the genetic analysis of seed color variation in barley. Genomics. 2016;107(2):100-107. DOI 10.1016/j.ygeno.2015.12.007.
10. Choo T.M., Vigier B., Ho K.M., Ceccarelli S., Grando S., Franckowiak J.D. Comparison of black, purple, and yellow barleys. Genet. Resour. Crop. Evol. 2005;52(2):121-126. DOI 10.1007/S10722-0033086-4.
11. Christensen A.B., Gregersen P.L., Schröder J., Collinge D.B. A chalcone synthase with an unusual substrate preference is expressed in barley leaves in response to UV light and pathogen attack. Plant Mol. Biol. 1998;37(5):849-857.
12. Cockram J., White J., Zuluaga D.L., Smith D., Comadran J., Macaulay M., Luo Z., Kearsey M.J., Werner P., Harrap D., Tapsell C., Liu H., Hedley P.E., Stein N., Schulte D., Steuernagel B., Marshall D.F., Thomas W.T., Ramsay L., Mackay I., Balding D.J., The AGOUEB Consortium, Waugh R., O’Sullivan D.M. Genome-wide association mapping to candidate polymorphism resolution in the unsequenced barley genome. Proc. Natl. Acad. Sci. USA. 2010;107(50):2161121616. DOI 10.1073/pnas.1010179107.
13. Costa J.M., Corey A., Hayes P.M., Jobet C., Kleinhofs A., KopischObusch A., Kramer S.F., Kudrna D., Li M., Riera-Lizarazu O., Sato K., Szucs P., Toojinda T., Vales M.I., Wolfe R.I. Molecular mapping of the Oregon Wolfe Barleys: a phenotypically polymorphic doubled-haploid population. Theor. Appl. Genet. 2001;103(2-3): 415-424.
14. 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 https://doi.org/10.1104/pp.122.2.403.
15. Di Ferdinando M., Brunetti C., Fini A., Tattini M. Flavonoids as antioxidants in plants under abiotic stresses. Ed. P. Ahmad, M.N.V. Prasad. Abiotic Stress Responses in Plants: Metabolism, Productivity and Sustainability. N. Y.: Springer, 2012;159-179. DOI 10.1007/978-14614-0634-1_9.
16. Druka A., Kudrna D., Rostoks N., Brueggeman R., von Wettstein D., Kleinhofs A. Chalcone isomerase gene from rice (Oryza sativa) and barley (Hordeum vulgare): physical, genetic and mutation mapping. Gene. 2003;302:171-178. DOI 10.1016/S0378-1119(02)01105-8.
17. Eslick R.F. Balanced male steriles and dominant pre-flowering selective genes for use in hybrid seed production. Barley Genetics II. 1971; 292-297.
18. Faris D.G. Physiology and genetics of the kernel color of barley. Doctoral dissertation, University of British Columbia, 1955.
19. Fedak G., Tsuchiya T., Helgason S.B. Use of monotelotrisomics for linkage mapping in barley. Can. J. Genet. Cytol. 1972;14:949-957. DOI 10.1139/g72-117
20. Finch R.A., Simpson E. New colours and complementary colour genes in barley. Z. Pflanzenzüchtg. 1978;81:40-53.
21. Franckowiak J.D., Lundqvist U. Descriptions of barley genetic stocks for 2012. Barley Genet. Newsl. 2012;42:36-173.
22. Franckowiak J.D., Lundqvist U., Konishi T. New and revised descriptions of barley genes. Barley Genet. Newsl. 1997;26:22-516.
23. Glagoleva A., Shmakov N., Shoeva O., Vasiliev G., Shatskaya N., Börner A., Afonnikov D.A., Khlestkina E.K. Metabolic pathways and genes identified by RNA-seq analysis of barley near-isogenic lines differing by allelic state of the Black lemma and pericarp (Blp) gene. BMC Plant Biol. 2017;17(1):182. DOI 10.1186/s12870-017-1124-1.
24. Gould K., Davies K.M., Winefield C. Anthocyanins: Biosynthesis, Functions, and Applications. N. Y. Media: Springer Science & Business, 2009.
25. Grotewold E. The Science of Flavonoids. N. Y.: Springer, 2006.
26. Hanson W.D., Kramer H.H. The genetic analysis of two chromosome interchanges in barley from F2 data. Genetics. 1949;34(6):687-700.
27. Harlan H.V. Some distinctions in our cultivated barleys with reference to their use in plant breeding. US Dept. Agric. Bul. 1914;137:38. DOI 10.5962/bhl.title.109258.
28. Himi E., Taketa S. Isolation of candidate genes for the barley Ant1 and wheat Rc genes controlling anthocyanin pigmentation in different vegetative tissues. Mol. Genet. Genomics. 2015;290(4):1287-1298. DOI 10.1007/s00438-015-0991-0.
29. Himi E., Yamashita Y., Haruyama N., Yanagisawa T., Maekawa M., Taketa S. Ant28 gene for proanthocyanidin synthesis encoding the R2R3 MYB domain protein (Hvmyb10) highly affects grain dormancy in barley. Euphytica. 2011;188(1):141-151. DOI 10.1007/s10681-011-0552-5.
30. Hisano H., Sakamoto K., Takagi H., Terauchi R., Sato K. Exome QTLseq maps monogenic locus and QTLs in barley. BMC Genomics. 2017;18(1):125. DOI 10.1186/s12864-017-3511-2.
31. Hori K., Kobayashi T., Sato K., Takeda K. QTL analysis of Fusarium head blight resistance using a high-density linkage map in barley. Theor. Appl. Genet. 2005;111(8):1661-1672. DOI 10.1007/s00122005-0102-4.
32. Hui C., Bin Y., Xiaoping Y., Long Y., Chunye C., Mantian M., Wenhua L. Anticancer activities of an anthocyanin-rich extract from black rice against breast cancer cells in vitro and in vivo. Nutr. Cancer. 2010;62:1128-1136. DOI 10.1080/01635581.2010.494821.
33. Immer F.R., Henderson M.T. Linkage studies in barley. Genetics. 1943; 28(5):419-440.
34. Jana B.K., Mukherjee S.K. Notes on the distribution of phytomelanin layer in higher plants – a short communication. J. Pharmaceutical Biol. 2014;4:131-132.
35. Jende-Strid B. Genetic control of flavonoid biosynthesis in barley. Hereditas. 1993;119:187-204. DOI 10.1111/j.1601-5223.1993.00187.x.
36. Jende-Strid B., Lundqvist U. Diallelic tests of anthocyanin-deficient mutants. Barley Genet. Newsl. 1978;8:57-59.
37. Jia Q., Wang J., Zhu J., Hua W., Shang Y., Yang J., Liang Z. Toward identification of black lemma and pericarp gene Blp1 in barley combining bulked segregant analysis and specific-locus amplified fragment sequencing. Front. Plant Sci. 2017;8:1414. DOI 10.3389/fpls.2017.01414.
38. Jia Q., Zhu J., Wang J., Yang J., Zhang G. Genetic mapping and molecular marker development for the gene Pre2 controlling purple grains in barley. Euphytica. 2016;208:215-223. DOI 10.1007/s10681-0151593-y.
39. Kervinen T., Peltonen S., Utriainen M., Kangasjarvi J., Teeri T.H., Karjalainen R. Cloning and characterization of cDNA clones encoding phenylalanine ammonialyase in barley. Plant Sci. 1997;123(1):143150. DOI 10.1016/S0168-9452(96)04570-0.
40. Khlestkina E.K. The adaptive role of flavonoids: emphasis on cereals. Cereal Res. Commun. 2013a;41:185-198. DOI 10.1556/CRC.2013. 0004.
41. Khlestkina E.K. Genes determining the coloration of different organs in wheat. Russ. J. Genet. Appl. Res. 2013b;3(1):54-65. DOI 10.1134/S2079059713010085.
42. Khlestkina E., Salina E., Matthies I., Leonova I., Börner A., Röder M. Comparative molecular marker-based genetic mapping of flavanone 3-hydroxylase genes in wheat, rye and barley. Euphytica. 2011;179:333-341. DOI 10.1007/s10681-010-0337-2.
43. Kim M.J., Hyun J.N., Kim J.A., Park J.C., Kim M.Y., Kim J.G., Lee S.J., Chun S.C., Chung I.M. Relationship between phenolic compounds, anthocyanins content and antioxidant activity in colored barley germplasm. J. Agric. Food Chem. 2007;55:4802-4809. DOI 10.1021/jf0701943.
44. Kristiansen K.N., Rohde W. Structure of the Hordeum vulgare gene encoding dihydroflavonol-4-reductase and molecular analysis of antl8 mutants blocked in flavonoid synthesis. Mol. Gen. Genet. 1991; 230:49-59. DOI 10.1007/BF00290650.
45. Kukoeva T., Gordeeva E., Glagoleva A., Shoeva O., Börner A., Khlestkina E. Purple-grained barley: marker-assisted development of NILs and genetic dissection. Proc. of the 1st Int. Workshop “Plant Genetics and Genomics for Food Security”. Novosibirsk, 26-28 August 2016. Novosibirsk, 2016;29.
46. Loskutov I.G., Blinova E.V., Gavrilova O.P., Gagkaeva T.Y. The valuable characteristics of oats genotypes and resistance to Fusarium disease. Russ. J. Genet. Appl. Res. 2016;20(3):286-294. DOI 10.18699/VJ16.151.
47. Lundqvist U., Franckowiak J.D. Diversity of barley mutants. Eds. R. von Bothmer, T. van Hintum, H. Knüpffer, K. Sato. Diversity in barley (Hordeum vulgare). Amsterdam: Elsevier, 2003;77-96.
48. Matthews D.E., Carollo V.L., Lazo G.R., Anderson O.D. GrainGenes, the genome database for small-grain crops. Nucleic Acids Res. 2003;31(1):183-186. DOI 10.1093/nar/gkg058.
49. Mauray A., Felgines C., Morand C., Mazur A., Scalbert A., Milenkovic D. Bilberry anthocyanin-rich extract alters expression of genes related to atherosclerosis development in aorta of apo E-deficient mice. Nutr. Metab. Cardiovasc. Dis. 2012;22(1):72-80. DOI 10.1016/j.numecd.2010.04.011.
50. Meldgaard M. Expression of chalcone synthase, dihydroflavonol reductase, and flavanone-3-hydroxylase in mutants of barley deficient in anthocyanin and proanthocyanidin biosynthesis. Theor. Appl. Genet. 1992;83:695-706.
51. Mol J., Grotewold E., Koes R. How genes paint flowers and seeds. Trends Plant Sci. 1998;3:212-217.
52. Myler J.L., Stanford E.H. Color inheritance in barley. J. Am. Soc. Agron. 1942;34:427-436.
53. Nesi N., Jond C., Debeaujon I., Caboche M., Lepiniec L. The Arabidopsis TT2 gene encodes an R2R3 MYB domain protein that acts as a key determinant for proanthocyanidin accumulation in de ve loping seed. Plant Cell. 2001;13(9):2099-2114. DOI 10.1105/TPC.010098.
54. Pecchioni N., Vale G., Toubia-Rahme H., Faccioli P., Terzi V., Delogu G. Barley-Pyrenophora graminea interaction: QTL analysis and gene mapping. Plant Breed. 1999;118(1):29-35. DOI 10.1046/j.14390523.1999.118001029.x.
55. Peukert M., Weise S., Röder M.S., Matthies I.E. Development of SNP markers for genes of the phenylpropanoid pathway and their association to kernel and malting traits in barley. BMC Genet. 2013;14:97. DOI 10.1186/1471-2156-14-97.
56. Reddivari L., Vanamala J., Chintharlapalli S., Safe S.H., Miller Jr J.C. Anthocyanin fraction from potato extracts is cytotoxic to prostate cancer cells through activation of caspase-dependent and caspaseindependent pathways. Carcinogenesis. 2007;28(10):2227-2235. DOI 10.1093/carcin/bgm117.
57. Rice-Evans C.A., Miller N.J., Paganga G. Structure-antioxidant activity relationships of flavonoids and phenolic acids. Free Radic. Biol. Med. 1996;20(7):933-956. DOI 10.1016/0891-5849(95)02227-9.
58. Robertson D.W. Inheritance in barley. Genetics. 1933;18(2):148-158.
59. Rohde W., Barzen E., Marocco A., Schwarz-Sommer Z., Saedler H., Salamini F. Isolation of genes that could serve as traps for transposable elements in Hordeum vulgare. Okayama, Barley Genetics V. Proc. 5th Int. Barley Genet. Symp. (Eds. S. Yasuda, T. Konishi). Okayama, 1987;553-541.
60. Rohde W., Dörr S., Salamini F., Becker D. Structure of a chalcone synthase gene from Hordeum vulgare. Plant Mol. Biol. 1991;16:11031106.
61. Shoeva O.Y., Kukoeva T.V., Börner A., Khlestkina E.K. Barley Ant1 is a homolog of maize C1 and its product is part of the regulatory machinery governing anthocyanin synthesis in the leaf sheath. Plant Breed. 2015;134:400-405. DOI 10.1111/pbr.12277.
62. Shoeva O.Y., Mock H.P., Kukoeva T.V., Börner A., Khlestkina E.K. Regulation of the flavonoid biosynthesis pathway genes in purple and black grains of Hordeum vulgare. PloS ONE. 2016;11(10):e0163782. DOI 10.1371/journal.pone.0163782.
63. Strathearn K.E., Yousef G.G., Grace M.H., Roy S.L., Tambe M.A., Ferruzzi M.G., Wu Q.L., Simon J.E., Lila M.A., Rochet J.C. Neuroprotective effects of anthocyanin-and proanthocyanidin-rich extracts in cellular models of Parkinson׳s disease. Brain Res. 2014;1555:60-77. DOI 10.1016/j.brainres.2014.01.047.
64. Strygina K.V., Börner A., Khlestkina E.K. Identification and characte rization of regulatory network components for anthocyanin synthesis in barley aleurone. BMC Plant Biol. 2017;17(1):184. DOI 10.1186/s12870-017-1122-3.
65. Szajdek A., Borowska E.J. Bioactive compounds and health-promoting properties of berry fruits: a review. Plant Foods Hum. Nutr. 2008; 63:147. DOI 10.1007/s11130-008-0097-5.
66. Tarahovskiy Yu.S., Kim Y.A., Abdrasilov B.S, Muzaffarov E.N. Flavonoidy: biokhimiya, biofizika, meditsina [Flavonoids: biochemistry, biophysics, medicine]. Pushchino: Synchrobook Publ., 2013. (in Russian)
67. The International Barley Genome Sequencing Consortium. A physical, genetic and functional sequence assembly of the barley genome. Nature. 2012;491:711-717. DOI 10.1038/nature11543.
68. Vihorev A.V., Strygina K.V., Khlestkina E.K. Identification and analysis of genes flavonoid 3′-hydroxylase and flavonoid 3′,5′-hydroxylase in the barley genome. Materialy 4-j Mezhdunarodnoj konferencii ‘‘Genofond i selekciya rastenij’’. Novosibirsk, 4–6 aprelya 2018 g. [Proceedings of the 4th International Conference “Gene pool and plant breeding”. Novosibirsk, April 4–6, 2018]. Novosibirsk: ICG SB RAS Publ., 2018;79-83. (in Russian)
69. von Wettstein D. From analysis of mutants to genetic engineering. Annu. Rev. Plant Biol. 2007;58:1-19. DOI 10.1146/annurev.arplant.58.032806.104003.
70. Winkel-Shirley B. Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol. 2001;126(2):485-493. DOI 10.1104/pp.126.2.485.
71. Wise R.P., Rohde W., Salamini F. Nucleotide sequence of the Bronze-1 homologous gene from Hordeum vulgare. Plant Mol. Biol. 1990; 14(2):277-279.
72. Woodward R.W. Inheritance of melanin-like pigment in the glumes and caryopses of barley. J. Agric. Res. 1941;63:21-28.
73. Woodward R.W. Linkage relationships between the allelomorphic series, B, Bmb, Bg, and Atat factors in barley. J. Am. Soc. Agron. 1942; 34:659-661.
74. Woodward R.W., Thieret J.W. A Genetic study of complementary genes for purple lemma, palea, and pericarp in barley (Hordeum vulgare L.). Agron. J. 1953;45(5):182-185.
75. Youdim K.A., Qaiser M.Z., Begley D.J., Rice-Evans C.A., Abbott N.J. Flavonoid permeability across an in situ model of the blood-brain barrier. Free Radic. Biol. Med. 2004;36(5):592-604. DOI 10.1016/j.freeradbiomed.2003.11.023.
76. Zhou X., Chao M., Liang X. Screening and testing of barley varieties for scab resistance (in Chinese with English abstract). Acta Phytophylacica Sin. 1991;18:261-265.