ГЕНЫ, КОНТРОЛИРУЮЩИЕ СИНТЕЗ ФЛАВОНОИДНЫХ И МЕЛАНИНОВЫХ ПИГМЕНТОВ ЯЧМЕНЯ

Помимо зеленой окраски, обусловленной хлорофиллом, у ячменя зерно и вегетативные органы могут быть окрашены соединениями фенольной природы, такими как меланины и флавоноидные пигменты антоцианы и проантоцианидины. В связи с широкой биологической активностью данных соединений и их неокрашенных предшественников в отношении растений и человека в последнее время наблюдается повышенный интерес к изучению генов, определяющих окраску у растений. Наиболее изученной является система генов, участвующих в синтезе флавоноидных пигментов. С семидесятых годов прошлого века в геноме ячменя идентифицированы и локализованы как структурные гены, кодирующие ферменты метаболизма флавоноидов, так и регуляторные гены, определяющие тканеспецифическое накопление данных пигментов в тканях зерна, а также в вегетативных органах. К настоящему времени выделены нуклеотидные последовательности регуляторных генов Ant1 и Ant2, определяющих накопление антоцианов в перикарпе зерна, гена Ant28, контролирующего биосинтез проантоцианидинов (конденсированных таннинов) в семенной оболочке, a также генов HvMpc2, HvMyc2, HvWD40, определяющих накопление антоцианов в алейроновом слое зерновки ячменя. Менее изучена меланиновая окраска. Ввиду сложной структуры и устойчивости к различным растворителям химическая природа данных пигментов до сих пор не установлена. Однако благодаря сравнительному анализу транскриптомов в окрашенных и неокрашенных чешуях колоса и зерна почти изогенных линий ячменя удалось идентифицировать метаболические пути, лежащие в осно- ве формирования меланиновой пигментации. В предложенной статье проводится обзор результатов работ, посвященных исследованиям генетического контроля формирования окраски у ячменя.

Hordeum vulgare L., антоцианы, проантоцианидины, таннины, меланины, флавоноиды

1. Aastrup S., Outtrup H., Erdal K. Location of the proanthocyanidins in the barley grain. Carlsberg Res. Commun. 1984;49:105-109. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. 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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/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.