Year: 2020
Pages: 8-26
Number: Volume 12, issue 1
Type: scientific article
DOI: https://doi.org/10.31301/2221-6197.bmcs.2020-2
Topic: Article
Authors: Ibragimova N.N., Kuluev Bulat R.
Rye (Secale sereale L.) is the most important agricultural crop in Russia, characterized by a stable harvest in temperate zone, high stress tolerance and the ability to grow on low-fertile soils. An important indicator of the quality of rye grain is the low content of pentosans (arabinoxylans), since they have a negative effect on the digestion processes in farm animals. Therefore, rye varieties with a low content of pentosans are characterized by good feed qualities, whereas rye varieties with a high content of pentosans in the grain are characterized by good baking qualities. Due to the fact that the use of rye for baking both in the Russian Federation and in other countries is decreasing every year, the creation of low-pentosan rye varieties becomes most urgent. The content of pentosans may depend on the growing conditions, but the genotype has a more significant effect, which suggests the possibility of the targeted creation of rye varieties with a low content of pentosans. The purpose of this review is to consider the molecular basis of the baking and fodder qualities of rye grain, including genetic determinants that may be associated with the content of pentosans in rye grain. The content of arabinoxylans in rye grain depends, first of all, on the functioning of both the enzymes of their biosynthesis, for example, glycosyltransferases, and the enzymes of their degradation - xylanases. In plants, glycosyltransferases of families GT8, 43, 47, and 75 are involved in the biosynthesis of arabinoxylans (pentosans), the genes of which are sequenced in common wheat, barley, and some other cereals, however, they still remain unstudied in rye. Due to the fact that rye is a close relative of Triticum aestivum, annotated nucleotide sequences of common wheat can be used in the study of rye glycosyltransferase genes.
rye, Secale sereale, pentosans, arabinoxylans, xylanases, glycosyltransferases
1.Amerah A.M., Mathis G., Hofacre C.L. Effect of xylanase and a blend of essential oils on performance and Salmonella colonization of broiler chickens challenged with Salmonella Heidelberg. Poult. Sci. 2012. V. 91. No 4. P. 943–947. doi: 10.3382/ps.2011- 01922
2.Anders N., Wilkinson M.D., Lovegrove A., Freeman J., Tryfona T., Pellny T.K., Weimar T., Mortimer J.C., Stott K., Baker J.M. Glycosyl transferases in family 61 mediate arabinofuranosyl transfer onto xylan in grasses. Proc Natl Acad Sci USA. 2012. V. 109. P. 989–993. doi: 10.1073/pnas.1115858109
3.Bach Knudsen K.E., Lærke H.N. Rye arabinoxylans: Molecular structure, physicochemical properties and physiological effects in the gastrointestinal tract. Cereal Chem. 2010. V. 87. P. 353–362. doi: 10.1094/CCHEM-87-4-0353
4.Bakhtizin N.R. Winter rye. Ufa, Bashknigoizdat, 1972. 260 p. (In Russian).
5. Balakshin M., Capanema E., Gracz H., Chang H., Jameel H. Quantification of lignin– carbohydrate linkages with high- resolution NMR spectroscopy. Planta 2011. V. 233. P. 1097–1110.
6.Bedford M.R., Cowieson A.J. Exogenous enzymes and their effects on intestinal microbiology. Anim. Feed Sci. Technol. 2012. V. 173. P. 76–85. doi: 10.1016/j.anifeedsci.2011.12.018
7.Belova O.V., Lisov A.V., Vinokurova N.G., Kostenevich A.A., Leontievsky A.A., Sapunova L.I., Lobanok A.G. Xylanase and cellulase of fungus Cerrena unicolor VKM F-3196: Production, properties, and applications for the saccharification of plant material. Applied Biochemistry and Microbiology. 2014. V. 50. № 2. P. 148-153.
8.Boros D., Marquardt R.R., Slominski B.A., Guenter W. Extract viscosity as an indirect assay for watersoluble pentosans content in rye. Cereal Chem. 1993. V. 70. Р. 575–580.
9.Boros D. Quality aspects of winter rye for feed purpose. Proceedings of International Symposium on Rye Breeding and Genetics. 28-30 June 2006. Vort. Pflanzenucht. 2007. P. 80–85.
10. Bromley J.R., Busse-Wicher M., Tryfona T., Mortimer J.C., Zhang Z., Brown D.M., Dupree P. GUX1 and GUX2 glucuronyltransferases decorate distinct domains of glucuronoxylan with different substitution patterns. Plant J. 2013. V. 74. P. 423–434.
11. Brown D., Wightman R., Zhang Z.N., Gomez L.D., Atanassov I., Bukowski J.P., Tryfona T., McQueen-Mason S.J., Dupree P., Turner S. Arabidopsis genes IRREGULAR XYLEM (IRX15) and IRX15L encode DUF579-containing proteins that are essential for normal xylan deposition in the secondary cell wall. Plant J. 2011. V. 66. P. 401–413. doi: 10.1111/j.1365-313X.2011.04501.x
12. Brown D.M., Goubet F., Wong V.W., Goodacre R., Stephens E., Dupree P., Turner S.R. Comparison of five xylan synthesis mutants reveals new insight into the mechanisms of xylan synthesis. Plant J. 2007. V. 52. P. 1154–1168. doi: 10.1111/j.1365-313X.2007.03307.x
13. Brown D.M., Zhang Z.N., Stephens E., Dupree P., Turner S.R. Characterization of IRX10 and IRX10-like reveals an essential role in glucuronoxylan biosynthesis in Arabidopsis. Plant J. 2009. V. 57. P. 732–746.
14. Burton R.A., Fincher G.B. Evolution and development of cell walls in cereal grains. Front Plant Sci. 2014. 5:456. doi: 10.3389/fpls.2014.00456 15. Bushuk V. Rye: production, chemistry and technology / V. Bushuk, W. Campbell, E. Drews. - M .: Kolos, 1980.247 p. (In Russian).
16. Chiniquy D., Sharma V., Schultink A., Baidoo E.E., Rautengarten C., Cheng K., Carroll A., Ulvskov P., Harholt J., Keasling J.D. XAX1 from glycosyltransferase family 61 mediates xylosyltransfer to rice xylan. Proc Natl Acad Sci USA. 2012. V. 109. P. 17117–17122. doi: 10.1073/pnas.1202079109
17. Cyran M., Cygankiewicz J. Content and composition of non-starch polysaccharide of rye flour in relation to its baking quality. Proceeding of the Eucarpia Rye Meeting. Radzikow. 2001. P. 291–298.
18. Denisenko Yu.A. Protein engineering of mushroom xylanases of the 10th family glycosidhydrolase. The dissertation for the degree of candidate of chemical sciences. 2018. Moscow. 138 p. (In Russian).
19. Ebringerova’ A, Heinze T. Xylan and xylan derivatives – biopolymers with valuable properties, 1. Naturally occurring xylans structures, isolation procedures and properties. Macromol Rapid Commun. 2000. V. 21. P. 542–556. doi: 10.1002/1521-3927(20000601)21:9<542::AIDMARC542>3.0.CO;2-7
20. Feoktistova N.V., Mardanova A.M., Lutfullin M.T., Bogomolnaya L.M., Sharipova M.R. Biological products of microbial origin in poultry. Uchenye Zapiski Kazanskogo Universiteta. Seriya Estestvennye Nauki. 2018. V. 160. No. 3. P. 395-418.
(In Russian).
21. Gan Y.T., McLeod J.G., Scoles G.L., Campbell G.L. Extract viscosity of winter rye: variation with temperature and precipitation. Canad. J. Plant Sc. 1997. V. 77. № 4. P. 555–560.
22. Golomolzin V.D., Gridin V.F., Lebedeva I.A. Feed and compound feeds for farm animals. Ekaterinburg. 2006. P. 142. (In Russian).
23. Goncharenko A.A., Ismagilov R.R., Berkutova N.S., Vanyushina T.N., Ayupov D.S. Evaluation of the baking qualities of winter rye grain by the viscosity of the water extract. Reports of the Russian Academy of Agricultural Sciences. 2005. No. 1. P. 6-13. (In Russian).
24. Goncharenko A.A., Ermakov S.A., Makarov A.V., Semenova T.V., Tochilin V.N., Tsygankova N.V. The use of divergent selection by viscosity of an aqueous extract in the selection of winter rye. Grain Farm of Russia. 2011. No. 5. P. 11–19. (In Russian).
25. Gridin V.F., Gafarov Sh.S. Organization of fullfledged feeding of dairy cows in the conditions of the Middle Urals. Yekaterinburg: Ural Agricultural Publishing House. 2012. P. 76. (In Russian).
26. Imamura T., Watanabe T., Kuwahara M., Koshijima T. Ester linkages between lignin and glucuronic acid in lignin–carbohydrate complexes from Fagus crenata. Phytochemistry. 1994. V. 37. P. 1165–1173.
27. Ismagilov R.R., Nurlygayanov R.B., Vanyushina T.N. Quality and production technology of food grain of winter rye. Academy of Sciences of the Republic of Bashkortostan. Moscow. 2001. (In Russian).
28. Ismagilov R.R., Vanyushina T.N., Ayupov D.S. Pentosans rye. Ufa: Publishing House of BGAU, 2006.113 p. (In Russian).
29. Ismagilov R.R., Akhiyarova L.M. Feed quality of grain of various varieties of winter rye. Achievements of science and technology of the agroindustrial complex. 2007. No. 11. P. 16–17. (In Russian).
30. Ismagilov R.R. Variability of the content of water-soluble pentosans in winter rye grain. Achievements of science and technology of the agroindustrial complex. 2012. No. 6. P.35–36. (In Russian).
31. Ismagilov R.R., Nazarov M.R., Gaysina L.F. Change in grain quality of winter rye depending on its size. Russian Electronic Scientific Journal. 2013. No. 6. P. 161–168. (In Russian).
32. Ismagilov R.R., Gaysina L.F. The dependence of the form stability of rye bread on the content of pentosans in the grain. Bulletin of the Bashkir State Agrarian University. 2014. No 2. P. 21-24. (In Russian).
33. Ismagilov R.R., Gaysina L.F. Bakery grain qualities of winter rye F1 hybrids. Achievements of science and technology of the agro-industrial complex. 2015. V. 29. No. 1. P. 24-26. (In Russian).
34. Izydorczyk M., Biliaderis C.G., Bushuk W. Physical properties of water-soluble pentosans from different wheat varieties. Cereal Chem. 1991. V. 68:145.
35. Izydorczyk M.S., Biliaderis C.G. Cereal arabinoxylans advances in structure and physicochemical properties. Carbohyd. Polym. 1995. V. 28. P. 33–48. doi: 10.1016/0144-8617(95)00077-1
36. Jensen J.K., Kim H., Cocuron J.C., Orler R., Ralph J., Wilkerson C.G. The DUF579 domain containing proteins IRX15 and IRX15-L affect xylan synthesis in Arabidopsis. Plant J. 2011. V. 66. P. 387–400. doi: 10.1111/j.1365-313X.2010.04475.x
37. Khadem A., Lourenzo M., Delezie E., Maertens L., Goderis A., Mombaerts R., Höfte M., Eeckhaut V., Van Immerseel F., Janssens G.P. Does release of encapsulated nutrients have an important role in the efficacy of xylanase in broilers? Poult. Sci. 2016. V. 95. P. 1066–1076. doi: 10.3382/ps/pew002
38. Kiarie E., Romero L.F., Nyachoti C.M. The role of added feed enzymes in promoting gut health in swine and poultry. Nutr. Res. Rev. 2013. V. 26. P. 71–88. doi: 10.1017/S0954422413000048
39. Kobylyansky D.V. Rye. Genetic basis of selection. M. 1982. (In Russian).
40. Kobylyansky V.D., Solodukhina O.V. Fundamentals of selection of low pentosan rye. Proceedings on Applied Botany, Genetics and Breeding. SPb: VIR. 2009a. T. 166. P. 112–118. (In Russian).
41. Kobylyansky V.D., Solodukhina O.V. Prospects for selection of low-pentosan grain feed rye. Winter rye: selection, seed production, technology and processing. Materials of the All-Russian Scientific and Practical Conference. July 1-3. - Ufa: GNU BashNIIISH, 2009b. 248 p. (In Russian).
42. Kobylyansky V.D., Solodukhina O.V. The theoretical basis of the selection of feed rye with a low content of water-soluble pentosans. Sel'skokhozyaistvennaya biologiya. 2013. No. 2. P. 31–39. (In Russian).
43. Kobylyansky V.D., Solodukhina O.V., Potapova G.N., Tkachenko I.V., Galimov K.A. Studying innovative grain-fed low-pentosan winter rye. Perm Bulletin. 2014. No. 1. P. 10–16. (In Russian).
44. Kobylyansky D.V., Solodukhina O.V. The use of donors of valuable plant traits in breeding new varieties of winter rye. Achievements of Science and Technology of AICis. 2015. V. 29. No. 7. P. 7-12. (In Russian).
45. Kobylyansky V.D., Solodukhina O.V., Lunegova I.V., Novikova S.P., Khlopyuk M.S., Makarov V.I. The creation of low-pentosan rye and the possibility of its use in animal feed. Proceedings on Applied Botany, Genetics and Breeding. 2017. V. 178. No. 1. P. 31–40. (In Russian).
46. Kuluev B.R., Safiullina M.G. 2015. Regulation of cell expansion in plants. Uspekhi sovremennoi biologii. 135 (2): 148–163. (In Russian).
47. Kunakbaev S.A. Guaranteed culture (winter rye). Agriculture of Bashkiria. 1961. No. 2. P. 8–10. (In Russian).
48. Lee C., O’Neill M.A., Tsumuraya Y., Darvill A.G., Ye Z-H. The irregular xylem9 mutant is deficient in xylan xylosyltransferase activity. Plant Cell Physiol. 2007. V. 48. P. 1624–1634.
49. Lee C., Teng Q., Huang W., Zhong R., Ye Z.H. The Arabidopsis family GT43 glycosyltransferases form two functionally nonredundant groups essential for the elongation of glucuronoxylan backbone. Plant Physiol. 2010. V. 153. P. 526–541. doi: 10.1104/pp.110.155309
50. Lee C., Teng Q., Huang W., Zhong R., Ye Z.H. The F8H glycosyltransferase is a functional paralog of FRA8 involved in glucuronoxylan biosynthesis in Arabidopsis. Plant Cell Physiol. 2009. V. 50. P. 812–827. doi: 10.1093/pcp/pcp025
51. Lee C., Teng Q., Zhong R., Ye Z.H. Arabidopsis GUX proteins are glucuronyltransferases responsible for the addition of glucuronic acid side chains onto xylan. Plant Cell Physiol. 2012. V. 53. P. 1204–1216. doi: 10.1093/pcp/pcs064
52. Lee C., Zhong R., Richardson E.A., Himmelsbach D.S., McPhail B.T., Ye Z.H. The PARVUS gene is expressed in cells undergoing secondary wall thickening and is essential for glucuronoxylan biosynthesis. Plant Cell Physiol. 2007. V. 48. P. 1659–1672. doi: 10.1093/pcp/pcm155
53. Lovegrove A., Wilkinson M.D., Freeman J., Pellny T.K., Tosi P., Saulnier L., Shewry P.R., Mitchell R.A. RNA interference suppression of genes in glycosyl transferase families 43 and 47 in wheat starchy endosperm causes large decreases in arabinoxylan content. Plant Physiol. 2013. V. 163. P. 95–107. doi: 10.1104/pp.113.222653
54. Lynd L.R., Weimer P.J., van Zyl W.H., Pretorius I.S. Microbial cellulose utilization: Fundamentals and biotechnology. Microbiol. Mol. Biol. Rev. 2002. V. 66. P. 506–577.
55. Markov A.V., Gusakov A.V., Dzedzyulya E.I., Ustinov B.B., Antonov A.A., Sinitsyn A.P., Okunev O.N., Bekkarevich A.O. Properties of hemicellulases of the enzyme complex from Trichoderma longibrachiatum. Applied Biochemistry and Microbiology. 2006. V. 42. No. 6. P. 573-583.
56. Marquardt R., Brenes A., Zhang Z., Boros D. Use of enzyme to improve nutrient availability in poultry feedstuffs. Animal Feed Science and Technology. 1996. August. Bd. 60. P. 321-330.
57. Matsumoto T., Tanaka T., Sakai H., Amano N., Kanamori H., Kurita K., Kikuta A., Kamiya K., Yamamoto M., Ikawa H., Fujii N., Hori K., Itoh T., Sato K. Comprehensive sequence analysis of 24,783 barley full-length cDNAs derived from 12 clone libraries. Plant Physiol. 2011. V. 156(1). P. 20–28. doi: 10.1104/pp.110.171579
58. Morozova Yu.A., Skvortsov E.V., Alimova F.K. Xylanases Trichoderma reesei- biosynthesis and use for the hydrolysis of grain feed. Uchenye Zapiski Kazanskogo Universiteta. 2013. V. 55, P. 126–137.
59. Mortimer J.C., Faria-Blanc N., Yu X., Tryfona T., Sorieul M., Ng Y.Z., Zhang Z., Stott K., Anders N., Dupree P. An unusual xylan in Arabidopsis primary cell walls is synthesised by GUX3, IRX9L, IRX10L and IRX14. Plant J. 2015. V. 83. P. 413–426. doi: 10.1111/tpj.12898
60. Park Y.H., Hamidon F., Rajangan Ch., Soh K.P., Gan Ch.Yu., Lim Th.S., Abdullah W.N.W., Liong M.T. Application of probiotics for the production of safe and high-quality poultry meat. Korean J. Food Sci. Anim. Resour. 2016. V. 36. Р. 567–576. doi: 10.5851/kosfa.2016.36.5.567
61. Peña M.J., Zhong R.Q., Zhou G.K., Richardson E.A., O’Neill M.A., Darvill A.G., York W.S., Ye Z.H. Arabidopsis irregular xylem8 and irregular xylem9: implications for the complexity of glucuronoxylan biosynthesis. Plant Cell. 2007. V. 19. P. 549–563.
62. Persson S., Caffall K.H., Freshour G., Hilley M.T., Bauer S., Poindexter P., Hahn M.G., Mohnen D., Somerville C. The Arabidopsis irregular xylem8 mutant is deficient in glucuronoxylan and homogalacturonan, which are essential for secondary cell wall integrity. Plant Cell. 2007. V. 19. P. 237–255.
63. Pichugin A.B. Bortnichestvo and agriculture of the Volga Bulgaria: to the history of borrowing in material culture. Bulletin of the Kostroma State University. 2016. V. 22. No. 3. P. 65–67. (In Russian).
64. Ponomareva M.L., Ponomarev S.N., Gilmullina L.F., Mannapova G.S. Phenotypic assessment of the content of pentosans in rye meal by determining the viscosity of the aqueous extract. Achievements of Science and Technology of AICis. 2015. V. 29. No. 11. P. 32–35. (In Russian).
65. Ponomareva M.L., Ponomarev S.N., Tagirov M.Sh., Gilmullina L.F., Mannapova G.S. Genotypic variability of the content of pentosans in winter rye grain. Sel'skokhozyaystvennaya biologiya. 2017. V. 52. No. 5. P. 1041–1048.
66. Potapova G.V., Tkachenko I.V., Galimov K.A. A new grain variety of winter rye Amber. Theory and practice of world science. 2017. No. 10. P. 66–69. (In Russian).
67. Rennie E.A., Hansen S.F., Baidoo E.E., Hadi M.Z., Keasling J.D., Scheller H.V. Three members of the Arabidopsis glycosyltransferase family 8 are xylan glucuronosyltransferases. Plant Physiol. 2012. V. 159. P. 1408–1417. doi: 10.1104/pp.112.200964
68. Sato K., Shin-I T., Seki M., Shinozaki K., Yoshida H., Takeda K., Yamazaki Y., Conte M., Kohara Y. Development of 5006 full-length CDNAs in barley: a tool for accessing cereal genomics resources. DNA Res. 2009. V. 16. P. 81–89. doi: 10.1093/dnares/dsn034
69. Sharma A., Tewari R., Rana S.S., Soni R., Soni S.K. Cellulases: Classification, methods of determination and industrial applications. Appl. Biochem. Biotechnol. 2016. V. 179. P. 1346–1380. doi: 10.1007/s12010-016-2070-3
70. Solodukhina O.V., Kobylyansky V.D., Kuznetsova L.I., Lavrentyeva N.S., Timina M.A. Prospects for the use of low pentosan rye for baking purposes. Russian Agricultural Science. 2018. No. 6. P. 3-5. (In Russian).
71. Sukhareva A.S., Kuluev B.R. DNA markers for genetic analysis of crops. Biomics. 2018. 10(1). P. 69-84. DOI: 10.31301/2221-6197.bmcs.2018-15 (In Russian).
72. Urbanowicz B.R., Pena M.J., Moniz H.A., Moremen K.W., York W.S. Two Arabidopsis proteins synthesize acetylated xylan in vitro. Plant J. 2014. V. 80. P. 197–206. doi: 10.1111/tpj.12643
73. Utkina E.I. Selection of winter rye in the VolgaVyatka region. The dissertation for the degree of Doctor of Agricultural Sciences. 2017. Kirov. 343 p. (In Russian).
74. Vinkx C.J.A., Delcou J.A. Rye (Secale cereale L.) arabinoxylans: A critical review. Journal of Cereal Science. 1996. V. 24. P. 1-14. doi: 10.1006/jcrs.1996.0032
75. Weipert D., Zwingelberg H. Quellstoff – Starkeverhaltnis bei unterschiedlichenRoggenqualitat. Getreid, Mehl und Brot. 1980. Bd. 34, No. 4. P. 97–100.
76. Wu A.M., Hornblad E., Voxeur A., Gerber L., Rihouey C., Lerouge P., Marchant A. Analysis of the Arabidopsis IRX9/IRX9-L and IRX14/IRX14-L pairs of glycosyltransferase genes reveals critical contributions to biosynthesis of the hemicellulose glucuronoxylan. Plant Physiol. 2010. V. 153. P. 542–554. doi: 10.1104/pp.110.154971
77. Wu A.M., Rihouey C., Seveno M., Hornblad E., Singh S.K., Matsunaga T., Ishii T., Lerouge P., Marchant A. The Arabidopsis IRX10 and IRX10-LIKE glycosyltransferases are critical for glucuronoxylan biosynthesis during secondary cell wall formation. Plant J. 2009. V. 57. P. 718–731. doi: 10.1111/j.1365-313X.2008.03724.x
78. Yang P., Habekuß A., Hofinger B.J., Kanyuka K., Kilian B., Graner A., Ordon F., Stein N. Sequence diversification in recessive alleles of two host factor genes suggests adaptive selection for bymovirus resistance in cultivated barley from East Asia. Theor Appl Genet. 2017. V. 130. P. 331–344. doi: 10.1007/s00122-016-2814-z
79. Zeng W., Jiang N., Nadella R., Killen T.L., Nadella V., Faik A. A glucurono(arabino)xylan synthase complex from wheat contains members of the GT43, GT47, and GT75 families and functions cooperatively. Plant Physiol. 2010. V. 154. P. 78–97. doi: 10.1104/pp.110.159749
80. Zhong R., Pena M.J., Zhou G.K., Nairn C.J., Wood-Jones A., Richardson E.A., Morrison W.H., Darvill A.G., York W.S., Ye Z.H. Arabidopsis fragile fiber8, which encodes a putative glucuronyltransferase, is essential for normal secondary wall synthesis. Plant Cell. 2005. V. 17. P. 3390–3408. doi: 10.1105/tpc.105.035501
81. Zverkova Z.N. Zootechnical assessment of the use of canning of winter rye grain in the diets of lactating cows. LLC. Kormoproyzvodstvo. M. 2010. P. 40–43. (In Russian).