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<article article-type="research-article" dtd-version="1.3" xmlns:mml="http://www.w3.org/1998/Math/MathML" xmlns:xlink="http://www.w3.org/1999/xlink" xmlns:xsi="http://www.w3.org/2001/XMLSchema-instance" xml:lang="ru"><front><journal-meta><journal-id journal-id-type="publisher-id">vavilov</journal-id><journal-title-group><journal-title xml:lang="ru">Вавиловский журнал генетики и селекции</journal-title><trans-title-group xml:lang="en"><trans-title>Vavilov Journal of Genetics and Breeding</trans-title></trans-title-group></journal-title-group><issn pub-type="epub">2500-3259</issn><publisher><publisher-name>Institute of Cytology and Genetics of Siberian Branch of the RAS</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="doi">10.18699/VJ18.339</article-id><article-id custom-type="elpub" pub-id-type="custom">vavilov-1372</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="section-heading" xml:lang="ru"><subject>МОЛЕКУЛЯРНЫЕ МАРКЕРЫ В ГЕНЕТИКЕ И СЕЛЕКЦИИ</subject></subj-group><subj-group subj-group-type="section-heading" xml:lang="en"><subject>BIOINFORMATICS AND SYSTEM BIOLOGY</subject></subj-group></article-categories><title-group><article-title>ПРЕДСКАЗАНИЕ МЕТОДАМИ СИСТЕМНОЙ БИОЛОГИИ НАИБОЛЕЕ ПЕРСПЕКТИВНЫХ ГЕНОВ-МИШЕНЕЙ ДЛЯ СЕЛЕКЦИИ НА УСТОЙЧИВОСТЬ К ОКИСЛИТЕЛЬНОМУ СТРЕССУ C3 И C4 КУЛЬТУРНЫХ ЗЛАКОВ</article-title><trans-title-group xml:lang="en"><trans-title>USING THE METHODS OF SYSTEMS BIOLOGY FOR PREDICTING PERSPECTIVE TARGET GENES TO SELECT C3 AND C4 CEREALS FOR OXIDATIVE STRESS RESISTANCE</trans-title></trans-title-group></title-group><contrib-group><contrib contrib-type="author" corresp="yes"><name-alternatives><name name-style="eastern" xml:lang="ru"><surname>Дорошков</surname><given-names>А. В.</given-names></name><name name-style="western" xml:lang="en"><surname>Doroshkov</surname><given-names>A. V.</given-names></name></name-alternatives><email xlink:type="simple">ad@bionet.nsc.ru</email><xref ref-type="aff" rid="aff-1"/></contrib><contrib contrib-type="author" corresp="yes"><name-alternatives><name name-style="eastern" xml:lang="ru"><surname>Бобровских</surname><given-names>А. В.</given-names></name><name name-style="western" xml:lang="en"><surname>Bobrovskikh</surname><given-names>A. V.</given-names></name></name-alternatives><xref ref-type="aff" rid="aff-1"/></contrib></contrib-group><aff-alternatives id="aff-1"><aff xml:lang="ru">Федеральный исследовательский центр Институт цитологии и генетики Сибирского отделения Российской академии наук; Новосибирский национальный исследовательский государственный университет<country>Россия</country></aff><aff xml:lang="en">Institute of Cytology and Genetics SB RAS; Novosibirsk State University<country>Russian Federation</country></aff></aff-alternatives><pub-date pub-type="collection"><year>2018</year></pub-date><pub-date pub-type="epub"><day>22</day><month>03</month><year>2018</year></pub-date><volume>22</volume><issue>1</issue><fpage>122</fpage><lpage>131</lpage><permissions><copyright-statement>Copyright &amp;#x00A9; Дорошков А.В., Бобровских А.В., 2018</copyright-statement><copyright-year>2018</copyright-year><copyright-holder xml:lang="ru">Дорошков А.В., Бобровских А.В.</copyright-holder><copyright-holder xml:lang="en">Doroshkov A.V., Bobrovskikh A.V.</copyright-holder><license license-type="creative-commons-attribution" xlink:href="https://creativecommons.org/licenses/by/4.0/" xlink:type="simple"><license-p>This work is licensed under a Creative Commons Attribution 4.0 License.</license-p></license></permissions><self-uri xlink:href="https://vavilov.elpub.ru/jour/article/view/1372">https://vavilov.elpub.ru/jour/article/view/1372</self-uri><abstract><p>Активные формы кислорода (АФК) – один из ключевых повреждающих факторов для живых организмов. АФК производятся в реакциях нормального метаболизма, в стрессовых условиях их выработка повышается. Улучшение характеристик ферментативной системы антиоксидантной защиты культурных растений позволит повысить их устойчивость к абиотическим стрессам, таким как засоленность, засуха и холод. Однако компоненты системы вырождены – каждая реакция катализируется серией ферментов, кодируемых разными генами. Выбор наиболее важных компонентов позволит ускорить нахождение оптимальной селекционной стратегии для улучшения свойств всей системы у хозяйственно ценных видов растений. В настоящей работе впервые проведен системно-биологический анализ особенностей молекулярной эволюции и характеристик экспрессии генов, принадлежащих к четырем функциональным группам ферментов антиоксидантной защиты (APX, GPX, SOD и CAT), у шести представителей C3 и трех представителей C4 злаковых растений. Выделены и проанализированы 25 ортологических групп генов. Выявлены шесть ортологических групп с наиболее высоким уровнем экспрессии и наибольшим давлением стабилизирующего отбора для дальнейшей верификации и использования в селекции. Эти шесть ортологических групп, предположительно, вносят больший вклад в функционирование антиоксидантной системы изученных C3 и C4 злаковых растений. Показано, что интеграция эволюционных характеристик и экспрессионных данных представляет перспективный подход к предсказанию важных для селекции генов в геномах хозяйственно ценных растений.</p></abstract><trans-abstract xml:lang="en"><p>Reactive oxygen species (ROS) are some of the most damaging factors for living systems. Cells produce ROS during normal metabolism reactions, but ROS production increases under stressful conditions. Improving the antioxidant system in cultivated plants will increase their tolerance to abiotic stresses, such as salinity, drought and cold. However, the biochemical components of the system are redundant, for each reaction is catalyzed by a series of enzymes encoded by different genes. Choosing the most perspective components of this system will help speed up evaluating the optimal breeding strategy for improving abiotic stress tolerance in economically valuable plants. In the present research article, we present the results of an integrative analysis of evolution- and expressionrelated characteristics. The work was carried out on a series of genes that belong to 4 functional groups (APX, GPX, SOD and CAT) of enzymatic components of the antioxidant defense system in six species of C3 cereal plants and 3 species of C4 cereal plants. As a result, 25 groups of orthologous genes were evaluated and described. The highest gene expression level and the greatest pressure of purifying selection were found to characterize six groups. These genes were chosen for further verification and use in breeding. Because these genes undergo the most conservative evolution and have the highest level of mRNA expression, we may assume that they contribute a lot to the antioxidant system functioning of the C3 and C4 cereal plants studied. We have shown that the integration of evolutionary characteristics and expression data represents a promising approach to predict target genes for plant breeding.</p></trans-abstract><kwd-group xml:lang="ru"><kwd>активные формы кислорода</kwd><kwd>антиоксидантная система</kwd><kwd>отношение Ka/Ks</kwd><kwd>уровень экспрессии</kwd><kwd>гены-кандидаты</kwd></kwd-group><kwd-group xml:lang="en"><kwd>reactive oxygen species</kwd><kwd>antioxidant system</kwd><kwd>Ka/Ks ratio</kwd><kwd>expression level</kwd><kwd>candidate genes</kwd></kwd-group><funding-group xml:lang="en"><funding-statement>Russian Science Foundation, project 17-74-10198. Use of equipment of the Bioinformatics Shared Access Center for the analysis was supported by State Budgeted Project 0324-2016-0008</funding-statement></funding-group></article-meta></front><back><ref-list><title>References</title><ref id="cit1"><label>1</label><citation-alternatives><mixed-citation xml:lang="ru">Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 1990;215(3):403-410. DOI 10.1016/S0022-2836(05)80360-2.</mixed-citation><mixed-citation xml:lang="en">Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 1990;215(3):403-410. DOI 10.1016/S0022-2836(05)80360-2.</mixed-citation></citation-alternatives></ref><ref id="cit2"><label>2</label><citation-alternatives><mixed-citation xml:lang="ru">Arvestad L. Efficient methods for estimating amino acid replacement rates. J. Mol. Evol. 2006;62(6):663-673. DOI 10.1007/s00239-004-0113-9.</mixed-citation><mixed-citation xml:lang="en">Arvestad L. Efficient methods for estimating amino acid replacement rates. J. Mol. Evol. 2006;62(6):663-673. DOI 10.1007/s00239-004-0113-9.</mixed-citation></citation-alternatives></ref><ref id="cit3"><label>3</label><citation-alternatives><mixed-citation xml:lang="ru">Das K., Roychoudhury A. Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front. Environ. Sci. 2014;2:53. DOI 10.3389/fenvs.2014.00053.</mixed-citation><mixed-citation xml:lang="en">Das K., Roychoudhury A. Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front. Environ. Sci. 2014;2:53. DOI 10.3389/fenvs.2014.00053.</mixed-citation></citation-alternatives></ref><ref id="cit4"><label>4</label><citation-alternatives><mixed-citation xml:lang="ru">De La Torre A.R., Lin Y., Van de Peer Y., Ingvarsson P.K. Genomewide analysis reveals diverged patterns of codon bias, gene expression, and rates of sequence evolution in Picea gene families. Genome Biol. Evol. 2015;7(4):1002-1015. DOI 10.1093/gbe/evv044.</mixed-citation><mixed-citation xml:lang="en">De La Torre A.R., Lin Y., Van de Peer Y., Ingvarsson P.K. Genomewide analysis reveals diverged patterns of codon bias, gene expression, and rates of sequence evolution in Picea gene families. Genome Biol. Evol. 2015;7(4):1002-1015. DOI 10.1093/gbe/evv044.</mixed-citation></citation-alternatives></ref><ref id="cit5"><label>5</label><citation-alternatives><mixed-citation xml:lang="ru">Ehleringer J.R., Sage R.F., Flanagan L.B., Pearcy R.W. Climate change and the evolution of C4 photosynthesis. Trends Ecol. Evol. 1991;6(3):95-99. DOI 10.1016/0169-5347(91)90183-X.</mixed-citation><mixed-citation xml:lang="en">Ehleringer J.R., Sage R.F., Flanagan L.B., Pearcy R.W. Climate change and the evolution of C4 photosynthesis. Trends Ecol. Evol. 1991;6(3):95-99. DOI 10.1016/0169-5347(91)90183-X.</mixed-citation></citation-alternatives></ref><ref id="cit6"><label>6</label><citation-alternatives><mixed-citation xml:lang="ru">Gill S.S., Tajrishi M., Madan M., Tuteja N. A DESD-box helicase functions in salinity stress tolerance by improving photosynthesis and antioxidant machinery in rice (Oryza sativa L. cv. PB1). Plant Mol. Biol. 2013;82(1-2):1-22. DOI 10.1007/s11103-013-0031-6.</mixed-citation><mixed-citation xml:lang="en">Gill S.S., Tajrishi M., Madan M., Tuteja N. A DESD-box helicase functions in salinity stress tolerance by improving photosynthesis and antioxidant machinery in rice (Oryza sativa L. cv. PB1). Plant Mol. Biol. 2013;82(1-2):1-22. DOI 10.1007/s11103-013-0031-6.</mixed-citation></citation-alternatives></ref><ref id="cit7"><label>7</label><citation-alternatives><mixed-citation xml:lang="ru">Gill S.S., Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 2010;48(12):909-930. DOI 10.1016/j.plaphy.2010.08.016.</mixed-citation><mixed-citation xml:lang="en">Gill S.S., Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 2010;48(12):909-930. DOI 10.1016/j.plaphy.2010.08.016.</mixed-citation></citation-alternatives></ref><ref id="cit8"><label>8</label><citation-alternatives><mixed-citation xml:lang="ru">Guindon S., Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 2003; 52(5):696-704. DOI 10.1080/10635150390235520.</mixed-citation><mixed-citation xml:lang="en">Guindon S., Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 2003; 52(5):696-704. DOI 10.1080/10635150390235520.</mixed-citation></citation-alternatives></ref><ref id="cit9"><label>9</label><citation-alternatives><mixed-citation xml:lang="ru">Gunbin K.V., Suslov V.V., Genaev M.A., Afonnikov D.A. Computer system for analysis of molecular evolution modes (SAMEM): analysis of molecular evolution modes at deep inner branches of the phylogenetic tree. In Silico Biol. 2012;11(3,4):109-123. DOI 10.3233/ISB-2012-0446.</mixed-citation><mixed-citation xml:lang="en">Gunbin K.V., Suslov V.V., Genaev M.A., Afonnikov D.A. Computer system for analysis of molecular evolution modes (SAMEM): analysis of molecular evolution modes at deep inner branches of the phylogenetic tree. In Silico Biol. 2012;11(3,4):109-123. DOI 10.3233/ISB-2012-0446.</mixed-citation></citation-alternatives></ref><ref id="cit10"><label>10</label><citation-alternatives><mixed-citation xml:lang="ru">Hammer Ø., Harper D.A.T., Ryan P.D. Paleontological statistics software: Package for education and data analysis. Palaeontol. Electronica. 2001;4. Available at: http://palaeo-electronica.org/2001_1/past/issue1_01.htm.</mixed-citation><mixed-citation xml:lang="en">Hammer Ø., Harper D.A.T., Ryan P.D. Paleontological statistics software: Package for education and data analysis. Palaeontol. Electronica. 2001;4. Available at: http://palaeo-electronica.org/2001_1/past/issue1_01.htm.</mixed-citation></citation-alternatives></ref><ref id="cit11"><label>11</label><citation-alternatives><mixed-citation xml:lang="ru">Hammond-Kosack K.E., Jones J.D. Resistance gene-dependent plant defense responses. Plant Cell. 1996;8(10):1773-1791.</mixed-citation><mixed-citation xml:lang="en">Hammond-Kosack K.E., Jones J.D. Resistance gene-dependent plant defense responses. Plant Cell. 1996;8(10):1773-1791.</mixed-citation></citation-alternatives></ref><ref id="cit12"><label>12</label><citation-alternatives><mixed-citation xml:lang="ru">Han M.V., Zmasek C.M. phyloXML: XML for evolutionary biology and comparative genomics. BMC Bioinformatics. 2009;10(1):356. DOI 10.1186/1471-2105-10-356.</mixed-citation><mixed-citation xml:lang="en">Han M.V., Zmasek C.M. phyloXML: XML for evolutionary biology and comparative genomics. BMC Bioinformatics. 2009;10(1):356. DOI 10.1186/1471-2105-10-356.</mixed-citation></citation-alternatives></ref><ref id="cit13"><label>13</label><citation-alternatives><mixed-citation xml:lang="ru">Hatch M.D. C4 photosynthesis: a unique elend of modified biochemistry, anatomy and ultrastructure. Biochim. Biophys. Acta – Rev. Bioenergetics. 1987;895(2):81-106. DOI 10.1016/S0304-4173(87)80009-5.</mixed-citation><mixed-citation xml:lang="en">Hatch M.D. C4 photosynthesis: a unique elend of modified biochemistry, anatomy and ultrastructure. Biochim. Biophys. Acta – Rev. Bioenergetics. 1987;895(2):81-106. DOI 10.1016/S0304-4173(87)80009-5.</mixed-citation></citation-alternatives></ref><ref id="cit14"><label>14</label><citation-alternatives><mixed-citation xml:lang="ru">Hatch M.D. C4 photosynthesis: discovery and resolution. In: Govindjee, Beatty J.T., Gest H., Allen J.F. (Eds.). Discoveries in Photosynthesis. Springer, 2005:875-880.</mixed-citation><mixed-citation xml:lang="en">Hatch M.D. C4 photosynthesis: discovery and resolution. In: Govindjee, Beatty J.T., Gest H., Allen J.F. (Eds.). Discoveries in Photosynthesis. Springer, 2005:875-880.</mixed-citation></citation-alternatives></ref><ref id="cit15"><label>15</label><citation-alternatives><mixed-citation xml:lang="ru">Henikoff S., Henikoff J.G. Amino acid substitution matrices from protein blocks. Proc. Natl. Acad. Sci. USA. 1992;89(22):10915-10919.</mixed-citation><mixed-citation xml:lang="en">Henikoff S., Henikoff J.G. Amino acid substitution matrices from protein blocks. Proc. Natl. Acad. Sci. USA. 1992;89(22):10915-10919.</mixed-citation></citation-alternatives></ref><ref id="cit16"><label>16</label><citation-alternatives><mixed-citation xml:lang="ru">Hohmann-Marriott M.F., Blankenship R.E. Evolution of photosynthesis. Annu. Rev. Plant Biol. 2011;62(1):515-548. DOI 10.1146/annurev-arplant-042110-103811.</mixed-citation><mixed-citation xml:lang="en">Hohmann-Marriott M.F., Blankenship R.E. Evolution of photosynthesis. Annu. Rev. Plant Biol. 2011;62(1):515-548. DOI 10.1146/annurev-arplant-042110-103811.</mixed-citation></citation-alternatives></ref><ref id="cit17"><label>17</label><citation-alternatives><mixed-citation xml:lang="ru">Ingvarsson P.K. Gene expression and protein length influence codon usage and rates of sequence evolution in Populus tremula. Mol. Biol. Evol. 2007;24(3):836-844. DOI 10.1093/molbev/msl212.</mixed-citation><mixed-citation xml:lang="en">Ingvarsson P.K. Gene expression and protein length influence codon usage and rates of sequence evolution in Populus tremula. Mol. Biol. Evol. 2007;24(3):836-844. DOI 10.1093/molbev/msl212.</mixed-citation></citation-alternatives></ref><ref id="cit18"><label>18</label><citation-alternatives><mixed-citation xml:lang="ru">Jia J., Zhao S., Kong X., Li Y., Zhao G., He W., Appels R., Pfeifer M., Tao Y., Zhang X., Jing R., Zhang C., Ma Y., Gao L., Gao C., Spannagl M., Mayer K., Li D., Pan S., Zheng F., Hu Q., Xia X., Li J., Liang Q., Chen J., Wicker T., Gou C., Kuang H., He G., Luo Y., Keller B., Xia Q., Lu P., Wang J., Zou H., Zhang R., Xu J., Gao J., Middleton C., Quan Z., Liu G., Wang J., International Wheat Genome Sequencing Consortium, Yang H., Liu X., He Z., Mao L., Wang J. Aegilops tauschii draft genome sequence reveals a gene repertoire for wheat adaptation. Nature. 2013;496:91-95. DOI 10.5524/100054.</mixed-citation><mixed-citation xml:lang="en">Jia J., Zhao S., Kong X., Li Y., Zhao G., He W., Appels R., Pfeifer M., Tao Y., Zhang X., Jing R., Zhang C., Ma Y., Gao L., Gao C., Spannagl M., Mayer K., Li D., Pan S., Zheng F., Hu Q., Xia X., Li J., Liang Q., Chen J., Wicker T., Gou C., Kuang H., He G., Luo Y., Keller B., Xia Q., Lu P., Wang J., Zou H., Zhang R., Xu J., Gao J., Middleton C., Quan Z., Liu G., Wang J., International Wheat Genome Sequencing Consortium, Yang H., Liu X., He Z., Mao L., Wang J. Aegilops tauschii draft genome sequence reveals a gene repertoire for wheat adaptation. Nature. 2013;496:91-95. DOI 10.5524/100054.</mixed-citation></citation-alternatives></ref><ref id="cit19"><label>19</label><citation-alternatives><mixed-citation xml:lang="ru">Karpilov Y.S. The distribution of radioactive carbon 14 amongst the products of photosynthesis of maize. Trudy Kazanskogo sel’skokhozyaystvennogo instituta = Works of the Kazan Agricultural Institute. 1960;41(1):15-24. (in Russian)</mixed-citation><mixed-citation xml:lang="en">Karpilov Y.S. The distribution of radioactive carbon 14 amongst the products of photosynthesis of maize. Trudy Kazanskogo sel’skokhozyaystvennogo instituta = Works of the Kazan Agricultural Institute. 1960;41(1):15-24. (in Russian)</mixed-citation></citation-alternatives></ref><ref id="cit20"><label>20</label><citation-alternatives><mixed-citation xml:lang="ru">Katoh K., Toh H. Recent developments in the MAFFT multiple sequence alignment program. Brief. Bioinform. 2008;9(4):286-298. DOI 10.1093/bib/bbn013.</mixed-citation><mixed-citation xml:lang="en">Katoh K., Toh H. Recent developments in the MAFFT multiple sequence alignment program. Brief. Bioinform. 2008;9(4):286-298. DOI 10.1093/bib/bbn013.</mixed-citation></citation-alternatives></ref><ref id="cit21"><label>21</label><citation-alternatives><mixed-citation xml:lang="ru">Khaliq A., Zia-ul-Haq M., Ali F., Aslam F., Matloob A., Navab A., Hussain S. Salinity tolerance in wheat cultivars is related to enhanced activities of enzymatic antioxidants and reduced lipid peroxidation. CLEAN – Soil, Air, Water. 2015;43(8):1248-1258. DOI 10.1002/clen.201400854.</mixed-citation><mixed-citation xml:lang="en">Khaliq A., Zia-ul-Haq M., Ali F., Aslam F., Matloob A., Navab A., Hussain S. Salinity tolerance in wheat cultivars is related to enhanced activities of enzymatic antioxidants and reduced lipid peroxidation. CLEAN – Soil, Air, Water. 2015;43(8):1248-1258. DOI 10.1002/clen.201400854.</mixed-citation></citation-alternatives></ref><ref id="cit22"><label>22</label><citation-alternatives><mixed-citation xml:lang="ru">Li W.L., Faris J.D., Chittoor J.M., Leach J.E., Hulbert S.H., Liu D.J., Chen P.D., Gill B.S. Genomic mapping of defense response genes in wheat. Theor. Appl. Genet. 1999;98(2):226-233. DOI 10.1007/s001220051062.</mixed-citation><mixed-citation xml:lang="en">Li W.L., Faris J.D., Chittoor J.M., Leach J.E., Hulbert S.H., Liu D.J., Chen P.D., Gill B.S. Genomic mapping of defense response genes in wheat. Theor. Appl. Genet. 1999;98(2):226-233. DOI 10.1007/s001220051062.</mixed-citation></citation-alternatives></ref><ref id="cit23"><label>23</label><citation-alternatives><mixed-citation xml:lang="ru">Li W.H., Yang J., Gu X. Expression divergence between duplicate genes. Trends Genet. 2005;21(11):602-607. DOI 10.1016/j.tig.2005.08.006.</mixed-citation><mixed-citation xml:lang="en">Li W.H., Yang J., Gu X. Expression divergence between duplicate genes. Trends Genet. 2005;21(11):602-607. DOI 10.1016/j.tig.2005.08.006.</mixed-citation></citation-alternatives></ref><ref id="cit24"><label>24</label><citation-alternatives><mixed-citation xml:lang="ru">Mittler R., Vanderauwera S., Gollery M., Van Breusegem F. Reactive oxygen gene network of plants. Trends Plant Sci. 2004;9(10):490-498. DOI 10.1016/j.tplants.2004.08.009.</mixed-citation><mixed-citation xml:lang="en">Mittler R., Vanderauwera S., Gollery M., Van Breusegem F. Reactive oxygen gene network of plants. Trends Plant Sci. 2004;9(10):490-498. DOI 10.1016/j.tplants.2004.08.009.</mixed-citation></citation-alternatives></ref><ref id="cit25"><label>25</label><citation-alternatives><mixed-citation xml:lang="ru">Neuman P.R., Hart G.E. Genetic control of the mitochondrial form of superoxide dismutase in hexaploid wheat. Biochem. Genet. 1986; 24(5-6):435-446.</mixed-citation><mixed-citation xml:lang="en">Neuman P.R., Hart G.E. Genetic control of the mitochondrial form of superoxide dismutase in hexaploid wheat. Biochem. Genet. 1986; 24(5-6):435-446.</mixed-citation></citation-alternatives></ref><ref id="cit26"><label>26</label><citation-alternatives><mixed-citation xml:lang="ru">Noctor G., Foyer C.H. Ascorbate and glutathione: keeping active oxygen under control. Annu. Rev. Plant Biol. 1998;49(1):249-279. DOI 10.1146/annurev.arplant.49.1.249.</mixed-citation><mixed-citation xml:lang="en">Noctor G., Foyer C.H. Ascorbate and glutathione: keeping active oxygen under control. Annu. Rev. Plant Biol. 1998;49(1):249-279. DOI 10.1146/annurev.arplant.49.1.249.</mixed-citation></citation-alternatives></ref><ref id="cit27"><label>27</label><citation-alternatives><mixed-citation xml:lang="ru">Orozco-Cardenas M., Ryan C.A. Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proc. Natl. Acad. Sci. USA. 1999;96(11):6553-6557. DOI 10.1073/pnas.96.11.6553.</mixed-citation><mixed-citation xml:lang="en">Orozco-Cardenas M., Ryan C.A. Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proc. Natl. Acad. Sci. USA. 1999;96(11):6553-6557. DOI 10.1073/pnas.96.11.6553.</mixed-citation></citation-alternatives></ref><ref id="cit28"><label>28</label><citation-alternatives><mixed-citation xml:lang="ru">Osipova S., Permyakov A., Permyakova M., Pshenichnikova T., Verkhoturov V., Rudikovsky A., Rudikovskaya E., Shishparenok A., Doroshkov A., Börner A. Regions of the bread wheat D genome associated with variation in key photosynthesis traits and shoot biomass under both well watered and water deficient conditions. J. Appl. Genet. 2016;57(2):151-163. DOI 10.1007/s13353-015-0315-4.</mixed-citation><mixed-citation xml:lang="en">Osipova S., Permyakov A., Permyakova M., Pshenichnikova T., Verkhoturov V., Rudikovsky A., Rudikovskaya E., Shishparenok A., Doroshkov A., Börner A. Regions of the bread wheat D genome associated with variation in key photosynthesis traits and shoot biomass under both well watered and water deficient conditions. J. Appl. Genet. 2016;57(2):151-163. DOI 10.1007/s13353-015-0315-4.</mixed-citation></citation-alternatives></ref><ref id="cit29"><label>29</label><citation-alternatives><mixed-citation xml:lang="ru">Peremyslov V.V., Mockler T.C., Filichkin S.A., Fox S.E., Jaiswal P., Makarova K.S., Koonin E.V., Dolja V.V. Expression, splicing, and evolution of the myosin gene family in plants. Plant Physiol. 2011; 155(3):1191-1204. DOI 10.1104/pp.110.170720.</mixed-citation><mixed-citation xml:lang="en">Peremyslov V.V., Mockler T.C., Filichkin S.A., Fox S.E., Jaiswal P., Makarova K.S., Koonin E.V., Dolja V.V. Expression, splicing, and evolution of the myosin gene family in plants. Plant Physiol. 2011; 155(3):1191-1204. DOI 10.1104/pp.110.170720.</mixed-citation></citation-alternatives></ref><ref id="cit30"><label>30</label><citation-alternatives><mixed-citation xml:lang="ru">Rambaut A. FigTree, version 1.4: tree figure drawing tool. 2008. http://tree.bio.ed.ac.uk/software/figtree/.</mixed-citation><mixed-citation xml:lang="en">Rambaut A. FigTree, version 1.4: tree figure drawing tool. 2008. http://tree.bio.ed.ac.uk/software/figtree/.</mixed-citation></citation-alternatives></ref><ref id="cit31"><label>31</label><citation-alternatives><mixed-citation xml:lang="ru">Reynolds M., Foulkes M.J., Slafer G.A., Berry P., Parry M.A., Snape J.W., Angus W.J. Raising yield potential in wheat. J. Exp. Bot. 2009;60(7):1899-1918. DOI 10.1093/jxb/erp016.</mixed-citation><mixed-citation xml:lang="en">Reynolds M., Foulkes M.J., Slafer G.A., Berry P., Parry M.A., Snape J.W., Angus W.J. Raising yield potential in wheat. J. Exp. Bot. 2009;60(7):1899-1918. DOI 10.1093/jxb/erp016.</mixed-citation></citation-alternatives></ref><ref id="cit32"><label>32</label><citation-alternatives><mixed-citation xml:lang="ru">Sage R.F., Sage T.L., Kocacinar F. Photorespiration and the evolution of C4 photosynthesis. Annu. Rev. Plant Biol. 2012;63:19-47. DOI 10.1146/annurev-arplant-042811-105511.</mixed-citation><mixed-citation xml:lang="en">Sage R.F., Sage T.L., Kocacinar F. Photorespiration and the evolution of C4 photosynthesis. Annu. Rev. Plant Biol. 2012;63:19-47. DOI 10.1146/annurev-arplant-042811-105511.</mixed-citation></citation-alternatives></ref><ref id="cit33"><label>33</label><citation-alternatives><mixed-citation xml:lang="ru">Trethowan R.M., Mujeeb-Kazi A. Novel germplasm resources for improving environmental stress tolerance of hexaploid wheat. Crop Sci. 2008;48(4):1255-1265. DOI 10.2135/cropsci2007.08.0477.</mixed-citation><mixed-citation xml:lang="en">Trethowan R.M., Mujeeb-Kazi A. Novel germplasm resources for improving environmental stress tolerance of hexaploid wheat. Crop Sci. 2008;48(4):1255-1265. DOI 10.2135/cropsci2007.08.0477.</mixed-citation></citation-alternatives></ref><ref id="cit34"><label>34</label><citation-alternatives><mixed-citation xml:lang="ru">Wang X., Cai J., Liu F., Dai T., Cao W., Wollenweber B., Jiang D. Multiple heat priming enhances thermo-tolerance to a later high temperature stress via improving subcellular antioxidant activities in wheat seedlings. Plant Physiol. Biochem. 2014;74:185-192. DOI 10.1016/j.plaphy.2013.11.014.</mixed-citation><mixed-citation xml:lang="en">Wang X., Cai J., Liu F., Dai T., Cao W., Wollenweber B., Jiang D. Multiple heat priming enhances thermo-tolerance to a later high temperature stress via improving subcellular antioxidant activities in wheat seedlings. Plant Physiol. Biochem. 2014;74:185-192. DOI 10.1016/j.plaphy.2013.11.014.</mixed-citation></citation-alternatives></ref><ref id="cit35"><label>35</label><citation-alternatives><mixed-citation xml:lang="ru">Wright S.I., Yau C.K., Looseley M., Meyers B.C. Effects of gene expression on molecular evolution in Arabidopsis thaliana and Arabidopsis lyrata. Mol. Biol. Evol. 2004;21(9):1719-1726. DOI 10.1093/molbev/msh191.</mixed-citation><mixed-citation xml:lang="en">Wright S.I., Yau C.K., Looseley M., Meyers B.C. Effects of gene expression on molecular evolution in Arabidopsis thaliana and Arabidopsis lyrata. Mol. Biol. Evol. 2004;21(9):1719-1726. DOI 10.1093/molbev/msh191.</mixed-citation></citation-alternatives></ref><ref id="cit36"><label>36</label><citation-alternatives><mixed-citation xml:lang="ru">Wu G., Wilen R.W., Robertson A.J., Gusta L.V. Isolation, chromosomal localization, and differential expression of mitochondrial manganese superoxide dismutase and chloroplastic copper/zinc superoxide dismutase genes in wheat. Plant Physiol. 1999;120(2):513-520. DOI 10.1104/pp.120.2.513.</mixed-citation><mixed-citation xml:lang="en">Wu G., Wilen R.W., Robertson A.J., Gusta L.V. Isolation, chromosomal localization, and differential expression of mitochondrial manganese superoxide dismutase and chloroplastic copper/zinc superoxide dismutase genes in wheat. Plant Physiol. 1999;120(2):513-520. DOI 10.1104/pp.120.2.513.</mixed-citation></citation-alternatives></ref><ref id="cit37"><label>37</label><citation-alternatives><mixed-citation xml:lang="ru">Zhang J. Evolution by gene duplication: an update. Trends Ecol. Evol. 2003;18(6):292-298. DOI 10.1016/S0169-5347(03)00033-8.</mixed-citation><mixed-citation xml:lang="en">Zhang J. Evolution by gene duplication: an update. Trends Ecol. Evol. 2003;18(6):292-298. DOI 10.1016/S0169-5347(03)00033-8.</mixed-citation></citation-alternatives></ref><ref id="cit38"><label>38</label><citation-alternatives><mixed-citation xml:lang="ru">Zmasek C.M. Archaeopteryx: visualization, analysis, and editing of phylogenetic trees. 2015. Available at: https://sites.google.com/site/cmzmasek/home/software/archaeopteryx.</mixed-citation><mixed-citation xml:lang="en">Zmasek C.M. Archaeopteryx: visualization, analysis, and editing of phylogenetic trees. 2015. Available at: https://sites.google.com/site/cmzmasek/home/software/archaeopteryx.</mixed-citation></citation-alternatives></ref></ref-list><fn-group><fn fn-type="conflict"><p>The authors declare that there are no conflicts of interest present.</p></fn></fn-group></back></article>
