Факторы транскрипции семейства MADS растений: связь с признаками доместикации и перспективы для селекции (обзор)

Автор: Нежданова А.В., Щенникова А.В.

Журнал: Сельскохозяйственная биология @agrobiology

Рубрика: Обзоры, проблемы

Статья в выпуске: 5 т.56, 2021 года.

Бесплатный доступ

Признаки доместикации, которые подразделяются на три группы (продуктивность, адаптивность и воспроизводство) и составляют в совокупности доместикацонный синдром, сближающий таксономически удаленные одомашненные формы, остаются хозяйственно значимыми и у современных возделываемых культур. Значительная часть генов, контролирующих у растений признаки доместикации, представлена генами факторов регуляции транскрипции, в частности принадлежащих семейству белков с MADS-доменом. MADS-белки служат ключевыми регуляторами практически всех аспектов репродуктивного развития растений, включая определение сроков цветения, строения соцветий, идентичности цветковых органов, развития корней, плодов и семян, а также адаптивной и стрессовой реакции растений на неблагоприятные условия окружающей среды. В представленном обзоре показано возможное участие MADS-box генов в процессах, происходивших при одомашнивании растений. Обсуждается роль MADS-box генов в реакции растений на длительное воздействие холодом (яровизацию), в регуляции состояния физиологического покоя почек, в формировании структуры соцветия и цветка, изменения фертильности растения и качественных признаков плода (процесс созревания, синтез каротиноидов и антоцианов, число семян, способность к растрескиванию, сроки хранения), а также в ответе растений на стрессы (засоление, засуха, изменение температуры). Рассмотрено явление плейотропии и избыточности функций MADS-box генов (за счет существования паралогов). Высказываетcя предположение, что высокий структурно-функциональный консерватизм может свидетельствовать о высоком потенциале MADS-box генов как инструментов для предсказуемой тонкой настройки фенотипов сельскохозяйственных культур посредством комбинирования (в том числе, дозозависимого) различных аллелей и паралогов MADS-box генов. Еще один возможный способ такой настройки - разделение плейотропных функций MADS-box гена посредством введения мутаций в его кодирующую или цис-регуляторную последовательность для изменения взаимодействий белок-белок или белок-ДНК, а также профиля и(или) уровня экспрессии, в том числе в ответ на различные внешние и внутренние сигналы. Сделано заключение о том, что фундаментальные и прикладные исследования MADS-box генов у различных видов растений (как дикорастущих, так и культурных) не только приведут к более глубокому пониманию эволюции и развития современных растений, но также внесут большой вклад в улучшение сельскохозяйственных культур, в том числе с помощью CRISPR/Cas и других современных технологий.

Еще

Регуляция транскрипции, факторы транскрипции, mads-box гены, консерватизм, плейотропный эффект, признаки одомашнивания, продуктивность, адаптация, воспроизводство, хозяйственно ценные признаки, целевые гены

Короткий адрес: https://sciup.org/142231385

IDR: 142231385   |   DOI: 10.15389/agrobiology.2021.5.823rus

Список литературы Факторы транскрипции семейства MADS растений: связь с признаками доместикации и перспективы для селекции (обзор)

  • Purugganan M.D., Fuller D.Q. The nature of selection during plant domestication. Nature, 2009, 457(7231): 843-848 (doi: 10.1038/nature07895).
  • Meyer R.S., DuVal A.E., Jensen H.R. Patterns and processes in crop domestication: an historical review and quantitative analysis of 203 global food crops. New Phytologist, 2012, 196(1): 29-48 (doi: 10.1111/j.1469-8137.2012.04253.x).
  • Fuller D.Q., Denham T., Arroyo-Kalin M., Lucas L., Stevens C.J., Qin L., Allaby R.G., Purugganan M.D. Convergent evolution and parallelism in plant domestication revealed by an expanding archaeological record. Proceedings of the National. Academy of Sciences of the USA, 2014, 111(17): 6147-6152 (doi: 10.1073/pnas.1308937110).
  • Larson G., Piperno D.R., Allaby R.G., Purugganan M.D., Andersson L., Arroyo-Kalin M., Barton L., Vigueira C.C., Denham T., Dobney K., Doust A.N., Gepts P., Gilbert M.T.P., Gremillion K.J., Lucas L., Lukens L., Marshall F.B., Olsen K.M., Pires J.C., Richerson P.J., de Casas R.R., Sanjur O.I., Thomas M.G., Fuller D.Q. Current perspectives and the future of domestication studies. Proceedings of the National Academy of Sciences of the USA, 2014, 111(17): 6139-6146 (doi: 10.1073/pnas.1323964111 ).
  • Martínez-Ainsworth N.E., Tenaillon M.I. Superheroes and masterminds of plant domestication. Comptes Rendus Biologies, 2016, 339(7-8): 268-273 (doi: 10.1016/j.crvi.2016.05.005).
  • Stetter M.G., Gates D.J., Mei W., Ross-Ibarra J. How to make a domesticate. Current Biology, 2017, 27(17): R896-R900 (doi: 10.1016/j.cub.2017.06.048).
  • Milla R., Bastida J.M., Turcotte M.M., Jones G., Violle C., Osborne C.P., Chacon-Labella J., Sosinski E.E., Kattge J., Laughlin D.C., Forey E., Minden V., Cornelissen J.H.C., Amiaud B., Kramer K., Boenisch G., He T., Pillar V.D., Byun C. Phylogenetic patterns and phenotypic profiles of the species of plants and mammals farmed for food. Nature Ecology and Evolution, 2018, 2(11): 1808-1817 (doi: 10.1038/s41559-018-0690-4).
  • Manning K., Pelling R., Higham T., Schwenniger J.-L., Fuller D.Q. 4500-year old domesticated pearl millet (Pennisetum glaucum) from the Tilemsi Valley, Mali: new insights into an alternative cereal domestication pathway. Journal of Archaeological Science, 2011, 38(2): 312-322 (doi: 10.1016/j.jas.2010.09.007).
  • Meyer R., Purugganan M.D. Evolution of crop species: genetics of domestication and diversification. Nature Reviews Genetics, 2013, 14(12): 840-852 (doi: 10.1038/nrg3605).
  • Purugganan M.D. Evolutionary insights into the nature of plant domestication. Current Biology, 2019, 29(14): R705-R714 (doi: 10.1016/j.cub.2019.05.053).
  • Purugganan M.D., Fuller D.Q. Archaeological data reveal slow rates of evolution during plant domestication. Evolution, 2011, 65(1): 171-183 (doi: 10.1111/j.1558-5646.2010.01093.x).
  • Wang L., Beissinger T.M., Lorant A., Ross-Ibarra C., Ross-Ibarra J., Hufford M.B. The interplay of demography and selection during maize domestication and expansion. Genome Biology, 2017, 18(1): 215 (doi: 10.1186/s13059-017-1346-4).
  • Ramos-Madrigal J., Smith B.D., Moreno-Mayar J.V., Gopalakrishnan S., Ross-Ibarra J., Gilbert M.T.P., Wales N. Genome sequence of a 5,310-year-old maize cob provides insights into the early stages of maize domestication. Current Biology, 2016, 26(23): 3195-3201 (doi: 10.1016/j.cub.2016.09.036).
  • Smith O., Nicholson W., Kistler L., Mace E., Clapham A., Rose P., Stevens C., Ware R., Samavedam S., Barker G., Jordan D., Fuller D.Q., Allaby R.G. A domestication history of dynamic adaptation and genomic deterioration in Sorghum. Nature Plants, 2019, 5(4): 369-379 (doi: 10.1038/s41477-019-0397-9).
  • Luo M., Yang Z.-L., You F.M., Kawahara T., Waines J.G., Dvorak J. The structure of wild and domesticated emmer wheat populations, gene flow between them, and the site of emmer domestication. Theoretical and Applied Genetics, 2007, 114(6): 947-959 (doi: 10.1007/s00122-006-0474-0).
  • Allaby R.G. Integrating the processes in the evolutionary system of domestication. Journal of Experimental Botany, 2010, 61(4): 935-944 (doi: 10.1093/jxb/erp382).
  • Zohary D. Unconscious selection and the evolution of domesticated plants. Economic Botany, 2004, 58: 5-10 (doi: 10.1663/0013-0001(2004)058[0005:USATEO]2.0.CO;2).
  • Arnold M.L. Natural hybridization and the evolution of domesticated, pest and disease organisms. Molecular Ecology, 2014, 13(5): 97-1007 (doi: 10.1111/j.1365-294X.2004.02145.x).
  • Janzen G.M., Wang L., Hufford M.B. The extent of adaptive wild introgression in crops. New Phytologist, 2018, 221(3): 1279-1288 (doi: 10.1111/nph.15457).
  • Heslop-Harrison J.S., Schwarzacher T. Domestication, genomics, and the future for banana. Annals of Botany, 2007, 100(5): 1073-1084 (doi: 10.1093/aob/mcm191).
  • Marcussen T., Sandve S.R., Heier L., Spannagl M., Pfeifer M., Internation Wheat Genome Sequencing Consortium, Jakobsen K.S., Wulff B.B., Steuernagel B., Mayer K.F., Olsen O.A. Ancient hybridizations among the ancestral genomes of bread wheat. Science, 2014, 345(6194): 1250092 (doi: 10.1126/science.1250092).
  • Choi J.Y., Purugganan M.D. Multiple origin but single domestication led to Oryza sativa. G3 (Bethesda), 2018, 8(3): 797-803 (doi: 10.1534/g3.117.300334).
  • Heerwaarden J., Doebley J., Briggs W.H., Glaubitz J.C., Goodman M.M., Sanchez Gonzalez J., Ross-Ibarra J. Genetic signals of origin, spread, and introgression in a large sample of maize landraces. Proceedings of the National. Academy of Sciences of the USA, 2011, 108(3): 1088-1092 (doi: 10.1073/pnas.1013011108).
  • Mascher M., Schuenemann V.J., Davidovich U., Marom N., Himmelbach A., Hubner S., Korol A., David M., Reiter E., Reihl S., Schreiber M., Vohr S.H., Green R.E., Dawson I.K., Russell J., Kilian B., Muehlbauer G.J., Waugh R., Fahima T., Krause J., Weiss E., Stein N. Genomic analysis of 6,000-year-old cultivated grain illuminates the domestication history of barley. Nature Genetics, 2016, 48(9): 1089-1093 (doi: 10.1038/ng.3611).
  • Cornille A., Giraud T., Smulders M.J., Roldán-Ruiz I., Gladieux P. The domestication and evolutionary ecology of apples. Trends in Genetics, 2014, 30(2): 57-65 (doi: 10.1016/j.tig.2013.10.002).
  • Miller A.J., Gross B.L. From forest to field: perennial fruit crop domestication. American Journal of Botany, 2011, 98(9): 1389-1414 (doi: 10.3732/ajb.1000522).
  • Gaut B.S., Seymour D.K., Liu Q., Zhou Y. Demography and its effects on genomic variation in crop domestication. Nature Plants, 2018, 4(8): 512-520 (doi: 10.1038/s41477-018-0210-1).
  • Lemmon Z.H., Reem N.T., Dalrymple J., Soyk S., Swartwood K.E., Rodriguez-Leal D., Van Eck J., Lippman Z.B. Rapid improvement of domestication traits in an orphan crop by genome editing. Nature Plants, 2018, 4(10): 766-770 (doi: 10.1038/s41477-018-0259-x).
  • Zsögön A., Cermak T., Naves E.R., Notini M.M., Edel K.H., Weinl S., Freschi L., Voytas V.F., Kudla J., Peres L.E.P. De novo domestication of wild tomato using genome editing. Nature Biotechnology, 2018, 36: 1211-1216 (doi: 10.1038/nbt.4272).
  • Li T., Yang X., Yu Y., Si X., Zhai X., Zhang H., Dong W., Gao C., Xu C. Domestication of wild tomato is accelerated by genome editing. Nature Biotechnology, 2018, 36: 1160-1163 (doi: 10.1038/nbt.4273).
  • Lenser T., Theißen G. Molecular mechanisms involved in convergent crop domestication. Trends in Plant Science, 2013, 18(12): 704-714 (doi: 10.1016/j.tplants.2013.08.007).
  • Kantar M.B., Nashoba A.R., Anderson J.E., Blackman B.K., Rieseberg L.H. The genetics and genomics of plant domestication. BioScience, 2017, 67(11): 971-982 (doi: 10.1093/biosci/bix114).
  • Schilling S., Pan S., Kennedy A., Melzer R. MADS-box genes and crop domestication: the jack of all traits. Journal of Experimental Botany, 2018, 69(7): 1447-1469 (doi: 10.1093/jxb/erx479).
  • Theißen G., Rümpler F., Gramzow L. Array of MADS-box genes: facilitator for rapid adaptation? Trends in Plant Sciences, 2018, 23(7): 563-576 (doi: 10.1016/j.tplants.2018.04.008).
  • Theißen G., Melzer R., Rümpler F. MADS-domain transcription factors and the floral quartet model of flower development: linking plant development and evolution. Development, 2016, 143(18): 3259-3271 (doi: 10.1242/dev.134080).
  • Jiao Y., Paterson A.H. Polyploidy-associated genome modifications during land plant evolution. Philosophical Transactions of the Royal Society B: Biological Sciences, 2014, 369(1648): 20130355 (doi: 10.1098/rstb.2013.0355).
  • Kim S., Park J., Yeom S.I., Kim Y.M., Seo E., Kim K.T., Kim M.S., Lee J.M., Cheong K., Shin H.S., Kim S.B., Han K., Lee J., Park M., Lee H.A., Lee H.Y., Lee Y., Oh S., Lee J.H., Choi E., Choi E., Lee S.E., Jeon J., Kim H., Choi G., Song H., Lee J., Lee S.C., Kwon J.K., Lee H.Y., Koo N., Hong Y., Kim R.W., Kang W.H., Huh J.H., Kang B.C., Yang T.J., Lee Y.H., Bennetzen J.L., Choi D. New reference genome sequences of hot pepper reveal the massive evolution of plant disease-resistance genes by retroduplication. Genome Biology, 2017, 18(1): 210 (doi: 10.1186/s13059-017-1341-9).
  • Smaczniak C., Immink R.G, Angenent G.C., Kaufmann K. Developmental and evolutionary diversity of plant MADS-domain factors: insights from recent studies. Development, 2012, 139(17): 3081-3098 (doi: 10.1242/dev.074674).
  • Castelán-Muñoz N., Herrera J., Cajero-Sánchez W., Arrizubieta M., Trejo C., García-Ponce B., Sánchez M.P., Álvarez-Buylla E.R., Garay-Arroyo A. MADS-box genes are key components of genetic regulatory networks involved in abiotic stress and plastic developmental responses in plants. Frontiers in Plant Science, 2019, 10: 853 (doi: 10.3389/fpls.2019.00853).
  • Parenicovа L., de Folter S., Kieffer M., Horner D.S., Favalli C., Busscher J., Cook H.E., Ingram R.M., Kater M.M., Davies B., Angenent G.C., Colombo L. Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world. The Plant Cell, 2003, 15(7): 1538-1551 (doi: 10.1105/tpc.011544).
  • Bowman J.L., Smyth D.R., Meyerowitz E.M. Genes directing flower development in Arabidopsis. The Plant Cell, 1989, 1(1): 37-52 (doi: 10.1105/tpc.1.1.37).
  • Sommer H., Beltrán J.P., Huijser P., Pape H., Lönnig W.E., Saedler H., Schwarz-Sommer Z. Deficiens, a homeotic gene involved in the control of flower morphogenesis in Antirrhinum majus: the protein shows homology to transcription factors. The EMBO Journal, 1990, 9(3): 605-61.
  • Gramzow L., Theißen G. Phylogenomics reveals surprising sets of essential and dispensable clades of MIKCc-group MADS-box genes in flowering plants. Journal of Experimental Zoology. Part B, Molecular and Developmental Evolution, 2015, 324(4): 353-362 (doi: 10.1002/jez.b.22598).
  • Lee J., Lee I. Regulation and function of SOC1, a flowering pathway integrator. Journal of Experimental Botany, 2010, 61(9): 2247-2254 (doi: 10.1093/jxb/erq098).
  • Airoldi C.A., Davies B. Gene duplication and the evolution of plant MADS-box transcription factors. Journal of Genetics and Genomics, 2012, 39(4): 157-165 (doi: 10.1016/j.jgg.2012.02.008).
  • Pinyopich A., Ditta G.S., Savidge B., Liljegren S.J., Baumann E., Wisman E., Yanofsky M.F. Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature, 2003, 424(6944): 85-88 (doi: 10.1038/nature01741).
  • Kempin S.A., Savidge B., Yanofsky M.F. Molecular basis of the cauliflower phenotype in Arabidopsis. Science, 1995, 267(5197): 522-525 (doi: 10.1126/science.7824951).
  • Mandel M.A., Gustafson-Brown C., Savidge B., Yanofsky M.F. Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature, 1992, 360(6401): 273-277 (doi: 10.1038/360273a0).
  • Alvarez-Buylla E.R., García-Ponce B., Garay-Arroyo A. Unique and redundant functional domains of APETALA1 and CAULIFLOWER, two recently duplicated Arabidopsis thaliana floral MADS-box genes. Journal of Experimental Botany, 2006, 57(12): 3099-3107 (doi: 10.1093/jxb/erl081).
  • Cho L.H., Yoon J., An G. The control of flowering time by environmental factors. The Plant Journal, 2017, 90(4): 708-719 (doi: 10.1111/tpj.13461).
  • Luo X., Chen T., Zeng X., He D., He Y. Feedback regulation of FLC by FLOWERING LOCUS T (FT) and FD through a 5' FLC promoter region in Arabidopsis. Molecular Plant, 2019, 12(3): 285-288 (doi: 10.1016/j.molp.2019.01.013).
  • Preston J., Sandve S. Adaptation to seasonality and the winter freeze. Frontiers in Plant Science, 2013, 4: 167 (doi: 10.3389/fpls.2013.00167).
  • Andrés F., Coupland G. The genetic basis of flowering responses to seasonal cues. Nature Reviews Genetics, 2012, 13(9): 627-639 (doi: 10.1038/nrg3291).
  • Sharma N., Geuten K., Giri B.S., Varma A. The molecular mechanism of vernalization in Arabidopsis and cereals: role of Flowering Locus C and its homologs. Physiologia Plantarum, 2020, 170(3): 373-383 (doi: 10.1111/ppl.13163).
  • Amasino R. Vernalization, competence, and the epigenetic memory of winter. The Plant Cell, 2004, 16(10): 2553-2559 (doi: 10.1105/tpc.104.161070).
  • Hou J., Long Y., Raman H., Zou X., Wang J., Dai S., Xiao Q., Li C., Fan L., Liu B., Meng J. A Tourist-like MITE insertion in the upstream region of the BnFLC.A10 gene is associated with vernalization requirement in rapeseed (Brassica napus L.). BMC Plant Biology, 2012, 12: 238 (doi: 10.1186/1471-2229-12-238).
  • Calderwood A., Lloyd A., Hepworth J., Tudor E.H., Jones D.M., Woodhouse S., Bilham L., Chinoy C., Williams K., Corke F., Doonan J.H., Ostergaard L., Irwin J.A., Wells R., Morris R.J. Total FLC transcript dynamics from divergent paralogue expression explains flowering diversity in Brassica napus. New Phytologist, 2020, 229(6): 3534-3548 (doi: 10.1111/nph.17131).
  • Kakizaki T., Kato T., Fukino N., Ishida M., Hatakeyama K., Matsumoto S. Identification of quantitative trait loci controlling late bolting in Chinese cabbage (Brassica rapa L.) parental line Nou 6 gou. Breeding Science, 2011, 61: 151-159 (doi: 10.1270/jsbbs.61.151).
  • Yuan Y.X., Wu J., Sun R.F., Zhang X.W., Xu D.H., Bonnema G., Wang X.W. A naturally occurring splicing site mutation in the Brassica rapa FLC1 gene is associated with variation in flowering time. Journal of Experimental Botany, 2009, 60(4): 1299-1308 (doi: 10.1093/jxb/erp010).
  • Xiao D., Zhao J.J., Hou X.L., Basnet R.K., Carpio D.P., Zhang N.W., Bucher J., Lin K., Cheng F., Wang X.W., Bonnema G. The Brassica rapa FLC homologue FLC2 is a key regulator of flowering time, identified through transcriptional co-expression networks. Journal of Experimental Botany, 2013, 64(14): 4503-4516 (doi: 10.1093/jxb/ert264).
  • Wu J., Wei K., Cheng F., Li S., Wang Q., Zhao J., Bonnema G., Wang X. A naturally occurring InDel variation in BraA.FLC.b (BrFLC2) associated with flowering time variation in Brassica rapa. BMC Plant Biology, 2012, 12: 151 (doi: 10.1186/1471-2229-12-151).
  • Irwin J.A., Soumpourou E., Lister C., Ligthart J.D., Kennedy S., Dean C. Nucleotide polymorphism affecting FLC expression underpins heading date variation in horticultural brassicas. The Plant Journal, 2016, 87(6): 597-605 (doi: 10.1111/tpj.13221).
  • Kennedy A., Geuten K. The role of FLOWERING LOCUS C relatives in cereals. Frontiers in Plant Science, 2020, 11: 617340 (doi: 10.3389/fpls.2020.617340).
  • Sharma N., Ruelens P., D’hauw M., Maggen T., Dochy N., Torfs S., Kaufmann K., Rohde A., Geuten K. A flowering locus C homolog is a vernalization-regulated repressor in Brachypodium and is cold regulated in wheat. Plant Physiology, 2017, 173(2): 1301-1315 (doi: 10.1104/pp.16.01161).
  • Bloomer R.H., Dean C. Fine-tuning timing: natural variation informs the mechanistic basis of the switch to flowering in Arabidopsis thaliana. Journal of Experimental Botany, 2017, 68(20): 5439-5452 (doi: 10.1093/jxb/erx270).
  • Ratcliffe O.J., Kumimoto R.W., Wong B.J., Riechmann J.L. Analysis of the Arabidopsis MADS AFFECTING FLOWERING gene family: MAF2 prevents vernalization by short periods of cold. The Plant Cell, 2003, 15(5): 1159-1169 (doi: 10.1105/tpc.009506).
  • Verhage L., Severing E.I., Bucher J., Lammers M., Busscher-Lange J., Bonnema G., Rodenburg N., Proveniers M.C., Angenent G.C., Immink R.G. Splicing-related genes are alternatively spliced upon changes in ambient temperatures in plants. PLoS ONE, 2017, 12(3): e0172950 (doi: 10.1371/journal.pone.0172950).
  • Airoldi C.A., McKay M., Davies B. MAF2 is regulated by temperature-dependent splicing and represses flowering at low temperatures in parallel with FLM. PLoS ONE, 2015, 10(5): e0126516 (doi: 10.1371/journal.pone.0126516).
  • Rosloski S.M., Jali S.S., Balasubramanian S., Weigel D., Grbic V. Natural diversity in flowering responses of Arabidopsis thaliana caused by variation in a tandem gene array. Genetics, 2010, 186(1): 263-276 (doi: 10.1534/genetics.110.116392).
  • Dondup D., Dong G., Xu D., Zhang L., Zha S., Yuan X., Tashi N., Zhang J., Guo G. Allelic variation and geographic distribution of vernalization genes HvVRN1 and HvVRN2 in Chinese barley germplasm. Molecular Breeding, 2016, 36: 11 (doi: 10.1007/s11032-016-0434-6).
  • Asp T., Byrne S., Gundlach H., Bruggmann R., Mayer K.F., Andersen J.R., Xu M., Greve M., Lenk I., Lübberstedt T. Comparative sequence analysis of VRN1 alleles of Lolium perenne with the co-linear regions in barley, wheat, and rice. Molecular Genetics and Genomics, 2011, 286(5-6): 433-447 (doi: 10.1007/s00438-011-0654-8).
  • Fu D., Szucs P., Yan L., Helguera M., Skinner J.S., von Zitzewitz J., Hayes P.M., Dubcovsky J. Large deletions within the first intron in VRN-1 are associated with spring growth habit in barley and wheat. Molecular Genetics and Genomics, 2005, 273(1): 54-65 (doi: 10.1007/s00438-004-1095-4).
  • Kippes N., Debernardi J.M., Vasquez-Gross H.A., Akpinar B.A., Budak H., Kato K., Chao S., Akhunov E., Dubcovsky J. Identification of the VERNALIZATION 4 gene reveals the origin of spring growth habit in ancient wheats from South Asia. Proceedings of the National Academy of Sciences of the USA, 2015, 112(39): E5401-E5410 (doi: 10.1073/pnas.1514883112).
  • Bielenberg D.G., Wang Y., Li Z., Zhebentyayeva T., Fan S., Reighard G.L., Scorza R., Abbott A.G. Sequencing and annotation of the evergrowing locus in peach [Prunus persica (L.) Batsch] reveals a cluster of six MADS-box transcription factors as candidate genes for regulation of terminal bud formation. Tree Genetics and Genomes, 2008, 4: 495-507 (doi: 10.1007/s11295-007-0126-9).
  • Falavigna V.D.S., Guitton B., Costes E., Andrés F. I want to (bud) break free: the potential role of DAM and SVP-like genes in regulating dormancy cycle in temperate fruit trees. Frontiers in Plant Sciences, 2019, 9: 1990 (doi: 10.3389/fpls.2018.01990).
  • Hoenicka H., Nowitzki O., Hanelt D., Fladung M. Heterologous overexpression of the birch FRUITFULL-like MADS-box gene BpMADS4 prevents normal senescence and winter dormancy in Populus tremula L. Planta, 2008, 227(5): 1001-1011 (doi: 10.1007/s00425-007-0674-0).
  • Carr S.M., Irish V.F. Floral homeotic gene expression defines developmental arrest stages in Brassica oleracea L. vars. botrytis and italica. Planta, 1997, 201(2): 179-188 (doi: 10.1007/BF01007702).
  • Duclos D.V., Björkman T. Meristem identity gene expression during curd proliferation and flower initiation in Brassica oleracea. Journal of Experimental Botany, 2008, 59(2): 421-433 (doi: 10.1093/jxb/erm327).
  • Purugganan M.D., Boyles A.L., Suddith J.I. Variation and selection at the CAULIFLOWER floral homeotic gene accompanying the evolution of domesticated Brassica oleracea. Genetics, 2000, 155(2): 855-862 (doi: 10.1093/genetics/155.2.855).
  • Soyk S., Lemmon Z.H., Oved M., Fisher J., Liberatore K.L., Park S.J., Goren A., Jiang K., Ramos A., van der Knaap E., Van Eck J., Zamir D., Eshed Y., Lippman Z.B. Bypassing negative epistasis on yield in tomato imposed by a domestication gene. Cell, 2017, 169(6): 1142-1155 (doi: 10.1016/j.cell.2017.04.032).
  • Sreenivasulu N., Schnurbusch T. A genetic playground for enhancing grain number in cereals. Trends in Plant Science, 2012, 17(2): 91-101 (doi: 10.1016/j.tplants.2011.11.003).
  • Guo S., Xu Y., Liu H., Mao Z., Zhang C., Ma Y., Zhang Q., Meng Z., Chong K. The interaction between OsMADS57 and OsTB1 modulates rice tillering via DWARF14. Nature Communications, 2013, 4: 1566 (doi: 10.1038/ncomms2542).
  • Jeon J.S., Lee S., Jung K.H., Yang W.S., Yi G.H., Oh B.G., An G.H. Production of transgenic rice plants showing reduced heading date and plant height by ectopic expression of rice MADS-box genes. Molecular Breeding, 2000, 6: 581-592 (doi: 10.1023/A:1011388620872).
  • Dubois A., Raymond O., Maene M., Baudino S., Langlade N.B., Boltz V., Vergne P., Bendahmane M. Tinkering with the C-function: a molecular frame for the selection of double flowers in cultivated roses. PLoS ONE, 2010, 5(2): e9288 (doi: 10.1371/journal.pone.0009288).
  • Liu Z., Zhang D., Liu D., Li F., Lu H. Exon skipping of AGAMOUS homolog PrseAG in developing double flowers of Prunus lannesiana (Rosaceae). Plant Cell Reports, 2013, 32(2): 227-237 (doi: 10.1007/s00299-012-1357-2).
  • Klocko A.L., Borejsza-Wysocka E., Brunner A.M., Shevchenko O., Aldwinckle H., Strauss S.H. Transgenic suppression of AGAMOUS genes in apple reduces fertility and increases floral attractiveness. PLoS ONE, 2016, 11(8): e0159421 (doi: 10.1371/journal.pone.0159421).
  • Yao J.L., Dong Y.H., Morris B.A.M. Parthenocarpic apple fruit production conferred by transposon insertion mutations in a MADS-box transcription factor. Proceedings of the National Academy of Sciences of the USA, 2001, 98(3): 1306-1311 (doi: 10.1073/pnas.031502498).
  • Lombardo F., Kuroki M., Yao S.G., Shimizu H., Ikegaya T., Kimizu M., Ohmori S., Akiyama T., Hayashi T., Yamaguchi T., Koike S., Yatou O., Yoshida H. The superwoman1-cleistogamy2 mutant is a novel resource for gene containment in rice. Plant Biotechnology Journal, 2017, 15(1): 97-106 (doi: 10.1111/pbi.12594).
  • Masiero S., Colombo L., Grini P.E., Schnittger A., Kater M.M. The emerging importance of type I MADS box transcription factors for plant reproduction. The Plant Cell, 2011, 23(3): 865-872 (doi: 10.1105/tpc.110.081737).
  • Mejía N., Soto B., Guerrero M., Casanueva X., Houel C., Miccono M., Ramos R., Le Cunff L., Boursiquot J.M., Hinrichsen P., Adam-Blondon A.F. Molecular, genetic and transcriptional evidence for a role of VvAGL11 in stenospermocarpic seedlessness in grapevine. BMC Plant Biology, 2011, 11: 57 (doi: 10.1186/1471-2229-11-57).
  • Bergamini C., Cardone M.F., Anaclerio A., Perniola R., Pichierri A., Genghi R., Alba V., Forleo L.R., Caputo A.R., Montemurro C., Blanco A., Antonacci D. Validation assay of p3_VvAGL11 marker in a wide range of genetic background for early selection of stenospermocarpy in Vitis vinifera L. Molecular Biotechnology, 2013, 54(3): 1021-1030 (doi: 10.1007/s12033-013-9654-8).
  • Ocarez N., Mejía N. Suppression of the D-class MADS-box AGL11 gene triggers seedlessness in fleshy fruits. Plant Cell Reports, 2016, 35(1): 239-254 (doi: 10.1007/s00299-015-1882-x).
  • Angenent G.C., Franken J., Busscher M., van Dijken A., van Went J.L., Dons H.J., van Tunen A.J. A novel class of MADS box genes is involved in ovule development in petunia. The Plant Cell, 1995, 7(10): 1569-1582 (doi: 10.1105/tpc.7.10.1569).
  • Kord H., Shakib A.M., Daneshvar M.H., Azadi P., Bayat V., Mashayekhi M., Zarea M., Seifi A., Ahmad-Raji M. RNAi-mediated down-regulation of SHATTERPROOF gene in transgenic oilseed rape. 3 Biotech., 2015, 5(3): 271-277 (doi: 10.1007/s13205-014-0226-9).
  • Ferrándiz C., Liljegren S.J., Yanofsky M.F. Negative regulation of the SHATTERPROOF genes by FRUITFULL during Arabidopsis fruit development. Science, 2000, 289(5478): 436-438 (doi: 10.1126/science.289.5478.436).
  • Chandler J., Corbesier L., Spielmann P., Dettendorfer J., Stahl D., Apel K., Melzer S. Modulating flowering time and prevention of pod shatter in oilseed rape. Molecular Breeding, 2005, 15: 87-94 (doi: 10.1007/s11032-004-2735-4).
  • Wang S., Lu G., Hou Z., Luo Z., Wang T., Li H., Zhang J., Ye Z. Members of the tomato FRUITFULL MADS-box family regulate style abscission and fruit ripening. Journal of Experimental Botany, 2014, 65(12): 3005-3014 (doi: 10.1093/jxb/eru137).
  • Liu D., Wang D., Qin Z., Zhang D., Yin L., Wu L., Colasanti J., Li A., Mao L. The SEPALLATA MADS-box protein SLMBP21 forms protein complexes with JOINTLESS and MACROCALYX as a transcription activator for development of the tomato flower abscission zone. The Plant Journal, 2014, 77(2): 284-296 (doi: 10.1111/tpj.12387).
  • Hileman L.C., Sundstrom J.F., Litt A., Chen M., Shumba T., Irish V.F. Molecular and phylogenetic analyses of the MADS-box gene family in tomato. Molecular Biology and Evolution, 2006, 23(11): 2245-2258 (doi: 10.1093/molbev/msl095).
  • Ireland H.S., Yao J.L., Tomes S., Sutherland P.W., Nieuwenhuizen N., Gunaseelan K., Winz R.A., David K.M., Schaffer R.J. Apple SEPALLATA1/2-like genes control fruit flesh development and ripening. The Plant Journal, 2013, 73(6): 1044-1056 (doi: 10.1111/tpj.12094).
  • Elitzur T., Yakir E., Quansah L., Zhangjun F., Vrebalov J., Khayat E., Giovannoni J.J., Friedman H. Banana MaMADS transcription factors are necessary for fruit ripening and molecular tools to promote shelf-life and food security. Plant Physiology, 2016, 171(1): 380-391 (doi: 10.1104/pp.15.01866).
  • Seymour G.B., Ryder C.D., Cevik V., Hammond J.P., Popovich A., King G.J., Vrebalov J., Giovannoni J.J., Manning K. A SEPALLATA gene is involved in the development and ripening of strawberry (Fragaria × ananassa Duch.) fruit, a non-climacteric tissue. Journal of Experimental Botany, 2011, 62(3): 1179-1188 (doi: 10.1093/jxb/erq360).
  • Vrebalov J., Ruezinsky D., Padmanabhan V., White R., Medrano D., Drake R., Schuch W., Giovannoni J. A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (rin) locus. Science, 2002, 296(5566): 343-346 (doi: 10.1126/science.1068181).
  • Bai Y., Lindhout P. Domestication and breeding of tomatoes: what have we gained and what can we gain in the future? Annals of Botany, 2007, 100(5): 1085-1094 (doi: 10.1093/aob/mcm150).
  • Ito Y., Nishizawa-Yokoi A., Endo M., Mikami M., Toki S. CRISPR/Cas9-mediated mutgenesis of the RIN locus that regulates tomato fruit ripening. Biochemical and Biophysical Research Communications, 2015, 467(1): 76-82 (doi: 10.1016/j.bbrc.2015.09.117).
  • Dhar M.K., Sharma R., Koul A., Kaul S. Development of fruit color in Solanaceae: a story of two biosynthetic pathways. Briefings in Functional Genomics, 2015, 14(3): 199-212 (doi: 10.1093/bfgp/elu018).
  • Martel C., Vrebalov J., Tafelmeyer P., Giovannoni J.J. The tomato MADS-box transcription factor RIPENING INHIBITOR interacts with promoters involved in numerous ripening processes in a COLORLESS NONRIPENING-dependent manner. Plant Physiology, 2011, 157(3): 1568-1579 (doi: 10.1104/pp.111.181107).
  • Pan I.L., McQuinn R., Giovannoni J.J., Irish V.F. Functional diversification of AGAMOUS lineage genes in regulating tomato flower and fruit development. Journal of Experimental Botany, 2010, 61(6): 1795-1806 (doi: 10.1093/jxb/erq046).
  • Li S., Xu H., Ju Z., Cao D., Zhu H., Fu D., Grierson D., Qin G., Luo Y., Zhu B. The RIN-MC Fusion of MADS-box transcription factors has transcriptional activity and modulates expression of many ripening genes. Plant Physiologist, 2018, 176(1): 891-909 (doi: 10.1104/pp.17.01449).
  • Zhang J., Hu Z., Yao Q., Guo X., Nguyen V., Li F., Chen G. A tomato MADS-box protein, SlCMB1, regulates ethylene biosynthesis and carotenoid accumulation during fruit ripening. Scientific Reports, 2018, 8(1): 3413 (doi: 10.1038/s41598-018-21672-8).
  • Zhao H.B., Jia H.M., Wang Y., Wang G.Y., Zhou C.C., Jia H.J., Gao Z.S.Dr. Genome-wide identification and analysis of the MADS-box gene family and its potential role in fruit development and ripening in red bayberry (Morella rubra). Gene, 2019, 717: 144045 (doi: 10.1016/j.gene.2019.144045).
  • Qi X., Liu C., Song L., Li M. PaMADS7, a MADS-box transcription factor, regulates sweet cherry fruit ripening and softening. Plant Science, 2020, 301: 110634 (doi: 10.1016/j.plantsci.2020.110634).
  • Wang R., Ming M., Li J., Shi D., Qiao X., Li L., Zhang S., Wu J. Genome-wide identification of the MADS-box transcription factor family in pear (Pyrus bretschneideri) reveals evolution and functional divergence. Peer Journal, 2017, 5: e3776 (doi: 10.7717/peerj.3776).
  • Zhao Q., Weber A.L., McMullen M.D., Guill K., Doebley J. MADS-box genes of maize: frequent targets of selection during domestication. Genetics Research, 2011, 93(1): 65-75 (doi: 10.1017/S0016672310000509).
  • Wills D.M., Fang Z., York A.M., Holland J.B., Doebley J.F. Defining the role of the MADS-box gene, Zea agamous-like1, a target of selection during maize domestication. Journal of Heredity, 2018, 109(3): 333-338 (doi: 10.1093/jhered/esx073).
  • Khong G.N., Pati P.K., Richaud F., Parizot B., Bidzinski P., Mai C.D., Bès M., Bourrié I., Meynard D., Beeckman T., Selvaraj M.G., Manabu I., Genga A.M., Brugidou C., Nang Do V., Guiderdoni E., Morel J.B., Gantet P. OsMADS26 negatively regulates resistance to pathogens and drought tolerance in rice. Plant Physiology, 2015, 169(4): 2935-2949 (doi: 10.1104/pp.15.01192).
  • Chen L., Zhao Y., Xu S., Zhang Z., Xu Y., Zhang J., Chong K. OsMADS57 together with OsTB1 coordinates transcription of its target OsWRKY94 and D14 to switch its organogenesis to defense for cold adaptation in rice. New Phytologist, 2018, 218(1): 219-231 (doi: 10.1111/nph.14977).
  • Wang Z., Wang F., Hong Y., Yao J., Ren Z., Shi H., Zhu J.-K. The flowering repressor SVP confers drought resistance in arabidopsis by regulating abscisic acid catabolism. Molecular Plant, 2018, 11(9): 1184-1197 (doi: 10.1016/j.molp.2018.06.009).
  • Guo X., Chen G., Cui B., Gao Q., Guo J.-E., Li A., Zhang L., Hu Z. Solanum lycopersicum agamous-like MADS-box protein AGL15-like gene, SlMBP11, confers salt stress tolerance. Molecular Breeding, 2016, 36: 125 (doi: 10.1007/s11032-016-0544-1).
  • Yin W., Hu Z., Cui B., Guo X., Hu J., Zhu Z., Chen G. Suppression of the MADS-box gene SlMBP8 accelerates fruit ripening of tomato (Solanum lycopersicum). Plant Physiology and Biochemistry, 2017, 118: 235-244 (doi: 10.1016/j.plaphy.2017.06.019).
  • Lozano R., Angosto T., Gómez P., Payán C., Capel J., Huijser P., Salinas J., Martinez-Zapater J.M. Tomato flower abnormalities induced by low temperatures are associated with changes of expression of MADS-Box genes. Plant Physiology, 1998, 117(1): 91-100 (doi: 10.1104/pp.117.1.91).
  • Müller F., Xu J., Kristensen L., Wolters-Arts M., de Groot P. F. M., Jansma S. Y., Mariani C., Park S., Rieu I. High-temperature-induced defects in tomato (Solanum lycopersicum) anther and pollen development are associated with reduced expression of B-class floral patterning genes. PLoS ONE, 2016, 11(12): e0167614 (doi: 10.1371/journal.pone.0167614).
  • Chen R., Ma J., Luo D., Hou X., Ma F., Zhang Y., Meng Y., Zhang H., Guo W. CaMADS, a MADS-box transcription factor from pepper, plays an important role in the response to cold, salt, and osmotic stress. Plant Science, 2019, 280: 164-174 (doi: 10.1016/j.plantsci.2018.11.020).
  • Yang F., Xu F., Wang X., Liao Y., Chen Q., Meng X. Characterization and functional analysis of a MADS-box transcription factor gene (GbMADS9) from Ginkgo biloba. Scientia Horticulture, 2016, 212: 104-114 (doi: 10.1016/j.scienta.2016.09.042).
  • Yu L.H., Wu J., Zhang Z.S., Miao Z.Q., Zhao P.X., Wang Z., Xiang C.B. Arabidopsis MADS-box transcription factor AGL21 acts as environmental surveillance of seed germination by regulating ABI5 expression. Molecular Plant, 2017, 10(6): 834-845 (doi: 10.1016/j.molp.2017.04.004).
  • Shi S.-Y., Zhang F.-F., Gao S., Xiao K. Expression pattern and function analyses of the MADS thranscription factor genes in wheat (Triticum aestivum L.) under phosphorus-starvation condition. Journal of Integrative Agriculture, 2016, 15(8): 1703-1715 (doi: 10.1016/S2095-3119(15)61167-4).
  • Zhang H., Forde B.G. An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science, 1998, 279(5349): 407-409 (doi: 10.1126/science.279.5349.407).
  • Swinnen G., Goossens A., Pauwels L. Lessons from domestication: targeting cis-regulatory elements for crop improvement. Trends in Plant Science, 2016, 21(6): 506-515 (doi: 10.1016/j.tplants.2016.01.014).
  • Singh R., Low E.T., Ooi L.C., Ong-Abdullah M., Ting N.C., Nagappan J., Nookiah R., Amiruddin M.D., Rosli R., Manaf M.A., Chan K.L., Halim M.A., Azizi N., Lakey N., Smith S.W., Budiman M.A., Hogan M., Bacher B., Van Brunt A., Wang C., Ordway J.M., Sambanthamurthi R., Martienssen R.A. The oil palm SHELL gene controls oil yield and encodes a homologue of SEEDSTICK. Nature, 2013, 500(7462): 340-344 (doi: 10.1038/nature12356).
  • Ditta G., Pinyopich A., Robles P., Pelaz S., Yanofsky M.F. The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity. Current Biology, 2014, 14(21): 1935-1940 (doi: 10.1016/j.cub.2004.10.028).
  • Bartlett M.E. Changing MADS-box transcription factor protein—protein interactions as a mechanism for generating floral morphological diversity. Integrative and Comparative Biology, 2017, 57(6): 1312-1321 (doi: 10.1093/icb/icx067).
  • He C., Si C., Teixeira da Silva J.A., Li M., Duan J. Genome-wide identification and classification of MIKC-type MADS-box genes in Streptophyte lineages and expression analyses to reveal their role in seed germination of orchid. BMC Plant Biology, 2019, 19(1): 223 (doi: 10.1186/s12870-019-1836-5).
  • Gramzow L., Weilandt L., Theißen G. MADS goes genomic in conifers: towards determining the ancestral set of MADS-box genes in seed plants. Annals of Botany, 2014, 114(7): 1407-1429 (doi: 10.1093/aob/mcu066).
  • Ma J., Yang Y., Luo W., Yang C., Ding P., Liu Y., Qiao L., Chang Z., Geng H., Wang P., Jiang Q., Wang J., Chen G., Wei Y., Zheng Y., Lan X. Genome-wide identification and analysis of the MADS-box gene family in bread wheat (Triticum aestivum L.). PLoS ONE, 2017, 12(7): e0181443 (doi: 10.1371/journal.pone.0181443).
  • Duan W., Song X., Liu T., Huang Z., Ren J., Hou X., Li Y. Genome-wide analysis of the MADS-box gene family in Brassica rapa (Chinese cabbage). Molecular Genetics and Genomics, 2015, 290(1): 239-255 (doi: 10.1007/s00438-014-0912-7).
  • Shu Y., Yu D., Wang D., Guo D., Guo C. Genome-wide survey and expression analysis of the MADS-box gene family in soybean. Molecular Biology Reports, 2013, 40(6): 3901-3911 (doi: 10.1007/s11033-012-2438-6).
  • Tian Y., Dong Q., Ji Z., Chi F., Cong P., Zhou Z. Genome-wide identification and analysis of the MADS-box gene family in apple. Gene, 2015, 555(2): 277-290 (doi: 10.1016/j.gene.2014.11.018).
  • Wang P., Wang S., Chen Y., Xu X., Guang X., Zhang Y. Genome-wide Analysis of the MADS-Box gene family in watermelon. Computational Biology and Chemistry, 2019, 80: 341-350 (doi: 10.1016/j.compbiolchem.2019.04.013).
  • Ning K., Han Y., Chen Z., Luo C., Wang S., Zhang W., Li L., Zhang X., Fan S., Wang Q. Genome-wide analysis of MADS-box family genes during flower development in lettuce. Plant, Cell & Environment, 2019, 42(6): 1868-1881 (doi: 10.1111/pce.13523).
  • Grimplet J., Martínez-Zapater J.M., Carmona M.J. Structural and functional annotation of the MADS-box transcription factor family in grapevine. BMC Genomics, 2016, 17: 80 (doi: 10.1186/s12864-016-2398-7).
Еще
Статья обзорная