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Nezhdanova A.V., Shchennikova A.V. Transcription factors of the mads family in plants: relationship with domestication traits and prospects for breeding (review). Sel'skokhozyaistvennaya Biologiya [Agricultural Biology], 2021, Vol. 56, № 5, p. 823-842.
(how to cite this article)

doi: 10.15389/agrobiology.2021.5.823eng

UDC: 631.522/.524:575:577.21

Acknowledgments:

Supported financially from the Russian Science Foundation (grant No. 21-16-0008), the Russian Foundation for Basic Research (grant No. 18-29-07007) and the Ministry of Science and Higher Education of the Russian Federation

 

TRANSCRIPTION FACTORS OF THE MADS FAMILY IN PLANTS: RELATIONSHIP WITH DOMESTICATION TRAITS AND PROSPECTS FOR BREEDING (review)

A.V. Nezhdanova, A.V. Shchennikova✉

Institute of Bioengineering, Federal Research Center Fundamentals of Biotechnology RAS, 33/2, Leninskii prospect, Moscow, 119071 Russia, e-mail anna-negdanova@mail.ru, shchennikova@yandex.ru (✉ corresponding author)

ORCID:
Nezhdanova A.V. orcid.org/0000-0003-4175-3175
Shchennikova A.V. orcid.org/0000-0003-4692-3727

Received June 9, 2021

 

The traits of domestication, which are subdivided into three groups (productivity, adaptability, and reproduction) and together make up a domesticated syndrome that brings together taxonomically distant domesticated forms, remain economically significant in modern cultivated crops as well. A significant part of the genes that control domestication traits in plants are represented by the genes of transcription factors, in particular, those belonging to the MADS-domain family. MADS-domain proteins are key regulators of almost all aspects of plant reproductive development, including the determination of the flowering time, the inflorescence structure, the flower organ identity, the development of roots, fruits, and seeds, as well as the adaptive and stress response to adverse environmental conditions. The presented review describes the possible involvement of MADS-box genes in plant domestication and breeding. We discuss the role of MADS-box genes in the regulation of vernalization (plant response to prolonged cold treatment), bud physiological dormancy, inflorescence and flower structure, plant fertility and fruit qualitative traits (ripening characteristics, synthesis of carotenoids and anthocyanins, the number of seeds, fruit shuttering, fruit shelf life), as well as plant stress response (salinity, drought, temperature changes). The phenomenon of MADS-box gene functional pleiotropy and redundancy (due to the existence of paralogs) is considered. It has been supposed that MADS-box genes high structural and functional conservatism may indicate their high potential as tools for predictable fine tuning of crop phenotypes by combining (including dose-dependent) different alleles and paralogs of MADS-box genes. Another possible method is the separation of the pleiotropic functions of the MADS-box gene by introducing mutations in its coding or cis-regulatory sequence to alter specific protein-protein or protein-DNA interactions, as well as the pattern and/or level of expression, including in response to various external and internal signals. It is concluded that fundamental and applied studies of MADS-box genes in various plant species (both wild and cultivated) will not only lead to a deeper understanding of the evolution and development of modern plants, but will also greatly contribute to the improvement of crops, including using CRISPR/Cas and other modern technologies.

Keywords: transcription regulation, transcription factors, MADS-box genes, conservatism, pleiotropy, domestication traits, productivity, adaptation, reproduction, economically valuable traits, target genes.

 

REFERENCES

  1. Purugganan M.D., Fuller D.Q. The nature of selection during plant domestication. Nature, 2009, 457(7231): 843-848 CrossRef
  2. 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 CrossRef
  3. 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 CrossRef
  4. 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 CrossRef
  5. Martínez-Ainsworth N.E., Tenaillon M.I. Superheroes and masterminds of plant domestication. Comptes Rendus Biologies, 2016, 339(7-8): 268-273 CrossRef
  6. Stetter M.G., Gates D.J., Mei W., Ross-Ibarra J. How to make a domesticate. Current Biology, 2017, 27(17): R896-R900 CrossRef
  7. 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 CrossRef
  8. 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 CrossRef
  9. Meyer R., Purugganan M.D. Evolution of crop species: genetics of domestication and diversification. Nature Reviews Genetics, 2013, 14(12): 840-852 CrossRef
  10. Purugganan M.D. Evolutionary insights into the nature of plant domestication. Current Biology, 2019, 29(14): R705-R714 CrossRef
  11. Purugganan M.D., Fuller D.Q. Archaeological data reveal slow rates of evolution during plant domestication. Evolution, 2011, 65(1): 171-183 CrossRef
  12. 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 CrossRef
  13. 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 CrossRef
  14. 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 CrossRef
  15. 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 CrossRef
  16. Allaby R.G. Integrating the processes in the evolutionary system of domestication. Journal of Experimental Botany, 2010, 61(4): 935-944 CrossRef
  17. Zohary D. Unconscious selection and the evolution of domesticated plants. Economic Botany, 2004, 58: 5-10 CrossRef
  18. Arnold M.L. Natural hybridization and the evolution of domesticated, pest and disease organisms. Molecular Ecology, 2014, 13(5): 97-1007 CrossRef
  19. Janzen G.M., Wang L., Hufford M.B. The extent of adaptive wild introgression in crops. New Phytologist, 2018, 221(3): 1279-1288 CrossRef
  20. Heslop-Harrison J.S., Schwarzacher T. Domestication, genomics, and the future for banana. Annals of Botany, 2007, 100(5): 1073-1084 CrossRef
  21. 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 CrossRef
  22. Choi J.Y., Purugganan M.D. Multiple origin but single domestication led to Oryza sativa. G3 (Bethesda), 2018, 8(3): 797-803 CrossRef
  23. 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 CrossRef
  24. 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 CrossRef
  25. 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 CrossRef
  26. Miller A.J., Gross B.L. From forest to field: perennial fruit crop domestication. American Journal of Botany, 2011, 98(9): 1389-1414 CrossRef
  27. 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 CrossRef
  28. 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 CrossRef
  29. 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 CrossRef
  30. 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 CrossRef
  31. Lenser T., Theißen G. Molecular mechanisms involved in convergent crop domestication. Trends in Plant Science, 2013, 18(12): 704-714 CrossRef
  32. 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 CrossRef
  33. 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 CrossRef
  34. Theißen G., Rümpler F., Gramzow L. Array of MADS-box genes: facilitator for rapid adaptation? Trends in Plant Sciences, 2018, 23(7): 563-576 CrossRef
  35. 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 CrossRef
  36. 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 CrossRef
  37. 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 CrossRef
  38. 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 CrossRef
  39. 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 CrossRef
  40. Parenicova 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 CrossRef
  41. Bowman J.L., Smyth D.R., Meyerowitz E.M. Genes directing flower development in Arabidopsis. The Plant Cell, 1989, 1(1): 37-52 CrossRef
  42. 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.
  43. 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 CrossRef
  44. Lee J., Lee I. Regulation and function of SOC1, a flowering pathway integrator. Journal of Experimental Botany, 2010, 61(9): 2247-2254 CrossRef
  45. 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 CrossRef
  46. 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 CrossRef
  47. Kempin S.A., Savidge B., Yanofsky M.F. Molecular basis of the cauliflower phenotype in Arabidopsis. Science, 1995, 267(5197): 522-525 CrossRef
  48. 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 CrossRef
  49. 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 CrossRef
  50. Cho L.H., Yoon J., An G. The control of flowering time by environmental factors. The Plant Journal, 2017, 90(4): 708-719 CrossRef
  51. 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 CrossRef
  52. Preston J., Sandve S. Adaptation to seasonality and the winter freeze. Frontiers in Plant Science, 2013, 4: 167 CrossRef
  53. Andrés F., Coupland G. The genetic basis of flowering responses to seasonal cues. Nature Reviews Genetics, 2012, 13(9): 627-639 CrossRef
  54. 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 CrossRef
  55. Amasino R. Vernalization, competence, and the epigenetic memory of winter. The Plant Cell, 2004, 16(10): 2553-2559 CrossRef
  56. 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 CrossRef
  57. 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 CrossRef
  58. 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 CrossRef
  59. 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 CrossRef
  60. 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 CrossRef
  61. 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 CrossRef
  62. 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 CrossRef
  63. Kennedy A., Geuten K. The role of FLOWERING LOCUS C relatives in cereals. Frontiers in Plant Science, 2020, 11: 617340 CrossRef
  64. 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 CrossRef
  65. 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 CrossRef
  66. 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 CrossRef
  67. 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 CrossRef
  68. 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 CrossRef
  69. 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 CrossRef
  70. 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 CrossRef
  71. 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 CrossRef
  72. 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 CrossRef
  73. 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 CrossRef
  74. 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 CrossRef
  75. 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 CrossRef
  76. 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 CrossRef
  77. 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 CrossRef
  78. 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 CrossRef
  79. 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 CrossRef
  80. 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 CrossRef
  81. Sreenivasulu N., Schnurbusch T. A genetic playground for enhancing grain number in cereals. Trends in Plant Science, 2012, 17(2): 91-101 CrossRef
  82. 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 CrossRef
  83. 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 CrossRef
  84. 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 CrossRef
  85. 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 CrossRef
  86. 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 CrossRef
  87. 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 CrossRef
  88. 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 CrossRef
  89. 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 CrossRef
  90. 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 CrossRef
  91. 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 CrossRef
  92. 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 CrossRef
  93. 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 CrossRef
  94. 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 CrossRef
  95. 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 CrossRef
  96. 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 CrossRef
  97. 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 CrossRef
  98. 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 CrossRef
  99. 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 CrossRef
  100. 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 CrossRef
  101. 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 CrossRef
  102. 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 CrossRef
  103. 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 CrossRef
  104. 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 CrossRef
  105. 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 CrossRef
  106. 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 CrossRef
  107. 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 CrossRef
  108. 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 CrossRef
  109. 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 CrossRef
  110. 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 CrossRef
  111. 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 CrossRef
  112. 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 CrossRef
  113. 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 CrossRef
  114. 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 CrossRef
  115. 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 CrossRef
  116. 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 CrossRef
  117. 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 CrossRef
  118. 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 CrossRef
  119. 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 CrossRef
  120. 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 CrossRef
  121. 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 CrossRef
  122. 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 CrossRef
  123. 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 CrossRef
  124. 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 CrossRef
  125. 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 CrossRef
  126. 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 CrossRef
  127. Zhang H., Forde B.G. An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science, 1998, 279(5349): 407-409 CrossRef
  128. 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 CrossRef
  129. 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 CrossRef
  130. 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 CrossRef
  131. 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 CrossRef
  132. 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 CrossRef
  133. 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 CrossRef
  134. 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 CrossRef
  135. 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 CrossRef
  136. 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 CrossRef
  137. 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 CrossRef
  138. 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 CrossRef
  139. 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 CrossRef
  140. 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 CrossRef

 

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