Genome-wide identification and expression profile of the MADS-box gene family in Erigeron breviscapus

Autoři: Wen Tang aff001;  Yayi Tu aff001;  Xiaojie Cheng aff002;  Lili Zhang aff003;  Hengling Meng aff003;  Xin Zhao aff003;  Wei Zhang aff003;  Bin He aff001
Působiště autorů: Jiangxi Key Laboratory of Bioprocess Engineering and Co-Innovation Center for In-vitro Diagnostic Reagents and Devices of Jiangxi Province, College of Life Sciences, Jiangxi Science & Technology Normal University, Nanchang, China aff001;  Key Laboratory of Bio-resources and Eco-environment, Ministry of Education, Sichuan Key Laboratory of Molecular Biology and Biotechnology, College of Life Sciences, Sichuan University, Chengdu, China aff002;  Honghe University, Mengzi, China aff003
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article


The MADS-box gene family encodes transcription factors with many biological functions that extensively regulate plant growth, development and reproduction. Erigeron breviscapus is a medicinal herb used widely in traditional Chinese medicine, and is believed to improve blood circulation and ameliorate platelet coagulation. In order to gain a detailed understanding of how transcription factor expression may regulate the growth of this potentially important medicinal plant, a genome-wide analysis of the MADS-box gene family of E. breviscapus is needed. In the present study, 44 MADS-box genes were identified in E. breviscapus and categorized into five subgroups (MIKC, Mα, Mβ, Mγ and Mδ) according to their phylogenetic relationships with the Arabidopsis MADS-box genes. Additionally, the functional domain, subcellular location and motif compositions of the E. breviscapus MADS-box gene products were characterized. The expression levels for each of the E. breviscapus MADS-box (EbMADS) genes were analyzed in flower, leaf, stem and root organs, and showed that the majority of EbMADS genes were expressed in flowers. Meanwhile, some MADS genes were found to express high levels in leaf, stem and root, indicating that the MADS-box genes are involved in various aspects of the physiological and developmental processes of the E. breviscapus. The results from gene expression analysis under different pollination treatments revealed that the MADS-box genes were highly expressed after non-pollinated treatment. To the best of our knowledge, this study describes the first genome-wide analysis of the E. breviscapus MADS-box gene family, and the results provide valuable information for understanding of the classification, cloning and putative functions of the MADS-box family.

Klíčová slova:

Arabidopsis thaliana – Flowers – Gene expression – Phylogenetic analysis – Pollination – Protein interaction networks – Sequence motif analysis – Transcription factors


1. Duan W, Song X, Liu T, Huang Z, Ren J, Hou X, et al. Genome-wide analysis of the MADS-box gene family in Brassica rapa (Chinese cabbage). Molecular Genetics & Genomics. 2015;290(1):239–55.

2. Passmore S, Maine GT, Elble R, Christ C, Tye BK. Saccharomyces cerevisiae protein involved in plasmid maintenance is necessary for mating of MAT alpha cells. Journal of Molecular Biology. 1988;204(3):593–606. doi: 10.1016/0022-2836(88)90358-0 3066908

3. Norman C, Runswick M, Pollock R, Treisman R. Isolation and properties of cDNA clones encoding SRF, a transcription factor that binds to the c-fos serum response element. Cell. 1988;55(6):989–1003. doi: 10.1016/0092-8674(88)90244-9 3203386

4. Sommer H, Beltrán JP, Huijser P, Pape H, Nnig WE, Saedler H, et al. Deficiens, a homeotic gene involved in the control of flower morphogenesis in Antirrhinum majus: the protein shows homology to transcription factors. Embo Journal. 1990;9(3):605–13. 1968830

5. Yanofsky MF, Ma H, Bowman JL, Drews GN, Feldmann KA, Meyerowitz EM. The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature. 1990;346(6279):35–9. doi: 10.1038/346035a0 1973265

6. Smaczniak C, Immink RG, Muiño JM, Blanvillain R, Busscher M, Busscher-Lange J, et al. Characterization of MADS-domain transcription factor complexes in Arabidopsis flower development. Proceedings of the National Academy of Sciences of the United States of America. 2012;109(5):1560–5. doi: 10.1073/pnas.1112871109 22238427

7. Fu Q, Huang Y, Wang Z, Chen F, Huang D, Lu Y, et al. Proteome Profile and Quantitative Proteomic Analysis of Buffalo (Bubalusbubalis) Follicular Fluid during Follicle Development. International Journal of Molecular Sciences. 2016;17(5):618.

8. Lu W and Xi WP. MADS-box Transcription Factors are Involved in Regulation for Fruit Ripening and Quality Development. Acta Horticulturae Sinica. 2018; 45(09):1802–1812.

9. Fan CM, Wang X, Wang YW, Hu RB, Zhang XM, Chen JX, et al. Genome-wide expression analysis of soybean MADS genes showing potential function in the seed development. Plos One. 2013;8(4):e62288. doi: 10.1371/journal.pone.0062288 23638026

10. Arora R, Agarwal P, Ray S, Singh AK, Singh VP, Tyagi AK, et al. MADS-box gene family in rice: genome-wide identification, organization and expression profiling during reproductive development and stress. Bmc Genomics. 2007;8(1):242.

11. Gu Q, Ferrándiz C, Yanofsky MF, Martienssen R. The FRUITFULL MADS-box gene mediates cell differentiation during Arabidopsis fruit development. Development. 1998;125(8):1509–17. 9502732

12. Heck GR, Perry SE, Nichols KW, Fernandez DE. AGL15, a MADS domain protein expressed in developing embryos. Plant Cell. 1995;7(8):1271–82. doi: 10.1105/tpc.7.8.1271 7549483

13. Ferrándiz C, Liljegren SJ, Yanofsky MF. Negative regulation of the SHATTERPROOF genes by FRUITFULL during Arabidopsis fruit development. Science. 2000;289(5478):436–8. doi: 10.1126/science.289.5478.436 10903201

14. Rounsley SD, Ditta GS, Yanofsky MF. Diverse roles for MADS box genes in Arabidopsis development. Plant Cell. 1995;7(8):1259–69. doi: 10.1105/tpc.7.8.1259 7549482

15. Parenicova L, De FS, Kieffer M, Horner DS, Favalli C, Busscher J, et al. Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world. Plant Cell. 2003;15(7):1538–51. doi: 10.1105/tpc.011544 12837945

16. Alvarez-Buylla ER, Liljegren SS, Gold SE, Burgeff C, Ditta. MADS-box gene evolution beyond flowers: expression in pollen, endosperm, guard cells, roots and trichomes. Plant Journal. 2010;24(4):457–66.

17. Becker A, Theiben G. The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Molecular Phylogenetics & Evolution. 2003;29(3):464–89.

18. Shore P, Sharrocks AD. The MADS-box family of transcription factors. Eur J Biochem. 1995;229(1):1–13. 7744019

19. Riechmann JL, Meyerowitz EM. MADS domain proteins in plant development. Biological Chemistry. 1997;378(10):1079–101. 9372178

20. Fan HY, Hu Y, Tudor M, Ma H. Specific interactions between the K domains of AG and AGLs, members of the MADS domain family of DNA binding proteins. Plant Journal. 2010;12(5):999–1010.

21. Honma T, Goto K. Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature. 2001;409(6819):525–9. doi: 10.1038/35054083 11206550

22. Lai X, Daher H, Galien A, Hugouvieux V, Zubieta C. Structural Basis for Plant MADS Transcription Factor Oligomerization. Comput Struct Biotechnol. 2019; 17: 946–953.

23. Bodt SD, Raes J, Florquin K, Rombauts S, Rouzé P, Theißen G, et al. Genomewide Structural Annotation and Evolutionary Analysis of the Type I MADS-Box Genes in Plants. Journal of molecular evolution. 2003;56(5):573–86. doi: 10.1007/s00239-002-2426-x 12698294

24. Stefanie DB, Jeroen R, Yves VdP, Günter T. And then there were many: MADS goes genomic. Trends in Plant Science. 2003;8(10):475–83. doi: 10.1016/j.tplants.2003.09.006 14557044

25. Lucie P, Stefan dF, Martin K, David S H, Cristina F, Jacqueline B, et al. 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):1538–51. doi: 10.1105/tpc.011544 12837945

26. Leseberg C, Li A, Kang H, Duvall M, Mao L. Genome-wide analysis of the MADS-box gene family in Populus trichocarpa. Gene. 2006;378(1):84–94.

27. Zongda X, Qixiang Z, Lidan S, Dongliang D, Tangren C, Huitang P, et al. Genome-wide identification, characterisation and expression analysis of the MADS-box gene family in Prunus mume. Molecular Genetics & Genomics. 2014;289(5):903–20.

28. 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, 2014, 555(2):277–290. doi: 10.1016/j.gene.2014.11.018 25447908

29. Nardeli SM, Artico S, Aoyagi GM, Moura SMD, Silva TDF, Grossi-De-Sa MF, et al. Genome-wide analysis of the MADS-box gene family in polyploid cotton (Gossypium hirsutum) and in its diploid parental species (Gossypium arboreum and Gossypium raimondii). Plant Physiology & Biochemistry. 2018;127:169–184.

30. Kong WL, Zhang KD, Wu JC, Zhang LP, Pan H, Tang JW, et al. Genome-wide identification and phylogenetic analysis of MADS-box family gene in Beta vulgaris. Acta Agriculturae Boreali-Sinica, 2018;33(1):86–95.

31. Wei X, Wang L, Yu J, Zhang Y, Li D, Zhang X. Genome-wide identification and analysis of the MADS-box gene family in sesame. Gene. 2015;569(1):66–76. doi: 10.1016/j.gene.2015.05.018 25967387

32. José DR, Diego L, José M MZ, María José C. Genome-wide analysis of MIKCC-type MADS box genes in grapevine. Plant Physiology. 2009;149(1):354–69. doi: 10.1104/pp.108.131052 18997115

33. Gan DF, Ding F, Zhuang D, Liang DD. Genome-wide sequence characterization analysis of MADS-box transcription factor gene family in cucumber (Cucumis sativus L.). Journal of Nuclear Agricultural Sciences. 2012;26(9):1249–1256.

34. Li HF, Jia HZ, Dong QL, Ran K, Wang HW. Cloning and Expression Analysis of Ten MADS-box Genes in Peach(Prunus persica var. nectarina ‘Luxing’). Scientia Agricultura Sinica. 2016; 49(23):4593–4605.

35. Sun JJ, Feng L, Wang DH, Liu XF, Xia L, Na L, et al. CsAP3: A Cucumber Homolog to Arabidopsis APETALA3with Novel Characteristics. Frontiers in Plant Science. 2016;7(e6144).

36. Yang J, Zhang G, Zhang J, Liu H, Chen W, Wang X, et al. Hybrid de novo genome assembly of the Chinese herbal fleabane Erigeron breviscapus. Gigascience. 2017;6(6):1.

37. Li X, Zhang S, Yang Z, Song K, Yi T. Conservation genetics and population diversity of Erigeron breviscapus (Asteraceae), an important Chinese herb. Biochemical Systematics & Ecology. 2013;49(2):156–66.

38. Wang J, Chen Y, Liu B, Wang Q, Zhang L, Wang Z, et al. Systematic Investigation of the Erigeron breviscapus Mechanism for Treating Cerebrovascular Disease. Journal of ethnopharmacology. 2018;224:429–440. doi: 10.1016/j.jep.2018.05.022 29783016

39. Zhang RW, Fan XE, Lai-Wei LI, Lin LZ, Harnly JM. Identification and Quantification of Phenolic Components of Erigeron breviscapus and Its Derived Drug Breviscapine. Natural Product Research & Development. 2015;27: 962–970.

40. Chu Q, Wu T, Liang F, Ye J. Simultaneous determination of active ingredients in Erigeron breviscapus (Vant.) Hand-Mazz. by capillary electrophoresis with electrochemical detection. Journal of Pharmaceutical & Biomedical Analysis. 2005;37(3):535–41.

41. Li Li L, Ai Jun L, Jian Guo L, Xue-Hong Y, Lu Ping Q, Ding Feng S. Protective effects of scutellarin and breviscapine on brain and heart ischemia in rats. J Cardiovasc Pharmacol. 2007;50(3):327–32. doi: 10.1097/FJC.0b013e3180cbd0e7 17878763

42. Li XL, Li YW, Li HY, Xu H, Zheng XX, Guo DW, et al. A study of the cardioprotective effect of breviscapine during hypoxia of cardiomyocytes. Planta Medica. 2004;70(11):1039–44. doi: 10.1055/s-2004-832644 15549659

43. Tao YH, Jiang DY, Xu HB, Yang XL. Inhibitory effect of Erigeron breviscapus extract and its flavonoid components on GABA shunt enzymes. Phytomedicine. 2008;15(1):92–7.

44. Yang S, Wang P, Yang J. Effects of Genotypic and Environmental on Yield and Scutellarin Content of Erigeron breviscapus. Chinese Agricultural Science Bulletin. 2011;27(8):140–3.

45. Zhao WJ, Yan SQ, Cui MK, Zhang YF, Guan HL. The Relationship between the Stage of Androgenesis and Flower Character in Erigeron breviscapus. Lishizhen Medicine & Materia Medica Research. 2010;21(5):1210–2.

46. Zhang W, Wei X, Meng H-L, Ma C-H, Jiang N-H, Zhang G-H, et al. Transcriptomic comparison of the self-pollinated and cross-pollinated flowers of Erigeron breviscapus to analyze candidate self-incompatibility-associated genes. Bmc Plant Biology. 2015;15(1):248.

47. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research. 1997;25(17):3389. doi: 10.1093/nar/25.17.3389 9254694

48. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, et al. Pfam: the protein families database. Nucleic Acids Research. 2014;42(Database issue):222–30.

49. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution, 2018; 35(6):1547–1549. doi: 10.1093/molbev/msy096 29722887

50. Tang W, Ouyang C, Liu L, Li H, Zeng C, Wang J, et al. Genome-wide identification of the fatty acid desaturases gene family in four Aspergillus species and their expression profile in Aspergillus oryzae. AMB Express. 2018;8:169. doi: 10.1186/s13568-018-0697-x 30324529

51. Akaike H. A new look at the statistical model identification. Automatic Control IEEE Transactions on. 1974;19(6): 716–723.

52. Posada D, Crandall K A. Selecting the best-fit model of nucleotide substitution. Systematic Biology. 2001; 50(4): 580–601. 12116655

53. Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 2001;17(8): 754–755. doi: 10.1093/bioinformatics/17.8.754 11524383

54. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, et al. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Research. 2009;37(Web Server issue):202–8.

55. He B, Gu Y, Xiang T, Cheng X, Wei C, Jian F, et al. De NovoTranscriptome Sequencing ofOryza officinalisWall ex Watt to Identify Disease-Resistance Genes. International Journal of Molecular Sciences. 2015;16(12):29482–95. doi: 10.3390/ijms161226178 26690414

56. Wankun D, Yongbo W, Zexian L, Han C, Yu X. HemI: a toolkit for illustrating heatmaps. Plos One. 2014;9(11):e111988. doi: 10.1371/journal.pone.0111988 25372567

57. He B, Ma L, Hu Z, Li H, Ai M, Long C, et al. Deep sequencing analysis of transcriptomes in Aspergillus oryzae in response to salinity stress. Applied Microbiology and Biotechnology. 2018; 102(2):897–906. doi: 10.1007/s00253-017-8603-z 29101425

58. Peter A. PASW Statistics by SPSS: A Practical Guide: Version 18.0. 2010.

59. Wang L. Advances in the Research of MADS-box Gene in Plant. Biotechnology Bulletin. 2010;8:12–19.

60. Cui Y, Zhang L, Huang M. Progress of MADS-Box Gene Research in Plant. Progress in Biotechnology. 2003; 23(9):50–54.

61. Nettancourt DD. Incompatibility and Incongruity in Wild and Cultivated Plants: Springer Berlin Heidelberg. 2001.

62. Zhang Y, Zhao Z, Xue Y. Roles of Proteolysis in Plant Self-Incompatibility. Annual Review of Plant Biology. 2009; 60(1):21–42.

63. Lu Q, Jia QL, Hong YU, Mei LC, Li HC, Min LA. Advances in studies on Erigeron breviscapus. Chinese Traditional & Herbal Drugs. 2005;36(1):141–144.

64. Wang Z, Wei QU, Liang JY. The research progress of Potentilla plants. Strait Pharmaceutical Journal. 2012;22(5):1–8.

65. Zhou Z, Zhang S, Hua L, Zhong W, Jin Z, Ding R. Study of Resisting Leukoplakia Canceration and Angiogenesis of Herba Erigerontis. Shanghai journal of stomatology. 2000;9(2):110. 15014824

66. Zhou Y, Hu L, Jiang L, Liu S. Genome-wide identification, characterization, and transcriptional analysis of the metacaspase gene family in cucumber (Cucumis sativus). Genome. 2018;61(3):187–94. doi: 10.1139/gen-2017-0174 29461868

67. Alvarez-Buylla ER, Pelaz S, Liljegren SJ, Gold SE, Burgeff C, Ditta GS et al. An ancestral MADS-box gene duplication occurred before the divergence of plants and animals. Proceedings of the National Academy of Sciences of the United States of America. 2000;97(10):5328–33. doi: 10.1073/pnas.97.10.5328 10805792

68. Pelaz S, Ditta GS, Baumann E, Wisman E, Yanofsky MF. B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature. 2000;405(6783):200–3. doi: 10.1038/35012103 10821278

69. Moore S, Vrebalov J, Payton P, Giovannoni J. Use of genomics tools to isolate key ripening genes and analyse fruit maturation in tomato. Journal of Experimental Botany. 2002;53(377):2023. doi: 10.1093/jxb/erf057 12324526

70. Yamaguchi T, Lee D, Miyao A, Hirochika H, An G, Hirano H. Functional diversification of the two C-class MADS box genes OSMADS3 and OSMADS58 in Oryza sativa. Plant Cell. 2006;18(1):15–28. doi: 10.1105/tpc.105.037200 16326928

71. Zhu YY, Shao X, Wang Y, Li YQ, Guo WD. Bioinformatics analysis of MADS-box genes and their expression in cherry. Plant Physiology Journal. 2015;51(3):354–62.

72. Tsaftaris AS, Polidoros AN, Pasentsis K, Kalivas A. Cloning, structural characterization, and phylogenetic analysis of flower MADS-box genes from crocus (Crocus sativus L.). Scientific world journal. 2014;7(1):1047–62.

73. Yang X, Wu F, Lin X, Du X, Chong K, Gramzow L, et al. Live and Let Die. The Bsister MADS-Box Gene OsMADS29 Controls the Degeneration of Cells in Maternal Tissues during Seed Development of Rice (Oryza sativa). PLOS ONE. 2012;7 (12):e51435. doi: 10.1371/journal.pone.0051435 23251532

74. Lid SE, Meeley RB, Min Z, Nichols S, Olsen OA. Knock-out mutants of two members of the AGL2 subfamily of MADS-box genes expressed during maize kernel development. Plant Science (Oxford). 2004;167(3):575–582.

75. Tang N, Deng W, Hu G, Hu N, Li Z. Transcriptome Profiling Reveals the Regulatory Mechanism Underlying Pollination Dependent and Parthenocarpic Fruit Set Mainly Mediated by Auxin and Gibberellin. PLOS ONE. 2015; 10(4): e0125355. doi: 10.1371/journal.pone.0125355 25909657

76. Li L, Yang L, Wang X, Gu A, Yang B, Yan S, et al. Preliminary Studies on Breeding System and Visiting Insects of Erigeron breviscapus. Southwest China Journal of Agricultural Sciences. 2009;22(2):454–458.

77. Zhang W, Meng HL, Meng ZG, Liang Q, Wei X, Yang SC. Methylation Analysis on the Coding Region of Self-incompatibility SRK Gene of Erigeron breviscapus. Journal of West China Forestry Science. 2016;45(6):8–13.

78. Zhang YJ, Zhao ZH, Xue YB. Roles of proteolysis in plant self-incompatibility. Annual review of plant biology. 2009;60(1):21.

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