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Whole-genome survey and characterization of MADS-box gene family in maize and sorghum

  • Yang Zhao
  • Xiaoyu Li
  • Wenjuan Chen
  • Xiaojian Peng
  • Xiao Cheng
  • Suwen Zhu
  • Beijiu ChengEmail author
Original Paper

Abstract

MADS-box genes comprise a large gene family, which codes for transcription factors, and play important functions in various aspects of flowering plant growth and development. However, little is known about the MADS-box genes in maize (Zea mays) and sorghum (Sorghum bicolor). Here, we performed a comprehensive bioinformatics analysis of the MADS-box gene family in the maize and sorghum genomes and identified 75 maize and 65 sorghum MADS-box genes. We subsequently carried out a comparative analysis of these genes, including the gene structure, phylogenetic relationship, conserved protein motifs, gene duplications, chromosomal locations and expression pattern between the two plants. According to these analyses, the MADS-box genes in both maize and sorghum were categorized into five (MIKCC, MIKC*, Mα, Mβ and Mγ) groups, and the MIKCC groups were further divided into 11 subfamilies. In addition, gene duplications of MADS-box genes were also investigated in the maize, sorghum, rice and Arabidopsis genomes. We found a higher percentage of MADS-box gene duplications in the maize and sorghum genomes, which contributed to the expansion of the MADS-box gene family. Furthermore, both tandem and segmental duplications played a major role in the MADS-box gene expansion in maize and sorghum. A survey of maize and sorghum EST sequences indicated that MADS-box genes exhibit a various expression pattern, suggesting diverse and novel functions of MADS-box gene families in the two plants. These results provided a useful reference for selection of candidate MADS-box genes for cloning and further functional analysis in both maize and sorghum.

Keywords

MADS-box Maize Sorghum Phylogenetic analysis Duplication Expression patterns 

Notes

Acknowledgments

This work was supported by grants from the National High-Tech Research and Development Program (863 Program) (No. 2008AA10Z408) and the National Natural Science Foundation of China (No. 10675002). We thank members of the Key Laboratory of Crop biology of Anhui province for their assistance in this study.

References

  1. Alvarez-Buylla ER, Liljegren SJ, Pelaz S, Gold SE, Burgeff C, Ditta GS, Vergara-Silva F, Yanofsky MF (2000) MADS-box gene evolution beyond flowers: expression in pollen, endosperm, guard cells, roots and trichomes. Plant J 24:457–466PubMedCrossRefGoogle Scholar
  2. Alwee SS, Van der Linden CG, Van der Schoot J, de Folter S, Angenent GC, Cheah SC, Smulders MJM (2006) Characterization of oil palm MADS box genes in relation to the mantled flower abnormality. Plant Cell Tissue Organ Cult 85:331–344CrossRefGoogle Scholar
  3. Arora R, Agarwal P, Ray S, Singh AK, Singh VP, Tyagi AK, Kapoor S (2007) MADS-box gene family in rice: genome-wide identification, organization and expression profiling during reproductive development and stress. BMC Genomics 8:242–263PubMedCrossRefGoogle Scholar
  4. Bailey TL, Elkan C (1995) The value of prior knowledge in discovering motifs with MEME. Proc Int Conf Intell Syst Mol Biol 3:21–29PubMedGoogle Scholar
  5. Becker A, Theißen G (2003) The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Mol Phylogenet Evol 29:464–489PubMedCrossRefGoogle Scholar
  6. Becker A, Winter KU, Meyer B, Saedler H, Theißen G (2000) MADS-box gene diversity in seed plants 300 million years ago. Mol Biol Evol 17:1425–1434PubMedGoogle Scholar
  7. Caetano-Anollés G (2001) Novel strategies to study the role of mutation and nucleic acid structure in evolution. Plant Cell Tissue Organ Cult 67:115–132CrossRefGoogle Scholar
  8. Cho S, Jang S, Chae S, Chung KM, Moon YH, An G, Jang SK (1999) Analysis of the C-terminal region of Arabidopsis thaliana APETALA1 as a transcription activation domain. Plant Mol Biol 40:419–429PubMedCrossRefGoogle Scholar
  9. Davies B, Egea-Cortines M, Silva ED, Saedler H, Sommer H (1996) Multiple interactions amongst floral homeotic MADS box proteins. EMBO J 15:4330–4343PubMedGoogle Scholar
  10. De Bodt S, Raes J, Van de Peer Y, Theißen G (2003) And then there were many: MADS goes genomic. Trends Plant Sci 8:475–483PubMedCrossRefGoogle Scholar
  11. Díaz-Riquelme J, Lijavetzky D, Martínez-Zapater JM, Carmona MJ (2009) Genome-wide analysis of MIKCC-type MADS-box genes in grapevine. Plant Physiol 149:354–369PubMedCrossRefGoogle Scholar
  12. Finn RD, Mistry J, Schuster-Bockler B, Griffiths-Jones S, Hollich V, Lassmann T, Moxon S, Marshall M, Khanna A, Durbin R, Eddy SR, Sonnhammer EL, Bateman A (2006) Pfam: clans, web tools and services. Nucleic Acids Res 34:247–251CrossRefGoogle Scholar
  13. Gojobori T, Li WH, Graur D (1982) Patterns of nucleotide substitution in pseudogenes and functional genes. J Mol Evol 18:360–369PubMedCrossRefGoogle Scholar
  14. Gu Q, Ferrándiz C, Yanofsky MF, Martienssen R (1998) The FRUITFULL MADS-box gene mediates cell differentiation during Arabidopsis fruit development. Development 125:1509–1517PubMedGoogle Scholar
  15. Gu ZL, Cavalcanti A, Chen FC, Bouman P, Li WH (2002) Extent of gene duplication in the genomes of drosophila, nematode, and yeast. Mol Biol Evol 19:256–262PubMedGoogle Scholar
  16. Hartmann U, Höhmann S, Nettesheim K, Wisman E, Seadler H, Huijser P (2000) Molecular cloning of SVP: a negative regulator of the floral transition in Arabidopsis. Plant J 21:351–360PubMedCrossRefGoogle Scholar
  17. Henschel K, Kofuji R, Hasebe M, Saedler H, Münster T, Theißen G (2002) Two ancient classes of MIKC-type MADS-box genes are present in the moss physcomitrella patens. Mol Biol Evol 19:801–814PubMedGoogle Scholar
  18. Holub E (2001) Arms race is ancient history in Arabidopsis, the wildflower. Nat Rev Genet 2:516–527PubMedCrossRefGoogle Scholar
  19. Honma T, Goto K (2001) Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409:525–529PubMedCrossRefGoogle Scholar
  20. Irish VF (2003) The evolution of floral homeotic gene function. Bioessays 25:637–646PubMedCrossRefGoogle Scholar
  21. Jain M, Khurana JP (2009) Transcript profiling reveals diverse roles of auxin-responsive genes during reproductive development and abiotic stress in rice. FEBS J 276:3148–3162PubMedCrossRefGoogle Scholar
  22. Kaufmann K, Melzer R, Theißen G (2005) MIKC-type MADS-domain proteins: structural modularity, protein interactions and network evolution in land plants. Gene 347:183–198PubMedCrossRefGoogle Scholar
  23. Kofuji R, Sumikawa N, Yamasaki M, Kondo K, Ueda K, Ito M, Hasebe M (2003) Evolution and divergence of the MADS-box gene family based on genome-wide expression analyses. Mol Biol Evol 20:1963–1977PubMedCrossRefGoogle Scholar
  24. Kramer EM, Irish VF (1999) Evolution of genetic mechanisms controlling petal development. Nature 399:144–148PubMedCrossRefGoogle Scholar
  25. Leseberg CH, Li A, Kang H, Duvall M, Mao L (2006) Genome-wide analysis of the MADS-box gene family in Populus trichocarpa. Gene 378:84–94PubMedCrossRefGoogle Scholar
  26. Liljegren SJ, Ditta GS, Eshed Y, Savidge B, Bowman JL, Yanofsky MF (2000) SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature 404:766–770PubMedCrossRefGoogle Scholar
  27. Ma H, Yanofsky MF, Meyerowitz EM (1991) AGL1-AGL6, an Arabidopsis gene family with similarity to floral homeotic and transcription factor genes. Gene 5:484–495CrossRefGoogle Scholar
  28. Mandel MA, Gustafson-Brown C, Savidge B, Yanofsky MF (1992) Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360:273–277PubMedCrossRefGoogle Scholar
  29. Mena M, Mandel MA, Lerner DR, Yanofsky MF, Schmidt RJ (1995) A characterization of the MADS-box gene family in maize. Plant J 8:845–854PubMedCrossRefGoogle Scholar
  30. Messenguy F, Dubois E (2003) Role of MADS box proteins and their cofactors in combinatorial control of gene expression and cell development. Gene 316:1–21PubMedCrossRefGoogle Scholar
  31. Michaels SD, Amasino RM (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11:949–956PubMedCrossRefGoogle Scholar
  32. Nam J, Kim J, Lee S, An G, Ma H, Nei M (2004) Type I MADS-box genes have experienced faster birth-and-death evolution than typeII MADS-box genes in angiosperms. Proc Natl Acad Sci USA 101:1910–1915PubMedCrossRefGoogle Scholar
  33. Nesi N, Debeaujon I, Jond C, Stewart AJ, Jenkins GI, Caboche M, Lepiniec L (2002) The TRANSPARENT TESTA16 locus encodes the Arabidopsis BSISTER MADS domain protein and is required for proper development and pigmentation of the seed coat. Plant Cell 14:2463–2479PubMedCrossRefGoogle Scholar
  34. Norman C, Runswick M, Pollock R, Treisman R (1988) Isolation and properties of cDNA clones encoding SRF, a transcription factor that binds to the c-fos serum response element. Cell 55:989–1003PubMedCrossRefGoogle Scholar
  35. Parenicova L, de Folter S, Kieffer M, Horner DS, Favalli C, Busscher J, Cook HE, Ingram RM, Kater MM, Davies B, Angenent GC, Colombo L (2003) Molecular phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world. Plant Cell 15:1538–1551PubMedCrossRefGoogle Scholar
  36. Passmore S, Maine GT, Elble R, Christ C, Tye BK (1988) Saccharomyces cerevisiae protein involved in plasmid maintenance is necessary for mating of MAT alpha cells. J Mol Biol 204:593–606PubMedCrossRefGoogle Scholar
  37. Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Hellsten U, Mitros T, Poliakov P, Schmutz J, Spannag M, Tang HB, Wang XY, Wicker T, Bharti AK, Chapman J, Feltus FA, Gowik U, Grigoriev IV, Lyons E, Maher CA, Martis M, Narechania A, Otillar RP, Penning BW, Salamov AA, Wang Y, Zhang LF, Carpita NC, Freeling M, Gingle AR, Peterson DG, Mehboob-ur-Rahman WareD, Westhoff P, Mayer KFX, Messing J, Rokhsar DS (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556PubMedCrossRefGoogle Scholar
  38. Pellegrini L, Tan S, Richmond TJ (1995) Structure of serum response factor core bound to DNA. Nature 376:490–498PubMedCrossRefGoogle Scholar
  39. Purugganan MD (1997) The MADS-box floral homeotic gene lineages predate the origin of seed plants: phylogenetic and molecular clock estimates. J Mol Evol 45:392–396PubMedCrossRefGoogle Scholar
  40. Riechmann JL, Meyerowitz EM (1997) MADS-domain protein in plant deveiopment. Biol Chem 378:1079–1101PubMedCrossRefGoogle Scholar
  41. Riechmann JL, Krizek BA, Meyerowitz EM (1996) Dimerization specificity of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA, and AGAMOUS. Proc Natl Acad Sci USA 93:4793–4798PubMedCrossRefGoogle Scholar
  42. Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer Z, Yanofsky MF, Coupland G (2000) Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288:1613–1616PubMedCrossRefGoogle Scholar
  43. Schnable PS, Ware D, Fulton RS, Wei FS, Pasternak S, Liang CZ, Zhang JW, Clifton SW, Wing RA, Wilson RK et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115PubMedCrossRefGoogle Scholar
  44. Scortecci KC, Michaels SD, Amasino RM (2001) Identification of a MADS-box gene, FLOWERING LOCUS M, that represses flowering. Plant J 26:229–236PubMedCrossRefGoogle Scholar
  45. Shore P, Sharrocks AD (1995) The MADS-box family of transcription factors. Eur J Biochem 229:1–13PubMedCrossRefGoogle Scholar
  46. Sommer H, Beltran JP, Huijser P, Pape H, Lönnig WE, Saedler H, Schwarz-Sommer Z (1990) Deficiens, a homeotic gene involved in the control of flower morphogenesis in Antirrhinum majus: the protein shows homology to transcription factors. EMBO J 9:605–613PubMedGoogle Scholar
  47. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA 4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599PubMedCrossRefGoogle Scholar
  48. Theißen G, Kim JT, Saedler H (1996) Classification and phylogeny of the MADS-box multigene family suggest defined roles of MADS-box gene subfamilies in the morphological evolution of eukaryotes. J Mol Evol 43:484–516PubMedCrossRefGoogle Scholar
  49. Theissen G, Becker A, Di Rosa A, Kanno A, Kim JT, Munster T, Winter KU, Saedler H (2000) A short history of MADS-box genes in plants. Plant Mol Biol 42:115–149PubMedCrossRefGoogle Scholar
  50. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedCrossRefGoogle Scholar
  51. Xiong YQ, Liu TY, Tian CG, Sun SH, Li JY, Chen MS (2005) Transcription factors in rice: a genome-wide comparative analysis between monocots and eudicots. Plant Mol Biol 59:191–203PubMedCrossRefGoogle Scholar
  52. Yang Y, Fanning L, Jack T (2003) The K domain mediates heterodimerization of the Arabidopsis floral organ identity proteins, APETALA3 and PISTILLATA. Plant J 33:47–59PubMedCrossRefGoogle Scholar
  53. Yang SH, Zhang XH, Yue JX, Tian DC, Chen JQ (2008) Recent duplications dominate NBS-encoding gene expansion in two woody species. Mol Genet Genomics 280:187–198PubMedCrossRefGoogle Scholar
  54. Yanofsky MF, Ma H, Bowman JL, Drews GN, Feldmann KA, Meyerowitz EM (1990) The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 346:35–39PubMedCrossRefGoogle Scholar
  55. Zhang H, Forde BG (1998) An Arabidopsis MADS-box gene that controls nutrient-induced changes in root architecture. Science 279:407–409PubMedCrossRefGoogle Scholar
  56. Zhou T, Wang Y, Chen JQ, Araki H, Jing Z, Jiang K, Shen J, Tian DC (2004) Genome-wide identification of NBS genes in rice reveals significant expansion of divergent non-TIR NBS genes. Mol Genet Genomics 271:402–415PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Yang Zhao
    • 1
  • Xiaoyu Li
    • 1
  • Wenjuan Chen
    • 1
  • Xiaojian Peng
    • 1
  • Xiao Cheng
    • 1
  • Suwen Zhu
    • 1
  • Beijiu Cheng
    • 1
    Email author
  1. 1.Key Laboratory of Crop Biology of Anhui ProvinceAnhui Agricultural UniversityHefeiChina

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