Identification and characterization of MADS box gene family in pigeonpea for their role during floral transition

Abstract

MADS box genes are class of transcription factors involved in various physiological and developmental processes in plants. To understand their role in floral transition-related pathways, a genome-wide identification was done in Cajanus cajan, identifying 102 members which were classified into two different groups based on their gene structure. The status of all these genes was further analyzed in three wild species i.e. C. scarabaeoides, C. platycarpus and C. cajanifolius which revealed absence of 31–34 MADS box genes in them hinting towards their role in domestication and evolution. We could locate only a single copy of both FLOWERING LOCUS C (FLC) and SHORT VEGETATIVE PHASE (SVP) genes, while three paralogs of SUPPRESSOR OF ACTIVATION OF CONSTANS 1 (SOC1) were found in C. cajan genome. One of those SOC1 paralogs i.e. CcMADS1.5 was found to be missing in all three wild relatives, also forming separate clade in phylogeny. This SOC1 gene was also lacking the characteristic MADS box domain in it. Expression profiling of major MADS box genes involved in flowering was done in different tissues viz shoot apical meristem, vegetative leaf, reproductive meristem, and reproductive bud. Gene-based time tree of FLC and SOC1 gene dictates their divergence from Arabidopsis before 71 and 23 million year ago (mya), respectively. This study provides valuable insights into the functional characteristics, expression pattern, and evolution of MADS box proteins in grain legumes with emphasis on C. cajan, which may help in further characterizing these genes.

This is a preview of subscription content, access via your institution.

We’re sorry, something doesn't seem to be working properly.

Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

References

  1. 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 Genom 8(1):242

    Google Scholar 

  2. 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(3):464–489

    CAS  PubMed  Google Scholar 

  3. Benovoy D, Drouin G (2006) Processed pseudogenes, processed genes, and spontaneous mutations in the Arabidopsis genome. J Mol Evol 62(5):511–522

    CAS  PubMed  Google Scholar 

  4. Bernier G, Périlleux C (2005) A physiological overview of the genetics of flowering time control. Plant Biotechnol J 3(1):3–16

    CAS  PubMed  Google Scholar 

  5. Castelán-Muñoz N, Herrera J, Cajero-Sánchez W, Arrizubieta M, Trejo C, García-Ponce B, MdlP Sánchez, Álvarez-Buylla ER, Garay-Arroyo A (2019) MADS-Box Genes Are Key Components of Genetic Regulatory Networks Involved in Abiotic Stress and Plastic Developmental Responses in Plants. Front Plant Sci 10:853. https://doi.org/10.3389/fpls.2019.00853

    Article  PubMed  PubMed Central  Google Scholar 

  6. Cho LH, Yoon J, An G (2017) The control of flowering time by environmental factors. Plant J 90(4):708–719

    CAS  PubMed  Google Scholar 

  7. Choudhury SR, Roy S, Nag A, Singh SK, Sengupta DN (2012) Characterization of an AGAMOUS-like MADS box protein, a probable constituent of flowering and fruit ripening regulatory system in banana. PLoS One 7(9):e44361

    Google Scholar 

  8. Conesa A, Götz S (2008) Blast2GO: a comprehensive suite for functional analysis in plant genomics. Int J Plant Genom 2008:1–12. https://doi.org/10.1155/2008/619832

    CAS  Article  Google Scholar 

  9. Deng W, Ying H, Helliwell CA, Taylor JM, Peacock WJ, Dennis ES (2011) FLOWERING LOCUS C (FLC) regulates development pathways throughout the life cycle of Arabidopsis. Proc Natl Acad Sci 108(16):6680–6685

    CAS  PubMed  Google Scholar 

  10. Dong Q, Wang F, Kong J, Xu Q, Li T, Chen L, Chen H, Jiang H, Li C, Cheng B (2019) Functional analysis of ZmMADS1 a reveals its role in regulating starch biosynthesis in maize endosperm. Sci Rep 9(1):1–11

    Google Scholar 

  11. Dorca-Fornell C, Gregis V, Grandi V, Coupland G, Colombo L, Kater MM (2011) The Arabidopsis SOC1-like genes AGL42, AGL71 and AGL72 promote flowering in the shoot apical and axillary meristems. Plant J 67(6):1006–1017

    CAS  PubMed  Google Scholar 

  12. Ferrándiz C, Gu Q, Martienssen R, Yanofsky MF (2000) Redundant regulation of meristem identity and plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER. Development 127(4):725–734

    PubMed  Google Scholar 

  13. Gan Y, Filleur S, Rahman A, Gotensparre S, Forde BG (2005) Nutritional regulation of ANR1 and other root-expressed MADS-box genes in Arabidopsis thaliana. Planta 222(4):730

    CAS  PubMed  Google Scholar 

  14. 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(6):801–814

    CAS  PubMed  Google Scholar 

  15. Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31(8):1296–1297

    Google Scholar 

  16. Jiang D, Gu X, He Y (2009) Establishment of the winter annual growth habit via FRIGIDA-mediated histone methylation at FLOWERING LOCUS C in Arabidopsis. Plant Cell 21(6):1733–1746

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Johanson U, West J, Lister C, Michaels S, Amasino R, Dean C (2000) Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290(5490):344–347

    CAS  PubMed  Google Scholar 

  18. Kim S, Choi K, Park C, Hwang HJ, Lee I (2006) SUPPRESSOR OF FRIGIDA4, encoding a C2H2-Type zinc finger protein, represses flowering by transcriptional activation of Arabidopsis FLOWERING LOCUS C. Plant Cell 18(11):2985–2998

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Köhler C, Hennig L, Spillane C, Pien S, Gruissem W, Grossniklaus U (2003) The Polycomb-group protein MEDEA regulates seed development by controlling expression of the MADS-box gene PHERES1. Genes Dev 17(12):1540–1553

    PubMed  PubMed Central  Google Scholar 

  20. Kumar G, Arya P, Gupta K, Randhawa V, Acharya V, Singh AK (2016) Comparative phylogenetic analysis and transcriptional profiling of MADS-box gene family identified DAM and FLC-like genes in apple (Malus x domestica). Sci Rep 6(1):1–13

    Google Scholar 

  21. Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Lee J, Lee I (2010) Regulation and function of SOC1, a flowering pathway integrator. J Exp Bot 61(9):2247–2254. https://doi.org/10.1093/jxb/erq098

    CAS  Article  PubMed  Google Scholar 

  23. Lee JH, Yoo SJ, Park SH, Hwang I, Lee JS, Ahn JH (2007) Role of SVP in the control of flowering time by ambient temperature in Arabidopsis. Genes Dev 21(4):397–402

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Lee TH, Tang H, Wang X, Paterson AH (2012) PGDD: a database of gene and genome duplication in plants. Nucleic Acids Res 41(D1):D1152–D1158

    PubMed  PubMed Central  Google Scholar 

  25. Li C, Wang Y, Xu L, Nie S, Chen Y, Liang D, Sun X, Karanja BK, Luo X, Liu L (2016) Genome wide characterization of the MADS Box gene family in radish (Raphanus sativus L.) and assessment of its roles in flowering and floral Organogenesis. Front Plant Sci 7:1390. https://doi.org/10.3389/fpls.2016.01390

    Article  PubMed  PubMed Central  Google Scholar 

  26. Li C, Gu H, Jiang W, Zou C, Wei D, Wang Z, Tang Q (2019) Protein interactions of SOC1 with SVP are regulated by a few crucial amino acids in flowering pathways of Brassica juncea. Acta Physiol Plant 41(4):43

    Google Scholar 

  27. Liu D, Wang D, Qin Z, Zhang D, Yin L, Wu L, Colasanti J, Li A, Mao L (2014) The SEPALLATA MADS-box protein SLMBP 21 forms protein complexes with JOINTLESS and MACROCALYX as a transcription activator for development of the tomato flower abscission zone. Plant J 77(2):284–296

    CAS  PubMed  Google Scholar 

  28. Liu X, Sun Z, Dong W, Wang Z, Zhang L (2018) Expansion and functional divergence of the SHORT VEGETATIVE PHASE (SVP) genes in eudicots. Genome Biol Evol 10(11):3026–3037

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Mandel MA, Yanofsky MF (1998) The ArabidopsisAGL9 MADS box gene is expressed in young flower primordia. Sex Plant Reprod 11(1):22–28

    CAS  Google Scholar 

  30. Marchler-Bauer A, Bo Y, Han L, He J, Lanczycki CJ, Lu S, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, Gwadz M (2017) CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res 45(D1):D200–D203

    CAS  Google Scholar 

  31. Messenguy F, Dubois E (2003) Role of MADS box proteins and their cofactors in combinatorial control of gene expression and cell development. Gene 316:1–21

    CAS  PubMed  Google Scholar 

  32. Mouradov A, Cremer F, Coupland G (2002) Control of flowering time: interacting pathways as a basis for diversity. Plant Cell 14(suppl 1):S111–S130

    CAS  PubMed  PubMed Central  Google Scholar 

  33. 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 type II MADS-box genes in angiosperms. Proc Natl Acad Sci 101(7):1910–1915

    CAS  PubMed  Google Scholar 

  34. Ortuño-Miquel S, Rodríguez-Cazorla E, Zavala-Gonzalez EA, Martínez-Laborda A, Vera A (2019) Arabidopsis HUA ENHANCER 4 delays flowering by upregulating the MADS-box repressor genes FLC and MAF4. Sci Rep 9(1):1–12

    Google Scholar 

  35. Parenicová L, De Folter S, Kieffer M, Horner DS, Favalli C, Busscher J, Angenent GC (2003) Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world. Plant Cell 15(7):1538–1551

    PubMed  PubMed Central  Google Scholar 

  36. Pazhamala LT, Purohit S, Saxena RK, Garg V, Krishnamurthy L, Verdier J, Varshney RK (2017) Gene expression atlas of pigeonpea and its application to gain insights into genes associated with pollen fertility implicated in seed formation. J Exp Bot 68(8):2037–2054

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Pelaz S, Ditta GS, Baumann E, Wisman E, Yanofsky MF (2000) B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405(6783):200–203

    CAS  PubMed  Google Scholar 

  38. Qiao X, Li Q, Yin H, Qi K, Li L, Wang R, Zhang S, Paterson AH (2019) Gene duplication and evolution in recurring polyploidization–diploidization cycles in plants. Genome Biol 20(1):38

    PubMed  PubMed Central  Google Scholar 

  39. Varshney RK, Chen W, Li Y, Bharti AK, Saxena RK, Schlueter JA, Donoghue MTA, Azam S, Fan G, Whaley AM, Farmer AD, Sheridan J, Iwata A, Tuteja R, Penmetsa RV, Wu W, Upadhyaya HD, Yang S-P, Shah T, Saxena KB, Michael T, McCombie WR, Yang B, Zhang G, Yang H, Wang J, Spillane C, Cook DR, May GD, Xu X, Jackson SA (2012) Draft genome sequence of pigeonpea (Cajanus cajan), an orphan legume crop of resource-poor farmers. Nat Biotechnol 30(1):83–89

    CAS  Google Scholar 

  40. Sandhya S, Rani SS, Pankaj B, Govind MK, Offmann B, Srinivasan N, Sowdhamini R (2009) Length variations amongst protein domain superfamilies and consequences on structure and function. PLoS ONE 4(3):e4981

    PubMed  PubMed Central  Google Scholar 

  41. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C T method. Nat Protoc 3(6):1101

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Schwarz-Sommer Z, Huijser P, Nacken W, Saedler H, Sommer H (1990) Genetic control of flower development by homeotic genes in Antirrhinum majus. Science 250(4983):931–936

    CAS  PubMed  Google Scholar 

  43. Seymour GB, Ryder CD, Cevik V, Hammond JP, Popovich A, King GJ, Vrebalov J, Giovannoni JJ, Manning K (2011) A SEPALLATA gene is involved in the development and ripening of strawberry (Fragaria× ananassa Duch.) fruit, a non-climacteric tissue. J Exp Bot 62(3):1179–1188

    CAS  PubMed  Google Scholar 

  44. Singh NK, Gupta DK, Jayaswal PK et al (2012) The first draft of the pigeonpea genome sequence. J Plant Biochem Biotechnol 21:98–112. https://doi.org/10.1007/s13562-011-0088-8

    Article  PubMed  Google Scholar 

  45. Smýkal P, Coyne CJ, Ambrose MJ, Maxted N, Schaefer H, Blair MW, Berger J, Greene SL, Nelson MN, Besharat N, Vymyslický T (2015) Legume crops phylogeny and genetic diversity for science and breeding. Crit Rev Plant Sci 34(1–3):43–104

    Google Scholar 

  46. Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, Simonovic M, Roth A, Santos A, Tsafou KP, Kuhn M (2015) STRING v10: protein–protein interaction networks, integrated over the tree of life. Nucleic Acids Res 43(D1):D447–D452

    CAS  PubMed  Google Scholar 

  47. Tamura K, Battistuzzi FU, Billing-Ross P, Murillo O, Filipski A, Kumar S (2012) Estimating divergence times in large molecular phylogenies. Proc Natl Acad Sci 109(47):19333–19338

    CAS  PubMed  Google 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(5):484–516

    PubMed  Google Scholar 

  49. Theißen G, Melzer R, Rümpler F (2016) MADS-domain transcription factors and the floral quartet model of flower development: linking plant development and evolution. Development 143(18):3259–3271

    PubMed  Google Scholar 

  50. Theissen G, Becker A, Di Rosa A, Kanno A, Kim JT, Münster T, Winter KU, Saedler H (2000) A short history of MADS-box genes in plants. Plant Mol Biol 42(1):115–149

    CAS  PubMed  Google Scholar 

  51. Tine M, Kuhl H, Beck A, Bargelloni L, Reinhardt R (2011) Comparative analysis of intronless genes in teleost fish genomes: insights into their evolution and molecular function. Marine Genom 4(2):109–119

    Google Scholar 

  52. Tröbner W, Ramirez L, Motte P, Hue I, Huijser P, Lönnig WE, Saedler H, Sommer Z, Schwarz-Sommer Z (1992) GLOBOSA: a homeotic gene which interacts with DEFICIENS in the control of Antirrhinum floral organogenesis. EMBO J 11(13):4693–4704

    PubMed  PubMed Central  Google Scholar 

  53. Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93(1):77–78

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Wu Y, Ke Y, Wen J, Guo P, Ran F, Wang M, Liu M, Li P, Li J, Du H (2018) Evolution and expression analyses of the MADS-box gene family in Brassica napus. PLoS ONE 13(7):e0200762

    PubMed  PubMed Central  Google Scholar 

  55. Xie Q, Hu Z, Zhu Z, Dong T, Zhao Z, Cui B, Chen G (2014) Overexpression of a novel MADS-box gene SlFYFL delays senescence, fruit ripening and abscission in tomato. Sci Rep 4(1):1–10

    Google Scholar 

  56. 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(6279):35–39

    CAS  PubMed  Google Scholar 

  57. Yu C, Su S, Xu Y, Zhao Y, Yan A, Huang L, Ali I, Gan Y (2014) The effects of fluctuations in the nutrient supply on the expression of five members of the AGL17 clade of MADS-box genes in rice. PLoS ONE 9(8):e105597

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We acknowledge the support provided by Director, ICAR-NIPB and ICAR-IARI (NAHEP-CAAST) for this work.

Funding

No funding was received for the current research.

Author information

Affiliations

Authors

Contributions

KG and KK conceived and designed the study. KK analysed, performed all the bioinformatics and expression analysis. HS, AD and KT contributed in all bioinformatics work. KD and RJ provided the samples for expression analysis. AD, KT, KD, RJ, and PK contributed in qRT-PCR and data analysis. KK, AD, HS, KT, KD, RJ, AM, NK and KG compiled and interpreted the data and wrote the manuscript. All authors have read and approved the final manuscript.

Corresponding author

Correspondence to Kishor Gaikwad.

Ethics declarations

Conflict of interest

Authors hereby declare that no conflict of interest exists.

Ethical approval

This article does not contain any studies with animals performed by any of the authors.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file 1 (DOCX 1821 KB)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kumar, K., Srivastava, H., Das, A. et al. Identification and characterization of MADS box gene family in pigeonpea for their role during floral transition. 3 Biotech 11, 108 (2021). https://doi.org/10.1007/s13205-020-02605-7

Download citation

Keywords

  • MADS box
  • Flower induction
  • FLC
  • SOC1
  • SVP