Advertisement

Journal of Plant Biochemistry and Biotechnology

, Volume 27, Issue 4, pp 435–442 | Cite as

Isolation and expression analysis of eight MADS-box genes in peach (Prunus persica var. nectarina ‘Luxing’)

  • Hui-feng Li
  • Qing-long Dong
  • Hou-zhen Jia
  • Gui-xiang Li
  • Kun Ran
Original Article
  • 122 Downloads

Abstract

The MADS-box transcription factor (TF) plays a crucial regulatory role in plant vegetative growth, flower and fruit development. Eight MADS-box genes (designated as PpMADS15, 16, 17, 26, 27, 36, 37, 38; GenBank accession nos. KU559581, KU559582, KU559583, KU559592, KU559593, KU559602, KU559603, KU559604, respectively) were isolated from ‘Luxing’ (Prunus persica var. nectarina ‘Luxing’) peach by homologous comparison and RT-PCR, which contained open reading frames (ORF) of 597, 750, 1062, 615, 699, 1 107, 678 and 564 bp, respectively. The results of phylogenetic analysis revealed that PpMADS15 belonged to the AG subgroup, PpMADS16 to the SEP subgroup, PpMADS17 to the MIKC* group, PpMADS26, 27, and 38 to the Mα group, and PpMADS36 and 37 to the Mγ group. The results of the prediction for subcellular localization showed that eight PpMADS proteins were located in the nucleus. The results of promoter analysis indicated that there were multiple putative cis-acting elements that were involved in responsiveness to the following variables: light, defense and stress, low-temperature, heat stress, wound, fungal elicitor, anaerobic induction, MeJA, gibberellin, ABA, auxin, and SA. RT-PCR results showed that PpMADS15 was expressed in leaves, stems, roots, sepals, ovaries, stamens, petals, during flower and fruit development. PpMADS16 was expressed in stems, sepals, ovaries, stamens, petals, during flower and fruit development. PpMADS17 was expressed in stems, sepals, ovaries, stamens, petals, during flower and fruit development (except for 30 d). All members in the Mα and Mγ subgroups were expressed in roots, stems, leaves, sepals, ovaries, stamens, petals and during flower development, but PpMADS27 was expressed only during fruit development. These results suggested that eight PpMADS genes played a crucial regulatory role in vegetative growth, flower and fruit development of peaches.

Keywords

‘Luxing’ peach MADS-box Transcription factor Gene cloning Expression analysis Bioinformatics 

Abbreviations

cDNA

Complementary DNA

ORF

Opening reading frame

qRT-PCR

Quantitative real-time PCR

TF

Transcription factor

Notes

Acknowledgements

This study was supported by National Natural Science Foundation of China (Grant No. 31501742), Shandong Agricultural Good Cultivar Project (Grant No. 2016LZGC034), and Key Research and Development Plan (Major Key Technologies) of Shandong Province (Grant No. 2016ZDJS10A01). I would like to thank Professor Thomas Alan Gavin, Cornell University, and Xu Yi, for help with editing the English in this paper.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

13562_2018_452_MOESM1_ESM.tif (23.9 mb)
Supplementary material 1 (TIFF 24462 kb)
13562_2018_452_MOESM2_ESM.tif (393 kb)
Supplementary material 2 (TIFF 393 kb)
13562_2018_452_MOESM3_ESM.tif (5.2 mb)
Supplementary material 3 (TIFF 5373 kb)
13562_2018_452_MOESM4_ESM.tif (5.5 mb)
Supplementary material 4 (TIFF 5653 kb)
13562_2018_452_MOESM5_ESM.tif (5.7 mb)
Supplementary material 5 (TIFF 5857 kb)
13562_2018_452_MOESM6_ESM.pptx (273 kb)
Supplementary material 6 (PPTX 272 kb)
13562_2018_452_MOESM7_ESM.pptx (129 kb)
Supplementary material 7 (PPTX 128 kb)
13562_2018_452_MOESM8_ESM.docx (16 kb)
Supplementary material 8 (DOCX 16 kb)
13562_2018_452_MOESM9_ESM.docx (16 kb)
Supplementary material 9 (DOCX 15 kb)
13562_2018_452_MOESM10_ESM.docx (17 kb)
Supplementary material 10 (DOCX 17 kb)
13562_2018_452_MOESM11_ESM.docx (17 kb)
Supplementary material 11 (DOCX 16 kb)
13562_2018_452_MOESM12_ESM.docx (16 kb)
Supplementary material 12 (DOCX 16 kb)

References

  1. Adamczyk BJ, Fernandez DE (2009) MIKC* MADS domain heterodimers are required for pollen maturation and tube growth in Arabidopsis. Plant Physiol 149(4):1713–1723CrossRefGoogle Scholar
  2. Ampomah-Dwamena C, Morris BA, Sutherland P, Veit B, Yao JL (2002) Down-regulation of TM29, a tomato SEPALLATA homolog, causes parthenocarpic fruit development and floral reversion. Plant Physiol 130(2):605–617CrossRefGoogle 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 Genom 8(1):242CrossRefGoogle Scholar
  4. Busi MV, Bustamante C, D’Angelo C, Hidalgo-Cuevas M, Boggio SB, Valle EM, Zabaleta E (2003) MADS-box genes expressed during tomato seed and fruit development. Plant Mol Biol 52(4):801–815CrossRefGoogle Scholar
  5. 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(1):354–369CrossRefGoogle Scholar
  6. Dong QL, Yu XM, Liu DD, Wang HR, An M, Yao YX, Wang CJ (2013) Cloning of NAD-malic enzymes and their expression analysis during tissues and fruit development of apple. Acta Hortic Sin 40(4):739–748Google Scholar
  7. Duan W, Song X, Liu T, Huang Z, Ren J, Hou X, Li Y (2015) Genome-wide analysis of the MADS-box gene family in Brassica rapa (Chinese cabbage). Mol Genet Genomics 290(1):239–255CrossRefGoogle Scholar
  8. Ferrandiz C, Liljegren SJ, Yanofsky MF (2000) Negative regulation of the SHATTERPROOF genes by FRUITFULL during Arabidopsis fruit development. Science 289(5478):436–438CrossRefGoogle Scholar
  9. Fujisawa M, Shima Y, Nakagawa H, Kitagawa M, Kimbara J, Nakano T, Kasumi T, Ito Y (2014) Transcriptional regulation of fruit ripening by tomato FRUITFULL homologs and associated MADS-box proteins. Plant Cell 26(1):89–101CrossRefGoogle Scholar
  10. Giménez E, Pineda B, Capel J, Antón MT, Atarés A, Pérez-Martín F, García-Sogo B, Angosto T, Moreno V, Lozano R (2010) Functional analysis of the Arlequin mutant corroborates the essential role of the Arlequin/TAGL1 gene during reproductive development of tomato. PLoS ONE 5(12):e14427CrossRefGoogle Scholar
  11. Grimplet J, Martínez-Zapater JM, Carmona MJ (2016) Structural and functional annotation of the MADS-box transcription factor family in grapevine. BMC Genom 17:80CrossRefGoogle Scholar
  12. Gu YB, Ji ZR, Chi FM, Qiao Z, Xu CN, Zhang JX, Zhou ZS, Dong QL (2016) Genome-wide identification and expression analysis of the WRKY gene family in peach. Hereditas (Beijing) 38(3):254–270Google Scholar
  13. Henschel K, Kofuji R, Hasebe M, Saedler H, Munster 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):801–814CrossRefGoogle Scholar
  14. Hileman LC, Sundstrom JF, Litt A, Chen M, Shumba T, Irish VF (2006) Molecular and phylogenetic analyses of the MADS-box gene family in tomato. Mol Biol Evol 23(11):2245–2258CrossRefGoogle Scholar
  15. Hu L, Liu S (2012) Genome-wide analysis of the MADS-box gene family in cucumber. Genome 55(3):245–256CrossRefGoogle Scholar
  16. Ireland HS, Yao JL, Tomes S, Sutherland PW, Nieuwenhuizen N, Gunaseelan K, Winz RA, David KM, Schaffer RJ (2013) Apple SEPALLATA1/2-like genes control fruit flesh development and ripening. Plant J 73(6):1044–1056CrossRefGoogle Scholar
  17. Ito Y, Kitagawa M, Ihashi N, Yabe K, Kimbara J, Yasuda J, Ito H, Inakuma T, Hiroi S, Kasumi T (2008) DNA-binding specificity, transcriptional activation potential, and the rin mutation effect for the tomato fruit-ripening regulator RIN. Plant J 55(2):212–223CrossRefGoogle Scholar
  18. Kang IH, Steffen JG, Portereiko MF, Lloyd A, Drews GN (2008) The AGL62 MADS domain protein regulates cellularization during endosperm development in Arabidopsis. Plant Cell 20(3):635–647CrossRefGoogle Scholar
  19. Kaufmann K, Melzer R, Theissen G (2005) MIKC-type MADS-domain proteins: structural modularity, protein interactions and network evolution in land plants. Gene 347(2):183–198CrossRefGoogle Scholar
  20. Kaufmann K, Muiño JM, Jauregui R, Airoldi CA, Smaczniak C, Krajewski P, Angenent GC (2009) Target genes of the MADS transcription factor SEPALLATA3: integration of developmental and hormonal pathways in the Arabidopsis flower. PLoS Biol 7(4):854–875CrossRefGoogle Scholar
  21. Liu JH, Xu BY, Zhang J, Jin ZQ (2010) The interaction of MADS-box transcription factors and manipulating fruit development and ripening. Hereditas (Beijing) 32(9):893–902Google Scholar
  22. Liu Y, Cui S, Wu F, Yan S, Lin X, Du X, Chong K, Schiling S, Theißen G, Meng Z (2013) Functional conservation of MIKC*-Type MADS-box genes in Arabidopsis and rice pollen maturation. Plant Cell 25(4):1288–1303CrossRefGoogle Scholar
  23. Ma H, dePamphilis C (2000) The ABCs of floral evolution. Cell 101(1):5–8CrossRefGoogle Scholar
  24. Ma J, Sun W, Wan J, Mu S, Li M (2014) Cloning and expression analysis of a late embryogenesis abundant protein gene CpLEA from Chimonanthus praecox. Acta Hortic Sin 41(8):1663–1672Google Scholar
  25. Mara CD, Irish VF (2008) Two GATA transcription factors are downstream effectors of floral homeotic gene action in Arabidopsis. Plant Physiol 147(2):707–718CrossRefGoogle Scholar
  26. Messenguy F, Dubois E (2003) Role of MADS-box proteins and their cofactors in combinatorial control of gene expression and cell development. Gene 316:1–21CrossRefGoogle Scholar
  27. Paenicová L, de-Folter S, Kieffer M, Horner DS, Favalli C, Busscher J, Cook HE, Ingram RM, Kater MM, Davies B, Angenent GC, Colombo L (2013) Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world. Plant Cell 15(7):1538–1551CrossRefGoogle Scholar
  28. Pnueli L, Hareven D, Rounsley SD, Yanofsky MF, Lifschitz E (1994) Isolation of the tomato AGAMOUS gene TAG1 and analysis of its homeotic role in transgenic plants. Plant Cell 6(2):163–173CrossRefGoogle Scholar
  29. Portereiko MF, Lloyd A, Steffen JG, Punwani JA, Otsuga D, Drews GN (2006) AGL80 is required for central cell and endosperm development in Arabidopsis. Plant Cell 18(8):1862–1872CrossRefGoogle Scholar
  30. Puig J, Meynard D, Khong GN, Pauluzzi G, Guiderdoni E, Gantet P (2013) Analysis of the expression of the AGL17-like clade of MADS-box transcription factors in rice. Gene Expr Patterns 13(5):160–170CrossRefGoogle Scholar
  31. Riechmann JL, Meyerowitz EM (1997) MADS domain proteins in plant development. Biol Chem 378(10):1079–1101PubMedGoogle Scholar
  32. 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):1179–1188CrossRefGoogle Scholar
  33. Shu Y, Yu D, Wang D, Guo D, Guo C (2013) Genome-wide survey and expression analysis of the MADS-box gene family in soybean. Mol Biol Rep 40(6):3901–3911CrossRefGoogle Scholar
  34. Sui S, Luo J, Ma J, Zhu Q, Lei X, Li M (2012) Generation and analysis of expressed sequence tags from Chimonanthus praecox (Wintersweet) flowers for discovering stress-responsive and floral development-related genes. Comp Funct Genom.  https://doi.org/10.1155/2012/134596 CrossRefGoogle Scholar
  35. Tian Y, Dong QL, Ji ZR, Chi FM, Cong PH, Zhou ZS (2015) Genome-wide identification and analysis of the MADS-box gene family in apple. Gene 555(2):277–290CrossRefGoogle Scholar
  36. Verde I, Abbott AG, Scalabrin S, Jung S, Shu S, Marroni F, Zhebentyayeva T, Dettori MT, Grimwood J, Cattonaro F, Zuccolo A, Rossini L, Jenkins J, Vendramin E, Meisel LA, Decroocq V, Sosinski B, Prochnik S, Mitros T, Policriti A, Cipriani G, Dondini L, Ficklin S, Goodstein DM, Xuan P, del Fabbro C, Aramini V, Copetti D, Gonzalez S, Horner DS, Falchi R, Lucas S, Mica E, Maldonado J, Lazzari B, Bielenberg D, Pirona R, Miculan M, Barakat A, Testolin R, Stella A, Tartarini S, Tonutti P, Arús P, Orellana A, Wells C, Main D, Vizzotto G, Silva HS, Alamini F, Schmutz J, Morgante M, Rokhsar MD (2013) The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nat Genet 45(5):487–493CrossRefGoogle Scholar
  37. Vrebalov J, Ruezinsky D, Padmanabhan V, White R, Medrano D, Drake R, Schuch W, Giovannoni JA (2002) MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (rin) locus. Science 296(5566):343–346CrossRefGoogle Scholar
  38. Wang CZ, Yu XM, Dong QL, Zhang AN, Liu W, Dong F, Wang SZ, Wang CJ (2015) Bioinformatic and expression analysis on the known MADS-box transcription factors at different development stages of flower in peach. J Nucl Agric Sci 29(5):849–858Google Scholar
  39. Wei B, Zhang R, Guo J, Liu D, Li A, Fan R, Mao L, Zhang X (2014) Genome-wide analysis of the MADS-box gene family in Brachypodium distachyon. PLoS ONE 9(1):e84781CrossRefGoogle Scholar
  40. Weigel D, Meyerowitz EM (1994) The ABCs of floral homeotic genes. Cell 78(2):203–209CrossRefGoogle Scholar
  41. Wells CE, Vendramin E, Tarodo SJ, Verde I, Bielenberg DG (2015) A genome-wide analysis of MADS-box genes in peach [Prunus persica (L.) Batsch]. BMC Plant Biol 15(1):41CrossRefGoogle Scholar
  42. Xu Z, Zhang Q, Sun L, Du D, Cheng T, Pan H, Yang W, Wang J (2014) Genome-wide identification, characterisation and expression analysis of the MADS-box gene family in Prunus mume. Mol Genet Genomics 289(5):903–920CrossRefGoogle Scholar

Copyright information

© Society for Plant Biochemistry and Biotechnology 2018

Authors and Affiliations

  • Hui-feng Li
    • 1
  • Qing-long Dong
    • 2
  • Hou-zhen Jia
    • 1
  • Gui-xiang Li
    • 1
  • Kun Ran
    • 1
  1. 1.Shandong Institute of PomologyTai’anChina
  2. 2.State Key Laboratory of Crop Stress Biology for Arid Areas, College of HorticultureNorthwest A and F UniversityYanglingChina

Personalised recommendations