Skip to main content
Log in

Comparative transcriptomic analyses of normal and peloric mutant flowers in Cymbidium goeringii Rchb.f identifies differentially expressed genes associated with floral development

  • Original Article
  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Cymbidium geringii has high ornamental and economic importance. Its traits, including flower shape, size, and color, are highly sought by orchid breeders. Gaining insights into the molecular basis of C. geringi flower development would accelerate genetic improvement of other orchids. Methods and Results: Here, C. goeringii RNA was purified from normal and peloric mutant flowers, and cDNA libraries constructed for Illumina sequencing. We generated 329,156,782 clean reads, integrated them, and then assembled into 236,811 unigenes averaging 595 bp long. A total of 11,992 differentially expressed genes s, of which 6119 were upregulated and 5873 downregulated, were uncovered in peloric mutant flower buds relative to normal flower buds. Kyoto Encyclopedia of Genes and Genomes enrichment assessments posited that these differentially expressed genes are associated with “Photosynthesis”, “Linoleic acid metabolism”, as well as “Plant hormone signal transduction” cascades. The DEGs were designated to 12 remarkably enriched GO terms, and 16 cell wall associated GO terms. The expression level of 16 determined genes were verified using RT-qPCR. Conclusions: Our gene expression data may be used to study the regulatory mechanism of flower organ development in C. geringi.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Tsai WC, Chen HH (2006) The orchid MADS-box genes controlling floral morphogenesis. ScientificWorldJournal 6:1933–1944. https://doi.org/10.1100/tsw.2006.321

    Article  PubMed  PubMed Central  Google Scholar 

  2. Xiang L, Chen Y, Chen L, Fu X, Zhao K, Zhang J, Sun C (2018) B and E MADS-box genes determine the perianth formation in Cymbidium goeringii Rchb.f. Physiol Plant 162(3):353–369. https://doi.org/10.1111/ppl.12647

    Article  CAS  PubMed  Google Scholar 

  3. Su SH, Shao XY, Zhu CF, Xu JY, Tang YH, Luo D, Huang X (2018) An AGAMOUS-like factor is associated with the origin of two domesticated varieties in Cymbidium sinense (Orchidaceae). Hortic Res. https://doi.org/10.1038/s41438-018-0052-z

    Article  PubMed  PubMed Central  Google Scholar 

  4. Sun Y, Wang G, Li Y, Jiang L, Yang Y, Guan S (2016) De novo transcriptome sequencing and comparative analysis to discover genes related to floral development in Cymbidium faberi Rolfe. Springerplus 5(1):1458. https://doi.org/10.1186/s40064-016-3089-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Chen Y, Shen Q, Lin R, Zhao Z, Shen C, Sun C (2017) De novo transcriptome analysis in Dendrobium and identification of critical genes associated with flowering. Plant Physiol Biochem 119:319–327. https://doi.org/10.1016/j.plaphy.2017.09.008

    Article  CAS  PubMed  Google Scholar 

  6. Chung MY, Chung MG (2000) Allozyme diversity in populations of Cymbidium goeringii (Orchidaceae). Plant Biol 2(1):77–82. https://doi.org/10.1055/s-2000-9152

    Article  CAS  Google Scholar 

  7. Krasileva KV, Vasquez-Gross HA, Howell T, Bailey P, Paraiso F, Clissold L, Simmonds J, Ramirez-Gonzalez RH, Wang XD, Borrill P, Fosker C, Ayling S, Phillips AL, Uauy C, Dubcovsky J (2017) Uncovering hidden variation in polyploid wheat. Proc Natl Acad Sci USA 114(6):E913–E921. https://doi.org/10.1073/pnas.1619268114

    Article  CAS  PubMed  Google Scholar 

  8. Brambilla V, Gomez-Ariza J, Cerise M, Fornara F (2017) The importance of being on time: regulatory networks controlling photoperiodic flowering in cereals. Front Plant Sci. https://doi.org/10.3389/fpls.2017.00665

    Article  PubMed  PubMed Central  Google Scholar 

  9. Liu KD, Li HL, Li WJ, Zhong JD, Chen Y, Shen CJ, Yuan CC (2017) Comparative transcriptomic analyses of normal and malformed flowers in sugar apple (Annona squamosa L.) to identify the differential expressed genes between normal and malformed flowers. BMC Plant Biol. https://doi.org/10.1186/s12870-017-1135-y

    Article  PubMed  PubMed Central  Google Scholar 

  10. Mendoza L, Thieffry D, Alvarez-Buylla ER (1999) Genetic control of flower morphogenesis in Arabidopsis thaliana: a logical analysis. Bioinformatics 15(7–8):593–606. https://doi.org/10.1093/bioinformatics/15.7.593

    Article  CAS  PubMed  Google Scholar 

  11. Krizek BA, Fletcher JC (2005) Molecular mechanisms of flower development: an armchair guide. Nat Rev Genet 6(9):688–698. https://doi.org/10.1038/nrg1675

    Article  CAS  PubMed  Google Scholar 

  12. Simpson GG, Dean C (2002) Flowering—Arabidopsis, the rosetta stone of flowering time? Science 296(5566):285–289. https://doi.org/10.1126/science.296.5566.285

    Article  CAS  PubMed  Google Scholar 

  13. Moon J, Lee H, Kim M, Lee I (2005) Analysis of flowering pathway integrators in Arabidopsis. Plant Cell Physiol 46(2):292–299. https://doi.org/10.1093/pcp/pci024

    Article  CAS  PubMed  Google Scholar 

  14. Fornara F, de Montaigu A, Coupland G (2010) SnapShot: control of flowering in Arabidopsis. Cell. https://doi.org/10.1016/j.cell.2010.04.024

    Article  PubMed  Google Scholar 

  15. Allnutt GV, Rogers HJ, Francis D, Herbert RJ (2007) A LEAFY-like gene in the long-day plant, Silene coeli-rosa is dramatically up-regulated in evoked shoot apical meristems but does not complement the Arabidopsis lfy mutant. J Exp Bot 58(8):2249–2259. https://doi.org/10.1093/jxb/erm090

    Article  CAS  PubMed  Google Scholar 

  16. Torti S, Fornara F (2012) AGL24 acts in concert with SOC1 and FUL during Arabidopsis floral transition. Plant Signal Behav 7(10):1251–1254. https://doi.org/10.4161/psb.21552

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Klintenas M, Pin PA, Benlloch R, Ingvarsson PK, Nilsson O (2012) Analysis of conifer FLOWERING LOCUS T/TERMINAL FLOWER1-like genes provides evidence for dramatic biochemical evolution in the angiosperm FT lineage. New Phytol 196(4):1260–1273. https://doi.org/10.1111/j.1469-8137.2012.04332.x

    Article  CAS  PubMed  Google Scholar 

  18. Zhang C, Dong W, Gen W, Xu B, Shen C, Yu C (2018) De novo transcriptome assembly and characterization of the synthesis genes of bioactive constituents in Abelmoschus esculentus (L.) Moench. Genes. https://doi.org/10.3390/genes9030130

    Article  PubMed  PubMed Central  Google Scholar 

  19. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng QD, Chen ZH, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29(7):644–652

    Article  CAS  Google Scholar 

  20. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11(10):R106. https://doi.org/10.1186/gb-2010-11-10-r106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Li B, Dewey C (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform. https://doi.org/10.1186/1471-2105-12-323

    Article  Google Scholar 

  22. Young MD, Wakefield MJ, Smyth GK, Oshlack A (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 11(2):R14. https://doi.org/10.1186/gb-2010-11-2-r14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T, Yamanishi Y (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36:D480–D484

    Article  CAS  Google Scholar 

  24. Zhang GQ, Liu KW, Li Z, Lohaus R, Hsiao YY, Niu SC, Wang JY, Lin YC, Xu Q, Chen LJ, Yoshida K, Fujiwara S, Wang ZW, Zhang YQ, Mitsuda N, Wang MN, Liu GH, Pecoraro L, Huang HX, Xiao XJ, Lin M, Wu XY, Wu WL, Chen YY, Chang SB, Sakamoto S, Ohme-Takagi M, Yagi M, Zeng SJ, Shen CY, Yeh CM, Luo YB, Tsai WC, Van de Peer Y, Liu ZJ (2017) The Apostasia genome and the evolution of orchids. Nature. https://doi.org/10.1038/nature23897

    Article  PubMed  PubMed Central  Google Scholar 

  25. Zhang GQ, Xu Q, Bian C, Tsai WC, Yeh CM, Liu KW, Yoshida K, Zhang LS, Chang SB, Chen F, Shi Y, Su YY, Zhang YQ, Chen LJ, Yin Y, Lin M, Huang H, Deng H, Wang ZW, Zhu SL, Zhao X, Deng C, Niu SC, Huang J, Wang M, Liu GH, Yang HJ, Xiao XJ, Hsiao YY, Wu WL, Chen YY, Mitsuda N, Ohme-Takagi M, Luo YB, Van de Peer Y, Liu ZJ (2016) The Dendrobium catenatum Lindl. genome sequence provides insights into polysaccharide synthase, floral development and adaptive evolution. Sci Rep 6(1):19029. https://doi.org/10.1038/srep19029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Zhang C, Xu B, Zhao CR, Sun J, Lai Q, Yu C (2019) Comparative de novo transcriptomics and untargeted metabolomic analyses elucidate complicated mechanisms regulating celery (Apium graveolens L.) responses to selenium stimuli. PLoS ONE 14(12):e0226752. https://doi.org/10.1371/journal.pone.0226752

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Honma T, Goto K (2001) Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409(6819):525–529. https://doi.org/10.1038/35054083

    Article  CAS  PubMed  Google Scholar 

  28. Zahn LM, Leebens-Mack JH, Arrington JM, Hu Y, Landherr LL, dePamphilis CW, Becker A, Theissen G, Ma H (2006) Conservation and divergence in the AGAMOUS subfamily of MADS-box genes: evidence of independent sub- and neofunctionalization events. Evol Dev 8(1):30–45. https://doi.org/10.1111/j.1525-142X.2006.05073.x

    Article  CAS  PubMed  Google Scholar 

  29. Wang SY, Lee PF, Lee YI, Hsiao YY, Chen YY, Pan ZJ, Liu ZJ, Tsai WC (2011) Duplicated C-class MADS-box genes reveal distinct roles in gynostemium development in Cymbidium ensifolium (Orchidaceae). Plant Cell Physiol 52(3):563–577. https://doi.org/10.1093/pcp/pcr015

    Article  CAS  PubMed  Google Scholar 

  30. Doyle MR, Davis SJ, Bastow RM, McWatters HG, Kozma-Bognar L, Nagy F, Millar AJ, Amasino RM (2002) The ELF4 gene controls circadian rhythms and flowering time in Arabidopsis thaliana. Nature 419(6902):74–77. https://doi.org/10.1038/nature00954

    Article  CAS  PubMed  Google Scholar 

  31. Hazen SP, Schultz TF, Pruneda-Paz JL, Borevitz JO, Ecker JR, Kay SA (2005) LUX ARRHYTHMO encodes a Myb domain protein essential for circadian rhythms. Proc Natl Acad Sci USA 102(29):10387–10392. https://doi.org/10.1073/pnas.0503029102

    Article  CAS  PubMed  Google Scholar 

  32. Bastow R, Mylne JS, Lister C, Lippman Z, Martienssen RA, Dean C (2004) Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427(6970):164–167. https://doi.org/10.1038/nature02269

    Article  CAS  PubMed  Google Scholar 

  33. Macknight R, Bancroft I, Page T, Lister C, Schmidt R, Love K, Westphal L, Murphy G, Sherson S, Cobbett C, Dean C (1997) FCA, a gene controlling flowering time in Arabidopsis, encodes a protein containing RNA-binding domains. Cell 89(5):737–745. https://doi.org/10.1016/S0092-8674(00)80256-1

    Article  CAS  PubMed  Google Scholar 

  34. Schomburg FM, Patton DA, Meinke DW, Amasino RM (2001) FPA, a gene involved in floral induction in Arabidopsis, encodes a protein containing RNA-recognition motifs. Plant Cell 13(6):1427–1436. https://doi.org/10.1105/tpc.13.6.1427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Thomas B (2006) Light signals and flowering. J Exp Bot 57(13):3387–3393. https://doi.org/10.1093/jxb/erl071

    Article  CAS  PubMed  Google Scholar 

  36. Tsai WC, Kuoh CS, Chuang MH, Chen WH, Chen HH (2004) Four DEF-like MADS box genes displayed distinct floral morphogenetic roles in Phalaenopsis orchid. Plant Cell Physiol 45(7):831–844. https://doi.org/10.1093/pcp/pch095

    Article  CAS  PubMed  Google Scholar 

  37. Tsai WC (2005) PeMADS6, a GLOBOSA/PISTILLATA-like gene in Phalaenopsis equestris involved in petaloid formation, and correlated with flower longevity and ovary development. Plant Cell Physiol 46(7):1125–1139

    Article  CAS  Google Scholar 

  38. Hsieh MH, Pan ZJ, Lai PH, Lu HC, Yeh HH, Hsu CC, Wu WL, Chung MC, Wang SS, Chen WH, Chen HH (2013) Virus-induced gene silencing unravels multiple transcription factors involved in floral growth and development in Phalaenopsis orchids. J Exp Bot 64(12):3869–3884. https://doi.org/10.1093/jxb/ert218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Kurokura T, Mimida N, Battey NH, Hytonen T (2013) The regulation of seasonal flowering in the Rosaceae. J Exp Bot 64(14):4131–4141. https://doi.org/10.1093/jxb/ert233

    Article  CAS  PubMed  Google Scholar 

  40. Davis SJ (2009) Integrating hormones into the floral-transition pathway of Arabidopsis thaliana. Plant Cell Environ 32(9):1201–1210. https://doi.org/10.1111/j.1365-3040.2009.01968.x

    Article  CAS  PubMed  Google Scholar 

  41. Yamaguchi N, Wu MF, Winter CM, Berns MC, Nole-Wilson S, Yamaguchi A, Coupland G, Krizek BA, Wagner D (2013) A molecular framework for auxin-mediated initiation of flower primordia. Dev Cell 24(3):271–282. https://doi.org/10.1016/j.devcel.2012.12.017

    Article  CAS  PubMed  Google Scholar 

  42. Przemeck GKH, Mattsson J, Hardtke CS, Berleth ST (1996) Studies on the role of the Arabidopsis gene MONOPTEROS in vascular development and plant cell axialization. Planta 200(2):229–237

    Article  CAS  Google Scholar 

  43. Nagpal P, Ellis CM, Weber H, Ploense SE, Barkawi LS, Guilfoyle TJ, Hagen G, Alonso JM, Cohen JD, Farmer EE, Ecker JR, Reed JW (2005) Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation. Development 132(18):4107–4118. https://doi.org/10.1242/dev.01955

    Article  CAS  PubMed  Google Scholar 

  44. Wu YF, Reed GW, Tian CQ (2006) Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 133(21):4211–4218

    Article  CAS  Google Scholar 

  45. Kinoshita-Tsujimura K, Kakimoto T (2011) Cytokinin receptors in sporophytes are essential for male and female functions in Arabidopsis thaliana. Plant Signal Behav 6:66–71

    Article  CAS  Google Scholar 

  46. Lu IL, Sutter E, Burger D (2001) Relationships between benzyladenine uptake, endogenous free IAA levels and peroxidase activities during upright shoot induction of Cymbidium ensifoilum cv. Yuh Hwa rhizomes in vitro. Plant Growth Regul 35(2):161–170

    Article  CAS  Google Scholar 

  47. Sakai WS, Ichihara K (2010) N6-benzyladenine induced flowering of potted nobile-type dendrobium red emperor “prince” orchid plants. Acta Hortic 878:317–320

    Article  CAS  Google Scholar 

  48. Wu PH, Chang DCN (2009) Use of N-6-benzyladenine to regulate flowering of Phalaenopsis orchids. Horttechnology 19(1):200–203

    Article  CAS  Google Scholar 

  49. Lang A (1957) The effect of gibberellin upon flower formation. Proc Natl Acad Sci USA 43(8):709–717. https://doi.org/10.1073/pnas.43.8.709

    Article  CAS  PubMed  Google Scholar 

  50. Matsumoto TK (2005) Gibberellic acid and benzyladenine promote early flowering and vegetative growth of Miltoniopsis orchid hybrids. HortScience 41(1):131–135

    Article  Google Scholar 

Download references

Acknowledgements

This study was supported by the National Natural Science Foundation of China (31801891, 41907213), the Tree Breeding Project of Zhejiang Province, China (2016C02065).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yue Chen.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

11033_2021_6216_MOESM1_ESM.tif

Electronic supplementary material 1 (TIF 9707 kb) Fig. S1 Flowers of both wild-type and peloric mutant flowers of Cymbidium goeringii. (A) Wild-type flower of C. goeringii. The flowers have three sepals and three petals. One petal is morphologically different in structure and is known as the lip. The male and female reproductive parts are fused in a structure, the column, in the center of the flower. (B) Peloric mutant flower of C. goeringii has three sepals, three lip-like petals, an arching column. S (sepal), P (petal), L (Lip).

11033_2021_6216_MOESM2_ESM.tif

Electronic supplementary material 2 (TIF 473 kb) Fig. S2 Expression validation of the key genes that participate in flowering and the hormonal network.

Electronic supplementary material 3 (XLSX 10 kb)

Electronic supplementary material 4 (XLSX 9 kb)

Electronic supplementary material 5 (XLSX 10 kb)

Electronic supplementary material 6 (XLSX 3673 kb)

Electronic supplementary material 7 (XLSX 28 kb)

Electronic supplementary material 8 (XLSX 846 kb)

Electronic supplementary material 9 (FASTA 144730 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shen, Q., Chen, Y., Sun, J. et al. Comparative transcriptomic analyses of normal and peloric mutant flowers in Cymbidium goeringii Rchb.f identifies differentially expressed genes associated with floral development. Mol Biol Rep 48, 2123–2132 (2021). https://doi.org/10.1007/s11033-021-06216-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-021-06216-0

Keywords

Navigation