Advertisement

Plant Molecular Biology

, Volume 94, Issue 4–5, pp 361–379 | Cite as

Analysis of global gene expression profiles during the flowering initiation process of Lilium × formolongi

  • Yu-Fan Li
  • Ming-Fang Zhang
  • Meng Zhang
  • Gui-Xia Jia
Article

Abstract

The onset of flowering is critical for the reproductive development of plants. Lilium × formolongi is a lily hybrid that flowers within a year after sowing. We successfully identified four important stages during vegetative growth and flowering initiation of L. × formolongi under long day conditions. The plant tissues from the four stages were used in a genome-wide transcriptional analysis to investigate stage-specific changes of gene expression in L. × formolongi. In total, the sequence reads of the four RNA-sequencing libraries were assembled into 52,824 unigenes, of which 37,031 (70.10%) were differentially expressed. The global expression dynamics of the differentially expressed genes were predominant in flowering induction phase I and the floral differentiation stage, but down-regulated in flowering induction phase II. Various transcription factor families relevant to flowering were elucidated, and the members of the MADS-box, SBP and CO-like transcription factor families were the most represented. There were 85 differentially expressed genes relevant to flowering. CONSTANS-LIKE, FLOWERING LOCUS T, TREHALOSE-6-PHOSPHATE SYNTHASE and SQUAMOSA PROMOTER BINDING PROTEIN-LIKE homologs were discovered and may play significant roles in the flowering induction and transition process of L. × formolongi. A putative gene regulatory network, including photoperiod, age-dependent and trehalose-6-phosphate flowering pathways, was constructed. This is the first expression dataset obtained from a transcriptome analysis of photoperiod-mediated flowering pathway in lily, and it is valuable for the exploration of the molecular mechanisms of flowering initiation and the short vegetative stage of L. × formolongi.

Keywords

Lilium × formolongi Flowering induction Photoperiod Gene expression RNA-seq 

Notes

Acknowledgements

This work has been supported by the National Natural Science Foundation of China (Grant No. 31470106) and the National Forestry Industry Research Special Funds for Public Welfare Projects (Grant No. 201204609).

Author contributions

G-X Jia and M-F Zhang designed the experiments. Y-F Li, M-F Zhang and M Zhang performed the experiments. Y-F Li performed the bioinformatics and the statistical analyses of the transcriptiome and wrote the article. All authors read and approved the final manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11103_2017_612_MOESM1_ESM.docx (133 kb)
Supplementary material 1 (DOCX 133 KB)

References

  1. Anderson NO, Berghauer E, Harris D, Johnson K, Lönnroos J, Morey M (2012) Discovery of novel traits in seed-propagated Lilium: non-vernalizationrequiring, day-neutral, reflowering, frost-tolerant, winter-hardy L. × formolongi. I. Characterization. Floric Ornam Biotechnol 6:63–72Google Scholar
  2. Andrés F, Coupland G (2012) The genetic basis of flowering responses to seasonal cues. Nat Rev Genet 13:627–639CrossRefPubMedGoogle Scholar
  3. asl Hamid B, Kim JH (2011) Cross compatibility between Lilium × fomolongi group and Lilium brownii. Afr J Agric Res 6:968–977Google Scholar
  4. Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 15:2730–2741CrossRefPubMedPubMedCentralGoogle Scholar
  5. Beattie D, White J (1993) Lilium-hybrids and species. In: De Hertogh A, Le Nard M (eds) The physiology of flower bulbs. Elsevier, Amsterdam, pp 423–454Google Scholar
  6. Bergonzi S et al (2013) Mechanisms of age-dependent response to winter temperature in perennial flowering of Arabis alpina. Science 340:1094–1097CrossRefPubMedGoogle Scholar
  7. Böhlenius H, Huang T, Charbonnel-Campaa L, Brunner AM, Jansson S, Strauss SH, Nilsson O (2006) CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312:1040–1043CrossRefPubMedGoogle Scholar
  8. Datta S, Hettiarachchi G, Deng X-W, Holm M (2006) Arabidopsis CONSTANS-LIKE 3 is a positive regulator of red light signaling and root growth. Plant Cell 18:70–84CrossRefPubMedPubMedCentralGoogle Scholar
  9. Du F et al (2015) De novo assembled transcriptome analysis and SSR marker development of a mixture of six tissues from Lilium Oriental hybrid ‘Sorbonne’. Plant Mol Biol Rep 33:281–293CrossRefGoogle Scholar
  10. Ernst J, Bar-Joseph Z (2006) STEM: a tool for the analysis of short time series gene expression data. BMC Bioinformatics 7:1CrossRefGoogle Scholar
  11. Gardner MJ, Hubbard KE, Hotta CT, Dodd AN, Webb AA (2006) How plants tell the time. Biochem J 397:15–24CrossRefPubMedPubMedCentralGoogle Scholar
  12. Grabherr MG et al (2011) Full-length transcriptome assembly from RNA-seq data without a reference genome. Nat Biotechnol 29:644–652CrossRefPubMedPubMedCentralGoogle Scholar
  13. Griffiths D (1934) Bulbs from seed. US Government Printing Office, Washington, D.C.Google Scholar
  14. Griffiths S, Dunford RP, Coupland G, Laurie DA (2003) The evolution of CONSTANS-like gene families in barley, rice, and Arabidopsis. Plant Physiol 131:1855–1867CrossRefPubMedPubMedCentralGoogle Scholar
  15. Hassidim M, Harir Y, Yakir E, Kron I, Green RM (2009) Over-expression of CONSTANS-LIKE 5 can induce flowering in short-day grown Arabidopsis. Planta 230:481–491CrossRefPubMedGoogle Scholar
  16. Horita M, Morohashi H, Komai F (2003) Production of fertile somatic hybrid plants between Oriental hybrid lily and Lilium × formolongi. Planta 217:597–601CrossRefPubMedGoogle Scholar
  17. Huang J, Liu X, Wang J, Lü Y (2014) Transcriptomic analysis of Asiatic lily in the process of vernalization via RNA-seq. Mol Biol Rep 41:3839–3852CrossRefPubMedGoogle Scholar
  18. Jain M (2011) Next-generation sequencing technologies for gene expression profiling in plants. Brief Funct Genomics 11:63–70Google Scholar
  19. Kardailsky I et al (1999) Activation tagging of the floral inducer FT. Science 286:1962–1965CrossRefPubMedGoogle Scholar
  20. Khan MRG, Ai XY, Zhang JZ (2014) Genetic regulation of flowering time in annual and perennial plants. Wiley Interdisc Rev RNA 5:347–359CrossRefGoogle Scholar
  21. Kim S-K, Yun C-H, Lee JH, Jang YH, Park H-Y, Kim J-K (2008) OsCO3, a CONSTANS-LIKE gene, controls flowering by negatively regulating the expression of FT-like genes under SD conditions in rice. Planta 228:355–365CrossRefPubMedGoogle Scholar
  22. Kojima S, Takahashi Y, Kobayashi Y, Monna L, Sasaki T, Araki T, Yano M (2002) Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions. Plant Cell Physiol 43:1096–1105CrossRefPubMedGoogle Scholar
  23. Lazare S, Zaccai M (2016) Flowering pathway is regulated by bulb size in Lilium longiflorum (Easter lily). Plant Biol 1–8. doi: 10.1111/plb.12440
  24. Ledger S, Strayer C, Ashton F, Kay SA, Putterill J (2001) Analysis of the function of two circadian-regulated CONSTANS-LIKE genes. Plant J 26:15–22CrossRefPubMedGoogle Scholar
  25. Liu X, Wang Q, Gu J, Lü Y (2014) Vernalization of Oriental hybrid lily ‘Sorbonne’: changes in physiology metabolic activity and molecular mechanism. Mol Biol Rep 41:6619–6634CrossRefPubMedGoogle Scholar
  26. Meng X, Muszynski MG, Danilevskaya ON (2011) The FT-like ZCN8 gene functions as a floral activator and is involved in photoperiod sensitivity in maize. Plant Cell 23:942–960CrossRefPubMedPubMedCentralGoogle Scholar
  27. Meyerowitz EM, Bowman JL, Brockman LL, Drews GN, Jack T, Sieburth LE, Weigel D (1991) A genetic and molecular model for flower development in Arabidopsis thaliana. Development 113:157–167Google Scholar
  28. Michaels SD, Himelblau E, Kim SY, Schomburg FM, Amasino RM (2005) Integration of flowering signals in winter-annual. Arabidopsis. Plant Physiol 137:149–156CrossRefPubMedPubMedCentralGoogle Scholar
  29. Mizoguchi T et al (2005) Distinct roles of GIGANTEA in promoting flowering and regulating circadian rhythms in Arabidopsis. Plant Cell 17:2255–2270CrossRefPubMedPubMedCentralGoogle Scholar
  30. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-SEq. Nat Methods 5:621–628CrossRefPubMedGoogle Scholar
  31. Mouradov A, Cremer F, Coupland G (2002) Control of flowering time interacting pathways as a basis for diversity. Plant Cell 14:S111–S130PubMedPubMedCentralGoogle Scholar
  32. O’Hara LE, Paul MJ, Wingler A (2013) How do sugars regulate plant growth and development? New insight into the role of trehalose-6-phosphate. Mol Plant 6:261–274CrossRefPubMedGoogle Scholar
  33. Okazaki K (1994) Lilium species native to Japan, and breeding and production of Lilium in Japan. Acta Hortic 414:81–92Google Scholar
  34. Optiz E, Anderson N, Younis A (2009) Development of colored, non-vernalization-requiring seed propagated lilies. In: 23rd International Eucarpia Symposium, Section Ornamentals: Colourful Breeding and Genetics 836:193–198Google Scholar
  35. Ozsolak F, Milos PM (2011) RNA sequencing: advances, challenges and opportunities. Nat Rev Genet 12:87–98CrossRefPubMedGoogle Scholar
  36. Par̆enicová L et al (2003) Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis new openings to the MADS world. Plant Cell 15:1538–1551CrossRefPubMedPubMedCentralGoogle Scholar
  37. Pertea G et al (2003) TIGR Gene Indices clustering tools (TGICL): a software system for fast clustering of large EST datasets. Bioinformatics 19:651–652CrossRefPubMedGoogle Scholar
  38. Proveniers M (2013) Sugars speed up the circle of life. Elife 2:e00625CrossRefPubMedPubMedCentralGoogle Scholar
  39. Putterill J, Robson F, Lee K, Simon R, Coupland G (1995) The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell 80:847–857CrossRefPubMedGoogle Scholar
  40. Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26(1):139–140CrossRefPubMedGoogle Scholar
  41. Robson F, Costa MMR, Hepworth SR, Vizir I, Reeves PH, Putterill J, Coupland G (2001) Functional importance of conserved domains in the flowering-time gene CONSTANS demonstrated by analysis of mutant alleles and transgenic plants. Plant J 28:619–631CrossRefPubMedGoogle Scholar
  42. Sakamoto H (2005) Acceleration of flowering by night break and heating treatment for harvesting in April and May in Lilium × foromolongi cv. Hayachine. Hortic Res 4:191–195CrossRefGoogle Scholar
  43. Samach A, Coupland G (2000) Time measurement and the control of flowering in plants. Bioessays 22:38–47CrossRefPubMedGoogle Scholar
  44. Singh VK, Garg R, Jain M (2013) A global view of transcriptome dynamics during flower development in chickpea by deep sequencing. Plant Biotechnol J 11:691–701CrossRefPubMedGoogle Scholar
  45. Suárez-López P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G (2001) CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410:1116–1120CrossRefPubMedGoogle Scholar
  46. Turck F, Fornara F, Coupland G (2008) Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annu Rev Plant Biol 59:573–594CrossRefPubMedGoogle Scholar
  47. Villacorta-Martin C, de Cáceres González FFN, de Haan J, Huijben K, Passarinho P, Hamo ML-B, Zaccai M (2015) Whole transcriptome profiling of the vernalization process in Lilium longiflorum (cultivar White Heaven) bulbs. BMC Genomics 16:1CrossRefGoogle Scholar
  48. Wahl V et al (2013) Regulation of flowering by trehalose-6-phosphate signaling in Arabidopsis thaliana. Science 339:704–707CrossRefPubMedGoogle Scholar
  49. Wang J-W, Czech B, Weigel D (2009) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138:738–749CrossRefPubMedGoogle Scholar
  50. Wellmer F, Riechmann JL (2010) Gene networks controlling the initiation of flower development. Trends Genet 26:519–527CrossRefPubMedGoogle Scholar
  51. Wellmer F, Alves-Ferreira M, Dubois A, Riechmann JL, Meyerowitz EM (2006) Genome-wide analysis of gene expression during early Arabidopsis flower development. PLoS Genet 2:e117CrossRefPubMedPubMedCentralGoogle Scholar
  52. Yamaguchi A, Kobayashi Y, Goto K, Abe M, Araki T (2005) TWIN SISTER OF FT (TSF) acts as a floral pathway integrator redundantly with FT. Plant Cell Physiol 46:1175–1189CrossRefPubMedGoogle Scholar
  53. Yamaguchi A, Wu M-F, Yang L, Wu G, Poethig RS, Wagner D (2009) The microRNA-regulated SBP-Box transcription factor SPL3 is a direct upstream activator of LEAFY, FRUITFULL, and APETALA1. Dev Cell 17:268–278CrossRefPubMedPubMedCentralGoogle Scholar
  54. Yoo SJ, Chung KS, Jung SH, Yoo SY, Lee JS, Ahn JH (2010) BROTHER OF FT AND TFL1 (BFT) has TFL1-like activity and functions redundantly with TFL1 in inflorescence meristem development in Arabidopsis. Plant J 63:241–253CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  • Yu-Fan Li
    • 1
  • Ming-Fang Zhang
    • 1
  • Meng Zhang
    • 1
  • Gui-Xia Jia
    • 1
  1. 1.Beijing Key Laboratory of Ornamental Plants Germplasm Innovation & Molecular Breeding, National Engineering Research Center for Floriculture, Beijing Laboratory of Urban and Rural Ecological Environment and College of Landscape ArchitectureBeijing Forestry UniversityBeijingChina

Personalised recommendations