Skip to main content
SpringerLink
Log in

Developmental transcriptome analysis of floral transition in Rosa odorata var. gigantea

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Key message

Expression analyses revealed that floral transition of Rosa odorata var. gigantea is mainly regulated by VRN1, COLs, DELLA and KSN, with contributions by the effects of phytohormone and starch metabolism.

Abstract

Seasonal plants utilize changing environmental and developmental cues to control the transition from vegetative growth to flowering at the correct time of year. This study investigated global gene expression profiles at different developmental stages of Rosa odorata var. gigantea by RNA-sequencing, combined with phenotypic characterization and physiological changes. Gene ontology enrichment analysis of the differentially expressed genes (DEGs) between four different developmental stages (vegetative meristem, pre-floral meristem, floral meristem and secondary axillary buds) indicated that DNA methylation and the light reaction played a large role in inducing the rose floral transition. The expression of SUF and FLC, which are known to play a role in delaying flowering until vernalization, was down-regulated from the vegetative to the pre-floral meristem stage. In contrast, the expression of VRN1, which promotes flowering by repressing FLC expression, increased. The expression of DELLA proteins, which function as central nodes in hormone signaling pathways, and probably involve interactions between GA, auxin, and ABA to promote the floral transition, was well correlated with the expression of floral integrators, such as AGL24, COL4. We also identified DEGs associated with starch metabolism correlated with SOC1, AGL15, SPL3, AGL24, respectively. Taken together, our results suggest that vernalization and photoperiod are prominent cues to induce the rose floral transition, and that DELLA proteins also act as key regulators. The results summarized in the study on the floral transition of the seasonal rose lay a foundation for further functional demonstration, and have profound economic and ornamental values.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

Abbreviations

VM:

Vegetative meristem

TM:

Pre-floral meristem

FM:

Floral meristem

VM-DHY:

Secondary vegetative meristem

SAM:

Shoot apical meristem

DEGs:

Differentially expressed genes

GA:

Gibberellin

ABA:

Abscisic acid

SCL13:

Scarecrow-like 13

YUC1:

Flavin-containing monooxygenase 1

AUX/IAA:

Auxin-induced protein

NCED:

9-cis-epoxycarotenoid dioxygenase

KING1/SnRK:

SNF1-related protein kinase regulatory subunit gamma-1-like

FKF1:

Flavin-binding, kelch repeat, f-box 1

CO:

Constans

COL:

Constans-like

SUS:

Sucrose synthase

SS:

Starch synthase

GBSS1:

Granule-bound starch synthase 1

AMY:

Alpha-amylase

BAM:

Beta-amylase

AP1:

Apetala11

LFY:

Leafy

VRN1:

Vernalization 1

PEP1:

Perpetual flowering 1

AGL:

Agamous-like

SOC1:

Suppressor of overexpression of co 1

SPL:

Squamosa promoter binding protein-like

FLC:

Flowering locus c

CAL:

Cauliflower

References

  • Achard P et al (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science 311:91–94

    Article  CAS  PubMed  Google Scholar 

  • Andrés F, Coupland G (2012) The genetic basis of flowering responses to seasonal cues. Nat Rev Genet 13:627–639

    Article  PubMed  Google Scholar 

  • Bai F, Demason DA (2008) Hormone interactions and regulation of PsPK2: GUS compared with DR5: GUS and PID: GUS in Arabidopsis thaliana American. J Bot 95:133–145

    Article  CAS  Google Scholar 

  • Bielenberg DG, Wang Y, Li ZG, Zhebentyayeva T, Fan SH, Reighard GL, Scorza R, Abbott AG (2008) Sequencing and annotation of the evergrowing locus in peach [Prunus persica (L.) Batsch] reveals a cluster of six MADS-box transcription factors as candidate genes for regulation of terminal bud formation. Tree Genet Genomes 4:495–507

    Article  Google Scholar 

  • Blumel M, Dally N, Jung C (2015) Flowering time regulation in crops-what did we learn from Arabidopsis? Curr Opin Biotechnol 32:121–129. https://doi.org/10.1016/j.copbio.2014.11.023

    Article  PubMed  Google Scholar 

  • Böhlenius H, Huang T, Charbonnelcampaa 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 312:1040–1043

    Article  PubMed  Google Scholar 

  • Boss PK, Thomas MR (2002) Association of dwarfism and floral induction with a grape ‘green revolution’ mutation. Nature 416:847–850

    Article  CAS  PubMed  Google Scholar 

  • Bouché F, D’Aloia M, Tocquin P, Lobet G, Detry N, Périlleux C (2016) Integrating roots into a whole plant network of flowering time genes in Arabidopsis thaliana. Sci Rep 6:203–214

    Article  Google Scholar 

  • Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679

    Article  CAS  PubMed  Google Scholar 

  • Ding L, Kim SY, Sd M (2013) FLOWERING LOCUS C EXPRESSOR family proteins regulate FLOWERING LOCUS C expression in both winter-annual and rapid-cycling Arabidopsis. Plant Physiol 163:243–252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dubois A et al. (2011) Genomic approach to study floral development genes in Rosa sp. PLoS ONE 6:e28455 https://doi.org/10.1371/journal.pone.0028455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eshghi S, Tafazoli E (2015) Possible role of non-structural carbohydrates in flower induction in strawberry. J Hortic Sci Biotechnol 81:854–858

    Article  Google Scholar 

  • Fan Z, Li J, Li X, Wu B, Wang J, Liu Z, Yin H (2015) Genome-wide transcriptome profiling provides insights into floral bud development of summer-flowering Camellia azalea. Sci Rep 5:9729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Foster T, Johnston R, Seleznyova A (2003) A morphological and quantitative characterization of early floral development in apple (malus × domestica borkh.). Ann Bot 92:199–206

    Article  PubMed  PubMed Central  Google Scholar 

  • Fu J, Wang L, Yi W, Yang L, Yang Y, Dai S (2014) Photoperiodic control of FT- like gene ClFT initiates flowering in Chrysanthemum lavandulifolium. Plant Physiol. Biochem. 74:230–238

    Article  CAS  PubMed  Google Scholar 

  • Gendall AR, Levy YY, Wilson A, Dean C (2001) The VERNALIZATION 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis. Cell 107:525–535

    Article  CAS  PubMed  Google Scholar 

  • Grabherr MG et al (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hararisteinberg O, Ohad I, Chamovitz DA (2001) Dissection of the light signal transduction pathways regulating the two early light-induced protein genes in Arabidopsis. Plant Physiol 127:986–997

    Article  CAS  Google Scholar 

  • He ZF (1985) The fast determination method for content of glucose, frutose by anthrone colorimetry. In: He ZF (ed) Grain quality and it’s analysis technology, Agricultural Press, Beijing, pp 144–150

    Google Scholar 

  • Hedden P, Thomas SG (2012) Gibberellin biosynthesis and its regulation. Biochem J 444:11–25

    Article  CAS  PubMed  Google Scholar 

  • Heisler MG, Ohno C, Das P, Sieber P, Reddy GV, Long JA, Meyerowitz EM (2005) Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr Biol 15:1899–1911

    Article  CAS  PubMed  Google Scholar 

  • Horibe T, Yamada K, Otagaki S, Matsumoto S, Kawamura K (2013) Molecular genetic studies on continuous-flowering roses that do not originate from Rosa chinensis. Acta Hortic 2013:1064

    Google Scholar 

  • Horvath DP, Anderson JV, Chao WS, Foley ME (2003) Knowing when to grow: signals regulating bud dormancy. Trends Plant Sci 8:534–540

    Article  CAS  PubMed  Google Scholar 

  • Ito A, Hayama H, Kashimura Y (2004) Possible roles of sugar concentration and its metabolism in the regulation of flower bud formation in Japanese Pear (Pyrus pyrifolia). Acta Hortic 636:365–373

    Article  CAS  Google Scholar 

  • Iwata H et al (2012) The TFL1 homologue KSN is a regulator of continuous flowering in rose and strawberry. Plant J 69:116–125. https://doi.org/10.1111/j.1365-313X.2011.04776.x

    Article  CAS  PubMed  Google Scholar 

  • Jin J et al (2015) An arabidopsis transcriptional regulatory map reveals distinct functional and evolutionary features of novel transcription factors. Mol Biol Evol 32:1767–1773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kai S et al (2015) ABSCISIC ACID-INSENSITIVE 4 negatively regulates flowering through directly promoting Arabidopsis FLOWERING LOCUS C transcription. J Exp Bot 67:195–205

    Google Scholar 

  • Kang C, Darwish O, Geretz A, Shahan R, Alkharouf N, Liu Z (2013) Genome-scale transcriptomic insights into early-stage fruit development in woodland strawberry Fragaria vesca. Plant Cell 25:1960–1978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kawamura K, Oyant HS, Thouroude T, Jeauffre J, Foucher F (2015) Inheritance of garden rose architecture and its association with flowering behaviour. Tree Genet Genomes 11:1–12

    Article  Google Scholar 

  • Khan MRG, Ai XY, Zhang JZ (2014) Genetic regulation of flowering time in annual and perennial plants. Wiley Interdisc Rev 5:347–359

    Article  CAS  Google Scholar 

  • Kim DH, Doyle MR, Sung SB, Amasino RM (2009) Vernalization: winter and the timing of flowering in plants. Annu Rev Cell Dev Biol 25:277–299

    Article  CAS  PubMed  Google Scholar 

  • Kinmonth-Schultz HA, Tong X, Lee J, Song YH, Ito S, Kim SH, Imaizumi T (2016) Cool night-time temperatures induce the expression of CONSTANS and FLOWERING LOCUS T to regulate flowering in Arabidopsis. New Phytol. https://doi.org/10.1111/nph.13883

    PubMed  PubMed Central  Google Scholar 

  • Kotoda N, Iwanami H, Takahashi S, Abe K (2006) Antisense expression of MdTFL1, a TFL1-like gene, reduces the juvenile phase in apple. J Am Soc Hortic Sci 131:74–81

    CAS  Google Scholar 

  • Lastdrager J, Smeekens S (2014) Sugar signals and the control of plant growth and development. J Exp Bot 65:799–807

    Article  CAS  PubMed  Google Scholar 

  • Lenhard M, Bohnert A, Jurgens G, Laux T (2001) Termination of stem cell maintenance in Arabidopsis floral meristems by interactions between WUSCHEL and AGAMOUS. Cell 105:805–814

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Reighard GL, Abbott AG, Bielenberg DG (2009) Dormancy-associated MADS genes from the EVG locus of peach [Prunus persica (L.) Batsch] have distinct seasonal and photoperiodic expression patterns. J Exp Bot 60:3521–3530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lohse M et al (2014) Mercator: a fast and simple web server for genome scale functional annotation of plant sequence data. Plant Cell Environ 37:1250–1258. https://doi.org/10.1111/pce.12231

    Article  CAS  PubMed  Google Scholar 

  • Matsoukas IG, Massiah AJ, Thomas B (2013) Starch metabolism and antiflorigenic signals modulate the juvenile-to-adult phase transition in Arabidopsis. Plant Cell Environ 36:1802–1811

    Article  CAS  PubMed  Google Scholar 

  • Minni (2005) Integration of light signaling with photo periodic flower in gand circadian rhythm. Cell Res 15:559–566

    Article  Google Scholar 

  • Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35:W182–W185

    Article  PubMed  PubMed Central  Google Scholar 

  • Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Nishikawa F, Endo T, Shimada T, Fujii H, Shimizu T, Omura M, Ikoma Y (2007) Increased CiFT abundance in the stem correlates with floral induction by low temperature in Satsuma mandarin (Citrus unshiu Marc.). J Exp Bot 58:3915–3927

    Article  CAS  PubMed  Google Scholar 

  • Nishikawa F, Endo T, Shimada T, Fujii H, Shimizu T, Omura M (2009) Differences in seasonal expression of flowering genes between deciduous trifoliate orange and evergreen Satsuma mandarin. Tree Physiol 29:921–926

    Article  CAS  PubMed  Google Scholar 

  • Ortiz-Marchena MI, Romero JM, Valverde F (2015) Photoperiodic control of sugar release during the floral transition: what is the role of sugars in the florigenic signal? Plant Signal Behav 10:e1017168. https://doi.org/10.1080/15592324.2015.1017168

    Article  PubMed  PubMed Central  Google Scholar 

  • Pan X, Welti R, Wang X (2010) Quantitative analysis of major plant hormones in crude plant extracts by high-performance liquid chromatography–mass spectrometry. Nat Protoc 5:986–992

    Article  CAS  PubMed  Google Scholar 

  • Preston JC, Kellogg EA (2006) Reconstructing the evolutionary history of paralogous APETALA1/FRUITFULL-like genes in grasses (Poaceae). Genetics 174:421–437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Randoux M et al (2012) Gibberellins regulate the transcription of the continuous flowering regulator, RoKSN, a rose TFL1 homologue. J Exp Bot. https://doi.org/10.1093/jxb/errs3130

    PubMed  PubMed Central  Google Scholar 

  • Randoux M et al (2014) RoKSN, a floral repressor, forms protein complexes with RoFD and RoFT to regulate vegetative and reproductive development in rose. New Phytol 202:161–173. https://doi.org/10.1111/nph.12625

    Article  CAS  PubMed  Google Scholar 

  • Sakamoto T et al (2006) Ectopic expression of KNOTTED1-like homeobox protein induces expression of cytokinin biosynthesis genes in rice. Plant Physiol 142:54–62

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101–1108

    Article  CAS  PubMed  Google Scholar 

  • Shimada S et al (2009) A genetic network of flowering-time genes in wheat leaves, in which an APETALA1/FRUITFULL-like gene, VRN1, is upstream of FLOWERING LOCUS T. Plant J 58:668–681. https://doi.org/10.1111/j.1365-313X.2009.03806.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sung S, Amasino RM (2004) Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN. Nature 427(3):159–164

    Article  CAS  PubMed  Google Scholar 

  • Sung S, Amasino RM (2005) Remembering winter: toward a molecular understanding of vernalization. Annu Rev Plant Biol 56:491–508

    Article  CAS  PubMed  Google Scholar 

  • Supek F, Bosnjak M, Skunca N, Smuc T (2011) REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS ONE 6:e21800. https://doi.org/10.1371/journal.pone.0021800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thissen D, Kuang D (2010) Quick and easy implementation of the Benjamini-Hochberg procedure for controlling the false positive rate in multiple comparisons. J Educ Behav Stat 27:77–83

    Article  Google Scholar 

  • Tsai AYL, Gazzarrini S (2014) Trehalose-6-phosphate and SnRK1 kinases in plant development and signaling: the emerging picture. Front Plant Sci 5:119–119

    Article  PubMed  PubMed Central  Google Scholar 

  • Usadel B, Poree F, Nagel A, Lohse M, Czedik-Eysenberg A, Stitt M (2009) A guide to using MapMan to visualize and compare Omics data in plants: a case study in the crop species, maize. Plant Cell Environ 32:1211–1229

    Article  PubMed  Google Scholar 

  • Wang R et al (2009) PEP1 regulates perennial flowering in Arabis alpina. Nature 459:423–427

    Article  CAS  PubMed  Google Scholar 

  • Wang F, Lian LJ, Liu QL (2015) Low expression of RTFL1c releases expression of RLFY, which induces recurrent flowering in rose. Acta Hortic 1064:131–134

    Article  Google Scholar 

  • Wolfe CJ, Kohane IS, Butte AJ (2005) Systematic survey reveals general applicability of “guilt-by-association” within gene coexpression networks. BMC Bioinform 6:227

    Article  Google Scholar 

  • Yamaguchi N et al (2013) A molecular framework for auxin-mediated initiation of flower primordia. Dev Cell 24:271–282. https://doi.org/10.1016/j.devcel.2012.12.017

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi N, Winter CM, Wu MF, Kanno Y, Yamaguchi A, Seo M, Wagner D (2014) Gibberellin acts positively then negatively to control onset of flower formation in Arabidopsis. Science 344:638–641

    Article  CAS  PubMed  Google Scholar 

  • Yang L, Conway SR, Poethig RS (2011) Vegetative phase change is mediated by a leaf-derived signal that represses the transcription of miR. Development 138(2):245–249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Young MD, Wakefield MJ, Smyth GK, Oshlack A (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 11:1

    Article  Google Scholar 

  • Yu JW et al (2009) COP1 and ELF3 control circadian function and photoperiodic flowering by regulating GI stability. Mol Cell 32:617–630

    Article  Google Scholar 

  • Yu S et al (2012) Gibberellin regulates the Arabidopsis floral transition through miR156-targeted SQUAMOSA PROMOTER BINDING–LIKE transcription factors. Plant Cell 24:3320–3332

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang ZL et al (2011) SCARECROW-LIKE 3 promotes gibberellin signaling by antagonizing master growth repressor DELLA in Arabidopsis. Proc Natl Acad Sci USA 108:2160–2165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao Y, Medrano L, Ohashi K, Fletcher JC, Yu H, Sakai H, Meyerowitz EM (2004) HANABA TARANU is a GATA transcription factor that regulates shoot apical meristem and flower development in Arabidopsis. Plant Cell 16:2586–2600

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Thanks are due to Yuyong Yang (Kunming Yang Chinese Rose Gardening Co., Ltd.) and Haiquan Huang (Southwest Forestry University) for the help and convenience of collecting samples. This work was supported by the Fundamental Research Funds for the Central Universities (No. 2016ZCQ02), National Natural Science Foundation of China (31600565), and Special Fund for Beijing Common Construction Project.

Author information

Authors and Affiliations

  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, Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants of Ministry of Education, School of Landscape Architecture, Beijing Forestry University, 100083, Beijing, China

    Xuelian Guo, Chao Yu, Le Luo, Huihua Wan, Ni Zhen, Yushu Li, Tangren Cheng, Jia Wang, Huitang Pan & Qixiang Zhang

  2. Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry University, 100083, Beijing, China

    Qixiang Zhang

Authors
  1. Xuelian Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chao Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Le Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Huihua Wan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ni Zhen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yushu Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Tangren Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jia Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Huitang Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Qixiang Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

ZQX and PHT contributed to the design of the research, GXL collected plant materials, carried out computational analysis and wrote the paper, YC and LL contributed to the design of the research and the manuscript modification. ZN contributed to collect plant materials and plant growing, WHH and LYS contributed to draw graphs, WJ and CTR contributed to modify the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Qixiang Zhang.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guo, X., Yu, C., Luo, L. et al. Developmental transcriptome analysis of floral transition in Rosa odorata var. gigantea. Plant Mol Biol 97, 113–130 (2018). https://doi.org/10.1007/s11103-018-0727-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-018-0727-8

Keywords

Search

Navigation