Skip to main content
SpringerLink
Log in

A comprehensive gene network for fine tuning floral development in poplar

  • Research Article
  • Published:
Genes & Genomics Aims and scope Submit manuscript

Abstract

Herbaceous model species, especially Arabidopsis has provided a wealth of information about the genes involved in floral induction and development of inflorescences and flowers. While the genus Populus is an important model system for the molecular biology of woody plant. These two genuses differ in many ways. This study was designed to improve understanding of flower development in poplar at a system level, as its regulatory pathway to a large extent remains poorly known, owing to the presently limited mutant pool. To address this issue, a poplar GeneChip was employed to detect genes expressed during the whole floral developmental process. Using the expressed floral genes, a systematic gene network was constructed with the aid of functional association with Arabidopsis. The results suggested that autonomous, gibberellin, vernalization, photoperiod, ethylene, brassinosteroid, stress-induced and floral suppression pathways are involved in poplar flowering. Modularity analysis revealed several pathways in common with Arabidopsis, such as autonomous, gibberellin, vernalization and photoperiod pathways. In addition, brassinosteroid, stress-induced and floral suppression pathways were implicated as additional novel pathways. Notably, a difference in vernalization between Arabidopsis and poplar was revealed. Autonomous, gibberellin, vernalization, photoperiod, ethylene, brassinosteroid, stress-induced and floral suppression pathways integrated into a systematic gene network in floral development of poplar. Compared to Arabidopsis, brassinosteroid, stress-induced and floral suppression pathways are additional in poplar, and FLC is absent in vernalization pathway in poplar. Preliminary conclusions drawn here provide a basis for both identification of key genes and elucidation of molecular mechanisms involved in poplar floral development.

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

Similar content being viewed by others

Abbreviations

ACS :

1-AMINOCYCLOPROPANE-1-CARBOXYLATE SYNTHASE

AG :

AGAMOUS

AGL19 :

AGAMOUS-LIKE 19

AGL20 :

AGAMOUS-LIKE 20

AGL24 :

AGAMOUS-LIKE 24

AGL8 :

AGAMOUS-LIKE 8

AP1 :

APETALA1

AP3 :

APETALA 3

ARF2 :

AUXIN RESPONSE FACTOR 2

BAS1 :

PHYB-4 ACTIVATION-TAGGED SUPPRESSOR 1

BES1 :

BRI1-EMS-SUPPRESSOR 1

BIM1 :

BES1-INTERACTING MYC-LIKE PROTEIN 1

BIM2 :

BES1-INTERACTING MYC-LIKE PROTEIN 2

BIN2 :

BRASSINOSTEROID-INSENSITIVE 2

BR:

Brassinosteroid

BRI1 :

BRASSINOSTEROID-INSENSITIVE 1

BZR1 :

BRASSINAZOLE-RESISTANT 1

CCA1 :

CIRCADIAN CLOCK ASSOCIATED 1

CDF1 :

CELL GROWTH DEFECT FACTOR 1

CLF :

CURLY LEAFICU1

CO :

CONSTANS

CTR1 :

CONSTITUTIVE TRIPLE RESPONSE1

CPD :

CONSTITUTIVE PHOTOMORPHOGENIC AND DWARF

COP1 :

CONSTITUTIVE PHOTOMORPHOGENIC 1

CRY1 :

CRYPTOCHROME 1

CRY2 :

CRYPTOCHROME 2

CTR1 :

CONSTITUTIVE TRIPLE RESPONSE 1

CUL4 :

CULLIN4

DDB1 :

DAMAGED DNA BINDING PROTEIN1

DET2 :

DEETIOLATED2

EFS :

EARLY FLOWERING IN SHORT DAYS

EIN2 :

ETHYLENE INSENSITIVE 2

EIN4 :

ETHYLENE INSENSITIVE 4

ELF3 :

EARLY FLOWERING 3

ELF6 :

EARLY FLOWERING 6

ELF7 :

EARLY FLOWERING 7

ELF8 :

EARLY FLOWERING 8

EMF2 :

EMBRYONIC FLOWER 2

ERA1 :

ENHANCED RESPONSE TO ABA 1

ETR1 :

ETHYLENE RESPONSE 1

ETR2 :

ETHYLENE RESPONSE 2

FCA :

A PROTEIN CONTAINING RNA-BINDING DOMAINS

FD :

A BZIP PROTEIN REQUIRED FOR POSITIVE REGULATION OF FLOWERING

FIE :

FERTILIZATION-INDEPENDENT ENDOSPERM

FKF1 :

FLAVIN-BINDING, KELCH REPEAT, F Box 1

FLC :

FLOWERING LOCUS C

FLD :

FLOWERING LOCUS D

FT :

FLOWERING LOCUS T

FTA :

FARNESYLTRANSFERASE A

FVE :

A RETINOBLASTOMA-ASSOCIATED PROTEIN

FWA :

FLOWERING WAGENINGEN

FY :

FLOWERING TIME CONTROL PROTEIN FY

GAI :

GIBBERELLIC ACID INSENSITIVE

GEO :

GENE EXPRESSION OMNIBUS

GI :

GIGANTEA

GID1C :

GA INSENSITIVE DWARF1C

HY5 :

ELONGATED HYPOCOTYL 5

LD :

LUMINIDEPENDENS

LFY :

LEAFY

LHY :

LATE ELONGATED HYPOCOTYL

MAF2 :

MADS AFFECTING FLOWERING 2

MAF3 :

MADS AFFECTING FLOWERING 3

MAF4 :

MADS AFFECTING FLOWERING 4

MSI1 :

MULTICOPY SUPRESSOR OF IRA1

PFT1 :

PHYTOCHROME AND FLOWERING TIME 1

PHOT1 :

PHOTOTROPIN 1

PHOT2 :

PHOTOTROPIN 2

PHYA :

PHYTOCHROME A

PHYB :

PHYTOCHROME B

PI :

PISTILLATA

PRC2 :

POLYCOMB-GROUP REPRESSIVE COMPLEX 2

PRR7 :

PSEUDO-RESPONSE REGULATOR 7

RGA1 :

REPRESSOR OF GA1-3 1

RGL1 :

RGA-LIKE 1

RGL2 :

RGA-LIKE 2

SEP1 :

SEPALLATA1

SEP3 :

SEPALLATA3

SLY1 :

SLEEPY1

SOB7 :

SUPPRESSOR OF PHYB-4 7

SOC1 :

SUPPRESSOR OF OVEREXPRESSION OF CO 1

SPA :

SUPPRESSOR OF PHYA

SPA3 :

SPA1-RELATED 3

SQN :

SQUINT

TFL2 :

TERMINAL FLOWER 2

TOC1 :

TIMING OF CAB EXPRESSION 1

TSF :

TWIN SISTER OF FT

VIN3 :

VERNALIZATION INSENSITIVE 3

VIP3 :

VERNALIZATION INDEPENDENCE 3

VIP4 :

VERNALIZATION INDEPENDENCE 4

VRN2 :

REDUCED VERNALIZATION RESPONSE 2

VRN5 :

VERNALIZATION 5

ZTL :

ZEITLUPE

References

  • Achard P, Cheng H, De Grauwe L, Decat J, Schoutteten H, Moritz T, Van Der Straeten D, Peng J, Harberd NP (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science 311:91–94

    Article  CAS  PubMed  Google Scholar 

  • Achard P, Baghour M, Chapple A, Hedden P, Van Der Straeten D, Genschik P, Moritz T, Harberd NP (2007) The plant stress hormone ethylene controls floral transition via DELLA-dependent regulation of floral meristem-identity genes. Proc Natl Acad Sci USA 104:6484–6489

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alabadi D, Oyama T, Yanovsky MJ, Harmon FG, Mas P, Kay SA (2001) Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science 293:880

    Article  CAS  PubMed  Google Scholar 

  • Alexandre CM, Hennig L (2008) FLC or not FLC: the other side of vernalization. J Exp Bot 59:1127–1135

    Article  CAS  PubMed  Google Scholar 

  • Amasino R (2010) Seasonal and developmental timing of flowering. Plant J 61:1001–1013

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Bäckström S, Elfving N, Nilsson R, Wingsle G, Björklund S (2007) Purification of a plant mediator from Arabidopsis thaliana identifies PFT1 as the Med25 subunit. Mol Cell 26:717–729

    Article  PubMed  Google Scholar 

  • 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 29:464–489

    Article  CAS  PubMed  Google Scholar 

  • Berardini TZ, Bollman K, Sun H, Scott Poethig R (2001) Regulation of vegetative phase change in Arabidopsis thaliana by cyclophilin 40. Science 291:2405

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Boes TK, Strauss SH (1994) Floral phenology and morphology of black cottonwood, Populus trichocarpa (Salicaceae). Am J Bot 81:562–567

    Article  Google Scholar 

  • Boss PK, Bastow RM, Mylne JS, Dean C (2004) Multiple pathways in the decision to flower: enabling, promoting, and resetting. Plant Cell 16:S18–S31

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bouveret R, Schönrock N, Gruissem W, Hennig L (2006) Regulation of flowering time by Arabidopsis MSI1. Development 133:1693–1702

    Article  CAS  PubMed  Google Scholar 

  • Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11:113–116

    Article  CAS  Google Scholar 

  • Chen H, Huang X, Gusmaroli G, Terzaghi W, Lau OS, Yanagawa Y, Zhang Y, Li J, Lee JH, Zhu D (2010) Arabidopsis CULLIN4-damaged DNA binding protein 1 interacts with CONSTITUTIVELY PHOTOMORPHOGENIC1-SUPPRESSOR OF PHYA complexes to regulate photomorphogenesis and flowering time. Plant Cell 22:108–123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Z, Ye M, Su X, Liao W, Ma H, Gao K, Lei B, An X (2015) Overexpression of AtAP1M3 regulates flowering time and floral development in Arabidopsis and effects key flowering-related genes in poplar. Transgenic Res 24:705–715

    Article  CAS  PubMed  Google Scholar 

  • Cheng H, Qin L, Lee S, Fu X, Richards DE, Cao D, Luo D, Harberd NP, Peng J (2004) Gibberellin regulates Arabidopsis floral development via suppression of DELLA protein function. Development 131:1055–1064

    Article  CAS  PubMed  Google Scholar 

  • Corbesier L, Vincent C, Jang S, Fornara F, Fan Q, Searle I, Giakountis A, Farrona S, Gissot L, Turnbull C (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316:1030

    Article  CAS  PubMed  Google Scholar 

  • Davis SJ (2002) Photoperiodism: the coincidental perception of the season. Curr Biol 12:R841–R843

    Article  CAS  PubMed  Google Scholar 

  • Davis SJ (2009) Integrating hormones into the floral-transition pathway of Arabidopsis thaliana. Plant Cell Environ 32:1201–1210

    Article  CAS  PubMed  Google Scholar 

  • Hamès C, Ptchelkine D, Grimm C, Thevenon E, Moyroud E, Gérard F, Martiel JL, Benlloch R, Parcy F, Müller CW (2008) Structural basis for LEAFY floral switch function and similarity with helix-turn-helix proteins. EMBO J 27:2628–2637

    Article  PubMed  PubMed Central  Google Scholar 

  • He Y, Amasino RM (2005) Role of chromatin modification in flowering-time control. Trends Plant Sci 10:30–35

    Article  CAS  PubMed  Google Scholar 

  • Hennig L, Taranto P, Walser M, Schönrock N, Gruissem W (2003) Arabidopsis MSI1 is required for epigenetic maintenance of reproductive development. Development 130:2555–2565

    Article  CAS  PubMed  Google Scholar 

  • Hsu CY, Liu Y, Luthe DS, Yuceer C (2006) Poplar FT2 shortens the juvenile phase and promotes seasonal flowering. Plant Cell 18:1846–1861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hsu CY, Adams JP, Kim H, No K, Ma C, Strauss SH, Drnevich J, Vandervelde L, Ellis JD, Rice BM et al (2011) FLOWERING LOCUS T duplication coordinates reproductive and vegetative growth in perennial poplar. Proc Natl Acad Sci USA 108:10756–10761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang H, Nusinow DA (2016) Into the evening: complex interactions in the Arabidopsis circadian clock. Trends Genet 32:674–686

    Article  CAS  PubMed  Google Scholar 

  • Huang B, Qian P, Gao N, Shen J, Hou S (2017) Fackel interacts with gibberellic acid signaling and vernalization to mediate flowering in Arabidopsis. Planta. doi:10.1007/s00425-017-2652-5

    Google Scholar 

  • Ito S, Niwa Y, Nakamichi N, Kawamura H, Yamashino T, Mizuno T (2008) Insight into missing genetic links between two evening-expressed pseudo-response regulator genes TOC1 and PRR5 in the circadian clock-controlled circuitry in Arabidopsis thaliana. Plant Cell Physiol 49:201–213

    Article  CAS  PubMed  Google Scholar 

  • Kazan K, Lyons R (2016) The link between flowering time and stress tolerance. J Exp Bot 67:47–60

    Article  CAS  PubMed  Google Scholar 

  • Koornneef M, Meinke D (2010) The development of Arabidopsis as a model plant. Plant J 61:909–921

    Article  CAS  PubMed  Google Scholar 

  • Lee I, Ambaru B, Thakkar P, Marcotte EM, Rhee SY (2010) Rational association of genes with traits using a genome-scale gene network for Arabidopsis thaliana. Nat Biotechnol 28:149–156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Levy YY, Dean C (1998) The transition to flowering. Plant cell 10:1973–1990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lohmann JU, Weigel D (2002) Building beauty: the genetic control of floral patterning. Dev Cell 2:135–142

    Article  CAS  PubMed  Google Scholar 

  • Más P, Kim WY, Somers DE, Kay SA (2003) Targeted degradation of TOC1 by ZTL modulates circadian function in Arabidopsis thaliana. Nature 426:567–570

    Article  PubMed  Google Scholar 

  • Moon J, Lee H, Kim M, Lee I (2005) Analysis of flowering pathway integrators in Arabidopsis. Plant Cell Physiol 46:292–299

    Article  CAS  PubMed  Google Scholar 

  • Nakamichi N, Kita M, Ito S, Yamashino T, Mizuno T (2005) PSEUDO-RESPONSE REGULATORS, PRR9, PRR7 and PRR5, together play essential roles close to the circadian clock of Arabidopsis thaliana. Plant Cell Physiol 46:686–698

    Article  CAS  PubMed  Google Scholar 

  • Okushima Y, Mitina I, Quach HL, Theologis A (2005) AUXIN RESPONSE FACTOR 2 (ARF2): a pleiotropic developmental regulator. Plant J 43:29–46

    Article  CAS  PubMed  Google Scholar 

  • Ratcliffe OJ, Kumimoto RW, Wong BJ, Riechmann JL (2003) Analysis of the Arabidopsis MADS AFFECTING FLOWERING gene family: MAF2 prevents vernalization by short periods of cold. Science 15:1159

    CAS  Google Scholar 

  • Razem FA, El-Kereamy A, Abrams SR, Hill RD (2006) The RNA-binding protein FCA is an abscisic acid receptor. Nature 439:290–294

    Article  CAS  PubMed  Google Scholar 

  • Riboni M, Galbiati M, Tonelli C, Conti L (2013) GIGANTEA enables drought escape response via abscisic acid-dependent activation of the florigens and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS. Plant Physiol 162:1706–1719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rottmann WH, Meilan R, Sheppard LA, Brunner AM, Skinner JS, Ma C, Cheng S, Jouanin L, Pilate G, Strauss SH (2000) Diverse effects of overexpression of LEAFY and PTLF, a poplar (Populus) homolog of LEAFY/FLORICAULA, in transgenic poplar and Arabidopsis. Plant J 22:235–245

    Article  CAS  PubMed  Google Scholar 

  • Santner A, Estelle M (2009) Recent advances and emerging trends in plant hormone signalling. Nature 459:1071–1078

    Article  CAS  PubMed  Google Scholar 

  • Sawa M, Nusinow DA, Kay SA, Imaizumi T (2007) FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis. Science 318:261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schönrock N, Bouveret R, Leroy O, Borghi L, Köhler C, Gruissem W, Hennig L (2006) Polycomb-group proteins repress the floral activator AGL19 in the FLC-independent vernalization pathway. Gene Dev 20:1667

    Article  PubMed  PubMed Central  Google Scholar 

  • Shibuya K, Barry KG, Ciardi JA, Loucas HM, Underwood BA, Nourizadeh S, Ecker JR, Klee HJ, Clark DG (2004) The central role of PhEIN2 in ethylene responses throughout plant development in petunia. Plant Physiol 136:2900–2912

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Somerville C, Koornneef M (2002) A fortunate choice: the history of Arabidopsis as a model plant. Nat Rev Genet 3:883–889

    Article  CAS  PubMed  Google Scholar 

  • Tsuchisaka A, Yu G, Jin H, Alonso JM, Ecker JR, Zhang X, Gao S, Theologis A (2009) A combinatorial interplay among the 1-aminocyclopropane-1-carboxylate isoforms regulates ethylene biosynthesis in Arabidopsis thaliana. Genetics 183:979–1003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vert G, Chory J (2006) Downstream nuclear events in brassinosteroid signalling. Nature 441:96–100

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Ying J, Kuzma M, Chalifoux M, Sample A, McArthur C, Uchacz T, Sarvas C, Wan J, Dennis DT et al (2005) Molecular tailoring of farnesylation for plant drought tolerance and yield protection. Plant J 43:413–424

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Beaith M, Chalifoux M, Ying J, Uchacz T, Sarvas C, Griffiths R, Kuzma M, Wan J, Huang Y (2009) Shoot-specific down-regulation of protein farnesyltransferase (α-subunit) for yield protection against drought in canola. Mol Plant 2:191–200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wellmer F, Riechmann JL (2010) Gene networks controlling the initiation of flower development. Trends Genet 26:519–527

    Article  CAS  PubMed  Google Scholar 

  • Wong CE, Singh MB, Bhalla PL (2009) Molecular processes underlying the floral transition in the soybean shoot apical meristem. Plant J 57:832–845

    Article  CAS  PubMed  Google Scholar 

  • Wood CC, Robertson M, Tanner G, Peacock WJ, Dennis ES, Helliwell CA (2006) The Arabidopsis thaliana vernalization response requires a polycomb-like protein complex that also includes VERNALIZATION INSENSITIVE 3. Proc Natl Acad Sci USA 103:14631–14636

    Article  PubMed  PubMed Central  Google Scholar 

  • Xue J, Li Y, Tan H, Yang F, Ma N, Gao J (2008) Expression of ethylene biosynthetic and receptor genes in rose floral tissues during ethylene-enhanced flower opening. J Exp Bot 59:2161–2169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu H, Ito T, Zhao Y, Peng J, Kumar P, Meyerowitz EM (2004) Floral homeotic genes are targets of gibberellin signaling in flower development. Proc Natl Acad Sci USA 101:7827

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu JW, Rubio V, Lee NY, Bai S, Lee SY, Kim SS, Liu L, Zhang Y, Irigoyen ML, Sullivan JA (2008) COP1 and ELF3 control circadian function and photoperiodic flowering by regulating GI stability. Mol Cell 32:617–630

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuceer C, Land SB Jr, Kubiske ME, Harkess RL (2003) Shoot morphogenesis associated with flowering in Populus deltoides (Salicaceae). Am J Bot 90:196–206

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the Fundamental Research Funds for the Central Universities (Grant No. BLYJ201410); the Graduate Training and Development Program of Beijing Municipal Commission of Education (Grant Nos. BLCXY201619 and BJCXY201611); and the National Natural Science Foundation of China (Grant No. 31570661).

Author information

Authors and Affiliations

  1. National Engineering Laboratory for Tree Breeding, Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants of the Ministry of Education, College of Biological Sciences and Biotechnology, Beijing Forestry University, Qinghua Eastern Road No.35, Haidian District, Beijing, 100083, China

    Zhong Chen, Xiaoyu Yang, Kai Gao, Pian Rao & Xinmin An

  2. Key Laboratory of Silviculture and Conservation of the Ministry of Education, College of Forestry, Beijing Forestry University, Beijing, 100083, China

    Zhong Chen

  3. Berry Genomics Co., Ltd., Beijing, 100015, China

    Xiaoxing Su

Authors
  1. Zhong Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiaoyu Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiaoxing Su
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kai Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Pian Rao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xinmin An
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xinmin An.

Ethics declarations

Conflict of interest

Zhong Chen, Xiaoyu Yang, Xiaoxing Su, Kai Gao, Pian Rao, Xinmin An declares that they have no conflict of interest.

Ethical approval

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

Additional information

Zhong Chen, Xiaoyu Yang and Xiaoxing Su have contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

13258_2017_546_MOESM1_ESM.tif

Supplementary material 1 (TIF 6639 KB) – Figure S1 Each part of the modularity analysis results. Results of the modularity analysis were derived from the original network shown in Fig. 1.

13258_2017_546_MOESM2_ESM.pdf

Supplementary material 2 (PDF 27963 KB) – Table S1 Detail of flowering-correlated genes used for network construction and the list of gene interactions.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, Z., Yang, X., Su, X. et al. A comprehensive gene network for fine tuning floral development in poplar. Genes Genom 39, 793–803 (2017). https://doi.org/10.1007/s13258-017-0546-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13258-017-0546-3

Keywords

Search

Navigation