Skip to main content
SpringerLink
Log in

Sexual dimorphic floral development in dioecious plants revealed by transcriptome, phytohormone, and DNA methylation analysis in Populus tomentosa

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Dioecious plants have evolved sex-specific floral development mechanisms. However, the precise gene expression patterns in dioecious plant flower development remain unclear. Here, we used andromonoecious poplar, an exceptional model system, to eliminate the confounding effects of genetic background of dioecious plants. Comparative transcriptome and physiological analysis allowed us to characterize sex-specific development of female and male flowers. Transcriptome analysis identified genes significantly differentially expressed between the sexes, including genes related to floral development, phytohormone synthesis and metabolism, and DNA methylation. Correlation analysis revealed a significant correlation between phytohormone signaling and gene expression, identifying specific phytohormone-responsive genes and their cis-regulatory elements. Two genes related to DNA methylation, METHYLTRANSFERASE1 (MET1) and DECREASED DNA METHYLATION 1 (DDM1), which are located in the sex determination region of Chromosome XIX, have differential expression between female and male flowers. A time-course analysis revealed that MET1 and DDM1 expression may produce different DNA methylation levels in female and male flowers. Understanding the interactions of phytohormone signaling, DNA methylation and target gene expression should lead to a better understanding of sexual differences in floral development. Thus, this study identifies a set of candidate genes for further studies of poplar sexual dimorphism and relates sex-specific floral development to physiological and epigenetic changes.

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

Similar content being viewed by others

Abbreviations

CT:

Cytokinins

Gas:

Gibberellins

IAA:

Indoleacetic acid

ABA:

Abscisic acid

References

  • Acosta IF, Laparra H, Romero SP, Schmelz E, Hamberg M et al (2009) tasselseed1 is a lipoxygenase affecting jasmonic acid signaling in sex determination of maize. Science 323:262

    Article  CAS  PubMed  Google Scholar 

  • Bartrina I, Otto E, Strnad M, Werner T, Schmülling T (2011) Cytokinin regulates the activity of reproductive meristems, flower organ size, ovule formation, and thus seed yield in Arabidopsis thaliana. Plant Cell 23:69–80

    Article  CAS  PubMed  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Stat Methodol 57:289–300

    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 

  • Böhlenius H, Huang T, Charbonnel-Campaa L, Brunner AM, Jansson S et al (2006) CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312:1040

    Article  PubMed  CAS  Google Scholar 

  • Boss PK, Bastow RM, Mylne JS, Dean C (2004) Multiple pathways in the decision to flower: enabling, promoting, and resetting. Plant Cell 16:18–31

    Google Scholar 

  • Boualem A, Fergany M, Ferandez R, Troadec C, Martin A, Morin H, Sari MA et al (2008) A conserved mutation in an ethylene biosynthesis enzyme leads to andromonoecy in melons. Science 321:836–838

    Article  CAS  PubMed  Google Scholar 

  • Boutrot F, Chantret N, Gautier MF (2008) Genome-wide analysis of the rice and Arabidopsis non-specific lipid transfer protein (nsLtp) gene families and identification of wheat nsLtp genes by EST data mining. BMC Genomics 9:86

    Article  PubMed  CAS  Google Scholar 

  • Brunner AM, Rottmann WH, Sheppard LA, Krutovskii K, DiFazio SP et al (2000) Structure and expression of duplicate AGAMOUS orthologues in poplar. Plant Mol Biol 44:619–634

    Article  CAS  PubMed  Google Scholar 

  • Brzeski J, Jerzmanowski A (2003) Deficient in DNA methylation 1 (DDM1) defines a novel family of chromatin-remodeling factors. J Biol Chem 278:823–828

    Article  CAS  PubMed  Google Scholar 

  • Burn JE, Bagnall DJ, Metzger JD, Dennis ES, Peacock WJ (1993) DNA methylation, vernalization, and the initiation of flowering. Proc Natl Acad Sci USA 90:287–291

    Article  CAS  PubMed  Google Scholar 

  • Byzova MV, Franken J, Aarts MGM, De Almeida-Engler J, Engler G et al (1999) Arabidopsis STERILE APETALA, a multifunctional gene regulating inflorescence, flower, and ovule development. Genes Dev 13:1002–1014

    Article  CAS  PubMed  Google Scholar 

  • Cao X, Springer NM, Muszynski MG, Phillips RL, Kaeppler S et al (2000) Conserved plant genes with similarity to mammalian de novo DNA methyltransferases. Proc Natl Acad Sci USA 97:4979–4984

    Article  CAS  PubMed  Google Scholar 

  • Cecchetti V, Altamura MM, Falasca G, Costantino P, Cardarelli M (2008) Auxin regulates Arabidopsis anther dehiscence, pollen maturation, and filament elongation. Plant Cell 20:1760–1774

    Article  CAS  PubMed  Google Scholar 

  • Chae E, Tan QKG, Hill TA, Irish VF (2008) An Arabidopsis F-box protein acts as a transcriptional co-factor to regulate floral development. Development 135:1235–1245

    Article  CAS  PubMed  Google Scholar 

  • Chailakyan MK, Khryanin VN (1978) Effect of growth regulators and role of roots in sex expression in spinach. Planta 142:207–210

    Article  Google Scholar 

  • Chen YH, Yang XY, He K, Liu MH, Li JG et al (2006) The MYB transcription factor superfamily of Arabidopsis: expression analysis and phylogenetic comparison with the rice MYB family. Plant Mol Biol 60:107–124

    Article  CAS  Google Scholar 

  • Cheng XF, Wang ZY (2005) Overexpression of COL9, a CONSTANS-LIKE gene, delays flowering by reducing expression of CO and FT in Arabidopsis thaliana. Plant J 43:758–768

    Article  CAS  PubMed  Google Scholar 

  • Choi Y, Gehring M, Johnson L, Hannon M, Harada JJ et al (2002) DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in arabidopsis. Cell 110:33–42

    Article  CAS  PubMed  Google Scholar 

  • Cseke LJ, Cseke SB, Ravinder N, Taylor LC, Shankar A et al (2005) SEP class genes in Populus tremuloides and their likely role in reproductive survival of poplar trees. Gene 358:1–16

    Article  CAS  PubMed  Google Scholar 

  • Delph LF, Gehring JL, Arntz AM, Levri M, Frey FM (2005) Genetic correlations with floral display lead to sexual dimorphism in the cost of reproduction. Am Nat 166:31–41

    Article  Google Scholar 

  • Demeulemeester MAC, Van Stallen N, De Proft MP (1999) Degree of DNA methylation in chicory (Cichorium intybus L.): influence of plant age and vernalization. Plant Sci 142:101–108

    Article  CAS  Google Scholar 

  • Finnegan EJ, Peacock WJ, Dennis ES (1996) Reduced DNA methylation in Arabidopsis thaliana results in abnormal plant development. Proc Natl Acad Sci USA 93:8449–8454

    Article  CAS  PubMed  Google Scholar 

  • Gälweiler L, Müller A, Guan C, Wisman E, Mendgen K et al (1998) Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282:2226–2230

    Article  PubMed  Google Scholar 

  • Golenberg EM, West NW (2013) Hormonal interactions and gene regulation can link monoecy and environmental plasticity to the evolution of dioecy in plants. Am J Bot 100:1022–1037

    Google Scholar 

  • Gong Z, Morales-Ruiz T, Ariza RR, Roldán-Arjona T, David L et al (2002) ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase. Cell 111:803–814

    Article  CAS  PubMed  Google Scholar 

  • Grant S, Houben A, Vyskot B, Siroky J, Pan WH et al (1994) Genetics of sex determination in flowering plants. Dev Genet 15:214–230

    Article  Google Scholar 

  • Gregis V, Sessa A, Dorca-Fornell C, Kater MM (2009) The Arabidopsis floral meristem identity genes AP1, AGL24 and SVP directly repress class B and C floral homeotic genes. Plant J 60:626–637

    Article  CAS  PubMed  Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 27:297–300

    Article  CAS  PubMed  Google Scholar 

  • Huang S, Cerny RE, Qi Y, Bhat D, Aydt CM et al (2003) Transgenic studies on the involvement of cytokinin and gibberellin in male development. Plant Physiol 131:1270–1282

    Article  CAS  PubMed  Google Scholar 

  • Hundertmark M, Hincha DK (2008) LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genomics 9:118

    Article  PubMed  CAS  Google Scholar 

  • Irish EE, Langdale JA, Nelson T (1999) Interactions between tassel seed genes and other sex determining genes in maize. Dev Genet 25:78

    Article  Google Scholar 

  • Jeddeloh JA, Stokes TL, Richards EJ (1999) Maintenance of genomic methylation requires a SWI2/SNF2-like protein. Nat Genet 22:94–97

    Article  CAS  PubMed  Google Scholar 

  • Kant S, Rothstein S (2009) Auxin-responsive SAUR39 gene modulates auxin level in rice. Plant Signal Behav 4:1174–1175

    Article  PubMed  Google Scholar 

  • Krokan HE, Standal R, Slupphaug G (1997) DNA glycosylases in the base excision repair of DNA. Biochem J 325:1–16

    CAS  PubMed  Google Scholar 

  • Li D, Liu C, Shen L, Wu Y, Chen HY et al (2008) A repressor complex governs the integration of flowering signals in Arabidopsis. Dev Cell 15:110–120

    Article  CAS  PubMed  Google Scholar 

  • Link BM, Cosgrove DJ (1998) Acid-growth response and a-Expansins in suspension cultures of bright yellow 2 tobacco. Plant Physiol 118:907–916

    Article  CAS  PubMed  Google Scholar 

  • Lippman Z, Gendrel AV, Black M, Vaughn MW, Dedhia N et al (2004) Role of transposable elements in heterochromatin and epigenetic control. Nature 430:471–476

    Article  CAS  PubMed  Google Scholar 

  • Malepszy S, Niemirowicz-szczytt K (1991) Sex determination in cucumber (Cucumis sativus) as a model system for molecular biology. Plant Sci 80:39–47

    Article  Google Scholar 

  • Martin A, Troadec C, Boualem A, Rajab M, Fernandez R et al (2009) A transposon-induced epigenetic change leads to sex determination in melon. Nature 461:1135–1138

    Article  CAS  PubMed  Google Scholar 

  • Mibus H, Tatlioglu T (2004) Molecular characterization and isolation of the F/f gene for femaleness in cucumber (Cucumis sativus L.). Theor Appl Genet 109:1669–1676

    Article  CAS  PubMed  Google Scholar 

  • Mohamed R, Wang CT, Ma C, Shevchenko O, Dye SJ et al (2010) Populus CEN/TFL1 regulates first onset of flowering, axillary meristem identity and dormancy release in Populus. Plant J 62:674–688

    Article  CAS  PubMed  Google Scholar 

  • Mutasa-Göttgens E, Hedden P (2009) Gibberellin as a factor in floral regulatory networks. J Exp Bot 6:1979–1989

    Article  CAS  Google Scholar 

  • Ni WM, Chen XY, Xu ZH, Xue HW (2002) A Pin gene families encoding components of auxin efflux carriers in Brassica juncea. Cell Res 12:247–255

    Article  PubMed  Google Scholar 

  • Pierce LK, Werner TC (1990) Review of genes and linkage groups in cucumber. HortScience 25:605–615

    CAS  Google Scholar 

  • Riefler M, Novak O, Strnad M, SchmÜlling T (2006) Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell 18:40–54

    Article  CAS  PubMed  Google Scholar 

  • Robson F, Costa MMR, Hepworth SR, Vizir I, Pinieiro M et al (2001) Functional importance of conserved domains in the flowering-time gene CONSTANS demonstrated by analysis of mutant alleles and transgenic plants. Plant J 28:619–631

    Article  CAS  PubMed  Google Scholar 

  • Searle I, Coupland G (2004) Induction of flowering by seasonal changes in photoperiod. EMBO J 23:1217–1222

    Article  CAS  PubMed  Google Scholar 

  • Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT et al (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504

    Article  CAS  PubMed  Google Scholar 

  • Sheppard LA, Brunner AM, Krutovskii KV, Rottmann WH, Skinner JS et al (2000) A DEFICIENS homolog from the dioecious tree black cottonwood is expressed in female and male floral meristems of the two-whorled, unisexual flowers. Plant Physiol 124:627–639

    Article  CAS  PubMed  Google Scholar 

  • Song YP, Ma KF, Bo WH, Zhang ZY, Zhang DQ (2012) Sex-specific DNA methylation and gene expression in andromonoecious poplar. Plant Cell Rep 31:1393–1405

    Article  CAS  PubMed  Google Scholar 

  • Teyssier E, Bernacchia G, Maury S, How Kit A, Stammitti-Bert L et al (2008) Tissue dependent variations of DNA methylation and endoreduplication levels during tomato fruit development and ripening. Planta 228:391–399

    Article  CAS  PubMed  Google Scholar 

  • Walford SA, Wu Y, Llewellyn D, Dennis ES (2011) GhMYB25-like: a key factor in early cotton fibre development. Plant J 65:785–797

    Article  CAS  PubMed  Google Scholar 

  • Wang WY, Chen WS, Chen WH, Hung LS, Chang PS (2002) Influence of abscisicacid on flowering in Phalaenopsis hybrida. Plant Physiol Biochem 40:97–100

    Article  Google Scholar 

  • Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. Ann Bot 111:1021–1058

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson MD, Haughn GW (1995) UNUSUAL FLORAL ORGANS controls meristem identity and organ primordia fate in Arabidopsis. Plant Cell 7:1485–1499

    CAS  PubMed  Google Scholar 

  • Wilson RN, Heckman JW, Somerville CR (1992) Gibberellin is required for flowering in required for flowering in Arabidopsis thaliana under short days. Plant Physiol 100:403–408

    Article  CAS  PubMed  Google Scholar 

  • Wyatt P, Hodge R, Smartt S, Draper J, Scott R (1992) The isolation and characterisation of the tapetum-specific Arabidopsis thaliana A9 gene. Plant Mol Biol 9:611–622

    Google Scholar 

  • Yamaguchi S, Smith MW, Brown RG, Kamiya Y, Sun T (1998) Phytochrome regulation and differential expression of gibberellin 3-beta-hydroxylase genes in germinating Arabidopsis seeds. Plant Cell 10:2115–2126

    CAS  PubMed  Google Scholar 

  • Yin T, Quinn JA (1992) A mechanistic model of a single hormone regulating both sexes in flowering plants. Bull Torrey Bot Club 119:431–441

    Article  Google Scholar 

  • Yin TM, DeFazio SP, Counter LE, Zhang XY, Sewell MM et al (2008) Genome structure and emerging evidence of an incipient sex chromosome in Populus. Genome Res 18:422–430

    Article  CAS  PubMed  Google Scholar 

  • Yu H, Ito T, Wellmer F, Meyerowitz EM (2004) Repression of AGAMOUS-LIKE 24 is a crucial step in promoting flower development. Nat Genet 36:157–161

    Article  CAS  PubMed  Google Scholar 

  • Zhang DQ, Du QZ, Xu BH, Zhang ZY, Li BL (2010) The actin multigene family in Populus: organization, expression and phylogenetic analysis. Mol Genet Genomics 284:105–119

    Article  CAS  PubMed  Google Scholar 

  • Zhang ZJ, Ai XY, Sun LM, Zhang DL, Guo WW et al (2011) Transcriptome profile analysis of flowering molecular process of early flowering trifoliate orange mutant and the wild-type (Poncirus trifoliata) by massively parallel signature sequencing. BMC Genomics 12:63

    Article  CAS  PubMed  Google Scholar 

  • Zhao D, Yang M, Solava J, Ma H (1999) The ASK1 gene regulates development and interacts with the UFO gene to control floral organ identity in Arabidopsis. Dev Genet 25:209–223

    Article  CAS  PubMed  Google Scholar 

  • Zluvova J, Zak J, Janousek B, Vyskot B (2010) Dioecious Silene latifolia plants show sexual dimorphism in the vegetative stage. BMC Plant Biol 10:208

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the following sources: Fundamental Research Funds for Central Universities (No. TD2012-01), and the Project of the National Natural Science Foundation of China (No. 31170622, 30872042). The authors would like to thank Dr. Jiehua Wang from Tianjin University for critical reading of the manuscript. We are grateful for the sequence information produced by the U.S. Department of Energy Joint Genome Institute (http://www.jgi.doe.gov).

Author information

Authors and Affiliations

  1. National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing, 100083, People’s Republic of China

    Yuepeng Song, Kaifeng Ma, Dong Ci, Qingqing Chen, Jiaxing Tian & Deqiang Zhang

  2. Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, No. 35, Qinghua East Road, Beijing, 100083, People’s Republic of China

    Yuepeng Song, Kaifeng Ma, Dong Ci, Qingqing Chen, Jiaxing Tian & Deqiang Zhang

Authors
  1. Yuepeng Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kaifeng Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dong Ci
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Qingqing Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jiaxing Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Deqiang Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Deqiang Zhang.

Additional information

Zhiyi Zhang: Deceased.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Song, Y., Ma, K., Ci, D. et al. Sexual dimorphic floral development in dioecious plants revealed by transcriptome, phytohormone, and DNA methylation analysis in Populus tomentosa . Plant Mol Biol 83, 559–576 (2013). https://doi.org/10.1007/s11103-013-0108-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-013-0108-2

Keywords

Search

Navigation