Skip to main content
SpringerLink
Log in

Differential expression of photosynthesis-related genes in pentaploid interspecific hybrid and its decaploid of Fragaria spp.

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

Abstract

Polyploidization always induces a series of changes in genome, transcriptome and epigenetics, of which changes in gene expression are the immediate causes of genotype alterations of polyploid plants. In our previous study on strawberry polyploidization, genes related to photosynthesis were found to undergo changes in gene expression and DNA methylation. Therefore, we chose 11 genes that were closely related to plant photosynthesis and analysed their expression during strawberry hybridization and chromosome doubling. Most genes of pentaploids showed expression levels between parents and were more similar to F. × ananassa. Gene expression levels of decaploids were higher than those of pentaploids and F. × ananassa. Different types of photosynthesis-related genes responded differently to hybridization and chromosome doubling. Chloroplast genes and regulatory genes showed complex responses. Structural genes of the photosynthetic system were expressed at a constant level and displayed a clear dosage effect. The methylation levels of one CG site on SIGE, which regulates expression of chloroplast genes, were negatively correlated with gene expression. In pentaploids and decaploids, more transcripts were from F. × ananassa than from F. viridis. The ratio of transcripts from from F. × ananassa to those from F. viridis was close to the ratio (4:1) of the genome of F. × ananassa to that of F. viridis in pentaploids and decaploids, but there were also some exceptions with obvious deviation.

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

Similar content being viewed by others

References

  • Bao Y, Xu Q (2015) Extensive reprogramming of cytosine methylation in Oryza allotetraploids. Genes Genom 37:517–524

    Article  CAS  Google Scholar 

  • Bekesiovai I, Nap JP, Mlynarova L (1999) Isolation of high quality DNA and RNA from leaves of the carnivorous plant Drosera rotundifolia. Plant Mol Biol Rep 17:269–277

    Article  Google Scholar 

  • Buggs RJ, Chamala S, Wu W, Gao L, May GD, Schnable PS, Soltis DE, Soltis PS, Barbazuk WB (2010) Characterization of duplicate gene evolution in the recent natural allopolyploid Tragopogon miscellus by next-generation sequencing and Sequenom iPLEX MassARRAY genotyping. Mol Ecol 19:132–146

    Article  CAS  PubMed  Google Scholar 

  • Chen ZJ (2013) Genomic and epigenetic insights into the molecular bases of herterosis. Nat Rev Genet 14:471–482

    Article  CAS  PubMed  Google Scholar 

  • Coate JE, Schlueter JA, Whaley AM, Doyle JJ (2011) Comparative evolution of photosynthetic genes in response to polyploid and nonpolyploid duplication. Plant Physiol 155:2081–2095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Comai L (2005) The advantages and disadvantages of being polyploid. Nat Rev Genet 6:836–846

    Article  CAS  PubMed  Google Scholar 

  • Combes MC, Dereeper A, Severac D, Bertrand B, Lashermes P (2013) Contribution of subgenomes to the transcriptome and their intertwined regulation in the allopolyploid Coffea arabica grown at contrasted temperatures. New Phytol 200:251–260

    Article  CAS  PubMed  Google Scholar 

  • Gaeta RT, Pires JC, Iniguez-Luy F, Leon E, Osborn TC (2007) Genomic changes in resynthesized Brassica napus and their effect on gene expression and phenotype. Plant Cell 19:3403–3417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Germer S, Holland MJ, Higuchi R (2000) High-throughput SNP allele-frequency determination in pooled DNA samples by kinetic PCR. Genome Res 10:258–266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo M, Davis D, Birchler JA (1996) Dosage effects on gene expression in a maize ploidy series. Genetics 142:1349–1355

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hegarty MJ, Barker GL, Wilson ID, Abbott RJ, Edwards KJ, Hiscock SJ (2006) Transcriptome shock after interspecific hybridization in Senecio is ameliorated by genome duplication. Curr Biol 16:1652–1659

    Article  CAS  PubMed  Google Scholar 

  • Hegarty MJ, Batstone TOM, Barker GL, Edwards KJ, Abbott RJ, Hiscock SJ (2011) Nonadditive changes to cytosine methylation as a consequence of hybridization and genome duplication in Senecio (Asteraceae). Mol Ecol 20:105–113

    Article  CAS  PubMed  Google Scholar 

  • Hummer K (2012) A new species of Fragaria (Rosaceae) from Oregon. J Bot Res Inst Texas 6:9–15

    Google Scholar 

  • Hummer K, Nathewet P, Yanagi T (2009) Decaploidy in Fragaria iturupensis (Rosaceae). Am J Bot 96:713–716

    Article  PubMed  Google Scholar 

  • Jia L, Lou Q, Jiang B, Wang D, Chen J (2014) LTR retrotransposons cause expression changes of adjacent genes inearly generations of the newly formed allotetraploid Cucumis hytivus. Sci Hortic 174:171–177

    Article  CAS  Google Scholar 

  • Jung Y, Kawaura K, Mishina K, Sakuma S, Kishii M, Ogihara Y (2014) Changes in genome-wide gene expression during allopolyploidization and genome stabilization in hexaploid wheat. Genes Genet Syst 89:215–225

    Article  CAS  PubMed  Google Scholar 

  • Kenneth JL, Thomas DS (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–∆∆CT method. Method 25:402–408

    Article  Google Scholar 

  • Lai J, Ma J, Swigoňová Z, Ramakrishna W, Linton E, Llaca V, Tanyolac B, Park YJ, Jeong OY, Bennetzen JL et al (2004) Gene loss and movement in the maize genome. Genome Res 14:1924–1931

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee HS, Chen ZJ (2001) Protein-coding genes are epigenetically regulated in Arabidopsis polyploids. Proc Natl Acad Sci USA 98:6753–6758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lei JJ, Xue L, Dai HP (2012) Obtaining dodecaploid interspecific hybrid in strawberry and its backcross. Sci Agric Sin 45:4651–4659

    CAS  Google Scholar 

  • Lei JJ, Xue L, Guo RX, Dai HP (2017) The Fragaria species native to china and their geographical distribution. Acta Hortic 1156:37–46

    Article  Google Scholar 

  • Martienssen RA, Colot V (2001) DNA methylation and epigenetic inheritance in plants and filamentous fungi. Science 293:1070–1074

    Article  CAS  PubMed  Google Scholar 

  • Mizoguchi T, Wheatley K, Hanzawa Y, Wright L, Mizoguchi M, Song HR, Carré IA, Coupland G (2002) LHY and CCA1 are partially redundant genes required to maintain circadian rhythms in Arabidopsis. Dev Cell 2:629–641

    Article  CAS  PubMed  Google Scholar 

  • Ni Z, Kim ED, Ha M, Lackey E, Liu J, Zhang Y, Sun Q, Chen ZJ (2009) Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature 457:327–331

    Article  CAS  PubMed  Google Scholar 

  • Noordally ZB, Ishii K, Atkins KA, Wetherill SJ, Kusakina J, Walton EJ, Kato M, Azuma M, Tanaka K, Hanaoka M et al (2013) Circadian control of chloroplast transcription by a nuclear-encoded timing signal. Science 339:1316–1319

    Article  CAS  PubMed  Google Scholar 

  • Osborn TC, Chris Pires J, Birchler JA, Auger DL, Jeffery Chen Z, Lee HS, Comai L, Madlung A, Doerge RW, Colot V et al (2003) Understanding mechanisms of novel gene expression in polyploids. Trends Genet 19:141–147

    Article  CAS  PubMed  Google Scholar 

  • Pecinka A, Fang W, Rehmsmeier M, Levy AA, Scheid OM (2011) Polyploidization increases meiotic recombination frequency in Arabidopsis. BMC Biol 9:24

    Article  PubMed  PubMed Central  Google Scholar 

  • Pikaard CS (1999) Nucleolar dominance and silencing of transcription. Trends Plant Sci 4:478–483

    Article  CAS  PubMed  Google Scholar 

  • Pumphrey M, Bai J, Laudencia-Chingcuanco D, Anderson O, Gill BS (2009) Nonadditive expression of homoeologous genes is established upon polyploidization in hexaploid wheat. Genetics 181:1147–1157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roose ML, Gottlieb LD (1980) Biochemical properties and level of expression of alcohol dehydrogenases in the allotetraploid plant Tragopogon miscellus and its diploid progenitors. Biochem Genet 18:1065–1085

    Article  CAS  PubMed  Google Scholar 

  • Sargent DJ, Davis TM, Simpson DW (2009) Strawberry (Fragaria spp.) structural genomics. In: Folta KM (ed) Genetics and genomics of Rosaceae, 6th edn. Springer, New York, pp 437–456

    Chapter  Google Scholar 

  • Schranz ME, Quijada P, Sung SB, Lukens L, Amasino R, Osborn TC (2002) Characterization and effects of the replicated flowering time gene FLC in Brassica rapa. Genetics 162:1457–1468

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shitsukawa N, Tahira C, Kassai KI, Hirabayashi C, Shimizu T, Takumi S, Mochida K, Kawaura K, Ogihara Y, Murai K (2007) Genetic and epigenetic alteration among three homoeologous genes of a class E MADS box gene in hexaploid wheat. Plant Cell 19:1723–1737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song Q, Chen ZJ (2015) Epigenetic and developmental regulation in plant polyploids. Curr Opin Plant Boil 24:101–109

    Article  CAS  Google Scholar 

  • Stupar RM, Bhaskar PB, Yandell BS, Rensink WA, Hart AL, Ouyang S, Veilleux RE, Busse JS, Erhardt RJ, Buell CR et al (2007) Phenotypic and transcriptomic changes associated with potato autopolyploidization. Genetics 176:2055–2067

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sui Y, Li B, Shi J, Chen M (2014) Genomic, regulatory and epigenetic mechanisms underlying duplicated gene evolution in the natural allotetraploid Oryza minuta. BMC Genom 15:11

    Article  Google Scholar 

  • Tian L, Li X, Ha M, Zhang C, Chen ZJ (2014) Genetic and epigenetic changes in a genomic region containing MIR172 in Arabidopsis allopolyploids and their progenitors. Heredity 112:207–214

    Article  CAS  PubMed  Google Scholar 

  • Tsunoyama Y, Ishizaki Y, Morikawa K, Nakahira Y, Takeba G, Toyoshima Y, Shiina T (2004) Blue light-induced transcription of plastid-encoded psbD gene is mediated by a nuclear-encoded transcription initiation factor, AtSig5. Proc Natl Acad Sci USA 101:3304–3309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Veitia RA, Bottani S, Birchler JA (2008) Cellular reactions to gene dosage imbalance: genomic, transcriptomic and proteomic effects. Trends Genet 24:390–397

    Article  CAS  PubMed  Google Scholar 

  • Wang JL, Tian L, Madlung A, Lee HS, Chen M, Lee JJ, Watson B, Kagochi T, Comai L, Chen ZJ (2004) Stochastic and epigenetic changes of gene expression in Arabidopsis polyploids. Genetics 167:1961–1973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang JL, Tian L, Lee HS, Chen ZJ (2006a) Nonadditive regulation of FRI and FLC loci mediates flowering-time variation in Arabidopsis allopolyploids. Genetics 173:965–974

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang JL, Tian L, Lee HS, Wei NE, Jiang H, Watson B, Madlung A, Osborn TC, Doerge RW, Comai L et al (2006b) Genomewide nonadditive gene regulation in Arabidopsis allotetraploids. Genetics 172:507–517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang B, Fu R, Zhang M, Ding Z, Chang L, Zhu X, Wang Y, Fan B, Ye W, Yuan Y (2015) Analysis of methylation-sensitive amplified polymorphism in different cotton accessions under salt stress based on capillary electrophoresis. Genes Genom 37:713–724

    Article  CAS  Google Scholar 

  • Wang T, Liu L, Ning C, Lü Z, Jia X, Gao Z, Qiao Y (2016) Alterations of DNA methylation and gene expression during hybridization and polyploidization in Fragaria spp. Sci Hortic 201:218–224

    Article  CAS  Google Scholar 

  • Wendel JF (2000) Genome evolution in polyploids. Plant Mol Biol 42:225–249

    Article  CAS  PubMed  Google Scholar 

  • Xu Y, Zhong L, Wu X, Fang X, Wang J (2009) Rapid alterations of gene expression and cytosine methylation in newly synthesized Brassica napus allopolyploids. Planta 229:471–483

    Article  CAS  PubMed  Google Scholar 

  • Xu Z, John ZY, Cho J, Yu J, Kohel RJ, Percy RG (2010) Polyploidization altered gene functions in cotton (Gossypium spp.). PLoS ONE 5:14351. https://doi.org/10.1371/journal.pone.0014351

    Article  Google Scholar 

  • Yao H, Kato A, Mooney B, Birchler JA (2011) Phenotypic and gene expression analyses of a ploidy series of maize inbred Oh43. Plant Mol Biol 75:237–251

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Bernatavichute YV, Cokus S, Pellegrini M, Jacobsen SE (2009) Genome-wide analysis of mono-, di- and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol 10:R62

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang T, Hu Y, Jiang W, Fang L, Guan X, Chen J, Zhang J, Saski CA, Scheffler BE, Stelly DM et al (2015) Sequencing of allotetraploid cotton (Gossypium hirsutum L. acc. TM-1) provides a resource for fiber improvement. Nat Biotechnol 33:531–540

    Article  CAS  PubMed  Google Scholar 

  • Zilberman D, Gehring M, Tran RK, Ballinger T, Henikoff S (2007) Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet 39:61–69

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The Jiangsu Province Agricultural Science and Technology Innovation Fund Projects (No. CX(15)1029) funded this work.

Author information

Author notes

  1. Tao Wang

    Present address: Institute of Botany, Jiangsu Province and Chinese Academy of Sciences, Nanjing, 210014, China

Authors and Affiliations

  1. Laboratory of Fruit Crop Biotechnology, College of Horticulture, Nanjing Agricultural University, Nanjing, 210095, China

    Tao Wang, Dongya Huang, Baoyu Chen & Yushan Qiao

  2. Zhenjiang Institute of Agricultural Sciences in Hilly Area of Jiangsu, Jurong, 212400, China

    Nini Mao & Muxiang Ji

Authors
  1. Tao Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dongya Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Baoyu Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nini Mao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yushan Qiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Muxiang Ji
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Yushan Qiao or Muxiang Ji.

Ethics declarations

Conflict of interest

Tao Wang declares that he does not have conflict of interest. Dongya Huang declares that she does not have conflict of interest. Baoyu Chen declares that she does not have conflict of interest. Nini Mao declares that she does not have conflict of interest. Yushan Qiao declares that he does not have conflict of interest. Muxiang Ji declares that he does not have conflict of interest.

Research involving human and animal participants

This article does not contain any human or animal experiments to be subjected with ethical standards.

Additional information

Tao Wang and Dongya Huang contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, T., Huang, D., Chen, B. et al. Differential expression of photosynthesis-related genes in pentaploid interspecific hybrid and its decaploid of Fragaria spp.. Genes Genom 40, 321–331 (2018). https://doi.org/10.1007/s13258-018-0647-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13258-018-0647-7

Keywords

Search

Navigation