Skip to main content
Log in

Pollen transcriptome analysis of Solanum tuberosum (2n = 4x = 48), S. demissum (2n = 6x = 72), and their reciprocal F1 hybrids

  • Original Paper
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

Pollen mRNAs were different in reciprocal F 1 hybrids, which were probably caused by a cytoplasm–nuclear chromosomal genes interaction.

Abstract

We have found reciprocal differences in crossability between F1 hybrids of Solanum tuberosum (T) and a Mexican wild potato species S. demissum (D). When the reciprocal hybrids were crossed as pollen parents with S. demissum, a significantly higher berry-setting rate was obtained in TD compared with DT. In this study, we performed a whole-genome transcript analysis of the pollen mRNA using a high-throughput sequencer. We obtained 12.6 billion bases that were aligned into 13,020 transcripts with 9,366 loci. All possible genetic modes were observed between the parents and their progeny, where over-dominance and under-recessive types were relatively frequent (15.7 and 15.3 %, respectively). We found that 59.1 % of transcripts were more abundant in TD and over fourfold higher transcription levels were found in 66 TD transcripts and three DT transcripts. A higher proportion of over-dominance and a lower proportion of under-recessive transcription types were also observed in TD. The percentage contributions of multiple transcripts at the same locus varied greatly and were transcribed differently between species. In the new allelic combinations created by hybridization, approximately three-fourth of the transcripts had intermediate percentage contributions between the parents but no differential transcription patterns were apparent between the reciprocal hybrids. A broad spectrum of functionally different nuclear genes was over-represented in TD pollen, some of which were directly related to pollen behavior. Since TD and DT pollen had the same composition of nuclear genes, a cytoplasm–nuclear chromosomal genes interaction is suggested for the cause of transcriptional and phenotypic differences between reciprocal hybrids.

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

Access this article

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

References

  • Adams KL, Cronn R, Percifield R, Wendel JF (2003) Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing. Proc Natl Acad Sci USA 100:4649–4654

    Article  PubMed  CAS  Google Scholar 

  • Alleman M, Doctor J (2000) Genomic imprinting in plants: observations and evolutionary implications. Plant Mol Biol 43:147–161

    Article  PubMed  CAS  Google Scholar 

  • Andorf S, Selbig J, Altmann T, Poos K, Witucka-Wall H, Repsilber D (2010) Enriched partial correlations in genome-wide gene expression profiles of hybrids (A. thaliana): a systems biological approach towards the molecular basis of heterosis. Theor Appl Genet 120:249–259

    Article  PubMed  CAS  Google Scholar 

  • Borges F, Gomes G, Gardner R, Moreno N, McCormick S, Feijó JA, Becker JD (2008) Comparative transcriptomics of Arabidopsis sperm cells. Plant Physiol 148:1168–1181

    Article  PubMed  CAS  Google Scholar 

  • Chung HJ, Jung JD, Park HW, Kim JH, Cha HW, Min SR, Jeong WJ, Liu J (2006) The complete chloroplast genome sequences of Solanum tuberosum and comparative analysis with Solanaceae species identified the presence of a 241-bp deletion in cultivated potato chloroplast DNA sequence. Plant Cell Rep 25:1369–1379

    Article  PubMed  CAS  Google Scholar 

  • Colmenero-Flores JM, Campos F, Garciarrubio A, Covarrubias AA (1997) Characterization of Phaseolus vulgaris cDNA clones responsive to water deficit: identification of a novel late embryogenesis abundant-like protein. Plant Mol Biol 35:393–405

    Article  PubMed  CAS  Google Scholar 

  • Comai L, Tyagi AP, Winter K, Holmes-Davis R, Reynolds SH, Stevens Y, Byers B (2000) Phenotypic instability and rapid gene silencing in newly formed Arabidopsis allotetraploids. Plant Cell 12:1551–1568

    PubMed  CAS  Google Scholar 

  • del Campo EM (2009) Post-transcriptional control of chloroplast gene expression. Gene Reg Syst Biol 3:31–47

    Google Scholar 

  • Dilkes BP, Comai L (2004) A differential dosage hypothesis for parental effects in seed development. Plant Cell 16:3174–3180

    Article  PubMed  Google Scholar 

  • Forner J, Weber B, Thuss S, Wildum S, Binder S (2007) Mapping of mitochondrial mRNA termini in Arabidopsis thaliana: t-elements contribute to 5′ and 3′ end formation. Nucleic Acids Res 35:3676–3692

    Article  PubMed  CAS  Google Scholar 

  • Gehring M, Choi Y, Fischer RL (2004) Imprinting and seed development. Plant Cell 16:S203–S213

    Article  PubMed  CAS  Google Scholar 

  • Gehring M, Missirian V, Henikoff S (2011) Genomic analysis of parent-of-origin allelic expression in Arabidopsis thaliana seeds. PLoS ONE 6:e23687

    Article  PubMed  CAS  Google Scholar 

  • Guo M, Rupe MA, Zinselmeier C, Habben J, Bowen BA, Smith OS (2004) Allelic variation of gene expression in maize hybrids. Plant Cell 16:1707–1716

    Article  PubMed  CAS  Google Scholar 

  • Guo M, Rupe MA, Yang X, Crasta O, Zinselmeier C, Smith OS, Bowen B (2006) Genome-wide transcript analysis of maize hybrids: allelic additive gene expression and yield heterosis. Theor Appl Genet 113:831–845

    Article  PubMed  CAS  Google Scholar 

  • Guo M, Yang S, Rupe M, Hu B, Bickel DR, Arthur L, Smith O (2008) Genome-wide allele-specific expression analysis using Massively Parallel Signature Sequencing (MPSSTM) reveals cis- and trans-effects on gene expression in maize hybrid meristem tissue. Plant Mol Biol 66:551–563

    Article  PubMed  CAS  Google Scholar 

  • Haerizadeh F, Wong CE, Bhalla PL, Gresshoff PM, Singh MB (2009) Genomic expression profiling of mature soybean (Glycine max) pollen. BMC Plant Biol 9:25

    Article  PubMed  Google Scholar 

  • Hafidh S, Breznenová K, Růžička P, Feciková J, Čapková V, Honys D (2012) Comprehensive analysis of tobacco pollen transcriptome unveils common pathways in polar cell expansion and underlying heterochronic shift during spermatogenesis. BMC Plant Biol 12:24

    Article  PubMed  CAS  Google Scholar 

  • He G, Zhu X, Elling AA, Chen L, Wang X, Guo L, Liang M, He H, Zhang H, Chen F, Qi Y, Chen R, Deng XW (2010) Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids. Plant Cell 22:17–33

    Article  PubMed  CAS  Google Scholar 

  • Honys D, Twell D (2003) Comparative analysis of the Arabidopsis pollen transcriptome. Plant Physiol 132:640–652

    Article  PubMed  CAS  Google Scholar 

  • Honys D, Twell D (2004) Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol 5:R85

    Article  PubMed  Google Scholar 

  • Huh J, Bauer M, Hsieh T, Fischer R (2007) Endosperm gene imprinting and seed development. Curr Opin Genet Dev 17:480–485

    Article  PubMed  CAS  Google Scholar 

  • Jacobsen SE, Meyerowitz EM (1997) Hypermethylated SUPERMAN epigenetic alleles in Arabidopsis. Science 277:1100–1103

    Article  PubMed  CAS  Google Scholar 

  • Jones PA, Takai D (2001) The role of DNA methylation in mammalian epigenetics. Science 293:1068–1070

    Article  PubMed  CAS  Google Scholar 

  • Josefsson C, Dilkes B, Comai L (2006) Parent-dependent loss of gene silencing during interspecies hybridization. Curr Biol 16:1322–1328

    Article  PubMed  CAS  Google Scholar 

  • Knight JC (2004) Allele-specific gene expression uncovered. Trends Genet 20:113–116

    Article  PubMed  CAS  Google Scholar 

  • Köhler C, Makarevich G (2006) Epigenetic mechanisms governing seed development in plants. EMBO Rep 7:1223–1227

    Article  PubMed  Google Scholar 

  • Köhler C, Scheid OM, Erilova A (2010) The impact of the triploid block on the origin and evolution of polyploidy plants. Trends Genet 26:142–148

    Article  PubMed  Google Scholar 

  • Krupková E, Immerzeel P, Pauly M, Schmülling T (2007) The TUMOROUS SHOOT DEVELOPMENT2 gene of Arabidopsis encoding a putative methyltransferase is required for cell adhesion and co-ordinated plant development. Plant J 50:735–750

    Article  PubMed  Google Scholar 

  • Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory- efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25

    Article  PubMed  Google Scholar 

  • Li N, Dickinson HG (2010) Balance between maternal and paternal alleles sets the timing of resource accumulation in the maize endosperm. Proc R Soc B 277:3–10

    Article  PubMed  CAS  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup (2009) The sequence alignment/map (SAM) format and SAMtools. Bioinformatics 25:2078–2079

    Article  PubMed  Google Scholar 

  • Luo M, Taylor JM, Spriggs A, Zhang H, Wu X, Russell S, Singh M, Koltunow A (2011) A genome-wide survey of imprinted genes in rice seeds reveals imprinting primarily occurs in the endosperm. PLoS Genet 7:e1002125

    Article  PubMed  CAS  Google Scholar 

  • Madlung A, Masuelli RW, Watson B, Reynolds SH, Davison J, Comai L (2002) Remodeling of DNA methylation and phenotypic and transcriptional changes in synthetic Arabidopsis allotetraploids. Plant Physiol 129:733–746

    Article  PubMed  CAS  Google Scholar 

  • Masuko H, Endo M, Saito H, Hakozaki H, Park JI, Kawagishi-Kobayashi M, Takada Y, Okabe T, Kamada M, Takahashi H, Higashitani A, Watanabe M (2006) Anther-specific genes, which expressed through microsporogenesis, are temporally and spatially regulated in model legume, Lotus japonicus. Genes Genet Syst 81:57–62

    Article  PubMed  CAS  Google Scholar 

  • Matsubayashi M (1991) Phylogenetic relationships in the potato and its related species. In: Tsuchiya T, Gupta PK (eds) Chromosome engineering in plants: genetics, breeding, evolution Part B. Elsevier, Amsterdam, pp 93–118

    Google Scholar 

  • Milne I, Bayer M, Cardle L, Shaw P, Stephen G, Wright F, Marshall D (2010) Tablet-next generation sequence assembly visualization. Bioinformatics 26:401–402

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Moscatelli A, Scali M, Prescianotto-Baschong C, Ferro M, Garin J, Vignani R, Ciampolini F, Cresti M (2005) A methionine synthase homolog is associated with secretory vesicles in tobacco pollen tubes. Planta 221:776–789

    Article  PubMed  CAS  Google Scholar 

  • Pennington PD, Costa LM, Gutierrez-Marcos JF, Greenland AJ, Dickinson HG (2008) When genomes collide: aberrant seed development following maize interploidy crosses. Ann Bot 101:833–843

    Article  PubMed  CAS  Google Scholar 

  • Pina C, Pinto F, Feijó JA, Becker JD (2005) Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control, and gene expression regulation. Plant Physiol 138:744–756

    Article  PubMed  CAS  Google Scholar 

  • Ranocha P, McNeil SD, Ziemak MJ, Li CJ, Tarczynski MC, Hanson AD (2001) The S-methylmethionine cycle in angiosperms: ubiquity, antiquity and activity. Plant J 25:575–584

    Article  PubMed  CAS  Google Scholar 

  • Riddle NC, Jiang H, An L, Doerge RW, Birchler JA (2010) Gene expression analysis at the intersection of ploidy and hybridity in maize. Theor Appl Genet 120:341–353

    Article  PubMed  CAS  Google Scholar 

  • Roach DA, Wulff RD (1987) Maternal effects in plants. Annu Rev Ecol Syst 18:209–235

    Article  Google Scholar 

  • Sanetomo R, Hosaka K (2011) Reciprocal differences in DNA sequence and methylation status of the pollen DNA between F1 hybrids of Solanum tuberosum × S. demissum. Euphytica 182:219–229

    Article  CAS  Google Scholar 

  • Sanetomo R, Ono S, Hosaka K (2011) Characterization of crossability in the crosses between Solanum demissum and S. tuberosum, and the F1 and BC1 progenies. Am J Potato Res 88:500–510

    Article  Google Scholar 

  • Swanson-Wagner RA, Jia Y, DeCook R, Borsuk LA, Nettleton D, Schnable PS (2006) All possible modes of gene action are observed in a global comparison of gene expression in a maize F1 hybrid and its inbred parents. Proc Natl Acad Sci USA 103:6805–6810

    Article  PubMed  CAS  Google Scholar 

  • Tebbji F, Nantel A, Matton DP (2010) Transcription profiling of fertilization and early seed development events in a solanaceous species using a 7.7 K cDNA microarray from Solanum chacoense ovules. BMC Plant Biol 10:174

    Article  PubMed  Google Scholar 

  • The Potato Genome Sequencing Consortium (2011) Genome sequence and analysis of the tuber crop potato. Nature 475:189–195

    Article  Google Scholar 

  • Vaughn MW, Tanurdžić M, Lippman Z, Jiang H, Carrasquillo R, Rabinowicz PD, Dedhia N, McCombie WR, Agier N, Bulski A, Colot V, Doerge RW, Martienssen RA (2007) Epigenetic natural variation in Arabidopsis thaliana. PLoS Biol 5:e174

    Article  PubMed  Google Scholar 

  • Vuylsteke M, van Eeuwijk F, Hummelen PV, Kuiper M, Zabeau M (2005) Genetic analysis of variation in gene expression in Arabidopsis thaliana. Genetics 171:1267–1275

    Article  PubMed  CAS  Google Scholar 

  • Walia H, Josefsson C, Dilkes B, Kirkbride R, Harada J, Comai L (2009) Dosage-dependent deregulation of an AGAMOUS-LIKE gene cluster contributes to interspecific incompatibility. Curr Biol 19:1128–1132

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Zhang WZ, Song LF, Zou JJ, Su Z, Wu WH (2008) Transcriptome analyses show changes in gene expression to accompany pollen germination and tube growth in Arabidopsis. Plant Physiol 148:1201–1211

    Article  PubMed  CAS  Google Scholar 

  • Wei G, Tao Y, Liu G, Chen C, Luo R, Xia H, Gan Q, Zeng H, Lu Z, Han Y, Li X, Song G, Zhai H, Peng Y, Li D, Xu H, Wei X, Cao M, Deng H, Xin Y, Fu X, Yuan L, Yu J, Zhu Z, Zhu L (2009) A transcriptomic analysis of superhybrid rice LYP9 and its parents. Proc Natl Acad Sci USA 106:7695–7701

    Article  PubMed  CAS  Google Scholar 

  • Willing RP, Mascarenhas JP (1984) Analysis of the complexity and diversity of mRNAs from pollen and shoots of Tradescantia. Plant Physiol 175:865–868

    Article  Google Scholar 

  • Willing RP, Bashe D, Mascarenhas JP (1988) An analysis of the quantity and diversity of messenger RNAs from pollen and shoots of Zea mays. Theor Appl Genet 75:751–753

    Article  CAS  Google Scholar 

  • Zerbino DR, Birney E (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821–829

    Article  PubMed  CAS  Google Scholar 

  • Zhao L, Huang J, Zhao Z, Li Q, Sims TL, Xue Y (2010) The Skp1-like protein SSK1 is required for cross-pollen compatibility in S-RNase-based self-incompatibility. Plant J 62:52–63

    Article  PubMed  CAS  Google Scholar 

  • Zhuang Y, Adams KL (2007) Extensive allelic variation in gene expression in Populous F1 hybrids. Genetics 177:1987–1996

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank the US Potato Genebank (NRSP-6), Sturgeon Bay, Wisconsin, for providing the Solanum seed used in this study and Dr. I. Sugimura, Hokkaido System Science Co. Ltd., for initial data handling and technical advice during high-throughput sequencing. We also thank Enago (http://www.enago.jp) for the English language review. This study was supported by Calbee Inc. and Calbee Potato Inc.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kazuyoshi Hosaka.

Additional information

Communicated by A.-C. Schmit.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLSX 66 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sanetomo, R., Hosaka, K. Pollen transcriptome analysis of Solanum tuberosum (2n = 4x = 48), S. demissum (2n = 6x = 72), and their reciprocal F1 hybrids. Plant Cell Rep 32, 623–636 (2013). https://doi.org/10.1007/s00299-013-1395-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-013-1395-4

Keywords

Navigation