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Genome wide gene expression in artificially synthesized amphidiploids of Arabidopsis

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Abstract

The merging of two different genomes occurs during the formation of amphidiploids, and the merged regulatory networks have the potential to generate a new gene expression pattern. We examined the genome-wide gene expression of two newly synthesized amphidiploids between Arabidopsis thaliana and the related species Arabidopsis lyrata subsp. lyrata and Arabidopsis halleri subsp. gemmifera. 1,137 (4.7%) and 1,316 (5.4%) of probesets showed differential gene expression in A. thalianaA. halleri and A. thalianaA. lyrata hybrids respectively, compared to the mid parent value and of these, 489 were in common. Genes that differed in expression between the parental lines tended to have an expression level in both hybrids differing from the mid parent value. In contrast to protein coding genes, there is little differential expression of transposons. Genes in the categories of chloroplast-targeted and response to stress were overrepresented in the non-additively expressed genes in both amphidiploids. As these genes have the potential to contribute directly to the plant phenotype, we suggest that rapid changes of gene expression in amphidiploids might be important for producing greater biomass.

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References

  • Adams KL, Percifield R, Wendel JF (2004) Organ-specific silencing of duplicated genes in a newly synthesized cotton allotetraploid. Genetics 168:2217–2226

    Article  PubMed  CAS  Google Scholar 

  • Beaulieu J, Jean M, Belzile F (2009) The allotetraploid Arabidopsis thalianaArabidopsis lyrata subsp. petraea as an alternative model system for the study of polyploidy in plants. Mol Genet Genomics 281:421–435

    Article  PubMed  CAS  Google Scholar 

  • Beck JB, Al-Shehbaz IA, O’Kane SL Jr, Schaal BA (2007) Further insights into the phylogeny of Arabidopsis (Brassicaceae) from nuclear Atmyb2 flanking sequence. Mol Phylogenet Evol 42:122–130

    Article  PubMed  CAS  Google Scholar 

  • Berardini TZ, Mundodi S, Reiser L, Huala E, Garcia-Hernandez M, Zhang P, Mueller LA, Yoon J, Doyle A, Lander G, Moseyko N, Yoo D, Xu I, Zoeckler B, Montoya M, Miller N, Weems D, Rhee SY (2004) Functional annotation of the Arabidopsis genome using controlled vocabularies. Plant Physiol 135:745–755

    Article  PubMed  CAS  Google Scholar 

  • Chen M, Ha M, Lackey E, Wang J, Chen ZJ (2008) RNAi of met1 reduces DNA methylation and induces genome-specific changes in gene expression and centromeric small RNA accumulation in Arabidopsis allopolyploids. Genetics 178:1845–1858

    Article  PubMed  CAS  Google Scholar 

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

    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

    Article  PubMed  CAS  Google Scholar 

  • Earley K, Lawrence RJ, Pontes O, Reuther R, Enciso AJ, Silva M, Neves N, Gross M, Viegas W, Pikaard CS (2006) Erasure of histone acetylation by Arabidopsis HDA6 mediates large-scale gene silencing in nucleolar dominance. Genes Dev 20:1283–1293

    Article  PubMed  CAS  Google Scholar 

  • Flagel LE, Wendel JF (2010) Evolutionary rate variation, genomic dominance and duplicate gene expression evolution during allotetraploid cotton speciation. New Phytol 186:184–193

    Article  PubMed  CAS  Google Scholar 

  • Flagel L, Udall J, Nettleton D, Wendel J (2008) Duplicate gene expression in allopolyploid Gossypium reveals two temporally distinct phases of expression evolution. BMC Biol 6:16

    Article  PubMed  Google Scholar 

  • Fujimoto R, Sasaki T, Inoue H, Nishio T (2008a) Hypomethylation and transcriptional reactivation of retrotransposon-like sequences in ddm1 transgenic plants of Brassica rapa. Plant Mol Biol 66:463–473

    Article  PubMed  CAS  Google Scholar 

  • Fujimoto R, Kinoshita Y, Kawabe A, Kinoshita T, Takashima K, Nordborg M, Nasrallah ME, Shimizu KK, Kudoh H, Kakutani T (2008b) Evolution and control of imprinted FWA genes in the genus Arabidopsis. PLoS Genet 4:e1000048

    Article  PubMed  Google Scholar 

  • Fujimoto R, Sasaki T, Kudoh H, Taylor JM, Kakutani T, Dennis ES (2011) Epigenetic variation in the FWA gene within the genus Arabidopsis. Plant J 66:831–843

    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  PubMed  CAS  Google Scholar 

  • Gaeta RT, Yoo SY, Pires JC, Doerge RW, Chen ZJ, Osborn TC (2009) Analysis of gene expression in resynthesized Brassica napus allopolyploids using Arabidopsis 70mer oligo microarrays. PLoS One 4:e4760

    Article  PubMed  Google Scholar 

  • Ha M, Kim ED, Chen ZJ (2009a) Duplicate genes increase expression diversity in closely related species and allopolyploids. Proc Natl Acad Sci USA 106:2295–2300

    Article  PubMed  CAS  Google Scholar 

  • Ha M, Lu J, Tian L, Ramachandran V, Kasschau KD, Chapman EJ, Carrington JC, Chen X, Wang XJ, Chen ZJ (2009b) Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids. Proc Natl Acad Sci USA 106:17835–17840

    Article  PubMed  CAS  Google Scholar 

  • He P, Friebe BR, Gill BS, Zhou JM (2003) Allopolyploidy alters gene expression in the highly stable hexaploid wheat. Plant Mol Biol 52:401–414

    Article  PubMed  CAS  Google Scholar 

  • Hirochika H, Okamoto H, Kakutani T (2000) Silencing of retrotransposons in Arabidopsis and reactivation by the ddm1 mutation. Plant Cell 12:357–369

    Article  PubMed  CAS  Google Scholar 

  • Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP (2003a) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4:249–264

    Article  PubMed  Google Scholar 

  • Irizarry RA, Gautier L, Cope LM (2003b) The analysis of gene expression data: methods and software, chapter 4. Springer, Berlin

    Google Scholar 

  • Johanson U, West J, Lister C, Michaels S, Amasino R, Dean C (2000) Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290:344–347

    Article  PubMed  CAS  Google Scholar 

  • Kashkush K, Feldman M, Levy AA (2002) Gene loss, silencing and activation in a newly synthesized wheat allotetraploid. Genetics 160:1651–1659

    PubMed  CAS  Google Scholar 

  • Kashkush K, Feldman M, Levy AA (2003) Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. Nat Genet 33:102–106

    Article  PubMed  CAS  Google Scholar 

  • Kato M, Miura A, Bender J, Jacobsen SE, Kakutani T (2003) Role of CG and non-CG methylation in immobilization of transposons in Arabidopsis. Curr Biol 13:421–426

    Article  PubMed  CAS  Google Scholar 

  • Koch MA, Haubold B, Mitchell-Olds T (2000) Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). Mol Biol Evol 17:1483–1498

    PubMed  CAS  Google Scholar 

  • Lawrence RJ, Earley K, Pontes O, Silva M, Chen ZJ, Neves N, Viegas W, Pikaard CS (2004) A concerted DNA methylation/histone methylation switch regulates rRNA gene dosage control and nucleolar dominance. Mol Cell 13:599–609

    Article  PubMed  CAS  Google Scholar 

  • Lewis MS, Pikaard DJ, Nasrallah M, Doelling JH, Pikaard CS (2007) Locus-specific ribosomal RNA gene silencing in nucleolar dominance. PLoS One 2:e815

    Article  PubMed  Google Scholar 

  • Lukens LN, Pires JC, Leon E, Vogelzang R, Oslach L, Osborn T (2006) Patterns of sequence loss and cytosine methylation within a population of newly resynthesized Brassica napus allopolyploids. Plant Physiol 140:336–348

    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 

  • Madlung A, Tyagi AP, Watson B, Jiang H, Kagochi T, Doerge RW, Martienssen R, Comai L (2005) Genomic changes in synthetic Arabidopsis polyploids. Plant J 41:221–230

    Article  PubMed  CAS  Google Scholar 

  • McClintock B (1984) The significance of responses of the genome to challenge. Science 226:792–801

    Article  PubMed  CAS  Google Scholar 

  • Mirouze M, Reinders J, Bucher E, Nishimura T, Schneeberger K, Ossowski S, Cao J, Weigel D, Paszkowski J, Mathieu O (2009) Selective epigenetic control of retrotransposition in Arabidopsis. Nature 461:427–430

    Article  PubMed  CAS  Google Scholar 

  • Miura A, Yonebayashi S, Watanabe K, Toyama T, Shimada H, Kakutani T (2001) Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis. Nature 411:212–214

    Article  PubMed  CAS  Google Scholar 

  • Nasrallah ME, Yogeeswaran K, Snyder S, Nasrallah JB (2000) Arabidopsis species hybrids in the study of species differences and evolution of amphiploidy in plants. Plant Physiol 124:1605–1614

    Article  PubMed  CAS  Google Scholar 

  • Nasrallah JB, Liu P, Sherman-Broyles S, Schmidt R, Nasrallah ME (2007) Epigenetic mechanisms for breakdown of self-incompatibility in interspecific hybrids. Genetics 175:1965–1973

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Parisod C, Alix K, Just J, Petit M, Sarilar V, Mhiri C, Ainouche M, Chalhoub B, Glandbastien MA (2010) Impact of transposable elements on the organization and function of allopolyploid genomes. New Phytol 186:37–45

    Article  PubMed  CAS  Google Scholar 

  • Preuss SB, Costa-Nunes P, Tucker S, Pontes O, Lawrence RJ, Mosher R, Kasschau KD, Carrington JC, Baulcombe DC, Viegas W, Pikaard CS (2008) Multimegabase silencing in nucleolar dominance involves siRNA-directed DNA methylation and specific methylcytosine-binding proteins. Mol Cell 32:673–684

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Rapp RA, Udall JA, Wendel JF (2009) Genomic expression dominance in allopolyploids. BMC Biol 7:18

    PubMed  Google Scholar 

  • Singer T, Yordan C, Martienssen RA (2001) Robertson’s Mutator transposons in A. thaliana are regulated by the chromatin-remodeling gene Decrease in DNA Methylation (DDM1). Genes Dev 15:591–602

    Article  PubMed  CAS  Google Scholar 

  • Slotkin RK, Vaughn M, Borges F, Tanurdzić M, Becker JD, Feijó JA, Martienssen RA (2009) Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136:461–472

    Article  PubMed  CAS  Google Scholar 

  • Tsukahara S, Kobayashi A, Kawabe A, Mathieu O, Miura A, Kakutani T (2009) Bursts of retrotransposition reproduced in Arabidopsis. Nature 461:423–426

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Dr. Tetsuji Kakutani because this work originally started in his laboratory at National Institute of Genetics. We thank Dr. Candice Sheldon and Dr. Michael Groszmann for critical comments on the manuscript and Dr. Masahiro Fujita for his technical advice. This work is supported by Research Fellowship of the Japan Society for the Promotion of Science (JSPS) for Young Scientists and Excellent Young Researcher Overseas Visit Program of the JSPS to R. Fujimoto.

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Correspondence to Ryo Fujimoto.

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Microarray data have been deposited with GEO under GSE23318.

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11103_2011_9820_MOESM1_ESM.ppt

Figure S1. Scatter plot of relative signal intensity. Relative signal intensity of each spot from 6 experiments was plotted. Two lines, #39-1 and #39-2, of the artificially synthesized amphidiploid between A. thaliana and A. halleri had highly correlated expression levels (shown in bold letters). Two lines, #77-1 and #77-2, of the artificially synthesized amphidiploid between A. thaliana and A. lyrata also had highly correlated expression levels (shown in bold letters). At–Al Hyb, hybrid between A. thaliana and A. lyrata; At–Ah Hyb, hybrid between A. thaliana and A. halleri. MPV At–Ah, mid parent value between A. thaliana and A. halleri; MPV At–Al, mid parent value between A. thaliana and A. lyrata; r, correlation coefficient. Supplementary material 1 (PPT 195 kb)

11103_2011_9820_MOESM2_ESM.ppt

Figure S2. GO classification. The ratio of the up- and down- regulated genes in At–Al hybrid detected by perfect match probeset. The relative ratios were calculated by dividing the percentage of all annotated genes in A. thaliana. Supplementary material 2 (PPT 88 kb)

11103_2011_9820_MOESM3_ESM.ppt

Figure S3. Verification of four transposons detected in microarrays (Array data) by RT-PCR. At, A. thaliana; Al, A. lyrata; Ah, A. halleri; AtAl, hybrid between A. thaliana and A. lyrata; AtAh, hybrid between A. thaliana, and A. halleri. Right panels are the results of PCR using genomic DNA as a template. Supplementary material 3 (PPT 103 kb)

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Supplementary material 11 (DOC 1,125 kb)

Supplementary material 12 (DOC 95 kb)

Supplementary material 13 (DOC 53 kb)

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Fujimoto, R., Taylor, J.M., Sasaki, T. et al. Genome wide gene expression in artificially synthesized amphidiploids of Arabidopsis . Plant Mol Biol 77, 419 (2011). https://doi.org/10.1007/s11103-011-9820-y

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