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Heritable gene expression differences between apomictic clone members in Taraxacum officinale: Insights into early stages of evolutionary divergence in asexual plants

. 2016 Mar 08 ; 17 () : 203. [epub] 20160308

Language English Country England, Great Britain Media electronic

Document type Journal Article, Research Support, Non-U.S. Gov't

Links

PubMed 26956152
PubMed Central PMC4782324
DOI 10.1186/s12864-016-2524-6
PII: 10.1186/s12864-016-2524-6
Knihovny.cz E-resources

BACKGROUND: Asexual reproduction has the potential to enhance deleterious mutation accumulation and to constrain adaptive evolution. One source of mutations that can be especially relevant in recent asexuals is activity of transposable elements (TEs), which may have experienced selection for high transposition rates in sexual ancestor populations. Predictions of genomic divergence under asexual reproduction therefore likely include a large contribution of transposable elements but limited adaptive divergence. For plants empirical insight into genome divergence under asexual reproduction remains limited. Here, we characterize expression divergence between clone members of a single apomictic lineage of the common dandelion (Taraxacum officinale) to contribute to our knowledge of genome evolution under asexuality. RESULTS: Using RNA-Seq, we show that about one third of heritable divergence within the apomictic lineage is driven by TEs and TE-related gene activity. In addition, we identify non-random transcriptional differences in pathways related to acyl-lipid and abscisic acid metabolisms which might reflect functional divergence within the apomictic lineage. We analyze SNPs in the transcriptome to assess genetic divergence between the apomictic clone members and reveal that heritable expression differences between the accessions are not explained simply by genome-wide genetic divergence. CONCLUSION: The present study depicts a first effort towards a more complete understanding of apomictic plant genome evolution. We identify abundant TE activity and ecologically relevant functional genes and pathways affecting heritable within-lineage expression divergence. These findings offer valuable resources for future work looking at epigenetic silencing and Cis-regulation of gene expression with particular emphasis on the effects of TE activity on asexual species' genome.

See more in PubMed

Otto SP. The evolutionary enigma of sex. Am Nat. 2009;174(Suppl 1):S1–S14. doi: 10.1086/599084. PubMed DOI

The Angiosperm Phylogeny Group An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II. Bot J Linn Soc. 2003;141:399–436. doi: 10.1046/j.1095-8339.2003.t01-1-00158.x. DOI

Baker H. Characteristics and modes of origin of weeds. In: Baker HG, Stebbins GL, editors. The Genetics of colonizing species. New York: Academic; 1965. pp. 147–168.

Peck JR, Yearsley JM, Waxman D. Explaining the geographic distributions of sexual and asexual populations. Nature. 1998;391:889–892. doi: 10.1038/36099. DOI

Hamilton WD, Axelrod R, Tanese R. Sexual reproduction as an adaptation to resist parasites (a review) Proc Natl Acad Sci. 1990;87:3566–3573. doi: 10.1073/pnas.87.9.3566. PubMed DOI PMC

Neiman M, Hehman G, Miller JT, Logsdon JM, Taylor DR. Accelerated mutation accumulation in asexual lineages of a freshwater snail. Mol Biol Evol. 2010;27:954–963. doi: 10.1093/molbev/msp300. PubMed DOI PMC

Tucker AE, Ackerman MS, Eads BD, Xu S, Lynch M. Population-genomic insights into the evolutionary origin and fate of obligately asexual Daphnia pulex. Proc Natl Acad Sci. 2013;110:15740–15745. doi: 10.1073/pnas.1313388110. PubMed DOI PMC

Nogler G. Gametophytic apomixis. In: Johri BM, editor. Embryology of Angiosperms. Berlin: Springer; 1984. p. 475.

Grossniklaus U, Nogler GA, van Dijk PJ. How to avoid sex: the genetic control of gametophytic apomixis. Plant Cell. 2001;13:1491–1498. doi: 10.1105/tpc.13.7.1491. PubMed DOI PMC

Koltunow AM, Grossniklaus U. Apomixis: a developmental perspective. Annu Rev Plant Biol. 2003;54:547–574. doi: 10.1146/annurev.arplant.54.110901.160842. PubMed DOI

Comai L. The advantages and disadvantages of being polyploid. Nat Rev Genet. 2005;6:836–846. doi: 10.1038/nrg1711. PubMed DOI

Rushworth CA, Song B-H, Lee C-R, Mitchell-Olds T. Boechera, a model system for ecological genomics. Mol Ecol. 2011;20:4843–4857. doi: 10.1111/j.1365-294X.2011.05340.x. PubMed DOI PMC

Adams KL. Evolution of duplicate gene expression in polyploid and hybrid plants. J Hered. 2007;98:136–141. doi: 10.1093/jhered/esl061. PubMed DOI

Otto SP. The evolutionary consequences of polyploidy. Cell. 2007;131:452–462. doi: 10.1016/j.cell.2007.10.022. PubMed DOI

Richards AJ. Apomixis in flowering plants: an overview. Philos Trans R Soc B Biol Sci. 2003;358:1085–1093. doi: 10.1098/rstb.2003.1294. PubMed DOI PMC

Finnigan GC, Hanson-Smith V, Stevens TH, Thornton JW. Evolution of increased complexity in a molecular machine. Nature. 2012;481:360–364. PubMed PMC

Mau M, Lovell JT, Corral JM, Kiefer C, Koch MA, Aliyu OM, Sharbel TF. Hybrid apomicts trapped in the ecological niches of their sexual ancestors. Proc Natl Acad Sci. 2015;112:E2357–65. PubMed PMC

Aliyu OM, Seifert M, Corral JM, Fuchs J, Sharbel TF. Copy number variation in transcriptionally active regions of sexual and apomictic Boechera demonstrates independently derived apomictic lineages. Plant Cell. 2013;25:3808–3823. doi: 10.1105/tpc.113.113860. PubMed DOI PMC

Pellino M, Hojsgaard D, Schmutzer T, Scholz U, Hörandl E, Vogel H, Sharbel TF. Asexual genome evolution in the apomictic Ranunculus auricomus complex: examining the effects of hybridization and mutation accumulation. Mol Ecol. 2013;22:5908–5921. doi: 10.1111/mec.12533. PubMed DOI

Hollister JD, Greiner S, Wang W, Wang J, Zhang Y, Wong GK-S, Wright SI, Johnson MTJ. Recurrent loss of sex is associated with accumulation of deleterious mutations in Oenothera. Mol Biol Evol. 2014;32(4):896–905. PubMed

Stapley J, Santure AW, Dennis SR. Transposable elements as agents of rapid adaptation may explain the genetic paradox of invasive species. Mol Ecol. 2015;24(9):2241–2252. doi: 10.1111/mec.13089. PubMed DOI

Mirouze M, Paszkowski J. Epigenetic contribution to stress adaptation in plants. Curr Opin Plant Biol. 2011;14:267–274. doi: 10.1016/j.pbi.2011.03.004. PubMed DOI

Slotkin RK, Nuthikattu S, Jiang N. The Impact of transposable elements on gene and genome evolution. In: Wendel JF, Greilhuber J, Dolezel J, Leitch IJ, editors. Plant Genome Diversity. Vienna: Springer; 2012. pp. 35–58.

Wright S, Finnegan D. Genome evolution. Sex and the transposable element. Curr Biol. 2001;11:R296–R299. doi: 10.1016/S0960-9822(01)00168-3. PubMed DOI

Arkhipova I, Meselson M. Deleterious transposable elements and the extinction of asexuals. Bioessays. 2005;27:76–85. doi: 10.1002/bies.20159. PubMed DOI

Tas ICQ, van Dijk PJ. Crosses between sexual and apomictic dandelions (Taraxacum). I. The inheritance of apomixis. Heredity. 1999;83:707–714. doi: 10.1046/j.1365-2540.1999.00619.x. PubMed DOI

Van Dijk PJ. Ecological and evolutionary opportunities of apomixis: insights from Taraxacum and Chondrilla. Philos Trans R Soc B Biol Sci. 2003;358:1113–1121. doi: 10.1098/rstb.2003.1302. PubMed DOI PMC

Verhoeven KJF, Van Dijk PJ, Biere A. Changes in genomic methylation patterns during the formation of triploid asexual dandelion lineages. Mol Ecol. 2010;19:315–324. doi: 10.1111/j.1365-294X.2009.04460.x. PubMed DOI

Verhoeven KJF, Jansen JJ, van Dijk PJ, Biere A. Stress-induced DNA methylation changes and their heritability in asexual dandelions. New Phytol. 2010;185:1108–1118. doi: 10.1111/j.1469-8137.2009.03121.x. PubMed DOI

Kirschner J, Oplaat C, Verhoeven KJF, Uhlemann I, Travnicek B, Rasanen J, Zeisek V, Wislchut RA, Stepanek J. Two sides of the coin: Taxonomic identity of oligoclonal agamospermous microspecies versus their microsatellite characterization. Preslia. In press

Rogstad SH. Saturated NaCl-CTAB solution as a means of field preservation of leaves for DNA analyses. Taxon. 1992;41:701–708. doi: 10.2307/1222395. DOI

Vijverberg K, Van Der Hulst RGM, Lindhout P, Van Dijk PJ. A genetic linkage map of the diplosporous chromosomal region in Taraxacum officinale (common dandelion; Asteraceae) TAG Theor Appl Genet Theor Angew Genet. 2004;108:725–732. doi: 10.1007/s00122-003-1474-y. PubMed DOI

Falque M, Keurentjes J, Bakx-Schotman JMT, Van Dijk PJ. Development and characterization of microsatellite markers in the sexual-apomictic complex Taraxacum officinale (dandelion) Theor Appl Genet. 1998;97:283–292. doi: 10.1007/s001220050897. DOI

Vašut RJ, Van Dijk PJ, Falque M, Trávníček B, De Jong JH. Development and characterization of nine new microsatellite markers in Taraxacum (Asteraceae) Mol Ecol Notes. 2004;4:645–648. doi: 10.1111/j.1471-8286.2004.00760.x. DOI

Gustafsson Å. Apomixis in higher plants. I. The mechanism of apomixis. Lunds Univ Årsskr. 1946;42:1–67.

Grimanelli D, Leblanc O, Perotti E, Grossniklaus U. Developmental genetics of gametophytic apomixis. Trends Genet. 2001;17:597–604. doi: 10.1016/S0168-9525(01)02454-4. PubMed DOI

Jiang L, Schlesinger F, Davis CA, Zhang Y, Li R, Salit M, Gingeras TR, Oliver B. Synthetic spike-in standards for RNA-seq experiments. Genome Res. 2011;21:1543–51. PubMed PMC

Baker SC, Bauer SR, Beyer RP, Brenton JD, Bromley B, Burrill J, Causton H, Conley MP, Elespuru R, Fero M, Foy C, Fuscoe J, Gao X, Gerhold DL, Gilles P, Goodsaid F, Guo X, Hackett J, Hockett RD, Ikonomi P, Irizarry RA, Kawasaki ES, Kaysser-Kranich T, Kerr K, Kiser G, Koch WH, 562 Lee KY, Liu C, Liu ZL, Lucas A, et al. The External RNA Controls Consortium: a progress report. Nat Methods. 2005;2:731–4. PubMed

Aronesty E. ea-utils: “Command-line tools for processing biological sequencing data.” 2011. Http://code.google.com/p/ea-utils. Accessed Feb 2014.

Van Gurp TP, McIntyre LM, Verhoeven KJF. Consistent errors in first strand cDNA due to random hexamer mispriming. Plos ONE. 2013;8:e85583. doi: 10.1371/journal.pone.0085583. PubMed DOI PMC

Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, Couger MB, Eccles D, Li B, Lieber M, macmanes MD, Ott M, Orvis J, Pochet N, Strozzi F, Weeks N, Westerman R, William T, Dewey CN, Henschel R, leduc RD, Friedman N, Regev A. De novo transcript sequence reconstruction from RNA-Seq: reference generation and analysis with Trinity. Nat Protoc. 2013;8:1494–512. PubMed PMC

Götz S, García-Gómez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ, Robles M, Talón M, Dopazo J Conesa A. High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res. 2008;36:3420–35. PubMed PMC

Blüthgen N, Brand K, Cajavec B, Swat M, Herzel H, Beule D. Biological profiling of gene groups utilizing Gene Ontology. Genome Inform Int Conf Genome Inform. 2005;16:106–115. PubMed

Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009;10:R25. doi: 10.1186/gb-2009-10-3-r25. PubMed DOI PMC

Li B, Dewey CN. RSEM: Accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics. 2011;12:323. doi: 10.1186/1471-2105-12-323. PubMed DOI PMC

Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010;11:R106. doi: 10.1186/gb-2010-11-10-r106. PubMed DOI PMC

Bourgon R, Gentleman R, Huber W. Independent filtering increases detection power for high-throughput experiments. Proc Natl Acad Sci U S A. 2010;107:9546–9551. doi: 10.1073/pnas.0914005107. PubMed DOI PMC

Benjamini Y, Hochberg Y. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. J R Stat Soc Ser B Methodol. 1995;57:289–300.

Peakall R, Smouse PE. Genalex 6.5: Genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics. 2012;28:2537–2539. doi: 10.1093/bioinformatics/bts460. PubMed DOI PMC

Katari MS, Nowicki SD, Aceituno FF, Nero D, Kelfer J, Thompson LP, Cabello JM, Davidson RS, Goldberg AP, Shasha DE, Coruzzi GM, Gutiérrez RA. Virtualplant: A software platform to support systems biology research. Plant Physiol. 2010;152:500–15. PubMed PMC

Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinforma Oxf Engl. 2009;25:1754–1760. doi: 10.1093/bioinformatics/btp324. PubMed DOI PMC

Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. 1000 Genome Project Data Processing Subgroup. The Sequence Alignment/Map format and Samtools. Bioinforma Oxf Engl. 2009;25:2078–9. PubMed PMC

Quinlan AR, Hall IM. Bedtools: A flexible suite of utilities for comparing genomic features. Bioinforma Oxf Engl. 2010;26:841–842. doi: 10.1093/bioinformatics/btq033. PubMed DOI PMC

R Core Team . R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing; 2013.

Hamming R. Error detecting and error correcting codes. Bell Syst Tech J. 1950;29:147–160. doi: 10.1002/j.1538-7305.1950.tb00463.x. DOI

Paradis E, Claude J, Strimmer K. APE: Analyses of Phylogenetics and Evolution in R language. Bioinforma Oxf Engl. 2004;20:289–290. doi: 10.1093/bioinformatics/btg412. PubMed DOI

Müllner D. Fastcluster: Fast Hierarchical, Agglomerative Clustering Routines for R and Python. J Stat Soft. 2013;53(9):1–18. doi: 10.18637/jss.v053.i09. DOI

Bonnet E, de Peer YV. Zt: A Sofware Tool for Simple and Partial Mantel Tests. J Stat Soft. 2002;7(10):1–12. doi: 10.18637/jss.v007.i10. DOI

Aziz RK, Breitbart M, Edwards RA. Transposases are the most abundant, most ubiquitous genes in nature. Nucleic Acids Res. 2010;38:4207–4217. doi: 10.1093/nar/gkq140. PubMed DOI PMC

Lee TI, Young RA. Transcription of eukaryotic protein-coding genes. Annu Rev Genet. 2000;34:77–137. doi: 10.1146/annurev.genet.34.1.77. PubMed DOI

Li-Beisson Y, Shorrosh B, Beisson F, Andersson MX, Arondel V, Bates PD, Baud S, Bird D, Debono A, Durrett TP, Franke RB, Graham IA, Katayama K, Kelly AA, Larson T, Markham JE, Miquel M, Molina I, Nishida I, Rowland O, Samuels L, Schmid KM, Wada H, Welti R, Xu C, Zallot R, Ohlrogge. Acyl-lipid metabolism. Arab Book Am Soc Plant Biol. 2013;11:e0161. PubMed PMC

Gillmor CS, Lukowitz W, Brininstool G, Sedbrook JC, Hamann T, Poindexter P, Somerville C. Glycosylphosphatidylinositol-anchored proteins are required for cell wall synthesis and morphogenesis in Arabidopsis. Plant Cell. 2005;17:1128–40. PubMed PMC

Posé D, Castanedo I, Borsani O, Nieto B, Rosado A, Taconnat L, Ferrer A, Dolan L, Valpuesta V, Botella MA. Identification of the Arabidopsis dry2/sqe1-5 mutant reveals a central role for sterols in drought tolerance and regulation of reactive oxygen species. Plant J Cell Mol Biol. 2009;59:63–76. PubMed

Kejnovsky E, Hawkins JS, Feschotte C. Plant Transposable Elements: Biology and Evolution. In: Wendel JF, Greilhuber J, Dolezel J, Leitch IJ, editors. Plant Genome Diversity. Vienna: Springer; 2012. pp. 17–34.

Zilberman D, Gehring M, Tran RK, Ballinger T, Henikoff S. Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet. 2007;39:61–69. doi: 10.1038/ng1929. PubMed DOI

Grandbastien M-A, Audeon C, Bonnivard E, Casacuberta JM, Chalhoub B, Costa A-PP, Le QH, Melayah D, Petit M, Poncet C, Tam SM, Van Sluys M-A, Mhiri C. Stress activation and genomic impact of Tnt1 retrotransposons in Solanaceae. Cytogenet Genome Res. 2005;110:229–41. PubMed

Parisod C, Senerchia N. Responses of Transposable Elements to Polyploidy. In: Grandbastien M-A, Casacuberta JM, editors. Plant Transposable Elements. Heidelberg: Springer Berlin; 2012. pp. 147–168.

Jiang N, Bao Z, Zhang X, Hirochika H, Eddy SR, McCouch SR, Wessler SR. An active DNA transposon family in rice. Nature. 2003;421:163–7. PubMed

Wang Q, Dooner HK. Remarkable variation in maize genome structure inferred from haplotype diversity at the bz locus. Proc Natl Acad Sci. 2006;103:17644–17649. doi: 10.1073/pnas.0603080103. PubMed DOI PMC

Glémin S, Galtier N. Genome evolution in outcrossing versus selfing versus asexual species. Methods Mol Biol Clifton NJ. 2012;855:311–335. doi: 10.1007/978-1-61779-582-4_11. PubMed DOI

Kraaijeveld K, Zwanenburg B, Hubert B, Vieira C, De Pater S, Van Alphen J, Den Dunnen Jt, De Knijff P. Transposon proliferation in an asexual parasitoid. Mol Ecol. 2012;21:3898–906. PubMed

Bui QT, Grandbastien M-A. LTR Retrotransposons as Controlling Elements of Genome Response to Stress? In: Grandbastien M-A, Casacuberta JM, editors. Plant Transposable Elements. Heidelberg: Springer Berlin; 2012. pp. 273–296.

Ito H, Yoshida T, Tsukahara S, Kawabe A. Evolution of the ONSEN retrotransposon family activated upon heat stress in Brassicaceae. Gene. 2013;518:256–261. doi: 10.1016/j.gene.2013.01.034. PubMed DOI

Makarevitch I, Waters AJ, West PT, Stitzer M, Hirsch CN, Ross-Ibarra J, Springer NM. Transposable elements contribute to activation of maize genes in response to abiotic stress. Plos Genet. 2015;11. http://www.ncbi.nlm.nih.gov/pubmed/25569788. PubMed PMC

Grandbastien MA, Spielmann A, Caboche M. Tnt1, a mobile retroviral-like transposable element of tobacco isolated by plant cell genetics. Nature. 1989;337:376–380. doi: 10.1038/337376a0. PubMed DOI

Gould SJ, Vrba ES. Exaptation; a missing term in the science of form. Paleobiology. 1982;8:4–15. doi: 10.1017/S0094837300004310. DOI

Hoen DR, Bureau TE. Transposable Element Exaptation in Plants. In: Grandbastien M-A, Casacuberta JM, editors. Plant Transposable Elements. Heidelberg: Springer Berlin; 2012. pp. 219–251.

Hudson ME, Lisch DR, Quail PH. The FHY3 and FAR1 genes encode transposase-related proteins involved in regulation of gene expression by the phytochrome A-signaling pathway. Plant J. 2003;34:453–471. doi: 10.1046/j.1365-313X.2003.01741.x. PubMed DOI

Lin R, Ding L, Casola C, Ripoll DR, Feschotte C, Wang H. Transposase-Derived Transcription Factors Regulate Light Signaling in Arabidopsis. Science. 2007;318:1302–1305. doi: 10.1126/science.1146281. PubMed DOI PMC

Oh D-H, Hong H, Lee SY, Yun D-J, Bohnert HJ, Dassanayake M. Genome structures and transcriptomes signify niche adaptation for the multiple-ion-tolerant extremophyte Schrenkiella parvula. Plant Physiol. 2014;164:2123–2138. doi: 10.1104/pp.113.233551. PubMed DOI PMC

Aharoni A, Dixit S, Jetter R, Thoenes E, van Arkel G, Pereira A. The SHINE clade of AP2 domain transcription factors activates wax biosynthesis, alters cuticle properties, and confers drought tolerance when overexpressed in Arabidopsis. Plant Cell. 2004;16:2463–2480. doi: 10.1105/tpc.104.022897. PubMed DOI PMC

Schaller A, Stintzi A. Enzymes in jasmonate biosynthesis - structure, function, regulation. Phytochemistry. 2009;70:1532–1538. doi: 10.1016/j.phytochem.2009.07.032. PubMed DOI

Mosblech A, Feussner I, Heilmann I. Oxylipins: Structurally diverse metabolites from fatty acid oxidation. Plant Physiol Biochem. 2009;47:511–517. doi: 10.1016/j.plaphy.2008.12.011. PubMed DOI

Verhage A, Vlaardingerbroek I, Raaymakers C, Van Dam NM, Dicke M, Van Wees SCM, Pieterse CMJ. Rewiring of the jasmonate signaling pathway in Arabidopsis during insect herbivory. Front Plant Sci. 2011;2. http://journal.frontiersin.org/article/10.3389/fpls.2011.00047/abstract. PubMed DOI PMC

Schwartz S, Zeevaart JD. Abscisic acid biosynthesis and metabolism. In: Davies P, editor. Plant Hormones. Netherlands: Springer; 2010. pp. 137–155.

Xiong L, Lee H, Ishitani M, Zhu J-K. Regulation of osmotic stress-responsive gene expression by thelos6/ABA1 locus in Arabidopsis. J Biol Chem. 2002;277:8588–8596. doi: 10.1074/jbc.M109275200. PubMed DOI

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