Gene expression variation in natural populations of hexaploid and allododecaploid Spartina species (Poaceae)
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Allopolyploidy is a peculiar process entailing the cohabitation of two (or more) divergent genomes. Consequences on plant genomes are varied and can utlimately alter gene expression and regulatory interactions. Most studies have explored polyploid expression evolution in experimental controlled conditions. Here, we analyzed global gene expression variation in natural populations of the Spartina polyploid complex including hexaploid parental species (S. maritima and S. alterniflora), two F1 hybrids (S. × townsendii and S. × neyrautii) and the allododecaploid S. anglica. In situ sampling and quantitative PCR were performed for comparing global expression of candidate genes involved in responses to abiotic stresses, lignin and cellulose metabolisms between five Spartina taxa. Illumina sequencing datasets and dedicated bioinformatic pipelines were employed to explore sequence heterogeneity in these highly duplicated genomes. Levels of gene expression were significantly higher in S. alterniflora (compared to the other hexaploid parent S. maritima) for seven of the analyzed genes. Effects of both hybridization and polyploidization are detected and consistent with previous global transcriptome analyses performed on Spartina plants grown in controlled conditions. Duplicated copies present in the hybrids and the allododecaploid were successfully assigned to either one of the parental genomes. Phylogenetic analyses identified for each of the parental hexaploid species, the presence of two distinct clades including two or more expressed copies. We provide here a comprehensive gene expression study based on individuals sampled in their natural habitat and detected the superimposed effect of environmental heterogeneity, hybridization and allopolyploidy.
KeywordsAllopolyploidy Gene expression Haplotype detection Hybridization Quantitative PCR Spartina
This work was supported by the International Associated Laboratory “Ecological Genomics of Polyploidy” supported by CNRS (INEE, UMR CNRS 6553 Ecobio), University of Rennes 1, Iowa State University (Ames, USA), and the Partner University Funds (to M. A., A. S.). The analyses benefited from the Molecular Ecology (UMR CNRS 6553 Ecobio) and Genouest (Bioinformatics) facilities. Authors J. Ferreira de Carvalho benefited from a PhD grant (ARED EVOSPART) from the Regional Council of Brittany and J. Boutte from a PhD scholarship from the University of Rennes 1. We thank two anonymous reviewers for helpful comments and suggestions on the manuscript.
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Conflict of interest
The authors declare that they have no conflict of interest.
Human and animal rights
This research does not involve human participants or animals.
- Baumel A, Ainouche ML, Misset MT, Gourret J-P, Bayer RJ (2003) Genetic evidence for hybridization between the native Spartina maritima and the introduced Spartina alterniflora (Poaceae) in South-West France: Spartina × neyrautii re-examined. Pl Syst Evol 237:87–97. doi: 10.1007/s00606-002-0251-8 CrossRefGoogle Scholar
- Boutte J, Aliaga B, Lima O, Ferreira de Carvalho J, Ainouche A, Macas J, Rousseau-Gueutin M, Coriton O, Ainouche M, Salmon A (2015) Haplotype detection from next-generation sequencing in high-ploidy-level species: 45S rDNA gene copies in the hexaploid Spartina maritima. Genes Genomes Genet 6:29–40. doi: 10.1534/g3.115.023242 Google Scholar
- Boutte J, Ferreira de Carvalho J, Rousseau-Gueutin M, Poulain J, Da Silva C, Wincker P, Ainouche M, Salmon A (2016) Reference transcriptomes and detection of duplicated copies in hexaploid and allododecaploid Spartina species (Poaceae). Genome Biol Evol 8:3030–3044. doi: 10.1093/gbe/evw209 PubMedCrossRefGoogle Scholar
- Chagué V, Just J, Mestiri I, Balzergue S, Tanguy A-M, Huneau C, Huteau V, Belcram H, Coriton O, Jahier J, Chalhoub B (2010) Genome-wide gene expression changes in genetically stable synthetic and natural wheat allohexaploids. New Phytol 187:1181–1194. doi: 10.1111/j.1469-8137.2010.03339.x PubMedCrossRefGoogle Scholar
- Ferreira de Carvalho J, Poulain J, Da Silva C, Wincker P, Michon-Coudouel S, Dheilly A, Naquin D, Boutte J, Salmon A, Ainouche M (2013) Transcriptome de novo assembly from next-generation sequencing and comparative analyses in the hexaploid salt marsh species Spartina maritima and Spartina alterniflora (Poaceae). Heredity 110:181–193. doi: 10.1038/hdy.2012.76 PubMedCrossRefGoogle Scholar
- Foucaud J (1897) Un Spartina inédit. Ann Soc Sci Nat Charente-Infér 32:220–222Google Scholar
- Groves H, Groves J (1880) Spartina townsendii. Nobis 1:37Google Scholar
- Hall T (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Res 41:95–98Google Scholar
- Hervé M (2014) RVAideMemoire: diverse basic statistical and graphical functions. R package version 09-32Google Scholar
- Huska D, Leitch IJ, Ferreira de Carvalho J, Leitch AR, Salmon A, Malika A, Kovarik A (2016) Persistence, dispersal and genetic evolution of recently formed Spartina homoploid hybrids and allopolyploids in Southern England. Biol Invas 18:2137–2151. doi: 10.1007/s10530-015-0956-6 CrossRefGoogle Scholar
- Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. doi: 10.1093/bioinformatics/bts199 PubMedPubMedCentralCrossRefGoogle Scholar
- Li B, Liao C, Zhang X, Chen H, Wang Q, Chen Z, Gan X, Wu J, Zhao B, Ma Z, Cheng X, Jiang L, Chen J (2009a) Spartina alterniflora invasions in the Yangtze River estuary, China: an overview of current status and ecosystem effects. Ecol Eng 35:511–520. doi: 10.1016/j.ecoleng.2008.05.013 CrossRefGoogle Scholar
- Mobberley DG (1956) Taxonomy and distribution of the genus Spartina. Iowa State Coll J Sci 30:471–574Google Scholar
- R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
- Rousseau-Gueutin M, Bellot S, Martin GE, Boutte J, Chelaifa H, Lima O, Michon-Coudouel S, Naquin D, Salmon A, Ainouche K, Ainouche M (2015) The chloroplast genome of the hexaploid Spartina maritima (Poaceae, Chloridoideae): comparative analyses and molecular dating. Molec Phylogen Evol 93:5–16. doi: 10.1016/j.ympev.2015.06.013 CrossRefGoogle Scholar
- Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Meth Molec Biol 132:365–386Google Scholar
- Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Sinauer Associates, SunderlandGoogle Scholar
- Tate JA, Ni Z, Scheen A-C, Koh J, Gilbert CA, Lefkowitz D, Chen ZJ, Soltis PS, Soltis DE (2006) Evolution and expression of homeologous loci in Tragopogon miscellus (Asteraceae), a recent and reciprocally formed allopolyploid. Genetics 173:1599–1611. doi: 10.1534/genetics.106.057646 PubMedPubMedCentralCrossRefGoogle Scholar
- Vandenbussche M, Zethof J, Souer E, Koes R, Tornielli GB, Pezzotti M, Ferrario S, Angenent GC, Gerats T (2003) Toward the analysis of the petunia MADS box gene family by reverse and forward transposon insertion mutagenesis approaches: B, C, and D floral organ identity functions require SEPALLATA-like MADS box genes in petunia. Pl Cell 15:2680–2693. doi: 10.1105/tpc.017376 CrossRefGoogle Scholar
- Yang Y, Ma C, Xu Y, Wei Q, Imtiaz M, Lan H, Gao S, Cheng L, Wang M, Fei Z, Hong B, Gao J (2014) A zinc finger protein regulates flowering time and abiotic stress tolerance in Chrysanthemum by modulating gibberellin biosynthesis. Pl Cell 26:2038–2054. doi: 10.1105/tpc.114.124867 CrossRefGoogle Scholar