Biological Invasions

, Volume 19, Issue 3, pp 875–893 | Cite as

Gene expression and drought response in an invasive thistle

  • Kathryn G. TurnerEmail author
  • Kristin A. Nurkowski
  • Loren H. Rieseberg
Original Paper


Though rapid phenotypic evolution has been observed in many invasive plant species, less is known about the associated genetic mechanisms. Some hypotheses invoke the evolution of trade-offs in resource allocation to explain phenotypic differences between the native and invaded ranges of a species. Alternately, invasive species may benefit from a generalist strategy and perform well in many environments. Identification of the molecular changes associated with successful invasions can offer clues regarding the mechanistic basis of such hypotheses, even in non-model organisms. To complement studies of phenotypic variation, we investigate gene expression during drought response that might underlie variation in drought tolerance between native and introduced populations of diffuse knapweed (Centaurea diffusa), and possibly contribute to invasion success. Using species-specific microarrays and tissue sampled under drought and control conditions at three time points, we identified genes whose expression either varied constitutively or responded to drought stress differently between ranges. Further, we functionally investigate these genes. Based on these data, invasive populations have constitutively higher levels of expression relating to energy production and lower levels of signal transduction expression relative to native populations. Under drought conditions, invasive populations may maintain energy production and react less strongly to drought than native populations, which may allow them to maintain fitness across moderate environmental variation. This supports the expectation of invasive populations consisting of generalist genotypes capable of fitness homeostasis, which may have facilitated the successful invasion of many environments in North America.


Centaurea diffusa Diffuse knapweed Invasion genetics Drought Trade-offs Gene expression Fitness homeostasis 



We thank A. Guggisberg and K. Hodgins for technical and experimental guidance, and J. Huang for collecting the array hybridization data. Feedback from Axios Review improved the quality of this manuscript. Funding provided by: US National Science Foundation Graduate Research Fellowship to KGT, Natural Sciences and Engineering Research Council of Canada Grant No. 353026 to LHR.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10530_2016_1308_MOESM1_ESM.docx (147 kb)
Supplementary material 1 (DOCX 147 kb)


  1. Alexa A, Rahnenführer J (2009) Gene set enrichment analysis with topGO. Available at
  2. Atkin OK, Macherel D (2009) The crucial role of plant mitochondria in orchestrating drought tolerance. Ann Bot 103:581–597CrossRefPubMedGoogle Scholar
  3. Baker HG, Stebbins GL (1965) The genetics of colonizing species: proceedings. Academic Press, CambridgeGoogle Scholar
  4. Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. arXiv:1406.5823 [stat]
  5. Blossey B, Notzold R (1995) Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. J Ecol 83:887–889CrossRefGoogle Scholar
  6. Bock DG, Caseys C, Cousens RD et al (2015) What we still don’t know about invasion genetics. Mol Ecol 24:2277–2297CrossRefPubMedGoogle Scholar
  7. Bolstad BM, Irizarry RA, Åstrand M, Speed TP (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19:185–193CrossRefPubMedGoogle Scholar
  8. Bossdorf O, Auge H, Lafuma L et al (2005) Phenotypic and genetic differentiation between native and introduced plant populations. Oecologia 144:1–11CrossRefPubMedGoogle Scholar
  9. Buswell JM, Moles AT, Hartley S (2011) Is rapid evolution common in introduced plant species? J Ecol 99:214–224CrossRefGoogle Scholar
  10. Butler DR, Landsberg JJ (1981) Respiration rates of apple trees, estimated by CO2-efflux measurements. Plant Cell Environ 4:153–159CrossRefGoogle Scholar
  11. Carvalho BS, Irizarry RA (2010) A framework for oligonucleotide microarray preprocessing. Bioinformatics 26:2363–2367CrossRefPubMedPubMedCentralGoogle Scholar
  12. Crawley MJ (2012) The R book. Wiley, West SussexCrossRefGoogle Scholar
  13. Dlugosch KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449CrossRefPubMedGoogle Scholar
  14. Felker-Quinn E, Schweitzer JA, Bailey JK (2013) Meta-analysis reveals evolution in invasive plant species but little support for evolution of increased competitive ability (EICA). Ecol Evol 3:739–751CrossRefPubMedPubMedCentralGoogle Scholar
  15. Feng YL, Lei YB, Wang RF, Callaway RM, Valiente-Banuet A (2009) Evolutionary tradeoffs for nitrogen allocation to photosynthesis versus cell walls in an invasive plant. Proc Natl Acad Sci 106:1853CrossRefPubMedPubMedCentralGoogle Scholar
  16. Flexas J, Galmes J, Ribas-Carbo M, Medrano H (2005) The effects of water stress on plant respiration. In: Lambers H, Ribas-Carbo M (eds) Plant respiration: advances in photosynthesis and respiration. Springer, Netherlands, pp 85–94CrossRefGoogle Scholar
  17. Ghashghaie J, Duranceau M, Badeck F-W et al (2001) δ13C of CO2 respired in the dark in relation to δ13C of leaf metabolites: comparison between Nicotiana sylvestris and Helianthus annuus under drought. Plant Cell Environ 24:505–515CrossRefGoogle Scholar
  18. Greuter W (2009) Compositae (pro parte majore). In: Greuter W & von Raab-Straube E (eds): Compositae. Euro+ med plantbase—the information resource for Euro-Mediterranean plant diversity. [WWW document] URL [Accessed 9 June 2013]
  19. Grossmann S, Bauer S, Robinson PN, Vingron M (2007) Improved detection of overrepresentation of gene-ontology annotations with parent–child analysis. Bioinformatics 23:3024–3031CrossRefPubMedGoogle Scholar
  20. Guggisberg A, Lai Z, Huang J, Rieseberg LH (2013) Transcriptome divergence between introduced and native populations of Canada thistle, Cirsium arvense. New Phytol 199:595–608CrossRefPubMedGoogle Scholar
  21. 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, Thomas W, Dewey CN, Henschel R, LeDuc RD, Friedman N, Regev A (2013) De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc 8:1494–1512Google Scholar
  22. Hahn MA, van Kleunen M, Müller-Schärer H (2012) Increased phenotypic plasticity to climate may have boosted the invasion success of polyploid Centaurea stoebe. PLoS ONE 7:e50284CrossRefPubMedPubMedCentralGoogle Scholar
  23. Hamrick JL, Godt MJW (1996) Effects of life history traits on genetic diversity in plant species. Philos Trans R Soc Lond. Ser B: Biol Sci 351:1291–1298CrossRefGoogle Scholar
  24. He W-M, Thelen GC, Ridenour WM, Callaway RM (2010) Is there a risk to living large? Large size correlates with reduced growth when stressed for knapweed populations. Biol Invasions 12:3591–3598CrossRefGoogle Scholar
  25. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978CrossRefGoogle Scholar
  26. Hodgins KA, Rieseberg L (2011) Genetic differentiation in life-history traits of introduced and native common ragweed (Ambrosia artemisiifolia) populations. J Evol Biol 24:2731–2749CrossRefPubMedGoogle Scholar
  27. Hodgins KA, Lai Z, Nurkowski K, Huang J, Rieseberg LH (2013) The molecular basis of invasiveness: differences in gene expression of native and introduced common ragweed (Ambrosia artemisiifolia) in stressful and benign environments. Mol Ecol 22:2496–2510CrossRefPubMedGoogle Scholar
  28. Hodgins KA, Bock DG, Hahn MA et al (2015) Comparative genomics in the Asteraceae reveals little evidence for parallel evolutionary change in invasive taxa. Mol Ecol 24:2226–2240CrossRefPubMedGoogle Scholar
  29. Hufbauer RA, Sforza R (2008) Multiple introductions of two invasive Centaurea taxa inferred from cpDNA haplotypes. Divers Distrib 14:252–261CrossRefGoogle Scholar
  30. Hufbauer RA, Facon B, Ravigné V et al (2012) Anthropogenically induced adaptation to invade (AIAI): contemporary adaptation to human-altered habitats within the native range can promote invasions. Evol Appl 5:89–101CrossRefPubMedGoogle Scholar
  31. Irizarry RA, Bolstad BM, Collin F et al (2003a) Summaries of affymetrix genechip probe level data. Nucleic Acids Res 31:e15–e15CrossRefPubMedPubMedCentralGoogle Scholar
  32. Irizarry RA, Hobbs B, Collin F et al (2003b) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4:249–264CrossRefPubMedGoogle Scholar
  33. Keller SR, Taylor DR (2008) History, chance and adaptation during biological invasion: separating stochastic phenotypic evolution from response to selection. Ecol Lett 11:852–866CrossRefPubMedGoogle Scholar
  34. Kuester A, Conner JK, Culley T, Baucom RS (2014) How weeds emerge: a taxonomic and trait-based examination using United States data. New Phytol 202:1055–1068CrossRefPubMedPubMedCentralGoogle Scholar
  35. Kumschick S, Hufbauer RA, Alba C, Blumenthal DM (2013) Evolution of fast-growing and more resistant phenotypes in introduced common mullein (Verbascum thapsus). J Ecol 101:378–387CrossRefGoogle Scholar
  36. Lachmuth S, Durka W, Schurr FM (2011) Differentiation of reproductive and competitive ability in the invaded range of Senecio inaequidens: the role of genetic Allee effects, adaptive and nonadaptive evolution. New Phytol 192:529–541CrossRefPubMedGoogle Scholar
  37. Lai Z, Gross BL, Yizou J, Rieseberg LH (2006) Microarray analysis reveals differential gene expression in hybrid sunflower species. Mol Ecol 15:1213CrossRefPubMedPubMedCentralGoogle Scholar
  38. Lai Z, Kane NC, Zou Y, Rieseberg LH (2008) Natural variation in gene expression between wild and weedy populations of Helianthus annuus. Genetics 179:1881CrossRefPubMedPubMedCentralGoogle Scholar
  39. Lai Z, Kane NC, Kozik A et al (2012) Genomics of Compositae weeds: EST libraries, microarrays, and evidence of introgression. Am J Bot 99:209–218CrossRefPubMedGoogle Scholar
  40. Lamesch P, Berardini TZ, Li D et al (2012) The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res 40:D1202–D1210CrossRefPubMedGoogle Scholar
  41. Lande R (2009) Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. J Evol Biol 22:1435–1446CrossRefPubMedGoogle Scholar
  42. Lande R (2015) Evolution of phenotypic plasticity in colonizing species. Mol Ecol 24:2038–2045CrossRefPubMedGoogle Scholar
  43. Lee CE, Gelembiuk GW (2008) Evolutionary origins of invasive populations. Evol Appl 1:427–448CrossRefPubMedPubMedCentralGoogle Scholar
  44. LeJeune KD, Seastedt TR (2001) Centaurea species: the forb that won the west. Conserv Biol 15:1568–1574CrossRefGoogle Scholar
  45. Marchand G, Huynh-Thu VA, Kane N, Arribat S, Varès D, Rengel D, Balzergue S, Rieseberg LH, Vincourt P, Geurts P, Vignes M, Langlade N (2014) Bridging physiological and evolutionary time scales in a gene regulatory network. New Phytol 203:685–696CrossRefPubMedGoogle Scholar
  46. Marrs RA, Sforza R, Hufbauer RA (2008) When invasion increases population genetic structure: a study with Centaurea diffusa. Biol Invasions 10:561–572CrossRefGoogle Scholar
  47. Mráz P, Španiel S, Keller A et al (2012) Anthropogenic disturbance as a driver of microspatial and microhabitat segregation of cytotypes of Centaurea stoebe and cytotype interactions in secondary contact zones. Ann Bot 110:615–627CrossRefPubMedPubMedCentralGoogle Scholar
  48. Nuzhdin SV, Wayne ML, Harmon KL, McIntyre LM (2004) Common pattern of evolution of gene expression level and protein sequence in Drosophila. Mol Biol Evol 21:1308–1317CrossRefPubMedGoogle Scholar
  49. Pavey SA, Collin H, Nosil P, Rogers SM (2010) The role of gene expression in ecological speciation. Ann N Y Acad Sci 1206:110–129CrossRefPubMedPubMedCentralGoogle Scholar
  50. Quartacci MF, Pinzino C, Sgherri C, Navari-Izzo F (1995) Lipid composition and protein dynamics in thylakoids of two wheat cultivars differently sensitive to drought. Plant Physiol 108:191–197CrossRefPubMedPubMedCentralGoogle Scholar
  51. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0Google Scholar
  52. Rengel D, Arribat S, Maury P et al (2012) A gene-phenotype network based on genetic variability for drought responses reveals key physiological processes in controlled and natural environments. PLoS ONE 7:e45249 (M Bendahmane, Ed,) CrossRefPubMedPubMedCentralGoogle Scholar
  53. Richards CL, Bossdorf O, Muth NZ, Gurevitch J, Pigliucci M (2006) Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecol Lett 9:981–993CrossRefPubMedGoogle Scholar
  54. Rizhsky L, Liang H, Mittler R (2002) The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiol 130:1143–1151CrossRefPubMedPubMedCentralGoogle Scholar
  55. Sheley RL, Jacobs JS, Carpinelli MF (1998) Distribution, biology, and management of diffuse knapweed (Centaurea diffusa) and spotted knapweed (Centaurea maculosa). Weed Technol 12:353–362Google Scholar
  56. Stewart CN, Tranel PJ, Horvath DP et al (2009) Evolution of weediness and invasiveness: charting the course for weed genomics. Weed Sci 57:451–462CrossRefGoogle Scholar
  57. Storey JD (2002) A direct approach to false discovery rates. J R Stat Soc: Ser B (Stat Methodol) 64:479–498CrossRefGoogle Scholar
  58. Thompson DJ, Stout DG (1991) Duration of the juvenile period in diffuse knapweed (Centaurea diffusa). Can J Bot 69:368–371CrossRefGoogle Scholar
  59. Todesco M, Balasubramanian S, Hu TT et al (2010) Natural allelic variation underlying a major fitness trade-off in Arabidopsis thaliana. Nature 465:632–636CrossRefPubMedPubMedCentralGoogle Scholar
  60. Toumi I, Gargouri M, Nouairi I et al (2008) Water stress induced changes in the leaf lipid composition of four grapevine genotypes with different drought tolerance. Biol Plant 52:161–164CrossRefGoogle Scholar
  61. Troyanskaya O, Cantor M, Sherlock G et al (2001) Missing value estimation methods for DNA microarrays. Bioinformatics 17:520–525CrossRefPubMedGoogle Scholar
  62. Turner KG, Hufbauer RA, Rieseberg LH (2014) Rapid evolution of an invasive weed. New Phytol 202:309–321CrossRefPubMedGoogle Scholar
  63. Turner KG, Fréville H, Rieseberg LH (2015) Adaptive plasticity and niche expansion in an invasive thistle. Ecol Evol 5:3183–3197CrossRefPubMedPubMedCentralGoogle Scholar
  64. Turner KG, Nurkowski KA, Rieseberg LH (2016) Data from: gene expression and drought response in an invasive thistle. Dryad Digit Repos. doi: 10.5061/dryad.r2k76 Google Scholar
  65. USDA NCRS (2014) Centaurea diffusa Lam. The PLANTS Database, National Plant Data Team. [WWW document] URL [Accessed 9 June 2014]
  66. Varone L, Gratani L (2015) Leaf respiration responsiveness to induced water stress in Mediterranean species. Environ Exp Bot 109:141–150CrossRefGoogle Scholar
  67. Warnes GR, Bolker B, Bonebakker L et al (2015) gplots: various R programming tools for plotting data. R package version 3.0.1.
  68. Whitehead A, Crawford DL (2006) Variation within and among species in gene expression: raw material for evolution. Mol Ecol 15:1197–1211CrossRefPubMedGoogle Scholar
  69. Whitney KD, Gabler CA (2008) Rapid evolution in introduced species, ‘invasive traits’ and recipient communities: challenges for predicting invasive potential. Divers Distrib 14:569–580CrossRefGoogle Scholar
  70. Whittall JB, Voelckel C, Kliebenstein DJ, Hodges SA (2006) Convergence, constraint and the role of gene expression during adaptive radiation: floral anthocyanins in Aquilegia. Mol Ecol 15:4645–4657CrossRefPubMedGoogle Scholar
  71. Yang SF, Hoffman NE (1984) Ethylene biosynthesis and its regulation in higher plants. Annual Review of Plant Physiology 35:155–189CrossRefGoogle Scholar
  72. Zenni RD, Lamy J-B, Lamarque LJ, Porté AJ (2014) Adaptive evolution and phenotypic plasticity during naturalization and spread of invasive species: implications for tree invasion biology. Biol Invasions 16:635–644CrossRefGoogle Scholar
  73. Zhu J-K (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Kathryn G. Turner
    • 1
    Email author
  • Kristin A. Nurkowski
    • 2
  • Loren H. Rieseberg
    • 2
    • 3
  1. 1.Department of Bioagricultural Sciences and Pest ManagementColorado State UniversityFort CollinsUSA
  2. 2.Department of Botany and Biodiversity Research CentreUniversity of British ColumbiaVancouverCanada
  3. 3.Department of BiologyIndiana UniversityBloomingtonUSA

Personalised recommendations