The molecular basis of invasiveness: Differences in gene expression of native and introduced common ragweed (Ambrosia artemisiifolia) in stressful and benign environments

Molecular Ecology

Volumn 22, Issue 9, 2013, Pages 2496-2510

  Hodgins, Kathryn A ^a   Lai, Zhao ^b   Nurkowski, Kristin ^a   Huang, Jie ^b   Rieseberg, Loren H ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b INDIANA UNIVERSITY   (United States)

Author keywords

Ambrosia artemisiifolia; common ragweed; gene expression; invasion biology; microarray; stress

Indexed keywords

MICROSATELLITE DNA;

ADAPTATION; ARTICLE; CLIMATE; ECOSYSTEM; EUROPE; GENE EXPRESSION; GENETIC VARIABILITY; GENETICS; GROWTH, DEVELOPMENT AND AGING; INTRODUCED SPECIES; MOLECULAR EVOLUTION; NORTH AMERICA; PHYLOGEOGRAPHY; PLANT GENE; RAGWEED; REAL TIME POLYMERASE CHAIN REACTION; REPRODUCIBILITY; REPRODUCTION;

ADAPTATION, PHYSIOLOGICAL; AMBROSIA; CLIMATE; ECOSYSTEM; EUROPE; EVOLUTION, MOLECULAR; GENE EXPRESSION; GENES, PLANT; GENETIC VARIATION; INTRODUCED SPECIES; MICROSATELLITE REPEATS; NORTH AMERICA; PHYLOGEOGRAPHY; REAL-TIME POLYMERASE CHAIN REACTION; REPRODUCIBILITY OF RESULTS; REPRODUCTION;

AMBROSIA; AMBROSIA ARTEMISIIFOLIA;

EID: 84876693716     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.12179     Document Type: Article

References (109)

1. Alex JF, Switzer CM, (1992) Ontario Weeds: Descriptions, Illustrations and Keys to Their Identification-Publication 505. University of Guelph, Guelph, Ontario.
2. Alpert P, Bone E, Holzapfel C, (2000) Invasiveness, invasibility and the role of environmental stress in the spread of non-native plants. Perspectives in Plant Ecology, Evolution and Systematics, 3, 52-66.
3. Amudha J, Balasubramani G, (2011) Recent molecular advances to combat abiotic stress tolerance in crop plants. Molecular Biology, 6, 31-58.
4. Bassett I, Crompton C, (1975) Biology of Canadian weeds. II. Ambrosia artemisiifolia L. and A. psilostachya D.C. Canadian Journal of Plant Science, 55, 463-476.
5. Bates D, Maechler M, (2011) lme4: LINEAR mixed effects models using S4 classes (R package version 0.999999-0). Available from http://cran.r-project. org/web/packages/lme4//index.html.
6. Blossey B, Notzold R, (1995) Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. Journal of Ecology, 83, 887-889.
7. Bolstad BM, Irizarry RA, Astrand M, Speed TP, (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics, 19, 185-193.
8. Brewer CE, Oliver LR, (2009) Confirmation and resistance mechanisms in glyphosate-resistant common ragweed (Ambrosia artemisiifolia) in Arkansas. Weed Science, 57, 567-573.
9. Broadley MR, White PJ, Hammond JP, et al,. (2008) Evidence of neutral transcriptome evolution in plants. New Phytologist, 180, 587-593.
10. Broz AK, Broeckling CD, He J, et al,. (2007) A first step in understanding an invasive weed through its genes: an EST analysis of invasive Centaurea maculosa. BMC plant biology, 7, 25.
11. Cai Y, Jia JW, Crock J, Lin ZX, Chen XY, Croteau R, (2002) A cDNA clone for beta-caryophyllene synthase from Artemisia annua. Phytochemistry, 61, 523-529.
12. Callaway RM, Ridenour WM, (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Frontiers in Ecology and the Environment, 2, 436-443.
13. Camon EB, Barrell DG, Dimmer EC, et al,. (2005) An evaluation of GO annotation retrieval for BioCreAtIvE and GOA. BMC Bioinformatics, 6, S17.
14. Carvalho BS, Irizarry RA, (2010) A framework for oligonucleotide microarray preprocessing. Bioinformatics, 26, 2363-2367.
15. Chauvel B, Dessaint F, Cardinal-Legrand C, Bretagnolle F, (2006) The historical spread of Ambrosia artemisiifolia L. in France from herbarium records. Journal of Biogeography, 33, 665-673.
16. Chen MS, (2008) Inducible direct plant defense against insect herbivores: a review. Insect Science, 15, 101-114.
17. Chun YJ, Fumanal B, Laitung B, Bretagnolle F, (2010) Gene flow and population admixture as the primary post-invasion processes in common ragweed (Ambrosia artemisiifolia) populations in France. The New Phytologist, 185, 1100-1107.
18. Chun YJ, Corre VLE, Bretagnolle F, (2011) Adaptive divergence for fitness-related traits among invasive Ambrosia artemisiifolia populations in France. Molecular Ecology, 20, 1378-1388.
19. Colautti RI, Bailey SA, van Overdijk CDA, Amundsen K, MacIsaac HJ, (2006) Characterized and projected costs of nonindigenous species in Canada. Biological Invasions, 8, 45-59.
20. Colautti RI, Maron JL, Barrett SCH, (2009) Common garden comparisons of native and introduced plant populations: latitudinal clines can obscure evolutionary inferences. Evolutionary Applications, 2, 187-199.
21. Colautti RI, Eckert CG, Barrett SCH, (2010) Evolutionary constraints on adaptive evolution during range expansion in an invasive plant. Proceedings of the Royal Society of London B: Biological sciences, 277, 1799-1806.
22. Conesa A, Götz S, (2008) Blast2GO: a comprehensive suite for functional analysis in plant genomics. International Journal of Plant Genomics, 2008, 619832.
23. Conesa A, Götz S, García-Gõmez JM, Terol J, Talõn M, Robles M, (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics, 21, 3674-3676.
24. Crawley M, (1987) What makes a community invasible? In: Colonization, Succession and Stability (eds, Gray AJ, Crawley MJ, Edwards PJ,), pp. 429-453. Blackwell Scientific Publications, Oxford.
25. Cui X, Churchill GA, (2003) Statistical tests for differential expression in cDNA microarray experiments. Genome Biology, 4, 210.
26. Dickerson C, Sweet R, (1971) Common ragweed ecotypes. Weed Science, 19, 64-66.
27. Dlugosch KM, Parker IM, (2008) Invading populations of an ornamental shrub show rapid life history evolution despite genetic bottlenecks. Ecology Letters, 11, 701-709.
28. Dodd AN, Salathia N, Hall A, et al,. (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science, 309, 630-633.
29. Elton CS, (1958) The Ecology of Invasions by Animals and Plants. University of Chicago Press, Chicago, Illinois.
30. Friedman J, Barrett SCH, (2008) High outcrossing in the annual colonizing species Ambrosia artemisiifolia (Asteraceae). Annals of Botany, 101, 1303-1309.
31. Gaines TA, Zhang W, Wang D, et al,. (2010) Gene amplification confers glyphosate resistance in Amaranthus palmeri. Proceedings of the National Academy of Sciences, 107, 1029-1034.
32. Galen C, Huddle J, Liscum E, (2004) An experimental test of the adaptive evolution of phototropins: blue-light photoreceptors controlling phototropism in Arabidopsis thaliana. Evolution, 58, 515-523.
33. Gaudeul M, Giraud T, Kiss L, Shykoff JA, (2011) Nuclear and chloroplast microsatellites show multiple introductions in the worldwide invasion history of common ragweed, Ambrosia artemisiifolia. PLoS ONE, 6, e17658.
34. Genton BJ, Shykoff JA, Giraud T, (2005a) High genetic diversity in French invasive populations of common ragweed, Ambrosia artemisiifolia, as a result of multiple sources of introduction. Molecular Ecology, 14, 4275-4285.
35. Genton BJ, Kotanen PM, Cheptou PO, Adolphe C, Shykoff JA, (2005b) Enemy release but no evolutionary loss of defence in a plant invasion: an inter-continental reciprocal transplant experiment. Oecologia, 146, 404-414.
36. Gharib WH, Robinson-Rechavi M, (2011) When orthologs diverge between human and mouse. Briefings in Bioinformatics, 12, 436-441.
37. Gladieux P, Giraud T, Kiss L, Genton BJ, Jonot O, Shykoff JA, (2011) Distinct invasion sources of common ragweed (Ambrosia artemisiifolia) in Eastern and Western Europe. Biological Invasions, 13, 933-944.
38. Grime J, (1977) Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. The American Naturalist, 111, 1169-1194.
39. Hamrick JL, Godt MJW, (1996) Effects of life history traits on genetic diversity in plant species. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 351, 1291-1298.
40. He WM, 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. Biological Invasions, 12, 3591-3598.
41. Heil M, Ton J, (2008) Long-distance signalling in plant defence. Trends in Plant Science, 13, 264-272.
42. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A, (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25, 1965-1978.
43. Hodgins KA, Rieseberg L, (2011) Genetic differentiation in life-history traits of introduced and native common ragweed (Ambrosia artemisiifolia) populations. Journal of Evolutionary Biology, 24, 2731-2749.
44. Irizarry RA, (2003) Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Research, 31, 15e.
45. Irizarry RA, Hobbs B, Collin F, et al,. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics, 4, 249-264.
46. Jordan T, Hager A, Peterson D, Sprague C, Bauman T, Nice G, (2010) The Glyphosate, Weeds, and Crop Series: Biology and Management of Common Ragweed Glyphosate Stewardship Working Group, www.glyphosateweedscrops.org.
47. Keane R, Crawley MJ, (2002) Exotic plant invasions and the enemy release hypothesis. Trends in Ecology & Evolution, 17, 164-170.
48. Keller SR, Sowell DR, Neiman M, Wolfe LM, Taylor DR, (2009) Adaptation and colonization history affect the evolution of clines in two introduced species. New Phytologist, 183, 678-690.
49. Kendziorski C, Irizarry RA, Chen KS, Haag JD, Gould MN, (2005) On the utility of pooling biological samples in microarray experiments. Proceedings of the National Academy of Sciences, 102, 4252-4257.
50. Khaitovich P, Weiss G, Lachmann M, et al,. (2004) A neutral model of transcriptome evolution. PLoS biology, 2, E132.
51. Khatri P, Draghici S, (2005) Ontological analysis of gene expression data: current tools, limitations, and open problems. Bioinformatics, 21, 3587-3595.
52. King OD, Foulger RE, Dwight SS, White JV, Roth FP, (2003) Predicting gene function from patterns of annotation. Genome Research, 13, 896-904.
53. Kiss L, Beres I, (2006) Anthropogenic factors behind the recent population expansion of common ragweed (Ambrosia artemisiifolia L.) in Eastern Europe: is there a correlation with political transitions? Journal of Biogeography, 33, 2155-2156.
54. Koonin EV, (2005) Orthologs, paralogs, and evolutionary genomics. Annual Review of Genetics, 39, 309-338.
55. Kreps JA, Wu Y, Chang H, et al,. (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiology, 130, 2129-2141.
56. Laaidi M, Laaidi K, Besancenot JP, Thibaudon M, (2003) Ragweed in France: an invasive plant and its allergenic pollen. Annals of Allergy, Asthma & Immunology, 91, 195-201.
57. Lackman P, González-Guzmán M, Tilleman S, et al,. (2011) Jasmonate signaling involves the abscisic acid receptor PYL4 to regulate metabolic reprogramming in Arabidopsis and tobacco. Proceedings of the National Academy of Sciences, 108, 5891-5896.
58. Lai Z, Gross BL, Zou Y, Andrews J, Rieseberg LH, (2006) Microarray analysis reveals differential gene expression in hybrid sunflower species. Molecular Ecology, 15, 1213-1227.
59. Lai Z, Kane NC, Zou Y, Rieseberg LH, (2008) Natural variation in gene expression between wild and weedy populations of Helianthus annuus. Genetics, 179, 1881-1890.
60. Lai Z, Kane NC, Kozik A, et al,. (2012) Genomics of Compositae weeds: EST libraries, microarrays, and evidence of introgression. American Journal of Botany, 99, 1-10.
61. Lavoie C, Jodoin Y, de Merlis AG, (2007) How did common ragweed (Ambrosia artemisiifolia L.) spread in Quebec? A historical analysis using herbarium records. Journal of Biogeography, 34, 1751-1761.
62. Lee CE, (2002) Evolutionary genetics of invasive species. Trends in Ecology & Evolution, 17, 386-391.
63. Linde M, Diel S, Neuffer B, (2001) Flowering ecotypes of Capsella bursa-pastoris (L.) Medik. (Brassicaceae) analysed by a cosegregation of phenotypic characters (QTL) and molecular markers. Annals of Botany, 87, 91-99.
64. Maron JL, Vilà M, Bommarco R, Elmendorf S, Beardsley P, (2004) Rapid evolution of an invasive plant. Ecological Monographs, 74, 261-280.
65. Martin DM, Bohlmann J, (2004) Identification of Vitis vinifera (-)-alpha-terpineol synthase by in silico screening of full-length cDNA ESTs and functional characterization of recombinant terpene synthase. Phytochemistry, 65, 1223-1229.
66. Martin RC, Mok MC, Mok DW, (1999) Isolation of a cytokinin gene, ZOG1, encoding zeatin O-glucosyltransferase from Phaseolus lunatus. Proceedings of the National Academy of Sciences, 96, 284-289.
67. Mayrose M, Kane NC, Mayrose I, Dlugosch KM, Rieseberg LH, (2011) Increased growth in sunflower correlates with reduced defences and altered gene expression in response to biotic and abiotic stress. Molecular Ecology, 20, 4683-4694.
68. McNeely J, (2001) Invasive species: a costly catastrophe for native biodiversity. Land Use and Water Resources Research, 1, 1-10.
69. Myers J, Bazely D, (2003) Ecology and Control of Introduced Plants. Cambridge University Press, Cambridge.
70. Nagalakshmi U, Wang Z, Waern K, et al,. (2008) The transcriptional landscape of the yeast genome defined by RNA sequencing. Science, 320, 1344-1349.
71. Narsai R, Howell KA, Millar AH, O'Toole N, Small I, Whelan J, (2007) Genome-wide analysis of mRNA decay rates and their determinants in Arabidopsis thaliana. The Plant Cell, 19, 3418-3436.
72. Oleksiak MF, Churchill GA, Crawford DL, (2002) Variation in gene expression within and among natural populations. Nature Genetics, 32, 261-266.
73. Paterson AH, Schertz KF, Lin YR, Liu SC, Chang YL, (1995) The weediness of wild plants: molecular analysis of genes influencing dispersal and persistence of johnsongrass, Sorghum halepense (L.) Pers. Proceedings of the National Academy of Sciences, 92, 6127-6131.
74. Pimentel D, Lach L, Zuniga R, Morrison D, (2000) Environmental and economic costs of nonindigenous species in the United States. BioScience, 50, 53-65.
75. Porta H, Figueroa-Balderas RE, Rocha-Sosa M, (2008) Wounding and pathogen infection induce a chloroplast-targeted lipoxygenase in the common bean (Phaseolus vulgaris L.). Planta, 227, 363-373.
76. Powles SB, (2008) Evolved glyphosate-resistant weeds around the world: lessons to be learnt. Pest Management Science, 365, 360-365.
77. Powles SB, Preston C, (2006) Evolved glyphosate resistance in plants: biochemical and genetic basis of resistance 1. Weed Technology, 20, 282-289.
78. Powles SB, Yu Q, (2010) Evolution in action: plants resistant to herbicides. Annual Review of Plant Biology, 61, 317-347.
79. Prentis PJ, Wilson JRU, Dormontt EE, Richardson DM, Lowe AJ, (2008) Adaptive evolution in invasive species. Trends in Plant Science, 13, 288-294.
80. Prosser I, Phillips AL, Gittings S, et al,. (2002) (+)-(10R)-Germacrene A synthase from goldenrod, Solidago canadensis; cDNA isolation, bacterial expression and functional analysis. Phytochemistry, 60, 691-702.
81. Qin D, Wu H, Peng H, et al,. (2008) Heat stress-responsive transcriptome analysis in heat susceptible and tolerant wheat (Triticum aestivum L.) by using Wheat Genome Array. BMC Genomics, 9, 432.
82. 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. Ecology Letters, 9, 981-993.
83. Richman A, Swanson A, Humphrey T, et al,. (2005) Functional genomics uncovers three glucosyltransferases involved in the synthesis of the major sweet glucosides of Stevia rebaudiana. The Plant Journal, 41, 56-67.
84. Robineau T, Batard Y, Nedelkina S, et al,. (1998) The chemically inducible plant cytochrome P450 CYP76B1 actively metabolizes phenylureas and other xenobiotics. Plant Physiology, 118, 1049-1056.
85. Rouhier N, Lemaire SD, Jacquot JP, (2008) The role of glutathione in photosynthetic organisms: emerging functions for glutaredoxins and glutathionylation. Annual Review of Plant Biology, 59, 143-166.
86. Scheipl F, Bolker B, (2011) RLRsim: Exact (Restricted) Likelihood Ratio tests for mixed and additive models. R package version 2.0-11.
87. Schmitt J, McCormac A, (1995) A test of the adaptive plasticity hypothesis using transgenic and mutant plants disabled in phytochrome-mediated elongation responses to neighbors. The American Naturalist, 146, 937-953.
88. Schmitt J, Stinchcombe JR, Heschel MS, Huber H, (2003) The adaptive evolution of plasticity: phytochrome-mediated shade avoidance responses. Integrative and Comparative Biology, 43, 459-469.
89. Schnoes AM, Brown SD, Dodevski I, Babbitt PC, (2009) Annotation error in public databases: misannotation of molecular function in enzyme superfamilies. PLoS Computational Biology, 5, e1000605.
90. Seitz C, Eder C, Deiml B, Kellner S, Martens S, Forkmann G, (2006) Cloning, functional identification and sequence analysis of flavonoid 3′-hydroxylase and flavonoid 3′,5′-hydroxylase cDNAs reveals independent evolution of flavonoid 3′,5′-hydroxylase in the Asteraceae family. Plant Molecular Biology, 61, 365-381.
91. Shalem O, Dahan O, Levo M, et al,. (2008) Transient transcriptional responses to stress are generated by opposing effects of mRNA production and degradation. Molecular Systems Biology, 4, 223.
92. Shinozaki K, Yamaguchi-Shinozaki K, (2007) Gene networks involved in drought stress response and tolerance. Journal of experimental Botany, 58, 221-227.
93. Stewart CN, Tranel PJ, Horvath DP, et al,. (2009) Evolution of weediness and invasiveness: charting the course for weed genomics. Weed Science, 57, 451-462.
94. Storey JD, (2002) A direct approach to false discovery rates. Journal of the Royal Statistical Society, 464, 79-498.
95. Storey JD, Madeoy J, Strout JL, Wurfel M, Ronald J, Akey JM, (2007) Gene-expression variation within and among human populations. American Journal of Human Genetics, 80, 502-509.
96. Teale WD, Paponov IA, Palme K, (2006) Auxin in action: signalling, transport and the control of plant growth and development. Nature Reviews. Molecular Cell Biology, 7, 847-859.
97. Teutsch HG, Hasenfrat MP, Lesot A, et al,. (1993) Isolation and sequence of a cDNA encoding the Jerusalem artichoke cinnamate 4-hydroxylase, a major plant cytochrome P450 involved in the general phenylpropanoid pathway. Proceedings of the National Academy of Sciences, 90, 4102-4106.
98. Thébaud C, Simberloff D, (2001) Are plants really larger in their introduced ranges? The American Naturalist, 157, 231-236.
99. Thomas PD, Wood V, Mungall CJ, Lewis SE, Blake JA, (2012) On the use of gene ontology annotations to assess functional similarity among orthologs and paralogs: a short report. PLoS Computational Biology, 8, e1002386.
100. Troyanskaya O, Cantor M, Sherlock G, (2001) Missing value estimation methods for DNA microarrays. Bioinformatics, 17, 520-525.
101. Tzin V, Galili G, (2010) The biosynthetic pathways for shikimate and aromatic amino acids in Arabidopsis thaliana. The Arabidopsis Book, 8, 1-18.
102. Wang R, Peng S, Zeng R, (2009) Cloning, expression and wounding induction of β-caryophyllene synthase gene from Mikania micrantha HBK and allelopathic potential of β-caryophyllene. Allelopathy Journal, 24, 35-44.
103. Warpeha KM, Lateef SS, Lapik Y, Anderson M, Lee BS, Kaufman LS, (2006) G-protein-coupled receptor 1, G-protein Gα-subunit 1, and prephenate dehydratase 1 are required for blue light-induced production of phenylalanine in etiolated Arabidopsis. Plant Physiology, 140, 844-855.
104. Weinig C, Brock MT, Dechaine JA, Welch SM, (2007) Resolving the genetic basis of invasiveness and predicting invasions. Genetica, 129, 205-216.
105. Werck-Reichhart D, Feyereisen R, (2000) Protein family review cytochromes P450: a success story. Genome Biology, 1, 1-9.
106. Whitehead A, Crawford DL, (2006) Variation within and among species in gene expression: raw material for evolution. Molecular Ecology, 15, 1197-1211.
107. Willemsen RW, (1975) Dormancy and germination of common ragweed seeds in the field. American Journal of Botany, 62, 639-643.
108. Willis AJ, Memmott J, Forrester RI, (2000) Is there evidence for the post-invasion evolution of increased size among invasive plant species? Ecology Letters, 3, 275-283.
109. Yamada T, Matsuda F, Kasai K, (2008) Mutation of a rice gene encoding a phenylalanine biosynthetic enzyme results in accumulation of phenylalanine and tryptophan. The Plant Cell, 20, 1316-1329.