Skip to main content Accessibility help
×
Home

Evolution of Weediness and Invasiveness: Charting the Course for Weed Genomics

  • C. Neal Stewart (a1), Patrick J. Tranel (a2), David P. Horvath (a3), James V. Anderson (a3), Loren H. Rieseberg (a4), James H. Westwood (a5), Carol A. Mallory-Smith (a6), Maria L. Zapiola (a6) and Katrina M. Dlugosch (a4)...

Abstract

The genetic basis of weedy and invasive traits and their evolution remain poorly understood, but genomic approaches offer tremendous promise for elucidating these important features of weed biology. However, the genomic tools and resources available for weed research are currently meager compared with those available for many crops. Because genomic methodologies are becoming increasingly accessible and less expensive, the time is ripe for weed scientists to incorporate these methods into their research programs. One example is next-generation sequencing technology, which has the advantage of enhancing the sequencing output from the transcriptome of a weedy plant at a reduced cost. Successful implementation of these approaches will require collaborative efforts that focus resources on common goals and bring together expertise in weed science, molecular biology, plant physiology, and bioinformatics. We outline how these large-scale genomic programs can aid both our understanding of the biology of weedy and invasive plants and our success at managing these species in agriculture. The judicious selection of species for developing weed genomics programs is needed, and we offer up choices, but no Arabidopsis-like model species exists in the world of weeds. We outline the roadmap for creating a powerful synergy of weed science and genomics, given well-placed effort and resources.

Copyright

Corresponding author

Corresponding author's E-mail: nealstewart@utk.edu

References

Hide All
Anderson, J. V. 2008. Emerging technologies: an opportunity for weed biology research. Weed Sci. 56:281282.
Anderson, J. V., Delseny, M., Fregene, M. A., et al. 2004. An EST resource for cassava and other species of Euphorbiaceae. Plant Mol. Biol. 56:527539.
Anderson, J. V., Horvath, D. P., Chao, W. S., et al. 2007. Characterization of an EST database for the perennial weed leafy spurge: an important resource for weed biology research. Weed Sci. 55:193203.
Baker, H. G. 1974. The evolution of weeds. Annu. Rev. Ecol. Syst. 5:124.
Barker, M. S., Kane, N. C., Kozik, A., Michelmore, R. W., Matvienko, M., Knapp, S. J., and Rieseberg, L. H. 2008. Multiple paleopolyploidizations during the evolution of the Asteraceae reveal parallel patterns of duplicate gene retention after millions of years. Mol. Biol. Evol. 25:24452455.
Barbazuk, W. B., Bedell, J. A., and Rabinowicz, P. D. 2005. Reduced representation sequencing: a success in maize and a promise for other plant genomes. Bioessays. 27:839848.
Barrett, S. C. H., Colautti, R. I., and Eckert, C. G. 2008. Plant reproductive systems and evolution during biological invasion. Mol. Ecol. 17:373383.
Barrett, S. C. H. 1983. Crop mimicry in weeds. Econ. Bot. 37:255282.
Basu, C., Halfhill, M. D., Mueller, T. C., and Stewart, C. N. Jr. 2004. Weed genomics: new tools to understand weed biology. Trends Plant Sci. 9:391398.
Bennett, M. D. and Leitch, I. J. 2003. Plant DNA C-values database. www.kew.org/cval.
Blödner, C., Goebel, C., Feussner, I., Gatz, C., and Polle, A. 2007. Warm and cold parental reproductive environments affect seed properties, fitness, and cold responsiveness in Arabidopsis thaliana progenies. Plant Cell Environ. 30:165175.
Bodo Slotta, T. A. 2008. What we know about weeds: insights from genetic markers. Weed Sci. 56:322326.
Bossard, C. C., Randall, J. M., and Hoshovsky, M. C. 2000. Invasive plants of California's wildlands. Berkeley, CA University of California Press, Berkeley. 360.
Broz, A. K., Broeckling, C. D., He, J., Dai, X., Zhao, P. X., and Vivanco, J. M. 2007. A first step in understanding an invasive weed through its genes: an EST analysis of invasive Centaurea maculosa . BMC Plant Biol. 7:25. http://www.biomedcentral.com/1471-2229/7/25.
Chao, W. S. 2008. Real-time PCR as a tool to study weed biology. Weed Sci. 56:290296.
Chao, W. S., Horvath, D. P., Anderson, J. V., and Foley, M. P. 2005. Potential model weeds to study genomics, ecology, and physiology in the 21st century. Weed Sci. 53:929937.
Charmet, G., Balfourier, F., and Chatard, V. 1996. Taxonomic relationships and interspecific hybridization in the genus Lolium (grasses). Genet. Resour. Crop Evol. 43:319327.
Church, S. A., Livingstone, K., Lai, Z., Kozik, A., Knapp, S. J., Michelmore, R. W., and Rieseberg, L. H. 2007. Using variable rate models to identify genes under selection in sequence pairs: their validity and limitations for EST sequences. J. Mol. Evol. 64:171180.
Ciannamea, S., Busscher-Lange, J., de Folter, S., Angenent, G. C., and Immink, R. G. H. 2006. Characterization of the vernalization response in Lolium perenne by a cDNA microarray approach. Plant Cell Physiol. 47:481492.
Devine, M. D. and Shukla, A. 2000. Altered target sites as a mechanism of herbicide resistance. Crop Prot. 19:881889.
Dlugosch, K. M. and Whitton, J. 2008. Can we stop transgenes from taking a walk on the wild side? Mol. Ecol. 17:11671169.
Eckes, P., van Almsick, C., and Weidler, M. 2004. Gene expression profiling, a revolutionary tool in Bayer CropScience herbicide discovery. Pflanzenschutz-Nachr. Bayer. 57:6277.
Ellstrand, N. C. and Schierenbeck, K. A. 2000. Hybridization as a stimulus for the evolution of invasiveness in plants? Proc. Natl. Acad. Sci. U.S.A. 97:70437050.
Emberton, J., Ma, J. X., Yuan, Y. N., SanMiguel, P., and Bennetzen, J. L. 2005. Gene enrichment in maize with hypomethylated partial restriction (HMPR) libraries. Genome Res. 15:14411446.
Evans, G. M., Rees, H., Snell, C. L., and Sun, S. 1972. The relation between nuclear DNA amount and the duration of the mitotic cycle. Chromosomes Today. 3:2431.
Gardner, S. N., Gressel, J., and Mangel, M. 1998. A revolving dose strategy to delay the evolution of both quantitative vs. major monogene resistances to pesticides and drugs. Int. J. Pest Manag. 44:161180.
Gressel, J. 2002. Molecular Biology of Weed Control. New York Taylor and Francis. 504.
Gressel, J. 2008. Genetic Glass Ceilings. Baltimore The Johns Hopkins University Press. 348.
Grime, J. P. 1977. Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am. Nat. 111:11691194.
Halfhill, M. D., Good, L. L., Basu, C., Burris, J., Main, C. L., Mueller, T. C., and Stewart, C. N. Jr. 2007. Transformation and segregation of GFP fluorescence and glyphosate resistance in horseweed (Conyza canadensis) hybrids. Plant Cell Rep. 26:303311.
Heimann, B. and Cussans, G. W. 1996. The importance of seeds and sexual reproduction in the population biology of Cirsium arvense—a literature review. Weed Res. (Oxf.) 36:493503.
Hieter, P. and Boguski, M. 1997. Functional genomics: it's all how you read it. Science. 278:601602.
Holm, L., Doll, J., Holm, E., Pancho, J. V., and Herberger, J. P. 1997. World Weeds: Natural Histories and Distribution. New York John Wiley and Sons. 1152.
Horvath, D. P. and Clay, S. 2007. Heterologous hybridization of cotton (Gossypium hirsutum) microarrays with velvetleaf (Abutilon theophrasti) reveals physiological responses due to corn competition. Weed Sci. 55:546557.
Horvath, D. P., Anderson, J. V., Soto-Suárez, M., and Chao, W. S. 2006a. Transcriptome analysis of leafy spurge (Euphorbia esula) crown buds during shifts in well-defined phases of dormancy. Weed Sci. 54:821827.
Horvath, D. P., Chao, W. S., Suttle, J. C., Thimmipuram, J., and Anderson, J. V. 2008. Transcriptome analysis identifies novel responses and potential regulatory genes involved in seasonal dormancy transitions of leafy spurge (Euphorbia esula L.). BMC Genomics. 9:536.
Horvath, D. P., Gulden, R., and Clay, S. A. 2006b. Microarray analysis of late-season velvetleaf (Abutilon theophrasti) effect on corn. Weed Sci. 54:983994.
Horvath, D. P., Schaffer, R., and Wisman, E. 2003. Identification of genes induced in emerging tillers of wild oat (Avena fatua) using Arabidopsis microarrays. Weed Sci. 51:503508.
Hudson, R. R., Kreitman, M., and Aguade, M. 1987. A test of neutral molecular evolution based on nucleotide data. Genetics. 116:153159.
Inderjit, R. M., Callaway, R., and Vivanco, J. M. 2006. Plant biochemistry helps to understand invasion ecology. Trends Plant Sci. 11:574580.
Jofre-Garfias, A. E., Villegas-Sepúlveda, N., Cabrera-Ponce, J. L., Adame-Alvarez, R. M., Herrera-Estrella, L., and Simpson, J. 1997. Agrobacterium-mediated transformation of Amaranthus hypochondriacus: light- and tissue-specific expression of a pea chlorophyll a/b-binding protein promoter. Plant Cell Rep. 16:847852.
Johnsen, Ø, Fossdal, C. G., Nagy, N., Mølmann, J., Daehlen, O. G., and Skrøppa, T. 2005. Climatic adaptation in Picea abies progenies is affected by the temperature during zygotic embryogenesis and seed maturation. Plant Cell Environ. 28:10901102.
Kane, N. C. and Rieseberg, L. H. 2007. Selective sweeps reveal candidate genes for adaptation to drought and salt tolerance in common sunflower, Helianthus annuus . Genetics. 175:18031812.
Kane, N. C. and Rieseberg, L. H. 2008. Genetics and evolution of weedy Helianthus annuus populations: evidence of multiple origins of an agricultural weed. Mol. Ecol. 7:384394.
Karrenberg, S. and Widmer, A. 2008. Ecologically relevant genetic variation from a non-Arabidopsis perspective. Curr. Opin. Plant Biol. 11:156162.
Kim, M., Cui, M-L., Cubas, P., Gillies, A., Lee, K., Chapman, M. A., Abbott, R. J., and Coen, E. 2008. Regulatory genes control a key morphological and ecological trait transferred between species. Science. 322:11161119.
Lai, Z., Gross, B. L., Zou, Y., Andrews, J., and Rieseberg, L. H. 2006. Microarray analysis reveals differential gene expression in hybrid sunflower species. Mol. Ecol. 15:12131227.
Lai, Z., Kane, N. C., Zou, Y., and Rieseberg, L. H. 2008. Natural variation in gene expression between wild and weedy populations of Helianthus annuus . Genetics. 179:18811890.
Landry, C. R., Lemos, B., Rifkin, S. A., Dickinson, W. J., and Hartl, D. K. 2007. Genetic properties influencing the evolvability of gene expression. Science. 317:118121.
Larrinua, I. M. and Belmar, S. B. 2008. Bioinformatics and its relevance to weed science. Weed Sci. 56:297305.
Lee, R. M. and Tranel, P. T. 2008. Utilization of DNA microarrays in weed science research. Weed Sci. 56:283289.
Lein, W., Börnke, F., Reindl, A., Ehrhardt, T., Stitt, M., and Sonnewald, U. 2004. Target-based discovery of novel herbicides. Curr. Opin. Plant Biol. 7:219225.
Liu, X. S. 2007. Getting started in tiling microarray analysis. PLoS Comput. Biol. 3:e183.
Lokko, Y., Anderson, J. V., Rudd, S., et al. 2007. Characterization of an 18,166 EST dataset for cassava (Manihot esculenta Crantz) enriched for drought-responsive genes. Plant Cell Rep. 26:16051618.
Mallory-Smith, C. and Zapiola, M. 2008. Gene flow from glyphosate-resistant crops. Pest. Manag. Sci. 64:428440.
Malone-Schonenberg, J., Scelonge, C. J., Burrus, M., and Bidney, D. L. 1994. Stable transformation of sunflower using Agrobacterium and split embryonic axis explants. Plant Sci. 103:199207.
Mardis, E. R. 2008. The impact of next-generation sequencing technology on genetics. Trends Genet. 24:133141.
McDonald, J. H. and Kreitman, M. 1991. Adaptive protein evolution at the Adh locus in Drosophila . Nature. 351:652654.
Michelmore, R., Marsh, E., Seely, S., and Landry, B. 1987. Transformation of lettuce Lactuca sativa mediated by Agrobacterium tumefaciens . Plant Cell Rep. 6:439–42.
Narumi, T., Aida, R., Ohmiya, A., and Satoh, S. 2005. Transformation of chrysanthemum with mutated ethylene receptor genes: mDG-ERS1 transgenes conferring reduced ethylene sensitivity and characterization of the transformants. Postharvest Biol. Technol. 37:101110.
Neale, D. B. and Ingvarsson, P. K. 2008. Population, quantitative and comparative genomics of adaptation in forest trees. Curr. Opin. Plant Biol. 11:149155.
Patzoldt, W. L., Tranel, P. J., and Hager, A. G. 2005. A waterhemp (Amaranthus tuberculatus) biotype with multiple resistance across three herbicide sites of action. Weed Sci. 53:3036.
Pimentel, D., Zuniga, R., and Morrison, D. 2005. Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol. Econ. 52:273288.
Prentis, P. J., Wilson, J. R. U., Dormontt, E. E., Richardson, D. M., and Lowe, A. J. 2008. Adaptive evolution in invasive species. Trends Plant Sci. 13:288294.
Raghavan, C., Ong, E. K., Dalling, M., and Stevenson, T. W. 2005. Effect of herbicidal application of 2,4-dichlorophenoxyacetic acid in Arabidopsis . Funct. Integr. Genomics. 5:417.
Raghavan, C., Ong, E. K., Dalling, M., and Stevenson, T. W. 2006. Regulation of genes associated with auxin, ethylene and ABA pathways by 2,4-dichlorophenoxyacetic acid in Arabidopsis . Funct. Integr. Genomics. 6:6070.
Rayburn, A. L., McLoskey, R., Jeschke, T. C., and Tranel, P. J. 2005. Genome size analysis of weedy Amaranthus species. Crop Sci. 45:25572562.
Renn, S. C., Aubin-Horth, N., and Hofmann, H. A. 2004. Biologically meaningful expression profiling across species using heterologous hybridization to a cDNA microarray. BMC Genomics. 5:42.
Sawbridge, T., Ong, E., Binnion, C., et al. 2003. Generation and analysis of expressed sequence tags in perennial ryegrass (Lolium perenne L.). Plant Sci. 165:10891100.
Shendure, J. 2008. The beginning of the end for microarrays. Nat. Methods. 5:585587.
Stevens, P. F. 2007. Angiosperm Phylogeny. Version 8. http://www.mobot.org/MOBOT/research/APweb/. Accessed: January 13, 2008.
Stewart, C. N. Jr. 2009. Weedy and Invasive Plant Genomics. Ames, IA Blackwell Scientific. 254 p.
Stinchcombe, J. R. and Hoekstra, H. E. 2008. Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits. Heredity. 100:158179.
Taji, T., Seki, M., Satou, M., et al. 2004. Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis microarray. Plant Physiol. 135:16971709.
Tajima, F. 1989. Statistical methods to test for nucleotide mutation hypothesis by DNA polymorphism. Genetics. 123:85595.
Tatematsu, K., Ward, S., Leyser, O., Kamiya, Y., and Nambara, E. 2005. Identification of cis-elements that regulate gene expression during initiation of axillary bud outgrowth in Arabidopsis. Plant Physiol. 138:757766.
Thomas, M. A. and Klaper, R. 2004. Genomics for the ecological toolbox. Trends Ecol. Evol. 19:439445.
Tranel, P. J. and Trucco, F. The Amaranthus complex: a model for weed genomics. In Stewart, C. N. Jr. Weedy and Invasive Plant Genomics. Ames, IA Blackwell. In press.
Tranel, P. J. and Wright, T. R. 2002. Resistance of weeds to ALS-inhibiting herbicides: what have we learned? Weed Sci. 50:700712.
VanGessel, M. J. 2001. Glyphosate-resistant horseweed from Delaware. Weed Sci. 49:703705.
Warwick, S. I. and Stewart, C. N. Jr. 2005. Crops come from wild plants: How domestication, transgenes, and linkage effects shape ferality. Pages 930. In Gressel, J. Crop Ferality and Volunteerism. Boca Raton, Florida CRC.
Weiss-Schneeweiss, H., Greilhuber, J., and Schneeweiss, G. M. 2005. Genome size evolution in holoparasitic Orobanche (Orobanchaceae) and related genera. Am. J. Bot. 93:148156.
Whitelaw, C. A., Barbazuk, W. B., Pertea, G., et al. 2003. Enrichment of gene-coding sequences in maize by genome filtration. Science. 302:21182120.
Whitney, K. D., Randell, R. A., and Rieseberg, L. H. 2006. Adaptive introgression of herbivore resistance traits in the weedy sunflower Helianthus annuus . Am. Nat. 167:794–707.
Wiehe, T., Nolte, V., Zivkovic, D., and Schlotterer, C. 2007. Identification of selective sweeps using a dynamically adjusted number of linked microsatellites. Genetics. 175:207218.
Wood, H. M., Grahame, J. W., Humphray, S., Rogers, J., and Butlin, R. K. 2008. Sequence differentiation in regions identified by a genome scan for local adaptation. Mol. Ecol. 17:31233135.
Wright, S. I. and Gaut, B. S. 2005. Molecular population genetics and the search for adaptive evolution in plants. Mol. Biol. Evol. 22:506519.
[WSSA] Weed Science Society of America 2008. Charting the course for weed genomics: the evolution of weediness. WSSA Annual Meeting, February 4–7, 2008, Chicago, Illinois.
Wu, C. A., Lowry, D. B., Cooley, A. M., Wright, K. M., Lee, Y. W., and Willis, J. H. 2008. Mimulus is an emerging model system for the integration of ecological and genomic studies. Heredity. 100:220230.
Wu, Y-Y., Chen, Q-J., Chen, M., Chen, J., and Wang, X-C. 2005. Salt-tolerant transgenic perennial ryegrass (Lolium perenne L.) obtained by Agrobacterium tumefaciens-mediated transformation of the vacuolar Na+/H+ antiporter gene. Plant Sci. 169:6573.
Yang, Z. 1998. Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol. Biol. Evol. 15:568573.
Yu, J., Hu, S., Wang, J., et al. 2002. A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science. 296:7992.
Yuan, J. S., Galbraith, S. Y., Dai, S. Y., Griffin, P., and Stewart, C. N. Jr. 2008. Plant systems biology comes of age. Trends Plant Sci. 13:165171.
Yuan, J. S., Reed, A., Chen, F., and Stewart, C. N. Jr. 2006. Statistical analysis of real-time PCR data. BMC Bioinformatics. 7:85.
Yuan, J. S., Tranel, P. J., and Stewart, C. N. Jr. 2007. Non-target herbicide resistance: a family business. Trends Plant Sci. 12:613.
Zayed, A. and Whitfield, C. W. 2008. A genome-wide signature of positive selection in ancient and recent invasive expansions of the honey bee Apis mellifera . Proc. Natl. Acad. Sci. U.S.A. 105:34213426.

Keywords

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed