Hostname: page-component-7c8c6479df-xxrs7 Total loading time: 0 Render date: 2024-03-27T21:33:38.969Z Has data issue: false hasContentIssue false

Population Genetics and Seed Set in Feral, Ornamental Miscanthus sacchariflorus

Published online by Cambridge University Press:  20 January 2017

Evans Mutegi
Affiliation:
Department of Evolution, Ecology, and Organismal Biology, Ohio State University, Columbus, OH 43210
Allison A. Snow*
Affiliation:
Department of Evolution, Ecology, and Organismal Biology, Ohio State University, Columbus, OH 43210
Catherine L. Bonin
Affiliation:
Department of Agronomy, Iowa State University, Ames, IA 50011
Emily A. Heaton
Affiliation:
Department of Agronomy, Iowa State University, Ames, IA 50011
Hsiaochi Chang
Affiliation:
Department of Evolution, Ecology, and Organismal Biology, Ohio State University, Columbus, OH 43210
Carole J. Gernes
Affiliation:
Ramsey Conservation District, c/o Ramsey Washington Metro Watershed District, 2665 Noel Drive, Little Canada, MN 55117
Destiny J. Palik
Affiliation:
Department of Evolution, Ecology, and Organismal Biology, Ohio State University, Columbus, OH 43210
Maria N. Miriti
Affiliation:
Department of Evolution, Ecology, and Organismal Biology, Ohio State University, Columbus, OH 43210
*
Corresponding author's E-mail: snow.1@osu.edu

Abstract

Ornamental grasses may become invasive weeds depending on their ability to naturalize and outcompete other species. Miscanthus sacchariflorus (Maxim) Franch. (Amur silvergrass) is a tall, self-incompatible, nonnative grass that has become naturalized in eastern North America, forming monospecific stands and raising concerns about its potential invasiveness. To understand the extent of clonal and sexual reproduction in feral populations, we examined their population genetic structure, seed production, and ploidy. We surveyed 21 populations in Iowa and Minnesota using eight polymorphic microsatellite markers. Only 34 multilocus genotypes (MLGs) were detected from a total of 390 samples. All of the study populations had more than one MLG, thereby allowing cross-pollination with near neighbors, but most were dominated by one or a few MLGs. Low genetic divergence suggests that all populations may have originated from similar cultivars. Cluster analysis showed that the six populations from Minnesota were extremely similar to each other, whereas the 15 populations from Iowa were somewhat more diverse. Seed production was quantified for 20 populations and ploidy for 11 populations. Average seed production was very low (< 0.30 seeds per panicle), although most populations did produce seeds. Because the populations were diploid (2x), they also may have the potential to hybridize with ornamental varieties of Miscanthus sinensis (Chinese silvergrass; eulaliagrass), a diploid close relative. Clonal growth, self-incompatibility, and spatial isolation of compatible clones may contribute to pollen-limited seed set in these populations. Low seed set may affect the rate of spread of feral M. sacchariflorus, which appears to disperse vegetatively as well as by seed. Although this species is not widely viewed as invasive, it is worth monitoring as a species that may become more widespread in the future.

Type
Research Article
Copyright
Copyright © 2016 Weed Science Society of America 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Adugna, A, Sweeney, PM, Snow, AA (2011) Optimization of high throughput, cost effective, and all-stage DNA extraction protocol for sorghum ( Sorghum bicolor). J Agric Sci Technol 5:243250 Google Scholar
Ahmad, R, Liow, P-S, Spencer, DF, Jasieniuk, M (2008) Molecular evidence for a single genetic clone of invasive Arundo donax in the United States. Aquat Bot 88:113120 Google Scholar
Anderson, EK, Hager, AG, Lee, D, Allen, DJ, Voigt, TB (2015) Responses of seeded Miscanthus × giganteus to PRE and POST herbicides. Weed Technol 29:274283 CrossRefGoogle Scholar
Arnaud-Haond, S, Belkhir, K (2007) GENCLONE: a computer program to analyse genotypic data, test for clonality and describe spatial clonal organization. Mol Ecol Notes 7:1517 Google Scholar
Arnaud-Haond, S, Duarte, CM, Alberto, F, Serrao, EA (2007) Standardizing methods to address clonality in population studies. Mol Ecol 16:51155139 CrossRefGoogle ScholarPubMed
Balloux, F, Lehmann, L, De Meeus, T (2003) The population genetics of clonal and partially clonal diploids. Genetics 164:16351644 Google Scholar
Bonin, CL, Heaton, EA, Barb, J (2014) Miscanthus sacchariflorus—biofuel parent or new weed? Glob Change Biol Bioenergy 6:629636 Google Scholar
Chae, WB, Hong, SJ, Gifford, JM, Rayburn, AL, Sacks, EJ, Juvik, JA (2014) Plant morphology, genome size, and SSR markers differentiate five distinct taxonomic groups among accessions in the genus Miscanthus . Glob Change Biol Bioenergy 6:646660 CrossRefGoogle Scholar
Clark, LV, Stewart, JR, Nishiwaki, A, Toma, Y, Kueldsens, JB, Jorgensens, U, Zhao, H, Peng, J, Yoo, JH, Kweon, H, Yu, CY, Yamada, T, Sacks, EJ (2015) Genetic structure of Miscanthus sinensis and M. sacchariflorus in Japan indicates a gradient of bidirectional but asymmetric introgression. J Exp Bot DOI: 10.1093/jxb/eru511Google Scholar
Culley, TM, Hardiman, NA (2007) The beginning of a new invasive plant: a history of the ornamental Callery pear in the United States. BioScience 57:956964 Google Scholar
D'Antonio, C, Vitousek, P (1992) Biological invasions by exotic grasses, the grass fire cycle, and global change. Annu Rev Ecol Syst 23:63879 Google Scholar
DeWoody, JA, Schupp, J, Kenefic, L, Busch, J, Murfitt, L, Keim, P (2004) Universal method for producing ROX-labeled size standards suitable for automated genotyping. BioTechniques 37:348 Google Scholar
Dorken, ME, Eckert, GC (2001) Severely reduced sexual reproduction in northern populations of a clonal plant, Decodon verticillatus (Lythraceae). J Ecol 89:339350 CrossRefGoogle Scholar
EDDMapS (2016) Early Detection and Distribution Mapping System. University of Georgia Center for Invasive Species and Ecosystem Health. http://www.eddmaps.org. Accessed May 2016Google Scholar
Galbraith, DW, Harkins, KR, Maddox, JM, Ayres, NM, Sharma, DP, Firoozabady, E (1983) Rapid flow cytometric analysis of the cell-cycle in intact plant-tissues. Science 220:10491051 Google Scholar
Gitzendanner, MA, Weekley, CW, Germain-Aubrey, CC, Soltis, DE, Soltis, PS (2012) Microsatellite evidence for high clonality and limited genetic diversity in Ziziphus celata (Rhamnaceae), an endangered, self-incompatible shrub endemic to the Lake Wales Ridge, Florida, USA. Conserv Genet 13:223234 CrossRefGoogle Scholar
Glowacka, K, Clark, LV, Adhikari, S, Peng, J, Stewart, JR, Nishiwaki, A, Yamada, T, Jorgensen, U, Hodkinson, TR, Gifford, J, Juvik, JA, Sacks, EJ (2015) Genetic variation in Miscanthus × giganteus and the importance of estimating genetic distance thresholds for differentiating clones. Glob Change Biol Bioenergy 7:386404 Google Scholar
Gustafson, DJ, Giunta, AP Jr, Echt, CS (2013) Extensive clonal growth and biased sex ratios of an endangered dioecious shrub, Lindera melissifolia (Walt) Blume (Lauraceae). J Torrey Bot Soc 140:133144 Google Scholar
Hager, HA, Quinn, LD, Barney, JN, Voigt, TB, Newman, JA (2015a) Germination and establishment of bioenergy grasses outside cultivation: a multi-region seed addition experiment. Plant Ecol 216:13851399 Google Scholar
Hager, HA, Rupert, R, Quinn, LD, Newmann, JA (2015b) Escaped Miscanthus sacchariflorus reduces the richness and diversity of vegetation and the soil seed bank. Biol Invasions 17:18331847 CrossRefGoogle Scholar
Hager, HA, Sinasac, SE, Gedakif, Z, Newman, JA (2014) Predicting potential global distributions of two Miscanthus grasses: implications for horticulture, biofuel production, and biological invasions. PLOS ONE 9(6):e100032 doi:10.1371/journal.pone.0100032CrossRefGoogle ScholarPubMed
Hardiman, NA, Culley, TM (2010) Reproductive success of cultivated Pyrus calleryana (Rosaceae) and establishment ability of invasive, hybrid progeny. Am J Bot 97:16981706 Google Scholar
Hodkinson, TR, Chase, MW, Lledo, MD, Salamin, N, Renvoize, SA (2002a) Phylogenetics of Miscanthus, Saccharum and related genera (Saccharinae, Andropogoneae, Poaceae) based on DNA sequences from ITS nuclear ribosomal DNA and plastid trnL intron and trnL-F intergenic spacers. J Plant Res 115:381392 CrossRefGoogle Scholar
Hodkinson, TR, Chase, MW, Takahashi, C, Leitch, IJ, Bennett, MD, Renvoize, SA (2002b) The use of DNA sequencing (ITS and trnL-F), AFLP, and fluorescent in situ hybridization to study allopolyploid Miscanthus (Poaceae). Am J Bot 89:279286 CrossRefGoogle ScholarPubMed
Hovick, SM, Whitney, KD (2014) Hybridization is associated with increased fecundity and size in invasive taxa: meta-analytic support for the hybridization-invasion hypothesis. Ecol Lett 17:14641477 Google Scholar
Jensen, E, Farrar, K, Thomas-Jones, S, Hastings, A, Donnison, I, Clifton-Brown, J (2011) Characterization of flowering time diversity in Miscanthus species. Glob Change Biol Bioenergy 3:387400 Google Scholar
Kim, C, Zhang, D, Auckland, SA, Rainville, LK, Jacob, K, Kronmiller, B, Sacks, EJ, Deuter, M, Paterson, AH (2012) SSR-based genetic maps of Miscanthus sinensis and M. sacchariflorus, and their comparison to sorghum. Theor Appl Genet 124:13251338 Google Scholar
Lavergne, S, Molofsky, J (2007) Increased genetic variation and evolutionary potential drive the success of an invasive grass. Proc Natl Acad Sci USA 104:33833888 Google Scholar
Li, Y, Cheng, ZM, Smith, WA, Ellis, DR, Chen, YQ, Zheng, XL, Pei, Y, Luo, KM, Zhao, DG, Yao, QH, Duan, H, Li, Q. (2004) Invasive ornamental plants: Problems, challenges, and molecular tools to neutralize their invasiveness. Crit Rev Plant Sci 23:381389 Google Scholar
Lin, J, Gibbs, JP, Smart, LB (2009) Population genetic structure of native versus naturalized sympatric shrub willows ( Salix; Salicaceae). Am J Bot 96:771785 Google Scholar
Linde-Laursen, I (1993) Cytogenetic analysis of Miscanthus × giganteus, an interspecific hybrid. Hereditas 119:297300 Google Scholar
Lockwood, JL, Cassey, P, Blackburn, T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20:223228 Google Scholar
Mack, R, Erneberg, M (2002) The United States naturalized flora: largely the product of deliberate introductions. Ann Mo Bot Gard 89:176189 Google Scholar
Meyer, MH, Tchida, CL (1999) Miscanthus Anderss. produces viable seed in four USDA hardiness zones. J Environ Hortic 17:137140 CrossRefGoogle Scholar
Minnesota Department of Natural Resources (2016) Amur Silver Grass (Miscanthus sacchariflorus). http://www.dnr.state.mn.us/invasives/terrestrialplants/grasses/amursilvergrass.html. Accessed August 16, 2016Google Scholar
Minton, MS, Mack, RN (2010) Naturalization of plant populations: the role of cultivation and population size and density. Oecologia 164:399409 Google Scholar
Nei, M (1972) Genetic distance between populations. Am Nat 106:283292 Google Scholar
Nei, M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583590 Google Scholar
Nishiwaki, A, Mizuguti, A, Kuwabara, S, Toma, Y, Ishigaki, G, Miyashita, T, Yamada, T, Matuura, H, Yamaguchi, S, Rayburn, AL, Akashi, R, Stewart, JR (2011) Discovery of natural Miscanthus (Poaceae) triploid plants in sympatric populations of Miscanthus sacchariflorus and Miscanthus sinensis in southern Japan. Am J Bot 98:154159 Google Scholar
Parks, JC, Werth, CR (1993) A study of spatial features of clones in a population of bracken fern, Pteridium aquilinum (Dennstaedtiaceae). Am J Bot 80:537544 Google Scholar
Peakall, R, Smouse, PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics. DOI: 10.1093/bioinformatics/bts460Google Scholar
Pilu, R, Cassani, E, Landoni, M, Badone, FC, Passera, A, Cantaluppi, E, Corno, L, Adani, F (2014) Genetic characterization of an Italian giant reed ( Arundo donax L.) clones collection: exploiting clonal selection. Euphytica 196:169181 Google Scholar
Quinn, LD, Culley, TM, Stewart, JR (2012) Genetic comparison of introduced and native populations of Miscanthus sinensis (Poaceae), a potential bioenergy crop. Grassland Sci 58:101111 Google Scholar
R Core Team (2015) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. http://www.R-project.org/. Accessed August 16, 2016Google Scholar
Rayburn, AL, Crawford, J, Rayburn, CM, Juvik, JA (2009) Genome size of three Miscanthus species. Plant Mol Biol Rep 27:184188 Google Scholar
Reichard, SH, White, P (2001) Horticulture as a pathway of invasive plant introductions in the United States. Bioscience 51:103113 Google Scholar
Sacks, E, Juvik, J, Lin, Q, Steward, JR, Yamada, T (2013a) The gene pool of Miscanthus species and its improvement. Pages 73101 in Paterson, AH, ed. Genomics of the Saccharinae. New York: Springer.Google Scholar
Sacks, EJ, Jakob, K, Gutterson, NI, inventors; Mendel Biotechnology Inc., assignee. (2013b) High biomass Miscanthus varieties. U.S. patent 2013/0111619 A1Google Scholar
Sakai, AK, Allendorf, FW, Holt, JS, Lodge, DM, Molofsky, J, With, KA, Baughman, S, Cabin, RJ, Cohen, JE, Ellstrand, NC, McCauley, DE, O'Neil, P, Parker, IM, Thompson, JN, Weller, SG (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305332 Google Scholar
Schnitzler, A, Essl, F (2015) From horticulture and biofuel to invasion: the spread of Miscanthus taxa in the USA and Europe. Weed Res 55:221225 Google Scholar
Simpson, EH (1949) Measurement of diversity. Nature 163:688688 Google Scholar
Smith, LL, Barney, JN (2014) The relative risk of invasion: evaluation of Miscanthus × giganteus seed establishment. Invasive Plant Sci Manage 7:93106 Google Scholar
Stenberg, P, Lundmark, M, Saura, A (2003) MLGsim: a program for detecting clones using a simulation approach. Mol Ecol Notes 3:329331 CrossRefGoogle Scholar
Tamura, K, Uwatoko, N, Yamashita, H, Fujimori, M, Akiyama, Y, Shoji, A, Sanada, Y, Okumura, K, Gau, M (2016) Discovery of natural interspecific hybrids between Miscanthus sacchariflorus and Miscanthus sinensis in southern Japan: morphological characterization, genetic structure, and origin. Bioenerg Res 9:315325 Google Scholar
Yan, J, Chen, W, Luo, F, Ma, H, Meng, A, Li, X, Zhu, M, Li, SS, Zhou, HF, Zhu, WX, Han, B, Ge, S, Li, JQ, Sang, T (2012) Variability and adaptability of Miscanthus species evaluated for energy crop domestication. Glob Change Biol Bioenergy 4:4960 Google Scholar