Abstract
Perennial tall-statured grasses are regarded as a sustainable source of renewable energy for their high yields of lignocellulosic biomass, low resource input, wide ecological tolerance and capacity for storing large amounts of atmospheric CO2 in their perennial underground rhizome systems. These same traits, that make such crops agronomically attractive and sustainable, make these species highly competitive and potentially invasive. Several perennial energy crop grasses are outbreeding species that belong to cosmopolitan polyploid species complexes, i.e. groups of interbreeding species with ploidy variation. The cultivation of such highly productive and genetically diverse crops can have unwanted consequences through the evolution of invasive species. The goal of this review is to provide the scientific community, including agronomists, breeders, users and nature managers, with an introduction to the genetic dynamics occurring within the polyploid species complexes of the emerging energy species Arundo donax, Miscanthus × giganteus, Panicum virgatum, Phalaris arundinacea and Phragmites australis, and the broad biogeographical extent of their gene flow impact. Such aspects are difficult to predict, and are not captured by invasion risk assessments and by the sustainability certifications of the bioenergy supply chain. The review integrates literature from the phylogenetic, cytology, population ecology and agronomic research and focuses on the evolutionary processes that shape invasiveness that can be activated post-introduction by the dispersal of pollen, seeds and plant fragments from the energy crops to the environment. Due to the high genetic diversity of the crops, the adverse effects that genetic drift and founder effect can have on the establishment of small populations are very unlikely. On the contrary the data collected suggests that the risk of fostering panmictic continental invasive populations is high. Agronomic measures, regulations and genetic improvements that can contain dispersal from crops are discussed, as well as urgent research needs.
Similar content being viewed by others
References
Ainouche ML, Fortune PM, Salmon A, Parisod C, Grandbastien M-A, Fukunaga K, Ricou M, Misset M-T (2009) Hybridization, polyploidy and invasion: lessons from Spartina (Poaceae). Biol Invasions 11:1159–1173
Anderson EK, Lee D, Allen DJ, Voigt TB (2015) Agronomic factors in the establishment of tetraploid seeded Miscanthus × giganteus. GCB Bioenergy 7:1075–1083
Anttila CK, King RA, Ferris C, Ayres DR, Strong DR (2000) Reciprocal hybrid formation of Spartina in San Francisco Bay. Mol Ecol 9:765–770. https://doi.org/10.1046/j.1365-294x.2000.00935.x
Ayres DR, Smith DL, Zaremba K, Klohr S, Strong RD (2004) Spread of exotic cordgrasses and hybrids (Spartina sp.) in the tidal marshes of San Francisco Bay, California, USA. Biol Invasions 6:221. https://doi.org/10.1023/B:BINV.0000022140.07404.b7
Ayres DR, Grotkopp E, Zaremba K, Sloop CM, Blum MJ, Bailey JP, Anttila CK, Strong DR (2008) Hybridization between invasive Spartina densiflora (Poaceae) and native S. foliosa in San Francisco Bay, California, USA. Am J Bot 95:713–719. https://doi.org/10.3732/ajb.2007358
Barney JN (2014) Bioenergy and invasive plants: quantifying and mitigating future risks. Invasive Plant Sci Manag 7:199–209
Barney JN, DiTomaso JM (2008) Nonnative species and bioenergy: Are we cultivating the next invader? Bioscience 58:64–70. https://doi.org/10.1641/B580111
Barney JN, DiTomaso JM (2011) Global climate niche estimates for bioenergy crops and invasive species of agronomic origin: potential problems and opportunities. PLoS ONE 6(3):e17222. https://doi.org/10.1371/journal.pone.0017222
Barrett SCH (2015) Clonality and plant sexual reproduction. Proc Natl Acad Sci USA 112:8859–8866. https://doi.org/10.1073/pnas.1501712112
Blackburn TM, Lockwood JL, Cassey P (2015) The influence of numbers on invasion success. Mol Ecol 24:1942–1953. https://doi.org/10.1111/mec.13075
Bone E (2007) Post-introduction evolution in invasive Bromus tectorum. Doctoral dissertations available from ProQuest. AAI3254960. https://scholarworks.umass.edu/dissertations/AAI3254960. Accessed 12 July 2019
Bonin CL, Heaton EA, Barb J (2014) Miscanthus sacchariflorus—biofuel parent or new weed? GCB Bioenergy 6:629–636. https://doi.org/10.1111/gcbb.12098
Bonin CL, Mutegi E, Snow AA, Miriti M, Chang H, Heaton EA (2017) Improved feedstock option or invasive risk? Comparing establishment and productivity of fertile Miscanthus × giganteus to Miscanthus sinensis. Bioenergy Res 10:317–328
Bucci A, Cassani E, Landoni M, Cantaluppoi E, Pilu R (2013) Analysis of chromosome number and speculations on the origin of Arundo donax L. (Giant Reed). Cytol Genet 47:237. https://doi.org/10.3103/S0095452713040038
Bui TT, Lambertini C, Eller F, Brix H, Sorrell BK (2017) Ammonium and nitrate are both suitable inorganic nitrogen forms for the highly productive wetland grass Arundo donax, a candidate species for wetland paludiculture. Ecol Eng 105:379–386. https://doi.org/10.1016/j.ecoleng.2017.04.054
Burgarella C, Barnaud A, Kane NA, Jankowski F, Scarcelli N, Billot C, Vigouroux Y, Berthouly-Salazar C (2019) Adaptive introgression: an untapped evolutionary mechanism for crop adaptation. Front Plant Sci 10:4. https://doi.org/10.3389/fpls.2019.00004
Calderon J, Alan E, Barrantes U (2000) Structure size and production of weed seeds in the humid tropic. Agronom Mesoam 11:31–39
Canavan K, Paterson ID, Hill MP (2017a) Exploring the origin and genetic diversity of the giant reed, Arundo donax in South Africa. Invasive Plant Sci Manag 10:53–60. https://doi.org/10.1017/inp.2016.5
Canavan S, Richardson DM, Visser V, Le Roux JJ, Vorontsova MS, Wilson JRU (2017b) The global distribution of bamboos: assessing correlates of introduction and invasion. AoB Plants 9:plw078. https://doi.org/10.1093/aobpla/plw078
Canavan K, Paterson ID, Lambertini C, Hill MP (2018a) Expansive reed populations—alien invasion or disturbed wetlands? AoB Plants 10:ply014. https://doi.org/10.1093/aobpla/ply014
Canavan S, Meyerson LA, Packer JG, Pyšek P, Maurel N, Lozano V, Richardson DM, Brundu G, Canavan K, Cicatelli A, Čuda J, Dawson W, Essl F, Guarino F, Guo WY, van Kleunen M, Kreft H, Lambertini C, Pergl J, Skálová H, Soreng RJ, Visser V, Vorontsova MS, Weigelt P, Winter M, Wilson RU (2018b) Tall-statured grasses: 1 a useful functional group for invasion science. Biol Invasions 21(1):37–58. https://doi.org/10.1007/s10530-018-1815-z
Casler MD (2012) Switchgrass breeding, genetics, and genomics. In: Monti A (ed) Switchgrass, green energy and technology. Springer, London. https://doi.org/10.1007/978-1-4471-2903-5_2
Cavallaro V, Scordia D, Cosentino SL, Copan V (2019) Up-scaling agamic propagation of giant reed (Arundo donax L.) by means of single-node stem cuttings. Ind Crops Prod 128:534–544. https://doi.org/10.1016/j.indcrop.2018.11.057
Chambers RM, Meyerson LA, Saltonstall K (1999) Expansion of Phragmites australis into tidal wetlands of North America. Aquat Bot 64:261–273
Chang Z, Chen Z, Wang N, Xie G, Lu J, Yan W, Zhou J, Tang X, Deng XW (2016) Construction of a male sterility system for hybrid rice breeding and seed production using a nuclear male sterility gene. Proc Natl Acad Sci USA 113:14145–14150
Chang H, Snow AA, Mutegi E, Lewis EM, Heaton EA (2018) Extent of pollen-mediated gene flow and seed longevity in switchgrass (Panicum virgatum L.): implications for biosafety procedures. Biomass Bioenergy 109:114–124
Chown SL, Hodgins KA, Griffin PC, Oakeshott JG, Byrne M, Hoffmann AA (2015) Biological invasions, climate change and genomics. Evol Appl 8(1):23–46. https://doi.org/10.1111/eva.12234
Chu H, Cho WK, Jo Y, Kim W-II, Rim Y, Kim R-Y (2011) Identification of natural hybrids in Korean Phragmites using haplotype and genotype analyses. Plant Systs Evol 293:247–253
Cibin R, Trybula E, Chaubey I, Brouder SM, Volenec JJ (2016) Watershed-scale impacts of bioenergy crops on hydrology and water quality using improved SWAT model. GCB Bioenergy 8:837–848. https://doi.org/10.1111/gcbb.12307
Clark LV, Stewart JR, Nishiwaki A, Toma Y, Bonderup Kjeldsen J, Joergensen U, Zhao H, Peng J, Yoo JH, Heo K, Yu CY, Yamada T, Sacks EJ (2015) Genetic structure of Mscanthus sinensis and Miscanthus sacchariflorus in Japan indicates a gradient of bidirectional but asymmetric introgression. J Exp Bot 66:4213–4225
Colmer TD, Pedersen O (2008) Underwater photosynthesis and respiration in leaves of submerged wetland plants: gas films improve CO2 and O2 exchange. New Phytol 177:918–926
D’Hont A, Glaszmann FP, Glaszmann JC (2002) Oligoclonal interspecific origin of ‘North Indian’ and ‘Chinese’ sugarcanes. Chromosome Res 10:253–262
D’Hont A, Ison D, Alix K, Roux C, Glaszmann JC (2011) Determination of basic chromosome numbers in the genus Saccharum by physical mapping of ribosomal RNA genes. Genome 41:221–225
Davis SC, Kucharik CJ, Fazio S, Monti A (2013) Environmental sustainability of advanced biofuels. Biofuels Bioprod Bioref 7:638–646. https://doi.org/10.1002/bbb.1439
Dempewolf H, Hodgins KA, Rummell SE, Ellstrand NC, Rieseberg LH (2012) Reproductive isolation during domestication. Plant Cell 24:2710–2717
Dibble KL, Meyerson LA (2012) Tidal flushing restores the physiological condition of fish residing in degraded salt marshes. PLoS ONE 7:e46161. https://doi.org/10.1371/journal.pone.0046161
Dong M, Yu FH, Alpert P (2014) Ecological consequences of plant clonality. Ann Bot 114(2):367. https://doi.org/10.1093/aob/mcu137
Ecker G, Zalapa J, Auer C (2015) Switchgrass (Panicum virgatum L.) genotypes differ between coastal sites and inland road corridors in the northeastern US. PLoS ONE 10(6):e0130414. https://doi.org/10.1371/journal.pone.0130414
Eller F, Skálová H, Caplan JS, Bhattarai GP, Burger MK, Cronin JT, Guo W, Guo X, Hazelton ELG, Kettenring KM, Lambertini C, McCormick MK, Meyerson LA, Mozdzer TJ, Pyšek P, Sorrell BK, Whigham DF, Brix H (2017) Cosmopolitan species as ecophysiological models for responses to global change: the common reed Phragmites australis. Front Plant Sci 8:1833. https://doi.org/10.3389/fpls.2017.01833
Fabbrini F, Ludovisi R, Alasia O, Flexas J, Douthe C, Ribas Carbó M, Robson MA, Taylor G, Scarascia-Mugnozza G, Keurentjes JJB, Harfouche A (2019) Characterization of phenology, physiology, morphology and biomass traits across a broad Euro-Mediterranean ecotypic panel of the lignocellulosic feedstock Arundo donax. GCB Bioenergy 11:152–170. https://doi.org/10.1111/gcbb.12555
FAIR-5-CT97-3701 (1998–2001) Switchgrass as an alternative energy crop in Europe. Initiation of a productivity network. Final report for the period from 01-04-1998 to 30-09-2001. https://www.switchgrass.nl/upload_mm/3/0/6/a0982a5d-bb01-4054-92bc-d7ba96c8fa7a_Elbersen%20et%20al%202003.%20Final%20report%20Eu%20switchgrass%20project.pdf. Accessed 12 July 2019
Fér T, Hroudová Z (2009) Genetic diversity and dispersal of Phragmites australis in a small river system. Aquat Bot 90:165–171
Gao L, Tang S, Zhuge L, Nie M, Zhu Z, Li B, Yang G (2012) Spatial genetic structure in natural populations of Phragmites australis in a mosaic of saline habitats in the Yellow River Delta, China. PLoS ONE 7(8):e43334. https://doi.org/10.1371/journal.pone.0043334
Geng Y, van Klinken RD, Sosa A, Li B, Chen J, Xu CY (2016) The relative importance of genetic diversity and phenotypic plasticity in determining invasion success of a clonal weed in the USA and China. Front Plant Sci 24(7):213. https://doi.org/10.3389/fpls.2016.00213
Germain RM, Weir JT, Gilbert B (2016) Species coexistence: macroevolutionary relationships and the contingency of historical interactions. Proc R Soc B 283:20160047. https://doi.org/10.1098/rspb.2016.0047
Glowacka K, Clark LV, Adhikari S, Peng J, Stewart R, Nishiwaki A, Yamada T, Joergensen U, Hodkinson TR, Gifford J, Juvik JA (2015) Genetic variation in Miscanthus × giganteus and the importance of estimating genetic distance thresholds for differentiating clones. GCB Bioenergy 7:386–404
Gramlich S, Sagmeister P, Dullinger S, Hadacek F, Hörandl E (2016) Evolution in situ: hybrid origin and establishment of willows (Salix L.) on alpine glacier forefields. Heredity 116:531–541
Greef JM, Deuter M, Jung C, Schondelmaier J (1997) Genetic diversity of European Miscanthus species revealed by AFLP fingerprinting. Genet Resour Crop Evol 44:185–195
Guarino F, Cicatelli A, Brundu G, Improta G, Triassi M, Castiglione S (2019) The use of MSAP reveals epigenetic diversity of the invasive clonal populations of Arundo donax L. PLoS ONE 14(4):e0215096. https://doi.org/10.1371/journal.pone.0215096
Guo WY, Lambertini C, Nguyen LX, Li XZ, Brix H (2014) Pre-adaptation and post-introduction evolution facilitate the invasiveness of Phragmites australis in North America. Ecol Evol 4:4567–4577. https://doi.org/10.1002/ece3.1286
Haddadchi A, Gross CL, Fatemi M (2013) The expansion of sterile Arundo donax (Poaceae) in southwestern Australia is accompanied by genotypic variation. Aquat Bot 104:153–161
Hamrick J, Godt M (1996) Effects of life history traits on genetic diversity in plant species. Philos Trans R Soc Lond B Biol Sci 351:1291–1298
Hardion L, Verlaque R, Baumel A, Juin M, Vila B (2012) Revised systematics of Mediterranean Arundo (Poaceae) based on AFLP fingerprints and morphology. Taxxon 61(6):1217–1226
Hardion L, Verlaque R, Rosato M, Rossello JA, Vila B (2015) Impact of polyploidy on fertility variation of Mediterranean Arundo L. (Poaceae). C R Biol 338:298–306. https://doi.org/10.1016/j.crvi.2015.03.013
Hastings A, Clifton-Brown JC, Wattenbach M, Stampfl P, Mitchell CP, Smith P (2009) Future energy potential of Miscanthus in Europe. GCB Bioenergy 1:180–196
Haworth M, Cosentino SL, Marino G, Brunetti C, Scordia D, Testa G, Riggi E, Avola G, Loreto F, Centritto M (2017) Physiological responses of Arundo donax ecotypes to drought: a common garden study. GCB Bioenergy 9:132–143. https://doi.org/10.1111/gcbb.12348
Hazelton EG, Mozdzer TJ, Burdick D, Kettenring KM, Whigham DF (2014) Phragmites australis management in the United States: 40 years of methods and outcomes. AoB Plants 6:plu001. https://doi.org/10.1093/aobpla/plu001
Herrera AM, Dudley TL (2003) Reduction of riparian arthropod abundance and diversity as a consequence of giant reed (Arundo donax) invasion. Biological Invasions 2003(5):167. https://doi.org/10.1023/A:1026190115521
Hodkinson TR, Chase MW, Liedò MD, Salamin N, Renovize AS (2002) 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 115:381–392
Holland RA, Eigenbrod F, Muggeridge A, Brown G, Clarke D, Taylor G (2015) A synthesis of the ecosystem services impact of second-generation bioenergy crop production. Renew Sustain Energy Rev. https://doi.org/10.1016/j.rser.2015.02.003
Hurry C, James EA, Thompson RM (2013) Connectivity, genetic structure and stress response of Phragmites australis: issues for restoration in a salinising wetland system. Aquat Bot 104:138–146. https://doi.org/10.1016/j.aquabot.2012.08.00
Huxel GR (1999) Rapid displacement of native species by invasive species: effects of hybridization. Biol Conserv 89:143–152
Hyldegaard B, Lambertini C, Brix H (2017) Phylogeography reveals a potential cryptic invasion in the Southern Hemisphere of Ceratophyllum demersum, New Zealand’s worst invasive macrophyte. Sci Rep 7:16569. https://doi.org/10.1038/s41598-017-16712-8
Jakubowski AR, Jackson RD, Johnson RC, Jinguo H, Casler MD (2011) Genetic diversity and population structure of Eurasian populations of reed canarygrass: cytotypes, cultivars and interspecific hyrbids. Crop Pasture Sci 62:982–991
Jannoo N, Grivet L, David J, D’Hont A, Glaszmann J-C (2004) Differential chromosome pairing affinities at meiosis in polyploid sugarcane revealed by molecular markers. Heredity 93:460–467
Kavova T, Kubatova B, Curn V, Anderson NO (2018) Genetic variability of US and Czech Phalaris arundinacea L. Wild and cultivated populations. In: Edvan RL, Bezerra LR (eds) New perspective in forage crops. Intech, Rijeka, pp 169–186. https://doi.org/10.5772/intechopen.69669
Kettenring KM, Mock KE (2012) Genetic diversity, reproductive mode, and dispersal differ between the cryptic invader, Phragmites australis, and its native conspecific. Biol Invasions. https://doi.org/10.1007/s10530-012-0246-5
Kettenring KM, de Blois S, Hauber DP (2012) Moving from a regional to a continental perspective of Phragmites australis invasion in North America. AoB Plants 2012:pls040. https://doi.org/10.1093/aobpla/pls040
Kiviat E (2013) Ecosystem services of Phragmites in North America with emphasis on habitat functions. AoB Plants 5:plt008. https://doi.org/10.1093/aobpla/plt008
Knight CA, Molinari NA, Petrov DA (2005) The large genome constraint hypothesis: evolution, ecology and phenotype. Ann Bot 95:177–190. https://doi.org/10.1093/aob/mci011
Lambertini C (2016) Heteroplasmy due to chloroplast paternal leakage: another insight into Phragmites haplotypic diversity in North America. Biol Invasions 18:2443–2455
Lambertini C, Gustafsson MHG, Frydenberg J, Lissner J, Speranza M, Brix H (2006) A phylogeographic study of the cosmopolitan genus Phragmites (Poaceae) based on AFLPs. Plant Syst Evol 258:161–182. https://doi.org/10.1007/s00606-006-0412-2
Lambertini C, Gustafsson MHG, Frydenberg J, Speranza M, Brix H (2008) Genetic diversity patterns in Phragmites australis at the population, regional and continental scales. Aquat Bot 88:160–170
Lambertini C, Riis T, Olesen B, Clayton JS, Sorrell BK, Brix H (2010) Genetic diversity in three invasive clonal aquatic species in New Zealand. BMC Genet 11:1–18
Lambertini C, Mendelsshon I, Gustafsson MGH, Olesen B, Riis T, Sorrell BK, Brix H (2012a) Tracing the origin of Gulf Coast Phragmites—a story of long distance dispersal and hybridization. Am J Bot 99:538–551
Lambertini C, Sorrell BK, Riis T, Olesen B, Brix H (2012b) Exploring the borders of European Phragmites within a cosmopolitan genus. AoB Plants 2012:pls020. https://doi.org/10.1093/aobpla/pls020
Landis D, Gratton C, Jackson R, Gross K, Duncan D, Liang C, Meehan T, Robertson B, Schmidt T, Stahlheber K, Tiedje J, Werling B (2018) Biomass and biofuel crop effects on biodiversity and ecosystem services in the North Central US. Biomass Bioenergy 114:18–29
Larkin DJ (2012) Lengths and correlates of lag phases in upper-Midwest plant invasions. Biol Invasions 14:827–838
Lavergne S, Molofsky J (2004) Reed canary grass (Phalaris arundinacea) as a biological model in the study of plant invasions. CRC Crit Rev Plant Sci 3:415–429. https://doi.org/10.1080/07352680490505934
Lavergne S, Molofsky J (2007) Increased genetic variation and evolutionary potential drive the success of an invasive grass. Proc Natl Acad Sci USA 104:3883–3888
Le Roux JJ, Wieczorek AM, Wright MG, Tran CT (2007) Super-genotype: global monoclonality defies the odds of nature. PLoS ONE 2(7):e590. https://doi.org/10.1371/journal.pone.0000590
Lee AK, Ayres DR, Pakenham-Walsh MR, Strong DR (2016) Responses to salinity of Spartina hybrids formed in San Francisco Bay, California (S. alterniflora × foliosa and S. densiflora × foliosa). Biol Invasions 18:2207. https://doi.org/10.1007/s10530-015-1011-3
Lewandowski I, Scurlock JMO, Lindvall E, Christou M (2003) The development and current status of perennial rhizomatous grasses as energy crops in the US and Europe. Biomass Bioenergy 25:335–361
Lewis KC, Porter RD (2014) Global approaches to addressing biofuel-related invasive species risks and incorporation into U.S. laws and policies. Ecol Monogr 84:171–201. https://doi.org/10.1890/13-1625.1
Linde-Laursen IB (1993) Cytogenic analysis of Miscanthus ‘Giganteus’ and interspecific hybrid. Hereditas 119:297–300
Liu H, Yang M, Wu K, Zhou X, Zhao Y (2013) Development, inheritance and breeding potential of a recessive genic male sterile line D248A in Sesame (Sesamum indicum L.). SpringerPlus 2:268. https://doi.org/10.1186/2193-1801-2-268
Liu Y, Zhang L, Xu X, Niu H (2015) Understanding the wide geographic range of a clonal perennial grass: plasticity versus local adaptation. AoB Plants 8:plv141. https://doi.org/10.1093/aobpla/plv141
Lowe S, Browne M, Boudjelas S, De Poorter M (2000) 100 of the world’s worst invasive alien species. A selection from the global invasive species database. In: ISSG (Invasive Species Specialist Group of the Species Survival Commission of the IUCN). Aliens 12. Hollands Printing Ltd., Aukland
Malone JA, Virtue JG, Williams C, Preston C (2017) Genetic diversity of giant reed (Arundo donax) in Australia. Weed Biol Manag 17:17–28
Marbuah G, Gren I-M, McKie B (2014) Economics of harmful invasive species: a review. Diversity 6:500–5023
Marchant CJ (1963) Corrected chromosome numbers for Spartina × townsendii and its parent species. Nature 31:929
Mariani C, Cabrini R, Danin A, Piffanelli P, Fricano A, Gomarasca S, Dicandilo M, Grassi F, Soave C (2010) Origin, diffusion and reproduction of the giant reed (Arundo donax L.): a promising weedy energy crop. Ann Appl Biol 157:191–202
Maron JL, Vilà M, Bommarco R, Elmendorf S, Beardsley P (2004) Rapid evolution of an invasive plant. Ecol Monogr 74:261–280. https://doi.org/10.1890/03-4027
Martin LJ, Blossey B (2013) The Runaway Weed: costs and Failures of Phragmites australis management in the USA. Estuaries Coast 36:626–632. https://doi.org/10.1007/s12237-013-9593-4
McCormick MK, Kettenring KM, Baron HM, Whigham DF (2010) Spread of invasive Phragmites australis in estuaries with differing degrees of development: genetic patterns, Allee effects and interpretation. J Ecol 98:1369–1378. https://doi.org/10.1111/j.1365-2745.2010.01712.x
Meyerson LA, Chambers RM, Vogt KA (1999) The effects of Phragmites removal on nutrient pools in a freshwater tidal marsh ecosystem. Biol Invasions 1:129–136
Meyerson LA, Cronin JT, Pysek P (2016) Phragmites australis as a model organism for studying plant invasions. Biol Invasions 18:2421–2431
Michel A, Arias RS, Scheffler BE, Duke SO, Netherland M, Dayan FE (2004) Somatic mutation-mediated evolution of herbicide resistance in the nonindigenous invasive plant hydrilla (Hydrilla verticillata). Mol Ecol 13:3229–3237. https://doi.org/10.1111/j.1365-294X.2004.02280.x
Milano ER, Lowry DB, Juenger TE (2016) The genetic basis of upland/lowland ecotype divergence in switchgrass (Panicum virgatum). G3 Genes Genom Genet 6(11):3561–3570. https://doi.org/10.1534/g3.116.032763
Milner S, Holland RA, Lovett A, Sunnenberg G, Hastings A, Smith P, Wang S, Taylor G (2016) Potential impacts on ecosystem services of land use transitions to second-generation bioenergy crops in GB. GCB Bioenergy 8:317–333. https://doi.org/10.1111/gcbb.12263
Miriti MN, Ibrahim T, Palik D, Bonin C, Heaton E, Mutegi E, Snow AA (2017) Growth and fecundity of fertile Miscanthus × giganteus (“PowerCane”) compared to feral and ornamental Miscanthus sinensis in a common garden experiment: implications for invasion. Ecol Evol 7:5703–5712
Mitsuda N, Hiratsu K, Todaka D, Nakashima K, Yamaguchi-Shinozaki K, Ohme-Takagi M (2006) Efficient production of male and female sterile plants by expression of a chimeric repressor in Arabidopsis and rice. Plant Biotechnol J 4:325–332. https://doi.org/10.1111/j.1467-7652.2006.00184.x
Monti A (2012) Switchgrass. A valuable biomass crop for energy. Springer, London
Moon Y-H, Cha Y-L, Choi Y-H, Yoon Y-M, Koo B-C, Ahn J-W, An G-H, Kim J-K, Park K-G (2013) Diversity in ploidy levels and nuclear DNA amounts in Korean Miscanthus species. Euphytica 193:317–326
Morais P, Reichard M (2018) Cryptic invasions: a review. Sci Total Environ 613:1438–1448
Mukherjee SK (1957) Origin and distribution of Saccharum. Bot Gaz 119:55–61
Mutegi E, Stottlemyer AL, Snow AA, Sweeney PM (2014) Genetic structure of remnant populations and cultivars of switchgrass (Panicum virgatum) in the context of prairie conservation and restoration. Restor Ecol 22:223–231. https://doi.org/10.1111/rec.12070
Mutegi E, Snow A, Bonin CL, Heaton EA, Chang H, Gernes CJ, Palik DJ, Miriti MN (2016) Population genetics and seed set in feral, ornamental Miscanthus sacchariflorus. Invasive Plant Sci Manag 9(3):214–228
Nageswara-Rao M, Hanson M, Agarwal S, Stewart CN Jr, Kwit C (2014) Genetic diversity analysis of switchgrass (Panicum virgatum L.) populations using microsatellites and chloroplast sequences. Agrofor Syst 88:834
Narasimhamoorthy B, Saha MC, Swaller T, Bouton JH (2008) Genetic diversity in switchgrass collections assessed by EST-SSR markers. Bioenergy Res 1:136–146
Nassi o Di Nasso N, Roncucci N, Triana F, Tozzini C, Bonari E (2011) Productivity of giant reed (Arundo donax L.) and miscanthus (Miscanthus × giganteus Greef et Deuter) as energy crops: growth analysis. Ital J Agron 6(3):e22. https://doi.org/10.4081/ija.2011.e22
Nelson MF, Anderson NO, Casler MD, Jakubowski AR (2014) Population genetic structure of N. American and European Phalaris arundinacea L. as inferred from inter-simple sequence repeat markers. Biol Invasions 16:353–363
Nielsen PN (1987) The productivity of the Miscanthus cultivar Giganteus. Tidsskrift Planteavl 91:361–368
Osabe K, Kawanabe T, Sasaki T, Ishikawa R, Okazaki K, Dennis ES, Kazama T, Fujimoto R (2012) Multiple mechanisms and challenges for the application of allopolyploidy in plants. Int J Mol Sci 13(7):8696–8721. https://doi.org/10.3390/ijms13078696
Otto SP, Whitton J (2000) Polyploid incidence and evolution. Ann Rev Genet 34:401–437
Ozudogru EA, Roncasaglia R, Correa da Silva DP, da Conceição Moreira F, Lambardi M (2016) Cryopreservation of embryogenic callus of Arundo donax L. Acta Hortic 1113:27–34. https://doi.org/10.17660/ActaHortic.2016.1113.4
Packer JG, Meyerson LA, Richardson DM, Brundu G, Allen WJ, Bhattarai GP, Brix H, Canavan S, Castiglione S, Cicatelli A, Čuda J, Cronin JT, Eller F, Guarino F, Guo WH, Guo WY, Guo X, Hierro J, Lambertini C, Liu J, Lozano V, Mozdzer TJ, Skálová H, Wang R, Pyšek P (2016) Global networks for invasion science: benefits, challenges and guidelines. Biol Invasions 19:1081–1096. https://doi.org/10.1007/s10530-016-1302-3
Packer JG, Meyerson LA, Skálová H, Pyšek P, Kueffer C (2017) Biological Flora of the British Isles: Phragmites australis. J Ecol 105:1123–1162. https://doi.org/10.1111/1365-2745.12797
Palik DJ, Snow AA, Stottlemyer AL, Miriti MN, Heaton EA (2016) Relative performance of non-local cultivars and local, wild populations of switchgrass (Panicum virgatum) in competition experiments. PLoS ONE 11(4):e0154444. https://doi.org/10.1371/journal.pone.0154444
Pandit MK, White SM, Pocock MJ (2014) The contrasting effects of genome size, chromosome number and ploidy level on plant invasiveness: a global analysis. New Phytol 203:697–703. https://doi.org/10.1111/nph.12799
Paul J, Kirk H, Freeland J (2011) Genetic diversity and differentiation of fragmented reedbeds (Phragmites australis) in the United Kingdom. Hydrobiologia 665:107–115
Perdereau A, Klaas M, Barth S, Hodkinson TR (2017) Plastid genome sequencing reveals biogeographical structure and extensive population genetic variation in wild populations of Phalaris arundinacea L. in north-western Europe. GCB Bioenergy 9:46–56
Pikaard CS, Mittelsten Scheid O (2014) Epigenetic regulation in plants. Cold Spring Harb Perspect Biol 6(12):a019315. https://doi.org/10.1101/cshperspect.a019315
Pinheiro F, Dantas-Queiroz MV, Palma-Silva C (2018) Plant species complexes as models to understand speciation and evolution: a review of South American studies. Critical Rev Plant Sci 37(1):54–80
Premachandran MN, Prathima PT, Lekshmi M (2011) Sugarcane and polyploidy, a review. J Sugarcane Res 1:1–15
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Pyšek P, Richardson DM (2008) Traits associated with invasiveness in alien plants: Where do we stand? In: Nentwig W (ed) Biological invasions. Ecological studies (analysis and synthesis), vol 193. Springer, Berlin
Ramirez-Almeyda J, Elbersen B, Monti A, Staritsky I, Panoutsou K, Alexopoulou E, Schrijver R, Elbersen W (2017) Assessing the potentials for non food crops. In: Panoutsou K (ed) Modeling and optimization of biomass supply chains. Top-down and Bottom-up assessment for agricultural, forest and waste feedstock. Elsevier, Amsterdam
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 9:981–993. https://doi.org/10.1111/j.1461-0248.2006.00950.x
Roques L, Garnier J, Hamel F, Klein EK (2012) Allee effect promotes diversity in traveling waves. Proc Natl Acad Sci USA 109:8828–8833. https://doi.org/10.1073/pnas.1201695109
Sablock G, Fu Y, Bobbio V, Laura M, Rotino GL, Bagnaresi P, Allavena A, Velikova V, Viola R, Loreto F, Li M, Varotto C (2014) Fuelling genetic and metabolic exploration of C3 bioenergy crops through the first reference transcriptome of Arundo donax L. Plant Biotechnol J 12:554–567
Sacks EJ, Jakob K, Gutterson NI (2013) Patent application US 2013/0111619 A1. United States Patent Application Publication
Sahramaa M (2004) Evaluating germplasm of reed canary grass, Phalaris arundinacea L. PhD thesis, University of Helsinki. ISBN 952-10-1836-4
Saltonstall K (2002) Cryptic invasion by a non-native genotype of the common reed, Phragmites australis, into North America. Proc Natl Acad Sci USA 99:2445–2449
Saltonstall K (2003) Microsatellite variation within and among North American lineages of Phragmites australis. Mol Ecol 12:1689–1702
Saltonstall K (2011) Remnant native Phragmites australis maintains genetic diversity despite multiple threats. Conserv Genet 12:1027. https://doi.org/10.1007/s10592-011-0205-1
Saltonstall K, Lambert A, Meyerson LA (2010) Genetics and reproduction of common (Phragmites australis) and giant reed (Arundo donax). Invasive Plant Sci Manag 3:495–505
Slomka A, Kuta E, Plazek A, Dubert F, Zur I, Dubas E, Kopec P, Zurek G (2012) Sterility of Miscanthus × giganteus results from hybrid incompatibility. Acta Biol Crac Ser Bot 54(1):113–120
Smith LL, Barney JN (2014) The relative risk of invasion: evaluation of Miscanthus × giganteus seed establishment. Invasive Plant Sci Manag 7:93–106
Smith L, Tekiela D, Barney J (2015) Predicting biofuel invasiveness: a relative comparison to crops and weeds. Invasive Plant Sci Manag 8(3):323–333. https://doi.org/10.1614/IPSM-D-15-00001.1
Soltis PS, Soltis DE (2000) The role of genetic and genomic attributes in the success of polyploids. Proc Natl Acad Sci USA 97:7051–7057
Spencer DF, Stocker RK, Liow PS, Whitehand LC, Ksander GG, Fox AM et al (2008) Comparative growth of giant reed (Arundo donax L.) from Florida, Texas, and California. J Aquat Plant Manag 46:89
Strong DR, Ayres DA (2016) Control and consequences of Spartina spp. invasions with focus upon San Francisco Bay. Biol Invasions 18:2237–2246. https://doi.org/10.1007/s10530-015-0980-6
Suda J, Meyerson LA, Leitch IJ, Pyšek P (2015) The hidden side of plant invasions: the role of genome size. New Phytol 205:994–1007. https://doi.org/10.1111/nph.13107
Sybenga J (1996) Chromosome pairing affinity and quadrivalent formation in polyploids: do segmental allopolyploids exist? Genome 39:1176–1184
Tanaka TST, Irbis C, Inamura T (2017) Phylogenetics analyses of Phragmites australis spp. in southwest China identified two lineages and their hybrids. Plant Syst Evol 303:699–707
Tarin D, Pepper AE, Goolsby JA, Moran PJ, Contreras A, Kirk AE, Manhart JR (2013) Microsatellites uncover multiple introductions of clonal gianY reed (Arundo donax). Invasive Plant Sci Manag 6:328–338
te Beest M, Le Roux JJ, Richardson DM, Brysting AK, Suda J, Kubešová M, Pyšek P (2012) The more the better? The role of polyploidy in facilitating plant invasions. Ann Bot 109:19–45. https://doi.org/10.1093/aob/mcr277
Triplett JK, Wang Y, Zhong J, Kellogg EA (2012) five nuclear loci resolve the polyploid history of switchgrass (Panicum virgatum L.) and relatives. PLoS ONE 7(6):e38702. https://doi.org/10.1371/journal.pone.0038702
Ueno S, Rodrigues JF, Alves-Pereira A, Pansarin ER, Veasey EA (2015) Genetic variability within and among populations of an invasive, exotic orchid. AoB Plants 7:plv077. https://doi.org/10.1093/aobpla/plv077
Valli F (2017) Physical mutagenesis in giant reed (Arundo donax L.) and phenotypic and genomic characterization of mutagenized clones. PhD thesis, University of Bologna, Italy. http://amsdottorato.unibo.it/8196/1/Fabio%20Valli%20tesi%20dottorato.pdf. Accessed 12 July 2019
Valli F, Trebbi D, Zegada-Lizarazu W, Monti A, Tuberosa S, Salvi S (2017) In vitro physical mutagenesis of giant reed (Arundo donax L.). GCB Bioenergy 9:1380–1389. https://doi.org/10.1111/gcbb.12458
van Kleunen M, Schlaepfer DR, Glaettli M, Fischer M (2011) Preadapted for invasiveness: do species traits or their plastic response to shading differ between invasive and non-invasive plant species in their native range? J Biogeogr 38:1294–1304. https://doi.org/10.1111/j.1365-2699.2011.02495.x
Voshell SM, Baldini RM, Hilu KW (2015) Infrageneric treatment of Phalaris (Canary grasses, Poaceae) based on molecular phylogenetics and floret structure. Aust Syst Bot 28:355–367
Wang B, Li W, Wang J (2005) Genetic diversity of Alternanthera philoxxeroides in China. Aquat Bot 81:277–283
Whitney KD, Gabler CA (2008) Rapid evolution in introduced species, ‘invasive traits’ and recipient communities: challenges for predicting invasive potential. Divers Distrib 14:569–580
Zanetti F, Zegada-Lizarazu W, Lambertini C, Monti A (2019) Salinity effects on germination, seedlings and full-grown plants of upland and lowland switchgrass cultivars. Biomass Bioenergy 120:273–280. https://doi.org/10.1016/j.biombioe.2018.11.031
Zhang Y, Zhang D, Barret SC (2010) Genetic uniformity characterizes the invasive spread of water hyacinth (Eichhornia crassipes), a clonal aquatic plant. Mol Ecol 19:1774–1786. https://doi.org/10.1111/j.1365-294X.2010.04609.x
Zhang Y, Zalapa JE, Jakubowski AR, Price DL, Acharya A, Wei Y, Brummer EC, Kaeppler SM, Casler MD (2011) Post-glacial evolution of Panicum virgatum: centers of diversity and gene pools revealed by SSR markers and cpDNA sequences. Genetica 139:933–948
Zhao H, Wang B, He J, Yang J, Pan L, Sun D, Peng J (2013) Genetic diversity and population structure of Miscanthus sinesis germplasm in China. PLoS ONE 8(10):e75672. https://doi.org/10.1371/journal.pone.0075672
Zhao Y, Basak S, Fleener CE, Egnin M, Sacks EJ, Prakash CS, He G (2016) Genetic diversity of Miscanthus sinensis in US naturalized populations. GCB Bioenergy 9:965–972
Acknowledgements
The colleagues at the Department of Agriculture and Food Sciences of the University of Bologna are thanked for their engagement in discussions on non-food crops. Mats H. G. Gustafsson and the Co-Editor in Chief of Biological Invasions, Laura A. Meyerson, the Editor, and three anonymous reviewers are thanked for the critical and valuable comments to the manuscript. Kim Canavan and Susan Canavan are thanked for the final critical reading of the manus and the text improvements.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Lambertini, C. Why are tall-statured energy grasses of polyploid species complexes potentially invasive? A review of their genetic variation patterns and evolutionary plasticity. Biol Invasions 21, 3019–3041 (2019). https://doi.org/10.1007/s10530-019-02053-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-019-02053-2