Why are tall-statured energy grasses of polyploid species complexes potentially invasive? A review of their genetic variation patterns and evolutionary plasticity

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.

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References

  1. 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

    Article  Google Scholar 

  2. Anderson EK, Lee D, Allen DJ, Voigt TB (2015) Agronomic factors in the establishment of tetraploid seeded Miscanthus × giganteus. GCB Bioenergy 7:1075–1083

    Article  Google Scholar 

  3. 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

    Article  CAS  PubMed  Google Scholar 

  4. 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

    Article  Google Scholar 

  5. 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

    Article  PubMed  Google Scholar 

  6. Barney JN (2014) Bioenergy and invasive plants: quantifying and mitigating future risks. Invasive Plant Sci Manag 7:199–209

    Article  Google Scholar 

  7. 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

    Article  Google Scholar 

  8. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Barrett SCH (2015) Clonality and plant sexual reproduction. Proc Natl Acad Sci USA 112:8859–8866. https://doi.org/10.1073/pnas.1501712112

    Article  CAS  PubMed  Google Scholar 

  10. 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

    Article  PubMed  Google Scholar 

  11. 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

  12. 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

    Article  Google Scholar 

  13. 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

    Article  Google Scholar 

  14. 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

    Article  Google Scholar 

  15. 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

    Article  Google Scholar 

  16. 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

    Article  PubMed  PubMed Central  Google Scholar 

  17. Calderon J, Alan E, Barrantes U (2000) Structure size and production of weed seeds in the humid tropic. Agronom Mesoam 11:31–39

    Article  Google Scholar 

  18. 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

    Article  Google Scholar 

  19. 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

    Article  Google Scholar 

  20. 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

    Article  PubMed  PubMed Central  Google Scholar 

  21. 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

    Article  Google Scholar 

  22. 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

    Google Scholar 

  23. 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

    Article  CAS  Google Scholar 

  24. Chambers RM, Meyerson LA, Saltonstall K (1999) Expansion of Phragmites australis into tidal wetlands of North America. Aquat Bot 64:261–273

    Article  Google Scholar 

  25. 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

    Article  CAS  PubMed  Google Scholar 

  26. 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

    Article  Google Scholar 

  27. 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

    Article  PubMed  Google Scholar 

  28. 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

    Article  Google Scholar 

  29. 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

    Article  Google Scholar 

  30. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. 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

    Article  CAS  PubMed  Google Scholar 

  32. D’Hont A, Glaszmann FP, Glaszmann JC (2002) Oligoclonal interspecific origin of ‘North Indian’ and ‘Chinese’ sugarcanes. Chromosome Res 10:253–262

    Article  PubMed  Google Scholar 

  33. 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

    Article  Google Scholar 

  34. 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

    Article  CAS  Google Scholar 

  35. Dempewolf H, Hodgins KA, Rummell SE, Ellstrand NC, Rieseberg LH (2012) Reproductive isolation during domestication. Plant Cell 24:2710–2717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Dong M, Yu FH, Alpert P (2014) Ecological consequences of plant clonality. Ann Bot 114(2):367. https://doi.org/10.1093/aob/mcu137

    Article  PubMed  PubMed Central  Google Scholar 

  38. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. 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

    Article  PubMed  PubMed Central  Google Scholar 

  40. 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

    Article  CAS  Google Scholar 

  41. 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

  42. Fér T, Hroudová Z (2009) Genetic diversity and dispersal of Phragmites australis in a small river system. Aquat Bot 90:165–171

    Article  Google Scholar 

  43. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. 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

    Article  Google Scholar 

  45. 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

    Article  PubMed  Google Scholar 

  46. 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

    Article  CAS  Google Scholar 

  47. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. 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

    Article  Google Scholar 

  49. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. 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

    Article  PubMed  PubMed Central  Google Scholar 

  51. 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

    Article  Google Scholar 

  52. 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

    Article  Google Scholar 

  53. 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

    Article  Google Scholar 

  54. 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

    Article  PubMed  Google Scholar 

  55. 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

    Article  Google Scholar 

  56. 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

    Article  CAS  Google Scholar 

  57. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. 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

    Article  Google Scholar 

  59. 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

    Article  CAS  PubMed  Google Scholar 

  60. 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

    Article  Google Scholar 

  61. 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

    Article  Google Scholar 

  62. Huxel GR (1999) Rapid displacement of native species by invasive species: effects of hybridization. Biol Conserv 89:143–152

    Article  Google Scholar 

  63. 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

    Article  CAS  Google Scholar 

  64. 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

    Article  Google Scholar 

  65. 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

    Article  CAS  PubMed  Google Scholar 

  66. 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

    Google Scholar 

  67. 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

    Article  Google Scholar 

  68. 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

    Article  PubMed  PubMed Central  Google Scholar 

  69. 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

    Article  PubMed Central  Google Scholar 

  70. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Lambertini C (2016) Heteroplasmy due to chloroplast paternal leakage: another insight into Phragmites haplotypic diversity in North America. Biol Invasions 18:2443–2455

    Article  Google Scholar 

  72. 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

    Article  Google Scholar 

  73. 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

    Article  CAS  Google Scholar 

  74. 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

    Article  CAS  Google Scholar 

  75. 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

    Article  CAS  PubMed  Google Scholar 

  76. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. 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

    Article  Google Scholar 

  78. Larkin DJ (2012) Lengths and correlates of lag phases in upper-Midwest plant invasions. Biol Invasions 14:827–838

    Article  Google Scholar 

  79. 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

    Article  Google Scholar 

  80. 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

    Article  CAS  PubMed  Google Scholar 

  81. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. 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

    Article  Google Scholar 

  83. 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

    Article  Google Scholar 

  84. 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

    Article  Google Scholar 

  85. Linde-Laursen IB (1993) Cytogenic analysis of Miscanthus ‘Giganteus’ and interspecific hybrid. Hereditas 119:297–300

    Article  Google Scholar 

  86. 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

    Article  PubMed  PubMed Central  Google Scholar 

  87. 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

    Article  PubMed  PubMed Central  Google Scholar 

  88. 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  

  89. Malone JA, Virtue JG, Williams C, Preston C (2017) Genetic diversity of giant reed (Arundo donax) in Australia. Weed Biol Manag 17:17–28

    Article  Google Scholar 

  90. Marbuah G, Gren I-M, McKie B (2014) Economics of harmful invasive species: a review. Diversity 6:500–5023

    Article  Google Scholar 

  91. Marchant CJ (1963) Corrected chromosome numbers for Spartina × townsendii and its parent species. Nature 31:929

    Article  Google Scholar 

  92. 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

    Article  Google Scholar 

  93. 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

    Article  Google Scholar 

  94. 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

    Article  Google Scholar 

  95. 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

    Article  Google Scholar 

  96. 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

    Article  Google Scholar 

  97. Meyerson LA, Cronin JT, Pysek P (2016) Phragmites australis as a model organism for studying plant invasions. Biol Invasions 18:2421–2431

    Article  Google Scholar 

  98. 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

    Article  CAS  PubMed  Google Scholar 

  99. 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

    CAS  Article  Google Scholar 

  100. 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

    Article  PubMed  Google Scholar 

  101. 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

    Article  PubMed  PubMed Central  Google Scholar 

  102. 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

    Article  CAS  PubMed  Google Scholar 

  103. Monti A (2012) Switchgrass. A valuable biomass crop for energy. Springer, London

    Google Scholar 

  104. 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

    Article  CAS  Google Scholar 

  105. Morais P, Reichard M (2018) Cryptic invasions: a review. Sci Total Environ 613:1438–1448

    Article  CAS  PubMed  Google Scholar 

  106. Mukherjee SK (1957) Origin and distribution of Saccharum. Bot Gaz 119:55–61

    Article  Google Scholar 

  107. 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

    Article  Google Scholar 

  108. 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

    Article  Google Scholar 

  109. 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

    Article  Google Scholar 

  110. Narasimhamoorthy B, Saha MC, Swaller T, Bouton JH (2008) Genetic diversity in switchgrass collections assessed by EST-SSR markers. Bioenergy Res 1:136–146

    Article  Google Scholar 

  111. 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

    Article  Google Scholar 

  112. 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

    Article  Google Scholar 

  113. Nielsen PN (1987) The productivity of the Miscanthus cultivar Giganteus. Tidsskrift Planteavl 91:361–368

    Google Scholar 

  114. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Otto SP, Whitton J (2000) Polyploid incidence and evolution. Ann Rev Genet 34:401–437

    Article  CAS  PubMed  Google Scholar 

  116. 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

    Article  Google Scholar 

  117. 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

    Article  Google Scholar 

  118. 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

    Article  Google Scholar 

  119. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. 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

    Article  CAS  PubMed  Google Scholar 

  121. Paul J, Kirk H, Freeland J (2011) Genetic diversity and differentiation of fragmented reedbeds (Phragmites australis) in the United Kingdom. Hydrobiologia 665:107–115

    Article  CAS  Google Scholar 

  122. 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

    Article  CAS  Google Scholar 

  123. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. 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

    Article  Google Scholar 

  125. Premachandran MN, Prathima PT, Lekshmi M (2011) Sugarcane and polyploidy, a review. J Sugarcane Res 1:1–15

    Google Scholar 

  126. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  127. 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

    Google Scholar 

  128. 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

    Google Scholar 

  129. 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

    Article  PubMed  Google Scholar 

  130. 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

    Article  PubMed  Google Scholar 

  131. 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

    Article  CAS  Google Scholar 

  132. Sacks EJ, Jakob K, Gutterson NI (2013) Patent application US 2013/0111619 A1. United States Patent Application Publication

  133. Sahramaa M (2004) Evaluating germplasm of reed canary grass, Phalaris arundinacea L. PhD thesis, University of Helsinki. ISBN 952-10-1836-4

  134. 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

    Article  CAS  PubMed  Google Scholar 

  135. Saltonstall K (2003) Microsatellite variation within and among North American lineages of Phragmites australis. Mol Ecol 12:1689–1702

    Article  CAS  PubMed  Google Scholar 

  136. 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

    Article  Google Scholar 

  137. 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

    Article  Google Scholar 

  138. 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

    Google Scholar 

  139. Smith LL, Barney JN (2014) The relative risk of invasion: evaluation of Miscanthus × giganteus seed establishment. Invasive Plant Sci Manag 7:93–106

    Article  Google Scholar 

  140. 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

    Article  Google Scholar 

  141. 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

    Article  CAS  PubMed  Google Scholar 

  142. 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

    Google Scholar 

  143. 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

    Article  Google Scholar 

  144. 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

    Article  PubMed  Google Scholar 

  145. Sybenga J (1996) Chromosome pairing affinity and quadrivalent formation in polyploids: do segmental allopolyploids exist? Genome 39:1176–1184

    Article  CAS  PubMed  Google Scholar 

  146. 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

    Article  Google Scholar 

  147. 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

    Article  Google Scholar 

  148. 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

    Article  Google Scholar 

  149. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. 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

  152. 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

    Article  CAS  Google Scholar 

  153. 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

    Article  Google Scholar 

  154. 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

    Article  Google Scholar 

  155. Wang B, Li W, Wang J (2005) Genetic diversity of Alternanthera philoxxeroides in China. Aquat Bot 81:277–283

    Article  Google Scholar 

  156. 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

    Article  Google Scholar 

  157. 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

    Article  CAS  Google Scholar 

  158. 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

    Article  CAS  PubMed  Google Scholar 

  159. 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

    Article  PubMed  Google Scholar 

  160. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. 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

    Article  CAS  Google Scholar 

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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.

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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

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Keywords

  • Adaptation
  • Dispersal
  • Gene flow
  • Hybridization
  • Polyploidy
  • Population structure
  • Seeds
  • Species complex
  • Vegetative