Breeding progress and preparedness for mass-scale deployment of perennial lignocellulosic biomass crops switchgrass, miscanthus, willow and poplar

Abstract

Genetic improvement through breeding is one of the key approaches to increasing biomass supply. This paper documents the breeding progress to date for four perennial biomass crops (PBCs) that have high output–input energy ratios: namely Panicum virgatum (switchgrass), species of the genera Miscanthus (miscanthus), Salix (willow) and Populus (poplar). For each crop, we report on the size of germplasm collections, the efforts to date to phenotype and genotype, the diversity available for breeding and on the scale of breeding work as indicated by number of attempted crosses. We also report on the development of faster and more precise breeding using molecular breeding techniques. Poplar is the model tree for genetic studies and is furthest ahead in terms of biological knowledge and genetic resources. Linkage maps, transgenesis and genome editing methods are now being used in commercially focused poplar breeding. These are in development in switchgrass, miscanthus and willow generating large genetic and phenotypic data sets requiring concomitant efforts in informatics to create summaries that can be accessed and used by practical breeders. Cultivars of switchgrass and miscanthus can be seed-based synthetic populations, semihybrids or clones. Willow and poplar cultivars are commercially deployed as clones. At local and regional level, the most advanced cultivars in each crop are at technology readiness levels which could be scaled to planting rates of thousands of hectares per year in about 5 years with existing commercial developers. Investment in further development of better cultivars is subject to current market failure and the long breeding cycles. We conclude that sustained public investment in breeding plays a key role in delivering future mass-scale deployment of PBCs.

REFERENCES Alburquerque, N., Baldacci-Cresp, F., Baucher, M., Casacuberta, J. M., Collonnier, C., ElJaziri, M., … Burgos, L. (2016) New transformation technologies for trees. In C. Vettori, F. Gallardo, H. Häggman, V. Kazana, F. Migliacci, G. Pilate& M. Fladung (Eds.), Biosafety of forest transgenic trees (pp. 31–66). Dordrecht, Netherlands: Springer. Argus, G. W. (2007). Salix (Salicaceae) distribution maps and a synopsis of their classification in North America, north of Mexico. Harvard Papers in Botany, 12, 335–368. https://doi.org/10.3100/1043-4534(2007)12[335:SSDMAA]2.0.CO;2 Atienza, S. G., Ramirez, M. C., & Martin, A. (2003). Mapping-QTLs controlling flowering date in Miscanthus sinensis Anderss. Cereal Research Communications, 31, 265–271. Atienza, S. G., Satovic, Z., Petersen, K. K., Dolstra, O., & Martin, A. (2003). Identification of QTLs influencing agronomic traits in Miscanthus sinensis Anderss. I. Total height, flag-leaf height and stem diameter. Theoretical and Applied Genetics, 107, 123–129. Atienza, S. G., Satovic, Z., Petersen, K. K., Dolstra, O., & Martin, A. (2003). Influencing combustion quality in Miscanthus sinensis Anderss.: Identification of QTLs for calcium, phosphorus and sulphur content. Plant Breeding, 122, 141–145. Bdeir, R., Muchero, W., Yordanov, Y., Tuskan, G. A., Busov, V., & Gailing, O. (2017). Quantitative trait locus mapping of Populus bark features and stem diameter. BMC Plant Biology, 17, 224. https://doi.org/10.1186/s12870-017-1166-4 Beard, T. R., Ford, G. S., Koutsky, T. M., & Spiwak, L. J. (2009). A Valley of Death in the innovation sequence: An economic investigation. Research Evaluation, 18, 343–356. https://doi.org/10.3152/095820209X481057 Berguson, W., McMahon, B., & Riemenschneider, D. (2017). Additive and non-additive genetic variances for tree growth in several hybrid poplar populations and implications regarding breeding strategy. Silvae Genetica, 66(1), 33–39. https://doi.org/10.1515/sg-2017-0005 Berlin, S., Trybush, S. O., Fogelqvist, J., Gyllenstrand, N., Hallingbäck, H. R., Åhman, I., … Hanley, S. J. (2014). Genetic diversity, population structure and phenotypic variation in European Salix viminalis L. (Salicaceae). Tree Genetics & Genomes, 10, 1595–1610. https://doi.org/10.1007/s11295-014-0782-5 Bernardo, R., & Yu, J. (2007). Prospects for genomewide selection for quantitative traits in maize. Crop Science, 47, 1082–1090. https://doi.org/10.2135/cropsci2006.11.0690 Biswal, A. K., Atmodjo, M. A., Li, M., Baxter, H. L., Yoo, C. G., Pu, Y., … Mohnen, D. (2018). Sugar release and growth of biofuel crops are improved by downregulation of pectin biosynthesis. Nature Biotechnology, 36, 249–257. Bmu (2009). National biomass action plan for Germany (p. 17). Bundesministerium für Umwelt Naturschutz und Reaktorsicherheit, Bundesministerium für Ernährung (BMU) & Landwirtschaft und Verbraucherschutz (BMELV), 11055 Berlin | Germany. Retrieved from http://www.bmel.de/SharedDocs/Downloads/EN/Publications/BiomassActionPlan.pdf?__blob=publicationFile Brummer, E. C. (1999). Capturing heterosis in forage crop cultivar development. Crop Science, 39, 943–954. https://doi.org/10.2135/cropsci1999.0011183X003900040001x Budsberg, E., Crawford, J. T., Morgan, H., Chin, W. S., Bura, R., & Gustafson, R. (2016). Hydrocarbon bio-jet fuel from bioconversion of poplar biomass: Life cycle assessment. Biotechnology for Biofuels, 9, 170. https://doi.org/10.1186/s13068-016-0582-2 Burris, K. P., Dlugosz, E. M., Collins, A. G., Stewart, C. N., & Lenaghan, S. C. (2016). Development of a rapid, low-cost protoplast transfection system for switchgrass (Panicum virgatum L.). Plant Cell Reports, 35, 693–704. https://doi.org/10.1007/s00299-015-1913-7 Casler, M. (2012). Switchgrass breeding, genetics, and genomics. In A. Monti (Ed.), Switchgrass (pp. 29–54). London, UK: Springer. Casler, M., Mitchell, R., & Vogel, K. (2012). Switchgrass. In C. Kole, C. P. Joshi, & D. R. Shonnard (Eds.), Handbook of bioenergy crop plants, Vol. 2. New York, NY: Taylor & Francis. Casler, M. D., & Ramstein, G. P. (2018). Breeding for biomass yield in switchgrass using surrogate measures of yield. BioEnergy Research, 11, 6–12. Casler, M. D., Sosa, S., Hoffman, L., Mayton, H., Ernst, C., Adler, P. R., … Bonos, S. A. (2017). Biomass Yield of Switchgrass Cultivars under High- versus Low-Input Conditions. Crop Science, 57, 821–832. https://doi.org/10.2135/cropsci2016.08.0698 Casler, M. D., & Vogel, K. P. (2014). Selection for biomass yield in upland, lowland, and hybrid switchgrass. Crop Science, 54, 626–636. https://doi.org/10.2135/cropsci2013.04.0239 Casler, M. D., Vogel, K. P., & Harrison, M. (2015). Switchgrass germplasm resources. Crop Science, 55, 2463–2478. https://doi.org/10.2135/cropsci2015.02.0076 Casler, M. D., Vogel, K. P., Lee, D. K., Mitchell, R. B., Adler, P. R., Sulc, R. M., … Moore, K. J. (2018). 30 Years of progress toward increasing biomass yield of switchgrass and big bluestem. Crop Science, 58, 1242. Clark, L. V., Brummer, J. E., Głowacka, K., Hall, M. C., Heo, K., Peng, J., … Sacks, E. J. (2014). A footprint of past climate change on the diversity and population structure of Miscanthus sinensis. Annals of Botany, 114, 97–107. https://doi.org/10.1093/aob/mcu084 Clark, L. V., Dzyubenko, E., Dzyubenko, N., Bagmet, L., Sabitov, A., Chebukin, P., … Sacks, E. J. (2016). Ecological characteristics and in situ genetic associations for yield-component traits of wild Miscanthus from eastern Russia. Annals of Botany, 118, 941–955. Clark, L. V., Jin, X., Petersen, K. K., Anzoua, K. G., Bagmet, L., Chebukin, P., … Sacks,, E. J.(2018). Population structure of Miscanthus sacchariflorus reveals two major polyploidization events, tetraploid-mediated unidirectional introgression from diploid M. sinensis, and diversity centred around the Yellow Sea. Annals of Botany, 20, 1–18. https://doi.org/10.1093/aob/mcy1161 Clark, L. V., Stewart, J. R., Nishiwaki, A., Toma, Y., Kjeldsen, J. B., Jørgensen, U., … Sacks, E. J. (2015). Genetic structure of Miscanthus sinensis and Miscanthus sacchariflorus in Japan indicates a gradient of bidirectional but asymmetric introgression. Journal of Experimental Botany, 66, 4213–4225. Clifton-Brown, J., Hastings, A., Mos, M., McCalmont, J. P., Ashman, C., Awty-Carroll, D., … Cracroft-Eley, W. (2017). Progress in upscaling Miscanthus biomass production for the European bio-economy with seed-based hybrids. Global Change Biology Bioenergy, 9, 6–17. Clifton-Brown, J., Schwarz, K. U., & Hastings, A. (2015). History of the development of Miscanthus as a bioenergy crop: From small beginnings to potential realisation. Biology and Environment-Proceedings of the Royal Irish Academy, 115B, 45–57. Clifton-Brown, J., Senior, H., Purdy, S., Horsnell, R., Lankamp, B.,Müennekhoff, A.-K. … Bentley, A. R. (2018). Investigating the potential of novel non-woven fabrics to increase pollination efficiency in plant breeding. PloS One (Accepted). Crawford, J. T., Shan, C. W., Budsberg, E., Morgan, H., Bura, R., & Gustafson, R. (2016). Hydrocarbon bio-jet fuel from bioconversion of poplar biomass: Techno-economic assessment. Biotechnology for Biofuels, 9, 141. https://doi.org/10.1186/s13068-016-0545-7 Dalton, S. (2013). Biotechnology of Miscanthus. In S. M. Jain & S. D. Gupta (Eds.), Biotechnology of neglected and underutilized crops (pp. 243–294). Dordrecht, Netherlands: Springer. Davey, C. L., Robson, P., Hawkins, S., Farrar, K., Clifton-Brown, J. C., Donnison, I. S., & Slavov, G. T. (2017). Genetic relationships between spring emergence, canopy phenology, and biomass yield increase the accuracy of genomic prediction in Miscanthus. Journal of Experimental Botany, 68, 5093–5102. https://doi.org/10.1093/jxb/erx339 David, X., & Anderson, X. (2002). Aspen and larch genetics cooperative annual report 13. St. Paul, MN: Department of Forest Resources, University of Minnesota. Deblock, M. (1990). Factors influencing the tissue-culture and the Agrobacterium-Tumefaciens-mediated transformation of hybrid aspen and poplar clones. Plant Physiology, 93, 1110–1116. https://doi.org/10.1104/pp.93.3.1110 Defra (2002). The role of future public research investment in the genetic improvement of UK-grown crops (p. 220). London. Retrieved from http://sciencesearch.defra.gov.uk/Default.aspx?Menu=Menu&Module=More&Location=None&Completed=220&ProjectID=10412 Dewoody, J., Trewin, H., & Taylor, G. (2015). Genetic and morphological differentiation in Populus nigra L.: Isolation by colonization or isolation by adaptation? Molecular Ecology, 24, 2641–2655. Dong, H., Liu, S., Clark, L. V., Sharma, S., Gifford, J. M., Juvik, J. A., … Sacks, E. J. (2018). Genetic mapping of biomass yield in three interconnected Miscanthus populations. Global Change Biology Bioenergy, 10, 165–185. Dukes (2017) Digest of UK Energy Statistics (DUKES) (p. 264). London, UK: Department for Business, Energy & Industrial Strategy. Retrieved from www.gov.uk/government/collections/digest-of-uk-energy-statistics-dukes Eckenwalder, J. (1996). Systematics and evolution of Populus. In R. Stettler, H. Bradshaw, J. Heilman, & T. Hinckley (Eds.), Biology of Populus and its implications for management and conservation (pp. 7-32). Ottawa, ON: National Research Council of Canada. Elshire, R. J., Glaubitz, J. C., Sun, Q., Poland, J. A., Kawamoto, K., Buckler, E. S., & Mitchell, S. E. (2011). A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PloS One, 6, e19379. Evans, H. (2016). Bioenergy crops in the UK: Case studies of successful whole farm integration (p. 23). Loughborough, UK: Energy Technologies Institute. Retrieved from https://www.eti.co.uk/library/bioenergy-crops-in-the-uk-case-studies-on-successful-whole-farm-integration-evidence-pack Evans, H. (2017). Increasing UK biomass production through more productive use of land (p. 7). Loughborough, UK: Energy Technologies Institute. Retrieved from https://www.eti.co.uk/library/an-eti-perspective-increasing-uk-biomass-production-through-more-productive-use-of-land Evans, J., Sanciangco, M. D., Lau, K. H., Crisovan, E., Barry, K., Daum, C., … Buell, C. R. (2018). Extensive genetic diversity is present within North American switchgrass germplasm. The Plant Genome, 11, 1–16. https://doi.org/10.3835/plantgenome2017.06.0055 Evans, L. M., Slavov, G. T., Rodgers-Melnick, E., Martin, J., Ranjan, P., Muchero, W., … DiFazio, S. P. (2014). Population genomics of Populus trichocarpa identifies signatures of selection and adaptive trait associations. Nature Genetics, 46, 1089–1096. https://doi.org/10.1038/ng.3075 Fabio, E. S., Volk, T. A., Miller, R. O., Serapiglia, M. J., Gauch, H. G., Van Rees, K. C. J., … Smart, L. B. (2017). Genotype× environment interaction analysis of North American shrub willow yield trials confirms superior performance of triploid hybrids. Global Change Biology Bioenergy, 9, 445–459. https://doi.org/10.1111/gcbb.12344 Fahrenkrog, A. M., Neves, L. G., Resende, M. F. R., Vazquez, A. I., de los Campos, G., Dervinis, C., … Kirst, M. (2017). Genome-wide association study reveals putative regulators of bioenergy traits in Populus deltoides. New Phytologist, 213, 799–811. Fan, D., Liu, T. T., Li, C. F., Jiao, B., Li, S., Hou, Y. S., & Luo, K. M. (2015). Efficient CRISPR/Cas9-mediated targeted mutagenesis in Populus in the first generation. Scientific Reports, 5, 12217. Feng, X. P., Lourgant, K., Castric, V., Saumitou-Laprade, P., Zheng, B. S., Jiang, D. M., & Brancourt-Hulmel, M. (2014). The discovery of natural accessions related to Miscanthus x giganteus using chloroplast DNA. Crop Science, 54, 1645–1655. Fillatti, J. J., Sellmer, J., Mccown, B., Haissig, B., & Comai, L. (1987). Agrobacterium-mediated transformation and regeneration of Populus. Molecular & General Genetics, 206, 192–199. Fu, Y. B. (2015). Understanding crop genetic diversity under modern plant breeding. Theoretical and Applied Genetics, 128, 2131–2142. https://doi.org/10.1007/s00122-015-2585-y Fu, C., Mielenz, J. R., Xiao, X., Ge, Y., Hamilton, C. Y., Rodriguez, M., … Wang, Z.-Y. (2011). Genetic manipulation of lignin reduces recalcitrance and improves ethanol production from switchgrass. Proceedings of the National Academy of Sciences of the United States of America, 108, 3803–3808. https://doi.org/10.1073/pnas.1100310108 Gao, C. (2018). The future of CRISPR technologies in agriculture. Nature Reviews. Molecular Cell Biology, 19(5), 275–276. Gegas, V., Gay, A., Camargo, A., & Doonan, J. (2014). Challenges of Crop Phenomics in the Post-genomic Era. In J. Hancock (Ed.), Phenomics (pp. 142–171). Boca Raton, FL: CRC Press. Geraldes, A., DiFazio, S. P., Slavov, G. T., Ranjan, P., Muchero, W., Hannemann, J., … Tuskan, G. A. (2013). A 34K SNP genotyping array for Populus trichocarpa: Design, application to the study of natural populations and transferability to other Populus species. Molecular Ecology Resources, 13, 306–323. Gifford, J. M., Chae, W. B., Swaminathan, K., Moose, S. P., & Juvik, J. A. (2015). Mapping the genome of Miscanthus sinensis for QTL associated with biomass productivity. Global Change Biology Bioenergy, 7, 797–810. Goggin, F. L., Lorence, A., & Topp, C. N. (2015). Applying high-throughput phenotyping to plant-insect interactions: Picturing more resistant crops. Current Opinion in Insect Science, 9, 69–76. https://doi.org/10.1016/j.cois.2015.03.002 Grabowski, P. P., Evans, J., Daum, C., Deshpande, S., Barry, K. W., Kennedy, M., … Casler, M. D. (2017). Genome-wide associations with flowering time in switchgrass using exome-capture sequencing data. New Phytologist, 213, 154–169. https://doi.org/10.1111/nph.14101 Greef, J. M., & Deuter, M. (1993). Syntaxonomy of Miscanthus x giganteus GREEF et DEU. Angewandte Botanik, 67, 87–90. Guerra, F. P., Richards, J. H., Fiehn, O., Famula, R., Stanton, B. J., Shuren, R., … Neale, D. B. (2016). Analysis of the genetic variation in growth, ecophysiology, and chemical and metabolomic composition of wood of Populus trichocarpa provenances. Tree Genetics & Genomes, 12, 6. https://doi.org/10.1007/s11295-015-0965-8 Guo, H. P., Shao, R. X., Hong, C. T., Hu, H. K., Zheng, B. S., & Zhang, Q. X. (2013). Rapid in vitro propagation of bioenergy crop Miscanthus sacchariflorus. Applied Mechanics and Materials, 260, 181–186. Hallingbäck, H. R., Fogelqvist, J., Powers, S. J., Turrion-Gomez, J., Rossiter, R., Amey, J., … Rönnberg-Wästljung, A.-C. (2016). Association mapping in Salix viminalis L. (Salicaceae)–Identification of candidate genes associated with growth and phenology. Global Change Biology Bioenergy, 8, 670–685. Hanley, S. J., & Karp, A. (2014). Genetic strategies for dissecting complex traits in biomass willows (Salix spp.). Tree Physiology, 34, 1167–1180. https://doi.org/10.1093/treephys/tpt089 Harfouche, A., Meilan, R., & Altman, A. (2011). Tree genetic engineering and applications to sustainable forestry and biomass production. Trends in Biotechnology, 29, 9–17. https://doi.org/10.1016/j.tibtech.2010.09.003 Harfouche, A., Meilan, R., & Altman, A. (2014). Molecular and physiological responses to abiotic stress in forest trees and their relevance to tree improvement. Tree Physiology, 34, 1181–1198. https://doi.org/10.1093/treephys/tpu012 Harfouche, A., Meilan, R., Kirst, M., Morgante, M., Boerjan, W., Sabatti, M., & Mugnozza, G. S. (2012). Accelerating the domestication of forest trees in a changing world. Trends in Plant Science, 17, 64–72. https://doi.org/10.1016/j.tplants.2011.11.005 Hastings, A., Clifton-Brown, J., Wattenbach, M., Mitchell, C. P., Stampfl, P., & Smith, P. (2009). Future energy potential of Miscanthus in Europe. Global Change Biology Bioenergy, 1, 180–196. Hastings, A., Mos,, M., Yesufu, J. A.Mccalmont, J., Schwarz, K., Shafei, R.…Clifton-Brown, J.. (2017). Economic and environmental assessment of seed and rhizome propagated Miscanthus in the UK. Frontiers in Plant Science, 8, 16. https://doi.org/10.3389/fpls.2017.01058 Héder, M. (2017). From NASA to EU: The evolution of the TRL scale in Public Sector Innovation. The Innovation Journal, 22, 1–23. https://doi.org/10.3389/fpls.2017.01058 Heffner, E. L., Sorrells, M. E., & Jannink, J. L. (2009). Genomic selection for crop improvement. Crop Science, 49, 1–12. https://doi.org/10.2135/cropsci2008.08.0512 Hodkinson, T. R., Klaas, M., Jones, M. B., Prickett, R., & Barth, S. (2015). Miscanthus: A case study for the utilization of natural genetic variation. Plant Genetic Resources-Characterization and Utilization, 13, 219–237. https://doi.org/10.1017/S147926211400094X Hodkinson, T. R., & Renvoize, S. (2001). Nomenclature of Miscanthus xgiganteus (Poaceae). Kew Bulletin, 56, 759–760. https://doi.org/10.2307/4117709 Houle, D., Govindaraju, D. R., & Omholt, S. (2010). Phenomics: The next challenge. Nature Reviews Genetics, 11, 855–866. https://doi.org/10.1038/nrg2897 Huang, X. H., Wei, X. H., Sang, T., Zhao, Q., Feng, Q., Zhao, Y., … Han, B. (2010). Genome-wide association studies of 14 agronomic traits in rice landraces. Nature Genetics, 42, 961–U976. Hwang, O.-J., Cho, M.-A., Han, Y.-J., Kim, Y.-M., Lim, S.-H., Kim, D.-S., … Kim, J.-I. (2014). Agrobacterium-mediated genetic transformation of Miscanthus sinensis. Plant Cell, Tissue and Organ Culture (PCTOC), 117, 51–63. Hwang, O.-J., Lim, S.-H., Han, Y.-J., Shin, A.-Y., Kim, D.-S., & Kim, J.-I. (2014). Phenotypic characterization of transgenic Miscanthus sinensis plants overexpressing Arabidopsis phytochrome B. International Journal of Photoenergy, 2014,501016. Ilstedt, B. (1996). Genetics and performance of Belgian poplar clones tested in Sweden. International Journal of Forest Genetics, 3, 183–195. Ingvarsson, P. K., Garcia, M. V., Hall, D., Luquez, V., & Jansson, S. (2006). Clinal variation in phyB2, a candidate gene for day-length-induced growth cessation and bud set, across a latitudinal gradient in European aspen (Populus tremula). Genetics, 172, 1845–1853. Ingvarsson, P. K., Garcia, M. V., Luquez, V., Hall, D., & Jansson, S. (2008). Nucleotide polymorphism and phenotypic associations within and around the phytochrome B2 locus in European aspen (Populus tremula, Salicaceae). Genetics, 178, 2217–2226. https://doi.org/10.1534/genetics.107.082354 Jannink, J.-L., Lorenz, A. J., & Iwata, H. (2010). Genomic selection in plant breeding: From theory to practice. Briefings in Functional Genomics, 9, 166–177. https://doi.org/10.1093/bfgp/elq001 Jiang, J., Guan, Y., Mccormick, S., Juvik, J., Lubberstedt, T., & Fei, S.-Z. (2017). Gametophytic self-incompatibility is operative in Miscanthus sinensis (Poaceae) and is affected by pistil age. Crop Science, 57, 1948–1956. Jones, H. D. (2015a). Future of breeding by genome editing is in the hands of regulators. GM Crops & Food, 6, 223–232. Jones, H. D. (2015b). Regulatory uncertainty over genome editing. Nature Plants, 1, 14011. Kalinina, O., Nunn, C., Sanderson, R., Hastings, A. F. S., van der Weijde, T., Özgüven, M., … Clifton-Brown, J. C. (2017). Extending Miscanthus cultivation with novel germplasm at six contrasting sites. Frontiers in Plant Science, 8, 563. https://doi.org/10.3389/fpls.2017.00563 Karp, A., Hanley, S. J., Trybush, S. O., Macalpine, W., Pei, M., & Shield, I. (2011). Genetic improvement of willow for bioenergy and biofuels free access. Journal of Integrative Plant Biology, 53, 151–165. https://doi.org/10.1111/j.1744-7909.2010.01015.x Kersten, B., Faivre Rampant, P., Mader, M., Le Paslier, M.-C., Bounon, R., Berard, A., … Fladung, M. (2016). Genome sequences of Populus tremula chloroplast and mitochondrion: Implications for holistic poplar breeding. PloS One, 11, e0147209. https://doi.org/10.1371/journal.pone.0147209 Kiesel, A., Nunn, C., Iqbal, Y., Van der Weijde, T., Wagner, M., Özgüven, M., … Lewandowski, I. (2017). Site-specific management of Miscanthus genotypes for combustion and anaerobic digestion: A comparison of energy yields. Frontiers in Plant Science, 8, 347. https://doi.org/10.3389/fpls.2017.00347 Kim, H., Kim, S. T., Ryu, J., Kang, B. C., Kim, J. S., & Kim, S. G. (2017). CRISPR/Cpf1-mediated DNA-free plant genome editing. Nature Communications, 8, 14406. https://doi.org/10.1038/ncomms14406 King, Z. R., Bray, A. L., Lafayette, P. R., & Parrott, W. A. (2014). Biolistic transformation of elite genotypes of switchgrass (Panicum virgatum L.). Plant Cell Reports, 33, 313–322. https://doi.org/10.1007/s00299-013-1531-1 Kopp, R. F., Maynard, C. A., De Niella, P. R., Smart, L. B., & Abrahamson, L. P. (2002). Collection and storage of pollen from Salix (Salicaceae). American Journal of Botany, 89, 248–252. Krzyżak, J., Pogrzeba, M., Rusinowski, S., Clifton-Brown, J., McCalmont, J. P., Kiesel, A., … Mos, M. (2017). Heavy metal uptake by novel miscanthus seed-based hybrids cultivated in heavy metal contaminated soil. Civil and Environmental Engineering Reports, 26, 121–132. https://doi.org/10.1515/ceer-2017-0040 Kuzovkina, Y. A., & Quigley, M. F. (2005). Willows beyond wetlands: Uses of Salix L. species for environmental projects. Water, Air, and Soil Pollution, 162, 183–204. https://doi.org/10.1007/s11270-005-6272-5 Lazarus, W., Headlee, W. L., & Zalesny, R. S. (2015). Impacts of supplyshed-level differences in productivity and land costs on the economics of hybrid poplar production in Minnesota, USA. BioEnergy Research, 8, 231–248. https://doi.org/10.1007/s12155-014-9520-y Lewandowski, I. (2015). Securing a sustainable biomass supply in a growing bioeconomy. Global Food Security, 6, 34–42. https://doi.org/10.1016/j.gfs.2015.10.001 Lewandowski, I. (2016). The role of perennial biomass crops in a growing bioeconomy. In S. Barth, D. Murphy-Bokern, O. Kalinina, G. Taylor, & M. Jones (Eds.), Perennial biomass crops for a resource-constrained world (pp. 3–13). Cham, Switzerland: Springer Switzerland AG. Li, J. L., Meilan, R., Ma, C., Barish, M., & Strauss, S. H. (2008). Stability of herbicide resistance over 8 years of coppice in field-grown, genetically engineered poplars. Western Journal of Applied Forestry, 23, 89–93. Li, R. Y., & Qu, R. D. (2011). High throughput Agrobacterium-mediated switchgrass transformation. Biomass & Bioenergy, 35, 1046–1054. https://doi.org/10.1016/j.biombioe.2010.11.025 Lindegaard, K. N., & Barker, J. H. A. (1997). Breeding willows for biomass. Aspects of Applied Biology, 49, 155–162. Linde-Laursen, I. B. (1993). Cytogenetic analysis of Miscanthus 'Giganteus', an interspecific hybrid. Hereditas, 119, 297–300. https://doi.org/10.1111/j.1601-5223.1993.00297.x Liu, Y., Merrick, P., Zhang, Z. Z., Ji, C. H., Yang, B., & Fei, S. Z. (2018). Targeted mutagenesis in tetraploid switchgrass (Panicum virgatum L.) using CRISPR/Cas9. Plant Biotechnology Journal, 16, 381–393. Liu, L. L., Wu, Y. Q., Wang, Y. W., & Samuels, T. (2012). A high-density simple sequence repeat-based genetic linkage map of switchgrass. G3 (Bethesda, Md.), 2, 357–370. Lovett, A., Sünnenberg, G., & Dockerty, T. (2014). The availability of land for perennial energy crops in Great Britain. Global Change Biology Bioenergy, 6, 99–107. https://doi.org/10.1111/gcbb.12147 Lozano-Juste, J., & Cutler, S. R. (2014). Plant genome engineering in full bloom. Trends in Plant Science, 19, 284–287. https://doi.org/10.1016/j.tplants.2014.02.014 Lu, F., Lipka, A. E., Glaubitz, J., Elshire, R., Cherney, J. H., Casler, M. D., … Costich, D. E. (2013). Switchgrass Genomic Diversity, Ploidy, and Evolution: Novel Insights from a Network-Based SNP Discovery Protocol. Plos Genetics, 9, e1003215. Ludovisi, R., Tauro, F., Salvati, R., Khoury, S., Mugnozza, G. S., & Harfouche, A. (2017). UAV-based thermal imaging for high-throughput field phenotyping of black poplar response to drought. Frontiers in Plant Science, 8,1681. Macalpine, W., Shield, I., & Karp, A. (2010). Seed to near market variety; the BEGIN willow breeding pipeline 2003–2010 and beyond. In: Bioten conference proceedings, Birmingham. pp. 21–23. Macalpine, W. J., Shield, I. F., Trybush, S. O., Hayes, C. M., & Karp, A. (2008). Overcoming barriers to crossing in willow (Salix spp.) breeding. Aspects of Applied Biology, 90, 173–180. Mahfouz, M. M. (2017). The efficient tool CRISPR-Cpf1. Nature Plants, 3, 17028. Malinowska, M., Donnison, I. S., & Robson, P. R. (2017). Phenomics analysis of drought responses in Miscanthus collected from different geographical locations. Global Change Biology Bioenergy, 9, 78–91. Maroder, H. L., Prego, I. A., Facciuto, G. R., & Maldonado, S. B. (2000). Storage behaviour of Salix alba and Salix matsudana seeds. Annals of Botany, 86, 1017–1021. https://doi.org/10.1006/anbo.2000.1265 Martinez-Reyna, J., & Vogel, K. (2002). Incompatibility systems in switchgrass. Crop Science, 42, 1800–1805. https://doi.org/10.2135/cropsci2002.1800 Maurya, J. P., & Bhalerao, R. P. (2017). Photoperiod-and temperature-mediated control of growth cessation and dormancy in trees: A molecular perspective. Annals of Botany, 120, 351–360. https://doi.org/10.1093/aob/mcx061 McCalmont, J. P., Hastings, A., Mcnamara, N. P., Richter, G. M., Robson, P., Donnison, I. S., & Clifton-Brown, J. (2017). Environmental costs and benefits of growing Miscanthus for bioenergy in the UK. Global Change Biology Bioenergy, 9, 489–507. McCracken, A. R., & Dawson, W. M. (1997). Using mixtures of willow clones as a means of controlling rust disease. Aspects of Applied Biology, 49, 97–103. McKown, A. D., Klápště, J., Guy, R. D., Geraldes, A., Porth, I., Hannemann, J., … Douglas, C. J. (2014). Genome-wide association implicates numerous genes underlying ecological trait variation in natural populations of Populus trichocarpa. New Phytologist, 203, 535–553. Merrick, P., & Fei, S. Z. (2015). Plant regeneration and genetic transformation in switchgrass – A review. Journal of Integrative Agriculture, 14, 483–493. https://doi.org/10.1016/S2095-3119(14)60921-7 Moreno-Mateos, M. A., Fernandez, J. P., Rouet, R., Lane, M. A., Vejnar, C. E., Mis, E., … Giraldez, A. J. (2017). CRISPR-Cpf1 mediates efficient homology-directed repair and temperature-controlled genome editing. Nature Communications, 8, 2024. https://doi.org/10.1038/s41467-017-01836-2 Mosseler, A. (1990). Hybrid performance and species crossability relationships in willows (Salix). Canadian Journal of Botany, 68, 2329–2338. Muchero, W., Guo, J., DiFazio, S. P., Chen, J.-G., Ranjan, P., Slavov, G. T., … Tuskan, G. A. (2015). High-resolution genetic mapping of allelic variants associated with cell wall chemistry in Populus. BMC Genomics, 16, 24. https://doi.org/10.1186/s12864-015-1215-z Neale, D. B., & Kremer, A. (2011). Forest tree genomics: Growing resources and applications. Nature Reviews Genetics, 12, 111–122. https://doi.org/10.1038/nrg2931 Nunn, C., Hastings, A. F. S. J., Kalinina, O., Özgüven, M., Schüle, H., Tarakanov, I. G., … Clifton-Brown, J. C. (2017). Environmental influences on the growing season duration and ripening of diverse Miscanthus germplasm grown in six countries. Frontiers in Plant Science, 8, 907. https://doi.org/10.3389/fpls.2017.00907 Ogawa, Y., Honda, M., Kondo, Y., & Hara-Nishimura, I. (2016). An efficient Agrobacterium-mediated transformation method for switchgrass genotypes using Type I callus. Plant Biotechnology, 33, 19–26. Ogawa, Y., Shirakawa, M., Koumoto, Y., Honda, M., Asami, Y., Kondo, Y., & Hara-Nishimura, I. (2014). A simple and reliable multi-gene transformation method for switchgrass. Plant Cell Reports, 33, 1161–1172. https://doi.org/10.1007/s00299-014-1605-8 Okada, M., Lanzatella, C., Saha, M. C., Bouton, J., Wu, R. L., & Tobias, C. M. (2010). Complete switchgrass genetic maps reveal subgenome collinearity, preferential pairing and multilocus interactions. Genetics, 185, 745–760. https://doi.org/10.1534/genetics.110.113910 Palomo-Ríos, E., Macalpine, W., Shield, I., Amey, J., Karaoğlu, C., West, J., … Jones, H. D. (2015). Efficient method for rapid multiplication of clean and healthy willow clones via in vitro propagation with broad genotype applicability. Canadian Journal of Forest Research, 45, 1662–1667. https://doi.org/10.1139/cjfr-2015-0055 Pilate, G., Allona, I., Boerjan, W., Déjardin, A., Fladung, M., Gallardo, F., … Halpin, C. (2016). Lessons from 25 years of GM tree field trials in Europe and prospects for the future. In C. Vettori, F. Gallardo, H. Häggman, V. Kazana, F. Migliacci, G. Pilate& M. Fladung (Eds.), Biosafety of forest transgenic trees (pp. 67–100). Dordrecht, Netherlands: Springer Switzerland AG. Pinosio, S., Giacomello, S., Faivre-Rampant, P., Taylor, G., Jorge, V., Le Paslier, M. C., & Marroni, F. (2016). Characterization of the poplar pan-genome by genome-wide identification of structural variation. Molecular Biology and Evolution, 33, 2706–2719. Porth, I., Klápště, J., Skyba, O., Friedmann, M. C., Hannemann, J., Ehlting, J., … Douglas, C. J. (2013). Network analysis reveals the relationship among wood properties, gene expression levels and genotypes of natural Populus trichocarpa accessions. New Phytologist, 200, 727–742. Pugesgaard, S., Schelde, K., Larsen, S. U., Lærke, P. E., & Jørgensen, U. (2015). Comparing annual and perennial crops for bioenergy production–influence on nitrate leaching and energy balance. Global Change Biology Bioenergy, 7, 1136–1149. https://doi.org/10.1111/gcbb.12215 Quinn, L. D., Allen, D. J., & Stewart, J. R. (2010). Invasiveness potential of Miscanthus sinensis: Implications for bioenergy production in the United States. Global Change Biology Bioenergy, 2, 310–320. https://doi.org/10.1111/j.1757-1707.2010.01062.x Rae, A. M., Robinson, K. M., Street, N. R., & Taylor, G. (2004). Morphological and physiological traits influencing biomass productivity in short-rotation coppice poplar. Canadian Journal of Forest Research-Revue Canadienne De Recherche Forestiere, 34, 1488–1498. https://doi.org/10.1139/x04-033 Rambaud, C., Arnoult, S., Bluteau, A., Mansard, M. C., Blassiau, C., & Brancourt-Hulmel, M. (2013). Shoot organogenesis in three Miscanthus species and evaluation for genetic uniformity using AFLP analysis. Plant Cell, Tissue and Organ Culture (PCTOC), 113, 437–448. https://doi.org/10.1007/s11240-012-0284-9 Ramstein, G. P., Evans, J., Kaeppler, S. M., Mitchell, R. B., Vogel, K. P., Buell, C. R., & Casler, M. D. (2016). Accuracy of genomic prediction in switchgrass (Panicum virgatum L.) improved by accounting for linkage disequilibrium. G3 (Bethesda, Md.), 6, 1049–1062. Rayburn, A. L., Crawford, J., Rayburn, C. M., & Juvik, J. A. (2009). Genome size of three Miscanthus species. Plant Molecular Biology Reporter, 27, 184. https://doi.org/10.1007/s11105-008-0070-3 Richardson, J., Isebrands, J., & Ball, J. (2014). Ecology and physiology of poplars and willows. In J. Isebrands, & J. Richardson (Eds.), Poplars and willows: Trees for society and the environment (pp. 92-123). Boston, MA and Rome: CABI and FAO. Robison, T. L., Rousseau, R. J., & Zhang, J. (2006). Biomass productivity improvement for eastern cottonwood. Biomass & Bioenergy, 30, 735–739. https://doi.org/10.1016/j.biombioe.2006.01.012 Robson, P. R., Farrar, K., Gay, A. P., Jensen, E. F., Clifton-Brown, J. C., & Donnison, I. S. (2013). Variation in canopy duration in the perennial biofuel crop Miscanthus reveals complex associations with yield. Journal of Experimental Botany, 64, 2373–2383. Robson, P., Jensen, E., Hawkins, S., White, S. R., Kenobi, K., Clifton-Brown, J., … Farrar, K. (2013). Accelerating the domestication of a bioenergy crop: Identifying and modelling morphological targets for sustainable yield increase in Miscanthus. Journal of Experimental Botany, 64, 4143–4155. Sanderson, M. A., Adler, P. R., Boateng, A. A., Casler, M. D., & Sarath, G. (2006). Switchgrass as a biofuels feedstock in the USA. Canadian Journal of Plant Science, 86, 1315–1325. https://doi.org/10.4141/P06-136 Scarlat, N., Dallemand, J. F., Monforti-Ferrario, F., & Nita, V. (2015). The role of biomass and bioenergy in a future bioeconomy: Policies and facts. Environmental Development, 15, 3–34. https://doi.org/10.1016/j.envdev.2015.03.006 Serapiglia, M. J., Gouker, F. E., & Smart, L. B. (2014). Early selection of novel triploid hybrids of shrub willow with improved biomass yield relative to diploids. BMC Plant Biology, 14, 74. https://doi.org/10.1186/1471-2229-14-74 Serba, D., Wu, L., Daverdin, G., Bahri, B. A., Wang, X., Kilian, A., … Devos, K. M. (2013). Linkage maps of lowland and upland tetraploid switchgrass ecotypes. BioEnergy Research, 6, 953–965. https://doi.org/10.1007/s12155-013-9315-6 Shakoor, N., Lee, S., & Mockler, T. C. (2017). High throughput phenotyping to accelerate crop breeding and monitoring of diseases in the field. Current Opinion in Plant Biology, 38, 184–192. https://doi.org/10.1016/j.pbi.2017.05.006 Shield, I., Macalpine, W., Hanley, S., & Karp, A. (2015). Breeding willow for short rotation coppice energy cropping. In Industrial crops Breeding for BioEnergy and Bioproducts. (pp. 67–80). New York, NY: Springer. Sjodin, A., Street, N. R., Sandberg, G., Gustafsson, P., & Jansson, S. (2009). The Populus Genome Integrative Explorer (PopGenIE): A new resource for exploring the Populus genome. New Phytologist, 182, 1013–1025. Slavov, G., & Davey, C. (2017). Integrated genomic prediction in bioenergy crops. In: Abstracts from the International Conference on 'Developing biomass crops for future climates' pp 34, 24–27 September 2017, Oriel College Oxford, www.watbio.eu. Slavov, G., Davey, C., Bosch, M., Robson, P., Donnison, I., & Mackay, I. (2018a). Genomic index selection provides a pragmatic framework for setting and refining multi-objective breeding targets in Miscanthus. Annals of Botany, (in press). Slavov, G. T., DiFazio, S. P., Martin, J., Schackwitz, W., Muchero, W., Rodgers-Melnick, E., … Tuskan, G. A. (2012). Genome resequencing reveals multiscale geographic structure and extensive linkage disequilibrium in the forest tree Populus trichocarpa. New Phytologist, 196, 713–725. Slavov, G., Davey, C., Robson, P., Donnison, I., & Mackay, I. (2018b). Domestication of Miscanthus through genomic index selection. In: Plant and Animal Genome Conference. 13 January 2018, San Diego, CA. Retrieved from https://pag.confex.com/pag/xxvi/meetingapp.cgi/Paper/30622 Slavov, G. T., Nipper, R., Robson, P., Farrar, K., Allison, G. G., Bosch, M., … Jensen, E. (2014). Genome-wide association studies and prediction of 17 traits related to phenology, biomass and cell wall composition in the energy grass Miscanthus sinensis. New Phytologist, 201, 1227–1239. Slavov, G., Robson, P., Jensen, E., Hodgson, E., Farrar, K., Allison, G., … Donnison, I. (2013). Contrasting geographic patterns of genetic variation for molecular markers vs. phenotypic traits in the energy grass Miscanthus sinensis. Global Change Biology Bioenergy, 5, 562–571. Ślusarkiewicz-Jarzina, A., Ponitka, A., Cerazy-Waliszewska, J., Wojciechowicz, M. K., Sobańska, K., Jeżowski, S., & Pniewski, T. (2017). Effective and simple in vitro regeneration system of Miscanthus sinensis, M.× giganteus and M. sacchariflorus for planting and biotechnology purposes. Biomass and Bioenergy, 107, 219–226. https://doi.org/10.1016/j.biombioe.2017.10.012 Smart, L., & Cameron, K. (2012). Shrub willow. In C. Kole, S. Joshi, & D. Shonnard (Eds.), Handbook of bioenergy crop plants (pp. 687–708). Boca Raton, FL: Taylor and Francis Group. Stanton, B. J. (2014). The domestication and conservation of Populus and Salix genetic resources (Chapter 4). In Isebrands, J., & Richardson, J. (Eds.), Poplars and willows: Trees for society and the environment (pp. 124–200). Rome, Italy: CAB International, Food and Agricultural Organization of the United Nations. Stanton, B. J., Neale, D. B., & Li, S. (2010). Populus breeding: From the classical to the genomic approach. In S. Jansson, R. Bhalerao, & A. T. Groover (Eds.), Genetics and genomics of populus (pp. 309–348). New York, NY: Springer. Stewart, J. R., Toma, Y., Fernandez, F. G., Nishiwaki, A., Yamada, T., & Bollero, G. (2009). The ecology and agronomy of Miscanthus sinensis, a species important to bioenergy crop development, in its native range in Japan: A review. Global Change Biology Bioenergy, 1, 126–153. Stott, K. G. (1992). Willows in the service of man. Proceedings of the Royal Society of Edinburgh. Section B. Biological Sciences, 98, 169–182. Strauss, S. H., Ma, C., Ault, K., & Klocko, A. L. (2016). Lessons from two decades of field trials with genetically modified trees in the USA: Biology and regulatory compliance. In C. Vettori, F. Gallardo, H. Häggman, V. Kazana, F. Migliacci, G. Pilate & M. Fladung (Eds.), Biosafety of forest transgenic trees (pp. 101–124). Dordrecht, Netherlands: Springer. Suda, Y., & Argus, G. W. (1968). Chromosome numbers of some North American Salix. Brittonia, 20, 191–197. https://doi.org/10.2307/2805440 Tan, B. (2018). Genomic selection and genome-wide association studies to dissect quantitative traits in forest trees. Umeå, Sweden: University. Tornqvist, C., Taylor, M., Jiang, Y., Evans, J., Buell, C., Kaeppler, S., & Casler, M. (2018). Quantitative trait locus mapping for flowering time in a lowland x upland switchgrass pseudo-F₂ population. The Plant Genome, 11, 170093. Tóth, G., Hermann, T., Da Silva, M., & Montanarella, L. (2016). Heavy metals in agricultural soils of the European Union with implications for food safety. Environment International, 88, 299–309. https://doi.org/10.1016/j.envint.2015.12.017 Tracy, W., Dawson, J., Moore, V., & Fisch, J. (2016). Intellectual property rights and public plant breeding: Recommendations, and proceedings of a conference on best practices for intellectual property protection of publically developed plant germplasm (p. 70). University of Wisconsin-Madison. Retrieved from https://host.cals.wisc.edu/agronomy/wp-content/uploads/sites/16/2016/2005/Proceedings-IPR-Final.pdf Trybush, S., Jahodová, Š., Macalpine, W., & Karp, A. (2008). A genetic study of a Salix germplasm resource reveals new insights into relationships among subgenera, sections and species. BioEnergy Research, 1, 67–79. https://doi.org/10.1007/s12155-008-9007-9 Tsai, C. J. (2013). Next-generation sequencing for next-generation breeding, and more. New Phytologist, 198, 635–637. https://doi.org/10.1111/nph.12245 Tuskan, G. A., Difazio, S., Jansson, S., Bohlmann, J., Grigoriev, I., Hellsten, U., … Rokhsar, D. (2006). The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science, 313, 1596–1604. Tuskan, G. A., & Walsh, M. E. (2001). Short-rotation woody crop systems, atmospheric carbon dioxide and carbon management: A US case study. The Forestry Chronicle, 77, 259–264. https://doi.org/10.5558/tfc77259-2 Van Den Broek, R., Treffers, D.-J., Meeusen, M., Van Wijk, A., Nieuwlaar, E., & Turkenburg, W. (2001). Green energy or organic food? A life-cycle assessment comparing two uses of set-aside land. Journal of Industrial Ecology, 5, 65–87. https://doi.org/10.1162/108819801760049477 Van Der Schoot, J., Pospiskova, M., Vosman, B., & Smulders, M. J. M. (2000). Development and characterization of microsatellite markers in black poplar (Populus nigra L.). Theoretical and Applied Genetics, 101, 317–322. https://doi.org/10.1007/s001220051485 Van Der Weijde, T., Dolstra, O., Visser, R. G., & Trindade, L. M. (2017a). Stability of cell wall composition and saccharification efficiency in Miscanthus across diverse environments. Frontiers in Plant Science, 7, 2004. Van der Weijde, T., Huxley, L. M., Hawkins, S., Sembiring, E. H., Farrar, K., Dolstra, O., … Trindade, L. M. (2017). Impact of drought stress on growth and quality of miscanthus for biofuel production. Global Change Biology Bioenergy, 9, 770–782. Van der Weijde, T., Kamei, C. L. A., Severing, E. I., Torres, A. F., Gomez, L. D., Dolstra, O., … Trindade, L. M. (2017). Genetic complexity of miscanthus cell wall composition and biomass quality for biofuels. BMC Genomics, 18, 406. Van der Weijde, T., Kiesel, A., Iqbal, Y., Muylle, H., Dolstra, O., Visser, R. G. F., … Trindade, L. M. (2017). Evaluation of Miscanthus sinensis biomass quality as feedstock for conversion into different bioenergy products. Global Change Biology Bioenergy, 9, 176–190. Vanholme, B., Cesarino, I., Goeminne, G., Kim, H., Marroni, F., Van Acker, R., … Boerjan, W. (2013). Breeding with rare defective alleles (BRDA): A natural Populus nigra HCT mutant with modified lignin as a case study. New Phytologist, 198, 765–776. Vogel, K. P., Mitchell, R. B., Casler, M. D., & Sarath, G. (2014). Registration of 'Liberty' Switchgrass. Journal of Plant Registrations, 8, 242–247. https://doi.org/10.3198/jpr2013.12.0076crc Wang, X., Yamada, T., Kong, F.-J., Abe, Y., Hoshino, Y., Sato, H., … Yamada, T. (2011). Establishment of an efficient in vitro culture and particle bombardment-mediated transformation systems in Miscanthus sinensis Anderss., a potential bioenergy crop. Global Change Biology Bioenergy, 3, 322–332. https://doi.org/10.1111/j.1757-1707.2011.01090.x Watrud, L. S., Lee, E. H., Fairbrother, A., Burdick, C., Reichman, J. R., Bollman, M., … Van de Water, P. K. (2004). Evidence for landscape-level, pollen-mediated gene flow from genetically modified creeping bentgrass with CP4 EPSPS as a marker. Proceedings of the National Academy of Sciences of the United States of America, 101, 14533–14538. Weisgerber, H. (1993). Poplar breeding for the purpose of biomass production in short-rotation periods in Germany – Problems and first findings. Forestry Chronicle, 69, 727–729. https://doi.org/10.5558/tfc69727-6 Wheeler, N. C., Steiner, K. C., Schlarbaum, S. E., & Neale, D. B. (2015). The evolution of forest genetics and tree improvement research in the United States. Journal of Forestry, 113, 500–510. https://doi.org/10.5849/jof.14-120 Whittaker, C., Macalpine, W. J., Yates, N. E., & Shield, I. (2016). Dry matter losses and methane emissions during wood chip storage: The impact on full life cycle greenhouse gas savings of short rotation coppice willow for heat. BioEnergy Research, 9, 820–835. https://doi.org/10.1007/s12155-016-9728-0 Xi, Q. (2000). Investigation on the distribution and potential of giant grasses in China. PhD thesis. Goettingen, Germany: Cuvillier Verlag. Xi, Q., & Jezowkski, S. (2004). Plant resources of Triarrhena and Miscanthus species in China and its meaning for Europe. Plant Breeding and Seed Science, 49, 63–77. Xue, S., Kalinina, O., & Lewandowski, I. (2015). Present and future options for the improvement of Miscanthus propagation techniques. Renewable and Sustainable Energy Reviews, 49, 1233–1246. Yin, K. Q., Gao, C. X., & Qiu, J. L. (2017). Progress and prospects in plant genome editing. Nature Plants, 3. https://doi.org/10.1038/nplants.2017.107 Yook, M. (2016). Genetic diversity and transcriptome analysis for salt tolerance in Miscanthus. PhD thesis, Seoul National University, Korea. Zaidi, S. S. E. A., Mahfouz, M. M., & Mansoor, S. (2017). CRISPR-Cpf1: A new tool for plant genome editing. Trends in Plant Science, 22, 550–553. https://doi.org/10.1016/j.tplants.2017.05.001 Zalesny, R. S., Stanturf, J. A., Gardiner, E. S., Perdue, J. H., Young, T. M., Coyle, D. R., … Hass, A. (2016). Ecosystem services of woody crop production systems. BioEnergy Research, 9, 465–491. https://doi.org/10.1007/s12155-016-9737-z Zhang, Q. X., Sun, Y., Hu, H. K., Chen, B., Hong, C. T., Guo, H. P., … Zheng, B. S. (2012). Micropropagation and plant regeneration from embryogenic callus of Miscanthus sinensis. Vitro Cellular & Developmental Biology-Plant, 48, 50–57. https://doi.org/10.1007/s11627-011-9387-y Zhang, Y., Zalapa, J. E., Jakubowski, A. R., Price, D. L., Acharya, A., Wei, Y., … Casler, M. D. (2011). Post-glacial evolution of Panicum virgatum: Centers of diversity and gene pools revealed by SSR markers and cpDNA sequences. Genetica, 139, 933–948. https://doi.org/10.1007/s10709-011-9597-6 Zhao, H., Wang, B., He, J., Yang, J., Pan, L., Sun, D., & Peng, J. (2013). Genetic diversity and population structure of Miscanthus sinensis germplasm in China. PloS One, 8, e75672. Zhou, X. H., Jacobs, T. B., Xue, L. J., Harding, S. A., & Tsai, C. J. (2015). Exploiting SNPs for biallelic CRISPR mutations in the outcrossing woody perennial Populus reveals 4-coumarate: CoA ligase specificity and redundancy. New Phytologist, 208, 298–301. Zhou, R., Macaya-Sanz, D., Rodgers-Melnick, E., Carlson, C. H., Gouker, F. E., Evans, L. M., … DiFazio, S. P. (2018). Characterization of a large sex determination region in Salix purpurea L. (Salicaceae). Molecular Genetics and Genomics, 1–16. https://doi.org/10.1007/s00438-018-1473-y Zsuffa, L., Mosseler, A., & Raj, Y. (1984). Prospects for interspecific hybridization in willow for biomass production. In K. L. Perttu (Ed.), Ecology and management of forest biomass production systems, Report 15 (pp. 261–281). Uppsala, Sweden: Swedish University of Agricultural Sciences.