Plant regeneration and genetic transformation in switchgrass-A review
Paul Merrick, Shuizhang Fei
1、Interdepartmental Graduate Major in Genetics and Genomics, Iowa State University, Ames IA 50011, USA
2、Department of Horticulture, Iowa State University, Ames IA 50011, USA
摘要 Switchgrass is native to the tallgrass prairie of North America. It is self-incompatible and has varied ploidy levels from diploid (2x) to dodecaploid (12x) with tetraploid and octoploid being the most common. The high yielding potential and the ability to grow well in marginal lands make switchgrass an ideal species as a dedicated biomass producer for lignocellulosic ethanol production. Genetic transformation is an important tool for studying gene function and for germplasm improvement in switchgrass, the genome of which has been sequenced recently. This paper intends to provide a comprehensive review on plant regeneration and genetic transformation in switchgrass. We first reviewed the effect of explants, basal medium and plant growth regulators on plant regeneration in switchgrass, which is a prerequisite for genetic transformation. We then reviewed the progresses on genetic transformation with either the biolistic or Agrobacterium-mediated method in switchgrass, and discussed various techniques employed to improve the transformation efficiency. Finally we reviewed the recent progresses on the use of genetic transformation in improving biomass quality such as the reduction of lignin, and in increasing biomass yield in switchgrass. We also provided a future perspective on the use of new genome editing technologies in switchgrass and its potential impact on regulatory processes.
Abstract Switchgrass is native to the tallgrass prairie of North America. It is self-incompatible and has varied ploidy levels from diploid (2x) to dodecaploid (12x) with tetraploid and octoploid being the most common. The high yielding potential and the ability to grow well in marginal lands make switchgrass an ideal species as a dedicated biomass producer for lignocellulosic ethanol production. Genetic transformation is an important tool for studying gene function and for germplasm improvement in switchgrass, the genome of which has been sequenced recently. This paper intends to provide a comprehensive review on plant regeneration and genetic transformation in switchgrass. We first reviewed the effect of explants, basal medium and plant growth regulators on plant regeneration in switchgrass, which is a prerequisite for genetic transformation. We then reviewed the progresses on genetic transformation with either the biolistic or Agrobacterium-mediated method in switchgrass, and discussed various techniques employed to improve the transformation efficiency. Finally we reviewed the recent progresses on the use of genetic transformation in improving biomass quality such as the reduction of lignin, and in increasing biomass yield in switchgrass. We also provided a future perspective on the use of new genome editing technologies in switchgrass and its potential impact on regulatory processes.
The senior author is supported by a grant from the Bill Melinda Gates Foundation. The corresponding author thanks the National Institute of Food and Agriculture of the United States Department of Agriculture for support (Award number 2013-33522-21091).
Paul Merrick, Shuizhang Fei.
2015.
Plant regeneration and genetic transformation in switchgrass-A review. Journal of Integrative Agriculture, 14(3): 483-493.
Albright III V C, Murphy I J, Anderson J A, Coats J R. 2013.Fate of atrazine in switchgrass-soil column system.Chemosphere, 90, 1847-1853
Alexandrova K, Denchev P, Conger B. 1996a. In vitrodevelopment of inflorescences from switchgrass nodalsegments. Crop Science, 36, 175-178
Alexandrova K, Denchev P, Conger B. 1996b. Micropropagationof switchgrass by node culture. Crop Science, 36, 1709-1711
Altpeter F, Baisakh N, Beachy R, Bock R, Capell T, ChristouP, Daniell H, Datta K, Datta S, Dix P, Fauquet C, Huang N,Kohli A, Mooibroek H, Nicholson L, Nguyen T, Nugent G,Raemakers K, Romano A, Somers D, et al. 2005. Particlebombardment and the genetic enhancement of crops: Mythsand realities. Molecular Breeding, 15, 305-327
Bilang R, Zhang S, Leduc N, Iglesias V A, Gisel A, SimmondsJ, Potrykus I, Sautter C. 1993. Transient gene expressionin vegetative shoot apical meristems of wheat after ballisticmicrotargeting. The Plant Journal, 4, 735-744
Brunken J N, Estes J R. 1975. Cytological and morphologicalvariation in Panicum virgatum L. The SouthwesternNaturalist, 19, 379-385
Burris J N, Mann D G, Joyce B L, Stewart Jr C. 2009. Animproved tissue culture system for embryogenic callusproduction and plant regeneration in switchgrass. BioEnergyResearch, 2, 267-274
Caplan A, Herrera-Estrella L, Inze D, van Haute E, van MontaguM, Schell J, Zambryski P. 1983. Introduction of geneticmaterial into plant cells. Science, 222, 815-821
Chen Q J, Zhou H M, Chen J, Wang X C. 2006. A Gatewaybasedplatform for multigene plant transformation. PlantMolecular Biology, 62, 927-936
Cheng M, Hu T, Layton J, Liu C, Fry J. 2003. Desiccation ofplant tissue post-agrobacterium infection enhances T-DNAdelivery and increase stable transformation efficiency inwheat. In Vitro Cellular & Developmental Biology-Plant,39, 595-604
Conger B, Gray D. 1984. In vitro culture in forage grassimprovement. In: Proceedings of the 28th Grass BreedersWork Planning Conference. College Station, TX, USDA,Mandan, ND, USA. pp. 50-64
Conger B, Hanning G, Gray D, McDaniel J. 1983. Directembryogenesis from mesophyll cells of orchardgrass.Science, 221, 850-851
Conger B, Trigiano R, Gray D. 1988. Cell culture of the Poaceae(Gramineae). Plant Cell Biotechnology, 18, 49-61
Costich D E , Friebe B, Sheehan M J, Casler M D, Buckler ES. 2010. Genome-size variation in switchgrass (Panicumvirgatum): Flow cytometry and cytology reveal rampantaneuploidy. The Plant Genome Journal, 3, 130-141
Dabney S M, Wilson G V, McGregor K C, Vieira D A. 2012.Runoff through and upslope of contour switchgrass hedges.Soil Science Society of America Journal, 76, 210-219
van Dam J, Faaij A P C, Hilbert J, Petruzzi H, Turkenburg W C.2009. Large-scale bioenergy production from soybeans andswitchgrass in Argentina: Part A: potential and economicfeasibility for national and international markets. Part B:environmental and socio-economic impacts on a regional level. Renewable and Sustainable Energy Reviews, 13,1679-1733
Denchev P, Conger B. 1994. Plant regeneration from calluscultures of switchgrass. Crop Science, 34, 1623-1627
Denchev P, Conger B. 1995. In vitro culture of switchgrass:Influence of 2,4-D and picloram in combination withbenzyladenine on callus initiation and regeneration. PlantCell, Tissue and Organ Culture, 40, 43-48
Edgerton M D. 2009. Increasing crop productivity to meet globalneeds for feed, food, and fuel. Plant Physiology, 149, 7-13
Ekman A, Wallberg O, Joelsson E, Borjesson P. 2013.Possibilities for sustainable biorefineries based onagricultural residues-A case study of potential strawbasedethanol production in Sweden. Applied Energy,102, 299-308
Fischer T. 1996. Switch grass (Panicum virgatum). Horticulture,The Magazine of American Gardening, 74, 82.Fraley R T, Rogers S G, Horsch R B, Eichholtz D A, Flick JS, Fink C L, Hoffmann N L, Sanders P R. 1985. The SEVsystem: A new disarmed Ti plasmid vector system for planttransformation. Biotechnology, 3, 629-635
de Framond A J, Barton K A, Chilton M D. 1983. Mini-Ti: A newvector strategy for plant genetic engineering. Biotechnology,1, 262-269
Fu C, Mielenz J R, Xiao X, Ge Y, Hamilton C Y, RodriguezM J, Chen F, Foston, M, Ragauskas A, Bouton J, DixonR A, Wang Z Y. 2011a. Genetic manipulation of ligninreduces recalcitrance and improves ethanol productionfrom switchgrass. Proceedings of the National Academy ofSciences of the United States of America, 108, 3803-3808
Fu C, Sunkar R, Zhou C, Shen H, Zhang J Y, Matts J, WolfJ, Mann D G J, Stewart C N, Tang Y, Wang Z Y. 2012.Overexpression of miR156 in switchgrass (Panicumvirgatum L.) results in various morphological alterations andleads to improved biomass production. Plant BiotechnologyJournal, 10, 443-452
Fu C, Xiao X, Xi Y, Ge Y, Chen F, Bouton J, Dixon R, Wang Z Y.2011b. Downregulation of cinnamyl alcohol dehydrogenase(CAD) leads to improved saccharification efficiency inswitchgrass. BioEnergy Research, 4, 153-164
Fulton L, Howes T, Hardy J. 2005. Biofuels for transport:An international perspective. GEFSTAP Liquid BiofuelsWorkshop.Gambley R L, Fond R, Smith G R. 1993. Microprojectiletransformation of sugarcane meristems and regeneration ofshoots expressing β-glucuronidase. Plant Cell Reports,12,343-346
Gandhi V P, Zhou Z. 2014. Food demand and the food securitychallenge with rapid economic growth in the emergingeconomies of India and China. Food Research International,63, 108-124
Ge Y, Cheng X, Hopkins A, Wang Z. 2007. Generation oftransgenic Lolium temulentum plants by agrobacteriumtumefaciens-mediated transformation. Plant Cell Reports,26, 783-789
Gray D, Conger B, Hanning G. 1984. Somatic embryogenesisin suspension and suspension-derived callus cultures ofDactylis glomerata. Protoplasma, 122, 196-202
Gupta S, Conger B. 1998. In vitro differentiation of multipleshoot clumps from intact seedlings. In Vitro Cellular &Developmental Biology-Plant, 34, 196-202
Gupta S, Conger B. 1999. Somatic embryogenesis and plantregeneration from suspension cultures. Crop Science, 39,243-247
Hoekema A, Hirsh P R, Hooykaas P J J, Schilperoort R A. 1983.A binary plant vector strategy based on separation of virandT-region of the Agrobacterium tumefaciens Ti-plasmid.Nature, 303, 179-180
Hopkins A A, Taliaferro C M, Murphy C D, Christian D. 1996.Chromosome number and nuclear DNA content of severalswitchgrass populations. Crop Science, 36, 1192-1195
Hultquist S J, Vogel K P, Arumuganathan K, Kaeppler S.1996. Chloroplast DNA and nuclear DNA variations amongcultivars of switchgrass, Panicum virgatum L. Crop Science,36, 1049-1052
Hultquist S J, Vogel K P, Lee D J, Arumuganathan K, KaepplerS. 1997. DNA content and chloroplast DNA polymorphismsamong switchgrasses from remnant Midwestern prairies.Crop Science, 37, 595-598
Iglesias V, Gisel A, Bilang R, Leduc N, Potrykus I, SautterC. 1994. Transient expression of visible marker genesin meristem cells of wheat embryos after ballistic microtargeting.Planta, 192, 84-91
Jiang W, Zhou H, Honghao B, Fromm M, Yang B, Weeks D P.2013. Demonstration of CRISPR/CAS9/sgRNA-mediatedtargeted gene modification in Arabidopsis, tobacco,sorghum and rice. Nucleic Acids Research, 41,12.Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna J A,Charpentier E. 2012. A programmable dual-RNA-guidedDNA endonuclease in adaptive bacterial immunity. Science,337, 816-821
King Z, Bray A, LaFayette P, Parrott W. 2014. Biolistictransformation of elite genotypes of switchgrass (Panicumvirgatum L.). Plant Cell Reports, 33, 313-322
Krautwig B, Lorz H. 1995. Cereal protoplasts. Plant Science,111, 1-10
Leal M R, Nogueira L A, Cortez L A. 2013. Land demand forethanol production. Applied Energy, 102, 266-271
Lewandowski I, Scurlock J M, Lindvall E, Christou M. 2003. Thedevelopment and current status of perennial rhizomatousgrasses as energy crops in the US and Europe. Biomassand Bioenergy, 25, 335-361
Li J F, Park E, von Arnim A, Nebenfuhr A. 2009. The FASTtechnique: A simplified Agrobacterium-based transformationmethod for transient gene expresion analysis in seedlings ofArabidopsis and other plant species. Plant Methods, 5, 15.Li L, Qu R, Kochko A, Fauquet C, Beachy R. 1993. An improvedrice transformation system using the biolistic method. PlantCell Reports, 12, 250-255
Li R, Qu R. 2011. High throughput Agrobacterium-mediatedswitchgrass transformation. Biomass & Bioenergy, 35,1046-1054
Li T, Huang S, Zhao X, Wright D A, Carpenter S, Spalding M H,Weeks D P, Yang B. 2011. Modularly assembled designerTAL effector nucleases for targeted gene knockout andgene replacement in eukaryotes. Nucleic Acids Research,39, 6315-6325
Littlewood J, Guo M, Boerjan W, Murphy R J. 2014. Bioethanolfrom poplar: A commercially viable alternative to fossil fuelin the European Union. Biotechnology for Biofuels, 7, 12.Lu J, Sivamani E, Li X, Qu R. 2008. Activity of the 5’ regulatoryregions of the rice polyubiquitin rubi3 gene in transgenic riceplants as analyzed by both GUS and GFP reporter genes.Plant Cell Reports, 27, 1587-1600
Ma Y, An Y, Shui J, Sun Z. 2011. Adaptability evaluation ofswitchgrass (Panicum virgatum L.) cultivars on the LoessPlateau of China. Plant Science, 181, 638-643
Mann D G, King Z R, Liu W, Joyce B L, Percifield R J,Hawkins J S, Lafayette P, Artelt B, Burris J, Mazarei M,Bennetzen J, Parrott W, Stewart Jr C. 2011. Switchgrass(Panicum virgatum L.) polyubiquitin gene (PvUbi1 andPvUbi2) promoters for use in plant transformation. BMCBiotechnology, 11, 74-87
Martinez-Reyna J M, Vogel K P, Caha C, Lee D J. 2001.Meiotic stability, chloroplast DNA polymorphisms, andmorphological traits of upland×lowland switchgrassreciprocal hybrids. Crop Science, 41, 1579-1583
Martinez-Reyna J M, Vogel K P. 2002. Incompatibility systemsin switchgrass. Crop Science, 42, 1800-1805
Mazarei M, Al-Ahmad H, Rudis M R, Joyce B L, Stewart Jr C.2011. Switchgrass (Panicum virgatum L.) cell suspensioncultures: Establishment, characterization, and application.Plant Science, 181, 712-715
Mazarei M, Al-Ahmed H, Rudis M, Stewart C. 2008. Protoplastisolation and transient gene expression in switchgrass,Panicum virgatum L. Biotechnology Journal, 3, 354-359
Minick K J, Strahm B D, Fox T R, Sucre E B, Leggett Z H,Zerpa J L. 2014. Switchgrass intercropping reduces soilinorganic nitrogen in a young loblolly pine plantation locatedin coastal North Carolina. Forest Ecology and Management,319, 161-168
Moore K J, Moser L E, Vogel K P, Waller S S, Johnson B E,Pedersen J F. 1991. Describing and quantifying growthstages of perennial forage grasses. Agronomy Journal,83, 1073-1077
Morrish F, Vasil V, Vasil I. 1987. Developmental morphogenesisand genetic manipulation in tissue and cell cultures ofGramineae. Advances in Genetics, 24, 431-499
Nageswara-Rao M, Soneji J R, Kwit C, Stewart C N. 2013.Advances in biotechnology and genomics of switchgrass.Biotechnology for Biofuels, 6, 15.Odjakova M, Conger B. 1999. The influence of osmoticpretreatment and inoculum age on the initiation andregenerability of switchgrass suspension cultures. In VitroCellular & Developmental Biology-Plant, 35, 442-444
Ogawa Y, Shirakawa M, Koumoto Y, Honda M, Asami Y, KondoY, Hara-Nishimura I. 2014. A simple and reliable multi-genetransformation method for switchgrass. Plant Cell Reports,33, 1161-1172
Pedersen J, Vogel K, Funnell D. 2005. Impact of reduced ligninon plant fitness. Crop Science, 45, 812-819
Ramamoorthy R, Kumar P P. 2012. A simplified protocol forgenetic transformation of switchgrass. Plant Cell Reports,31, 1923-1931
Richards H, Rudas V, Sun H, McDaniel J, Tomaszewski Z,Conger B. 2001. Construction of a GFP-BAR plasmid andits use. Plant Cell Reports, 20, 48-54
Saathoff A J, Sarath G, Chow E K, Dien B S, Tobias C M. 2011.Downregulation of cinnamyl-alcohol dehydrogenase inswitchgrass by RNA silencing results in enhanced glucoserelease after cellulase treatment. PLoS ONE, 6, e16416.
Searchinger T, Heimlich R, Houghton R A, Dong F, Elobeid A,Fabiosa J, Tokgoz S, Hayes D, Yu T H. 2008. Use of U.S.croplands for biofuels increases greenhouse gases throughemissions from land-use change. Science, 319, 1238-1240
Seo M S, Takahara M, Ebina M, Takamizo T. 2008. Evaluationof tissue culture response from mature seeds of Panicumspp. Grassland Science, 54, 125-130
Shen H, He X, Poovaiah C R, Wuddineh W A, Ma J, Mann DG, Wang H, Jackson L, Tang Y, Neal S C, Chen F, DixonR A. 2012. Functional characterization of the switchgrass(Panicum virgatum) R2R3-MYB transcription factorPvMYB4 for improvement of lignocellulosic feedstocks.New Phytologist, 193, 121-136
Shen H, Poovaiah C R, Ziebell A, Tschaplinski T J, Pattathil S,Gjersing E, Engle N L, Katahira R, Pu Y, Sykes R, Chen F,Ragauskas A J, Mielenz J R, Hahn M G, Davis M, Stewart CN, Dixon R A. 2013. Enhanced characteristics of geneticallymodified switchgrass (Panicum virgatum L.) for high biofuelproduction. Biotechnology for Biofuels, 6, 71-85
Sladen S E, Bransby D I, Aiken G E. 1991. Biomass, yields,composition, and production costs for eight switchgrassvarieties in Alabama. Biomass and Bioenergy, 1, 119-122
Somleva M, Snell K, Beaulieu J, Peoples O, Garrison B,Patterson N. 2008. Production of polyhydroxybutyratein switchgrass, a value-added coproduct in an importantlignocellulosic biomass crop. Plant Biotechnology Journal,6, 663-678
Somleva M, Tomaszewski Z, Conger B. 2002. Agrobacteriummediatedgenetic transformation of switchgrass. CropScience, 42, 2080-2087
Song G Q, Walworth A, Hancock J F. 2012. Factors influencingAgrobacterium-mediated transformation of switchgrasscultivars. Plant Cell, Tissue and Organ Culture (PCTOC),108, 445-453
Sullivan T, Christensen A, Quail P. 1989. Isolation andcharacterization of a maize chlorophyll a/b binding proteingene that produces high levels of mRNA in the dark.Molecular and General Genetics, 215, 431-440
Tomes D. 1990. Transformation in corn: Non-sexual genetransfer. In: Twenty-Sixth Annual Illinois Corn BreedersSchool Symposium at the University of Illinois. Urbana-Champaign, USA. pp. 1-13
Tschaplinski T J, Standaert R F, Engle N L, Martin M Z, Sangha A K, Parks J M, Smith J C, Samuel R, Jiang N, Pu Y,Ragauskas A J, Hamilton C Y, Fu C, Wang Z Y, DavisonB H, Dixon R A, Mielenz J R. 2012. Down-regulation ofthe caffeic acid O-methyltransferase gene in switchgrassreveals a novel monolignol analog. Biotechnology forBiofuels, 5, 71.
Valentina P, Stefanovska T, Lewis E E, Erickson L E, DavisL C. 2014. Miscanthus as a productive biofuel crop forphytoremediation. Critical Reviews in Plant Sciences, 33,1-19
VanderGheynst J, Guo H, Simmons C. 2008. Response surfacestudies that elucidate the role of infiltration conditions onAgrobacterium tumefaciens-mediated transient transgeneexpression in harvested switchgrass (Panicum virgatum).Biomass and Bioenergy, 32, 372-379
Vasil I. 1987. Developing cell and tissue culture systems for theimprovement of cereal and grass crops. Journal of PlantPhysiology, 128, 193-218
Vasil I, Vasil V. 1992. Advances in cereal protoplast research.Physiologia Plantarum, 85, 279-283
Vincent M, Pometto A L, van Leeuwen J H. 2011. Simultaneoussaccharification and fermentation of ground cornstoverfor the production of fuel ethanol using Phanerochaetechrysosporium, Gloeophyllum trabeum, Saccharomycescerevisiae, and Escherichia coli K011. Journal ofMicrobiology and Biotechnology, 21, 703-710
Vogel J, Hill T. 2008. High-efficiency Agrobacterium-mediatedtransformation of Brachypodium distachyon inbred lineBd21-3. Plant Cell Reports, 27, 471-478
Vogel K P. 2004. Switchgrass. In: Moser L E, Burson B L,Sollenberger L E, eds., Warm-Season (C4) Grasses.Agronomy Monograph 45. American Society of Agronomy,Inc., Crop Science Society of America, Inc., Soil ScienceSociety of America, Inc., Madison, Wisconsin, USA. pp.561-588
Wang Z, Ge Y. 2005. Agrobacterium-mediated high efficiencytransformation of tall fescue (Festuca arundinacea). Journalof Plant Physiology, 162, 103-113
Wedin D A. 2004. C4 Grasses: resource use, ecology, andglobal change. In: Moser L E, Burson B L, Sollenberger LE, eds., Warm-Season (C4) Grasses. Agronomy Monograph45. American Society of Agronomy, Inc., Crop ScienceSociety of America, Inc., Soil Science Society of America,Inc., Madison, Wisconsin, USA. pp. 15-50
Wright L, Turhollow A. 2010. Switchgrass selection as a “model”bioenergy crop: A history of the process. Biomass andBioenergy, 34, 851-868
Wright L L, Cushman J H, Ehrenshaft A R, McLaughlin SB, Martin S A, McNabb W A, Ranney J W, Tuskan G A,Turhollow A F. 1993. Biofuels Feedstock DevelopmentProgram Annual Progress Report for 1992. ORNL-6781.Oak Ridge National Laboratory, Oak Ridge, TN 37831.
Xi Y, Fu C, Nandakumar R, Hisano H, Bouton J, Wang ZY. 2009. Agrobacterium-mediated transformation ofswitchgrass and inheritance of the transgenes. BioEnergyResearch, 2, 275-283
Xu B, Escamilla-Trevino L L, Sathitsuksanoh N, Shen Z, ShenH, Zhang Y H P, Dixon R A, Zhao B. 2011a. Silencing of4-coumarate: Coenzyme A ligase in switchgrass leadsto reduced lignin content and improved fermentablesugar yields for biofuel production. New Phytologist, 192,611-625
Xu B, Huang L, Shen Z, Welbaum G E, Zhang X, Zhao B.2011b. Selection and characterization of a new switchgrass(Panicum virgatum L.) line. Scientia Horticulturae, 129,854-861
Yin Z, Wang G L. 2000. Evidence of multiple complex patternsof T-DNA integration into the rice genome. Theoretical andApplied Genetics, 100, 461-470
Zhang S, Zhong H, Stricklen M. 1996. Production of multipleshoots from apical meristems of oat (Avena sativa L.).Journal of Plant Physiology, 148, 667-671
Zhao Q, Dixon R A. 2014. Altering the cell wall and its impacton plant disease: From forage to bioenergy. Annual Reviewof Phytopathology, 52, 69-91
Zhao Z Y, Gu W, Cai T, Tagliani L, Hondred D, Bond D,Schroeder S, Rudert M, Pierce D. 2002. High throughputgenetic transformation mediated by Agrobacteriumtumefaciens in maize. Molecular Breeding, 8, 323-333