Abstract
Switchgrass is a key component of plans to develop sustainable cellulosic ethanol production for bioenergy in the USA. We sought quantitative trait loci (QTL) for leaf structure and function, using the Albany full-sib mapping population, an F1 derived from lowland tetraploid parents. We also assessed both genotype × environment interactions (G×E) in response to drought and spatial trends within experimental plots, using the mapping population and check clones drawn from the parent cultivars. Phenotypes for leaf structure and physiological performance were determined under well-watered conditions in two consecutive years, and we applied drought to one of two replicates to test for G×E. Phenotypes for check clones varied with location in our plot and were impacted by drought, but there was limited evidence of G×E except in quantum yield (ΦPSII). Phenotypes of Albany were also influenced by plant location within our plot, and after correcting for experimental design factors and spatial effects, we detected QTL for leaf size, tissue density (LMA), and stomatal conductance (g s ). Clear evidence of G×E was detected at a QTL for intrinsic water use efficiency (iWUE) that was expressed only under drought. Loci influencing physiological traits had small additive effects, showed complex patterns of heritability, and did not co-localize with QTL for morphological traits. These insights into the genetic architecture of leaf structure and function set the stage for consideration of leaf physiological phenotypes as a component of switchgrass improvement for bioenergy purposes.
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U.S. Congress (2007) Energy independence and security act of 2007. Public Law 1492–1801. doi: papers2://publication/uuid/364DB882-E966-450B-959F-AEAD6E702F42
Tilman D, Socolow R, Foley JA, Hill J, Larson E, Lynd L, Pacala S, Reilly J, Searchinger T, Somerville C, Williams R (2009) Energy. Beneficial biofuels--the food, energy, and environment trilemma. Science 325:270–271. doi:10.1126/science.1177970
Searchinger T, Heimlich R, Houghton RA, Dong F, Elobeid A, Fabiosa J, Tokgoz S, Hayes D, Yu T-H (2008) Use of U.S. croplands for biofuels increases greenhouse gases through emissions from land-use change. Science 319:1238–1240. doi:10.1126/science.1151861
Gregory PJ, George TS (2011) Feeding nine billion: the challenge to sustainable crop production. J Exp Bot 62:5233–5239. doi:10.1093/jxb/err232
Denison RF (2012) Darwinian agriculture: how understanding evolution can improve agriculture. Princeton University Press, Princeton
Wullschleger SD, Davis EB, Borsuk ME, Gunderson CA, Lynd LR (2010) Biomass production in switchgrass across the United States: database description and determinants of yield. Agron J 102:1158–1168. doi:10.2134/agronj2010.0087
Behrman KD, Kiniry JR, Winchell M, Juenger TE, Keitt TH (2013) Spatial forecasting of switchgrass productivity under current and future climate change scenarios. Ecol Appl 23:73–85
Gelfand I, Sahajpal R, Zhang X, Izaurralde RC, Gross KL, Robertson GP (2013) Sustainable bioenergy production from marginal lands in the US Midwest. Nature 493:514–517. doi:10.1038/nature11811
Fargione J, Hill J, Tilman D, Polasky S, Hawthorne P (2008) Land clearing and the biofuel carbon debt. Science 319:1235–1238. doi:10.1126/science.1152747
Heaton EA, Dohleman FG, Long SP (2008) Meeting US biofuel goals with less land: the potential of Miscanthus. Glob Chang Biol 14:2000–2014. doi:10.1111/j.1365-2486.2008.01662.x
Sanderson MA, Adler PR, Boateng AA, Casler MD, Sarath G (2006) Switchgrass as a biofuels feedstock in the USA. Can J Plant Sci 86:1315–1325. doi:10.4141/P06-136
Casler MD, Tobias CM, Kaeppler SM, Buell CR, Wang Z-Y, Cao P, Schmutz J, Ronald P (2011) The switchgrass genome: tools and strategies. Plant Genome 4:273. doi:10.3835/plantgenome2011.10.0026
Vogel KP, Mitchell RB, Casler MD, Sarath G (2014) Registration of “liberty” switchgrass. J Plant Regist 8:242. doi:10.3198/jpr2013.12.0076crc
Cassida KA, Muir JP, Hussey MA, Read JC, Venuto BC, Ocumpaugh WR (2005) Biomass yield and stand characteristics of switchgrass in south central U.S. environments. Crop Sci 45:673. doi: 10.2135/cropsci2005.0673
Lemus R, Brummer EC, Moore KJ, Molstad NE, Burras CL, Barker MF (2002) Biomass yield and quality of 20 switchgrass populations in southern Iowa, USA. Biomass and Bioenergy 23:433–442
Dohleman FG, Heaton EA, Leakey ADB, Long SP (2009) Does greater leaf-level photosynthesis explain the larger solar energy conversion efficiency of Miscanthus relative to switchgrass? Plant, Cell Environ 32:1525–1537. doi:10.1111/j.1365-3040.2009.02017.x
Zegada-Lizarazu W, Wullschleger SD, Nair SS, Monti A (2012) Crop Physiology. In: Monti A (ed) Switchgrass a valuable biomass crop for energy. Springer-Verlag, London, pp 55–86
Kiniry JR, Lynd L, Greene N, Johnson M-V V, Casler MD, Laser MS (2008) Biofuels and water use: comparison of maize and switchgrass and general perspectives. In: Wright JH, Evans DA (eds) New research on biofuels. Nova Science Publishers Inc., New-York, pp 17–30
Long SP, Farage PK, Garcia RL (2009) Measurement of leaf and canopy photosynthetic C02 exchange in the field. J Exp Bot 47:1629–1642
Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668
Farquhar GD, von Caemmerer S, Berry JA (2001) Models of photosynthesis. Plant Physiol 125:42–45
Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas M-L, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428:821–827. doi:10.1038/nature02403
Osnas JLD, Lichstein JW, Reich PB, Pacala SW (2013) Global leaf trait relationships: mass, area, and the leaf economics spectrum. Science 340:741–744. doi:10.1126/science.1231574
Raschke K (1975) Stomatal action. Annu Rev Plant Physiol 26:309–340
Jones HG (2014) Plants and microclimate: a quantitative approach to environmental plant physiology, 3rd edn. Cambridge University Press, Cambridge
Nobel PS (2009) Physicochemical and environmental plant physiology, 4th edn. Academic Press, Oxford
Donovan LA, Maherali H, Caruso CM, Huber H, de Kroon H (2011) The evolution of the worldwide leaf economics spectrum. Trends Ecol Evol 26:88–95. doi:10.1016/j.tree.2010.11.011
Richards RA, Rebetzke GJ, Condon AG, van Herwaarden AF (2002) Breeding opportunities for increasing the efficiency of water use and crop yield in temperate cereal. Crop Sci 42:111–121
Condon AG, Richards RA, Rebetzke GJ, Farquhar GD (2002) Improving intrinsic water-use efficiency and crop yield. Crop Sci 42:122–131
Donovan LA, Mason CM, Bowsher AW, Goolsby EW, Ishibashi CDA (2014) Ecological and evolutionary lability of plant traits affecting carbon and nutrient cycling. J Ecol 102:302–314. doi:10.1111/1365-2745.12193
Mason CM, Goolsby EW, Humphreys DP, Donovan LA (2015) Phylogenetic structural equation modelling reveals no need for an “origin” of the leaf economics spectrum. Ecol Lett 19:54–61. doi:10.1111/ele.12542
Warner DA, Ku MSB, Edwards GE (1987) Photosynthesis, leaf anatomy, and cellular constituents in the polyploid C4 grass Panicum virgatum. Plant Physiol 84:461–466
Wullschleger SD, Sanderson MA, McLaughlin SB, Biradar DP, Rayburn AL (1996) Photosynthetic rates and ploidy levels among populations of switchgrass. Crop Sci 36:306–312
Porter CL Jr (1966) An analysis of variation between upland and lowland switchgrass, Panicum virgatum L., in central Oklahoma. Ecology 47:980–992
McMillan C (1959) The role of ecotypic variation in the distribution of the central grassland of North America. Ecol Monogr 29:286–308
Lowry DB, Behrman KD, Grabowski P, Morris GP, Kiniry JR, Juenger TE (2014) Adaptations between ecotypes and along environmental gradients in Panicum virgatum. Am Nat 183:682–692. doi:10.1086/675760
Casler MD, Vogel KP, Taliaferro CM, Wynia RL (2004) Latitudinal adaptation of switchgrass populations. Crop Sci 44:293–303
Casler MD (2005) Ecotypic variation among switchgrass populations from the northern USA. Crop Sci 45:388–398
Aspinwall MJ, Lowry DB, Taylor SH, Juenger TE, Hawkes CV, Johnson MV, Kiniry JR, Fay PA (2013) Genotypic variation in traits linked to climate and aboveground productivity in a widespread C4 grass: evidence for a functional trait syndrome. New Phytol 199:966–980. doi:10.1111/nph.12341
Hartman JC, Nippert JB, Springer CJ (2012) Ecotypic responses of switchgrass to altered precipitation. Funct Plant Biol 39:126–136
Casler MD (2012) Switchgrass breeding, genetics, and genomics. In: Monti A (ed) Switchgrass a valuable biomass crop for energy. Springer-Verlag, London, pp 29–53
Fiedler JD, Lanzatella CL, Okada M, Jenkins J, Schmutz J, Tobias CM (2015) High-density SNP linkage map of lowland switchgrass using genotyping by sequencing. Plant Genome 8. doi: 10.3835/plantgenome2014.10.0065
Li G, Serba DD, Saha MC, Bouton JH, Lanzatella CL, Tobias CM (2014) Genetic linkage mapping and transmission ratio distortion in a three-generation four-founder population of Panicum virgatum (L.). G3: Genes, Genomes, Genet 4:913–923. doi:10.1534/g3.113.010165
Liu L, Wu Y, Wang Y, Samuels T (2012) A high-density simple sequence repeat-based genetic linkage map of switchgrass. G3: Genes, Genomes, Genet 2:357–370. doi:10.1534/g3.111.001503
Milano ER (2015) The genetic architecture of quantitative traits in locally adapted plant ecotypes. Dissertation, University of Texas at Austin.
Missaoui AM, Paterson AH, Bouton JH (2005) Investigation of genomic organization in switchgrass (Panicum virgatum L.) using DNA markers. Theor Appl Genet 110:1372–1383
Okada M, Lanzatella C, Saha MC, Bouton J, Wu R, Tobias CM (2010) Complete switchgrass genetic maps reveal subgenome collinearity, preferential pairing and multilocus interactions. Genetics 185:745–760. doi:10.1534/genetics.110.113910
Serba DD, Daverdin G, Bouton JH, Devos KM, Brummer EC, Saha MC (2014) Quantitative Trait Loci (QTL) underlying biomass yield and plant height in switchgrass. BioEnergy Res doi. doi:10.1007/s12155-014-9523-8
Lowry DB, Taylor SH, Bonnette J, Aspinwall MJ, Asmus AL, Keitt TH, Tobias CM, Juenger TE (2015) QTLs for biomass and developmental traits in switchgrass (Panicum virgatum). BioEnergy Res doi. doi:10.1007/s12155-015-9629-7
Dong H, Thames S, Liu L, Smith MW, Yan L, Wu Y (2015) QTL mapping for reproductive maturity in lowland switchgrass populations. BioEnergy Res 8:1925–1937. doi:10.1007/s12155-015-9651-9
Abràmoff MD, Magalhães PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics Int 11:36–41. doi:10.1117/1.3589100
Pinheiro J, Bates D, DebRoy S, Sarkar D, Core Team R (2015) nlme: linear and nonlinear mixed effects models. Version 3:1–120, http://cran.r-project.org/package=nlme. Accessed 21 March 2016
Kuhn M, Weston S, Wing J, Forester J, Thaler T (2013) Contrast: a collection of contrast methods. Version 0.19. http://cran.r-project.org/package=contrast. Accessed 21 March 2016
Broman KW, Wu H, Sen S, Churchill GA (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19:889–890
Margarido GRA, Souza AP, Garcia AAF (2007) OneMap: software for genetic mapping in outcrossing species. Hereditas 144:78–79
Serba D, Wu L, Daverdin G, Bahri BA, Wang X, Kilian A, Bouton JH, Brummer EC, Saha MC, Devos KM (2013) Linkage maps of lowland and upland tetraploid switchgrass ecotypes. Bioenergy Res 6:953–965. doi:10.1007/s12155-013-9315-6
Lowry DB, Hernandez K, Taylor SH, Meyer E, Logan TL, Barry K, Chapman J, Rokhsar DS, Schmutz J, Juenger TE (2015) The genetics of divergence and reproductive isolation between ecotypes of Panicum hallii. New Phytol 205:402–414. doi:10.1111/nph.13027
Condon AG, Richards RA, Rebetzke GJ, Farquhar GD (2004) Breeding for high water-use efficiency. J Exp Bot 55:2447–2460. doi:10.1093/jxb/erh277
Campitelli BE, Des Marais DL, Juenger TE (2016) Ecological interactions and the fitness effect of water-use efficiency: competition and drought alter the impact of natural MPK12 alleles in Arabidopsis. Ecol Lett 19:424–434. doi:10.1111/ele.12575
Liu Y, Zhang X, Tran H, Shan L, Kim J, Childs K, Ervin EH, Frazier T, Zhao B (2015) Assessment of drought tolerance of 49 switchgrass (Panicum virgatum) genotypes using physiological and morphological parameters. Biotechnol Biofuels 8:1–18. doi:10.1186/s13068-015-0342-8
Demmig-Adams B, Adams WW (2006) Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytol 172:11–21. doi:10.1111/j.1469-8137.2006.01835.x
Heckathorn SA, DeLucia EH (1991) Effect of leaf rolling on gas exchange and leaf temperature of Andropogon gerardii and Spartina pectinata. Bot Gaz 152:263. doi:10.1086/337888
Redmann RE (1985) Adaptation of grasses to water stress-leaf rolling and stomate distribution. Ann Missouri Bot Gard 72:833–842
O’Toole JC, Cruz RT (1980) Response of leaf water potential, stomatal resistance, and leaf rolling to water stress. Plant Physiol 65:428–432
Maseda PH, Fernández RJ (2006) Stay wet or else: three ways in which plants can adjust hydraulically to their environment. J Exp Bot 57:3963–3977. doi:10.1093/jxb/erl127
Acknowledgments
The authors thank two anonymous reviewers and M.D. Casler for their editorial comments. We wish to thank T.S. Quedensley for assistance with clonal propagation and planting and A. Asmus for technical assistance; W. Skillern, D. Dillon, L. Taranow, Ca. Timmerman, Co. Timmerman, A. Hiers, L. Villareal, C. Lee, all students in the Freshman Research Initiative, and E. Worchel helped to collect physiological measurements. John Crutchfield and the staff of Brackenridge Field Labs were invaluable resources, particularly during construction and development of the experimental rainout shelters utilized in the study. This study was funded by a National Science Foundation Plant Genome Research Program grant to TEJ and PAF (NSF IOS-0922457). A US Department of Agriculture-Agriculture and Food Research Initiative Postdoctoral Fellowship (2011-67012-30696) supported DBL during the time that the experiments were being conducted. SHT was supported by Bowdoin College during data analysis and manuscript preparation.
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Taylor, S.H., Lowry, D.B., Aspinwall, M.J. et al. QTL and Drought Effects on Leaf Physiology in Lowland Panicum virgatum . Bioenerg. Res. 9, 1241–1259 (2016). https://doi.org/10.1007/s12155-016-9768-5
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DOI: https://doi.org/10.1007/s12155-016-9768-5