期刊论文详细信息
BMC Genomics
Integrating transcriptional, metabolomic, and physiological responses to drought stress and recovery in switchgrass (Panicum virgatum L.)
Thomas E Juenger1  Philip A Fay2  Tierney L Logan1  Juan Diego Palacio-Mejía1  David B Lowry1  Michael J Aspinwall3  Eli Meyer1 
[1] Department of Integrative Biology, University of Texas at Austin, 1 University Station C0930, Austin, TX 78712, USA;USDA-ARS Grassland Soil and Water Research Laboratory, Temple, TX 76502, USA;Hawkesbury Institute for the Environment, University of Western Sydney, Penrith, NSW 2751, Australia
关键词: RNA-seq;    Gene expression;    Panicum virgatum;    Switchgrass;    Recovery;    Drought;   
Others  :  1216547
DOI  :  10.1186/1471-2164-15-527
 received in 2014-01-09, accepted in 2014-06-05,  发布年份 2014
PDF
【 摘 要 】

Background

In light of the changes in precipitation and soil water availability expected with climate change, understanding the mechanisms underlying plant responses to water deficit is essential. Toward that end we have conducted an integrative analysis of responses to drought stress in the perennial C4 grass and biofuel crop, Panicum virgatum (switchgrass). Responses to soil drying and re-watering were measured at transcriptional, physiological, and metabolomic levels. To assess the interaction of soil moisture with diel light: dark cycles, we profiled gene expression in drought and control treatments under pre-dawn and mid-day conditions.

Results

Soil drying resulted in reduced leaf water potential, gas exchange, and chlorophyll fluorescence along with differential expression of a large fraction of the transcriptome (37%). Many transcripts responded differently depending on time of day (e.g. up-regulation pre-dawn and down-regulation mid-day). Genes associated with C4 photosynthesis were down-regulated during drought, while C4 metabolic intermediates accumulated. Rapid changes in gene expression were observed during recovery from drought, along with increased water use efficiency and chlorophyll fluorescence.

Conclusions

Our findings demonstrate that drought responsive gene expression depends strongly on time of day and that gene expression is extensively modified during the first few hours of drought recovery. Analysis of covariation in gene expression, metabolite abundance, and physiology among plants revealed non-linear relationships that suggest critical thresholds in drought stress responses. Future studies may benefit from evaluating these thresholds among diverse accessions of switchgrass and other C4 grasses.

【 授权许可】

   
2014 Meyer et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150701043443411.pdf 955KB PDF download
Figure 3. 26KB Image download
Figure 7. 53KB Image download
Figure 6. 71KB Image download
Figure 5. 36KB Image download
Figure 4. 107KB Image download
Figure 3. 52KB Image download
Figure 2. 32KB Image download
Figure 1. 32KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

Figure 3.

【 参考文献 】
  • [1]Bohnert HJ, Nelson DE, Jensen RG: Adaptations to environmental stresses. Plant cell 1995, 7(7):1099.
  • [2]Bray EA: Plant responses to water deficit. Trends Plant Sci 1997, 2(2):48-54.
  • [3]Cattivelli L, Rizza F, Badeck F-W, Mazzucotelli E, Mastrangelo AM, Francia E, Mare C, Tondelli A, Stanca AM: Drought tolerance improvement in crop plants: an integrated view from breeding to genomics. Field Crop Res 2008, 105(1):1-14.
  • [4]Passioura J: Drought and Drought Tolerance. In Drought Tolerance In Higher Plants: Genetical, Physiological And Molecular Biological Analysis. Springer; 1997:1-5.
  • [5]Wittaker RH: Communities And Ecosystems. In Communities And Ecosystems . New York: McMillan; 1975.
  • [6]Zhao M, Running SW: Drought-induced reduction in global terrestrial net primary production from 2000 through 2009. Science 2010, 329(5994):940-943.
  • [7]Groisman PY, Knight RW: Prolonged dry episodes over the conterminous United States: new tendencies emerging during the last 40 years. J Clim 2008, 21(9):1850-1862.
  • [8]Karl TR, Melillo JM, Peterson TC: Global Climate Change Impacts In The United States. In In Global Climate Change Impacts In The United States . Cambridge: Cambridge University Press; 2009.
  • [9]Climate Change 2007: The Physical Science Basis, Contribution Of Working Group 1 To The Fourth Assessment Report Of The Intergovernmental Panel On Climate Change Cambridge, UK & New York, NY, USA: Cambridge University Press; 2007.
  • [10]Lawlor DW, Tezara W: Causes of decreased photosynthetic rate and metabolic capacity in water-deficient leaf cells: a critical evaluation of mechanisms and integration of processes. Ann Bot 2009, 103(4):561-579.
  • [11]Boyle MG, Boyer JS, Morgan PW: Stem infusion of liquid culture medium prevents reproductive failure of maize at low water potential. Crop Sci 1991, 31(5):1246-1252.
  • [12]McDowell NG: Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality. Plant Physiol 2011, 155(3):1051-1059.
  • [13]Foyer CH, Bloom AJ, Queval G, Noctor G: Photorespiratory metabolism: genes, mutants, energetics, and redox signaling. Annu Rev Plant Biol 2009, 60:455-484.
  • [14]Wingler A, Lea PJ, Quick WP, Leegood RC: Photorespiration: metabolic pathways and their role in stress protection. Philos Trans R Soc Lond Ser B Biol Sci 2000, 355(1402):1517-1529.
  • [15]Chaves MM, Maroco JP, Pereira JS: Understanding plant responses to drought—from genes to the whole plant. Funct Plant Biol 2003, 30(3):239-264.
  • [16]Shinozaki K, Yamaguchi-Shinozaki K: Gene expression and signal transduction in water-stress response. Plant Physiol 1997, 115(2):327.
  • [17]Reddy AR, Chaitanya KV, Vivekanandan M: Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. J Plant Physiol 2004, 161(11):1189-1202.
  • [18]Schulze E: Carbon dioxide and water vapor exchange in response to drought in the atmosphere and in the soil. Annu Rev Plant Physiol 1986, 37(1):247-274.
  • [19]Des Marais DL, McKay JK, Richards JH, Sen S, Wayne T, Juenger TE: Physiological genomics of response to soil drying in diverse Arabidopsis accessions. Plant Cell Online 2012, 24(3):893-914.
  • [20]Hayano-Kanashiro C, Calderon-Vazquez C, Ibarra-Laclette E, Herrera-Estrella L, Simpson J: Analysis of gene expression and physiological responses in three Mexican maize landraces under drought stress and recovery irrigation. PLoS One 2009, 4(10):e7531.
  • [21]Huang D, Wu W, Abrams SR, Cutler AJ: The relationship of drought-related gene expression in Arabidopsis thaliana to hormonal and environmental factors. J Exp Bot 2008, 59(11):2991-3007.
  • [22]Juenger TE, Sen S, Bray E, Stahl E, Wayne T, Mckay J, Richards JH: Exploring genetic and expression differences between physiologically extreme ecotypes: comparative genomic hybridization and gene expression studies of Kas-1 and Tsu-1 accessions of Arabidopsis thaliana. Plant Cell Environ 2010, 33(8):1268-1284.
  • [23]Kilian J, Whitehead D, Horak J, Wanke D, Weinl S, Batistic O, D’Angelo C, Bornberg‒Bauer E, Kudla J, Harter K: The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV‒B light, drought and cold stress responses. Plant J 2007, 50(2):347-363.
  • [24]Kreps JA, Wu Y, Chang H-S, Zhu T, Wang X, Harper JF: Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 2002, 130(4):2129-2141.
  • [25]Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T: Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high‒salinity stresses using a full‒length cDNA microarray. Plant J 2002, 31(3):279-292.
  • [26]Shinozaki K, Yamaguchi-Shinozaki K: Gene networks involved in drought stress response and tolerance. J Exp Bot 2007, 58(2):221-227.
  • [27]Des Marais DL, Juenger TE: Pleiotropy, plasticity, and the evolution of plant abiotic stress tolerance. Ann N Y Acad Sci 2010, 1206(1):56-79.
  • [28]Fujita Y, Fujita M, Shinozaki K, Yamaguchi-Shinozaki K: ABA-mediated transcriptional regulation in response to osmotic stress in plants. J Plant Res 2011, 124(4):509-525.
  • [29]Kakumanu A, Ambavaram MM, Klumas C, Krishnan A, Batlang U, Myers E, Grene R, Pereira A: Effects of drought on gene expression in maize reproductive and leaf meristem tissue revealed by RNA-Seq. Plant Physiol 2012, 160(2):846-867.
  • [30]Casler MD, Tobias CM, Kaeppler SM, Buell CR, Wang Z-Y, Cao P, Schmutz J, Ronald P: The switchgrass genome: tools and strategies. Plant Genome 2011, 4(3):273-282.
  • [31]McMillan C: Ecotypic differentiation within four North American prairie grasses. II. Behavioral variation within transplanted community fractions. Am J Bot 1965, 52:55-65.
  • [32]Porter CL: An analysis of variation between upland and lowland switchgrass, Panicum virgatum L., in central Oklahoma. Ecology 1966, 47(6):980-992.
  • [33]Parrish DJ, Fike JH: The biology and agronomy of switchgrass for biofuels. BPTS 2005, 24(5–6):423-459.
  • [34]Perlack RD, Wright LL, Turhollow AF, Graham RL, Stokes BJ, Erbach DC: Biomass As Feedstock For A Bioenergy And Bioproducts Industry: The Technical Feasibility Of A Billion-Ton Annual Supply. (U.S. Department of Energy and U.S. Department of Agriculture 2005. available at http://feedstockreview.ornl.gov/pdf/billion_ton_vision.pdf webcite)
  • [35]Wright L: Historical Perspective On How And Why Switchgrass Was Selected As A “Model” High-Potential Energy Crop. In Bioenergy Resources and Engineering Systems. Edited by Energy USDO. Oak Ridge, Tennessee: Oak Ridge National Laboratory; 2007.
  • [36]Gopalakrishnan G, Cristina Negri M, Snyder SW: A novel framework to classify marginal land for sustainable biomass feedstock production. J Environ Qual 2011, 40(5):1593-1600.
  • [37]King JS, Ceulemans R, Albaugh JM, Dillen SY, Domec J-C, Fichot R, Fischer M, Leggett Z, Sucre E, Trnka M: The challenge of lignocellulosic bioenergy in a water-limited world. Bioscience 2013, 63(2):102-117.
  • [38]Sanderson M, Reed R, McLaughlin S, Wullschleger S, Conger B, Parrish D, Wolf D, Taliaferro C, Hopkins A, Ocumpaugh W: Switchgrass as a sustainable bioenergy crop. Bioresour Technol 1996, 56(1):83-93.
  • [39]Schmer MR, Vogel KP, Mitchell RB, Perrin RK: Net energy of cellulosic ethanol from switchgrass. Proc Natl Acad Sci 2008, 105(2):464-469.
  • [40]Lopes MS, Araus JL, Van Heerden PD, Foyer CH: Enhancing drought tolerance in C4 crops. J Exp Bot 2011, 62(9):3135-3153.
  • [41]Travers SE, Tang Z, Caragea D, Garrett KA, Hulbert SH, Leach JE, Bai J, Saleh A, Knapp AK, Fay PA: Variation in gene expression of Andropogon gerardii in response to altered environmental conditions associated with climate change. J Ecol 2010, 98(2):374-383.
  • [42]Barney JN, Mann JJ, Kyser GB, Blumwald E, Van Deynze A, DiTomaso JM: Tolerance of switchgrass to extreme soil moisture stress: ecological implications. Plant Sci 2009, 177(6):724-732.
  • [43]Meyer E, Aglyamova G, Matz M: Profiling gene expression responses of coral larvae (Acropora millepora) to elevated temperature and settlement inducers using a novel RNA‒Seq procedure. Mol Ecol 2011, 20(17):3599-3616.
  • [44]Meyer E, Logan TL, Juenger TE: Transcriptome analysis and gene expression atlas for Panicum hallii var. filipes, a diploid model for biofuel research. Plant J 2012, 70(5):879-890.
  • [45]Zhang J-Y, Lee Y-C, Torres-Jerez I, Wang M, Yin Y, Chou W-C, He J, Shen H, Srivastava AC, Pennacchio C: Development of an integrated transcript sequence database and a gene expression atlas for gene discovery and analysis in switchgrass (Panicum virgatum L.). Plant J 2013, 74(1):160-173.
  • [46]Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Müller LA, Rhee SY, Stitt M: Mapman: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 2004, 37(6):914-939.
  • [47]Lohse M, Nagel A, Herter T, May P, Schroda M, Zrenner R, Tohge T, Fernie AR, Stitt M, Usadel B: Mercator: a fast and simple web server for genome scale functional annotation of plant sequence data. Plant Cell Environ 2014, 37(5):1250-1258.
  • [48]David M, Dzamba M, Lister D, Ilie L, Brudno M: SHRiMP2: sensitive yet practical short read mapping. Bioinformatics 2011, 27(7):1011-1012.
  • [49]Anders S, Huber W: Differential expression analysis for sequence count data. Genome Biol 2010, 11(10):R106.
  • [50]Smyth GK: Limma: linear models for microarray data. In Bioinformatics and Computational Biology Solutions using R and Bioconductor. Edited by Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W. New York: Springer; 2005:397-420.
  • [51]Maier A, Zell MB, Maurino VG: Malate decarboxylases: evolution and roles of NAD (P)-ME isoforms in species performing C4 and C3 photosynthesis. J Exp Bot 2011, 62(9):3061-3069.
  • [52]Schmittgen TD, Livak KJ: Analyzing real-time PCR data by the comparative CT method. Nat Protoc 2008, 3(6):1101-1108.
  • [53]Fiehn O, Wohlgemuth G, Scholz M: Setup And Annotation Of Metabolomic Experiments By Integrating Biological And Mass Spectrometric Metadata. In Data Integration In The Life Sciences: 2005. Berlin Heidelberg: Springer; 2005:224-239.
  • [54]Reshef DN, Reshef YA, Finucane HK, Grossman SR, McVean G, Turnbaugh PJ, Lander ES, Mitzenmacher M, Sabeti PC: Detecting novel associations in large data sets. Science 2011, 334(6062):1518-1524.
  • [55]Hatch MD: C4 photosynthesis, a unique blend of modified biochemistry, anatomy, and ultrastructure. Biochim Biophys Acta 1988, 895:81-106.
  • [56]Hartman JC, Nippert JB, Springer CJ: Ecotypic responses of switchgrass to altered precipitation. Funct Plant Biol 2012, 39(2):126-136.
  • [57]Heckathorn SA, DeLucia EH: Drought-induced nitrogen retranslocation in perennial C4 grasses of tallgrass prairie. Ecology 1994, 75(7):1877-1886.
  • [58]Bogeat-Triboulot M-B, Brosché M, Renaut J, Jouve L, Le Thiec D, Fayyaz P, Vinocur B, Witters E, Laukens K, Teichmann T: Gradual soil water depletion results in reversible changes of gene expression, protein profiles, ecophysiology, and growth performance in Populus euphratica, a poplar growing in arid regions. Plant Physiol 2007, 143(2):876-892.
  • [59]Swarbreck SM, Lindquist EA, Ackerly DD, Andersen GL: Analysis of leaf and root transcriptomes of soil-grown Avena barbata plants. Plant Cell Physiol 2011, 52(2):317-332.
  • [60]Chaves M, Flexas J, Pinheiro C: Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 2009, 103(4):551-560.
  • [61]Lawlor D, Cornic G: Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. Plant Cell Environ 2002, 25(2):275-294.
  • [62]Hummel I, Pantin F, Sulpice R, Piques M, Rolland G, Dauzat M, Christophe A, Pervent M, Bouteillé M, Stitt M: Arabidopsis plants acclimate to water deficit at low cost through changes of carbon usage: an integrated perspective using growth, metabolite, enzyme, and gene expression analysis. Plant Physiol 2010, 154(1):357-372.
  • [63]Brodribb TJ: Xylem hydraulic physiology: the functional backbone of terrestrial plant productivity. Plant Sci 2009, 177(4):245-251.
  • [64]Feder ME, Hofmann GE: Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 1999, 61(1):243-282.
  • [65]Heckathorn SA, Downs CA, Sharkey TD, Coleman JS: The small, methionine-rich chloroplast heat-shock protein protects photosystem II electron transport during heat stress. Plant Physiol 1998, 116(1):439-444.
  • [66]Cramer GR, Ergül A, Grimplet J, Tillett RL, Tattersall EA, Bohlman MC, Vincent D, Sonderegger J, Evans J, Osborne C: Water and salinity stress in grapevines: early and late changes in transcript and metabolite profiles. Funct Integr Genomics 2007, 7(2):111-134.
  • [67]Doherty CJ, Kay SA: Circadian control of global gene expression patterns. Annu Rev Genet 2010, 44:419-444.
  • [68]Wilkins O, Bräutigam K, Campbell MM: Time of day shapes Arabidopsis drought transcriptomes. Plant J 2010, 63(5):715-727.
  • [69]Wilkins O, Waldron L, Nahal H, Provart NJ, Campbell MM: Genotype and time of day shape the populus drought response. Plant J 2009, 60(4):703-715.
  • [70]Evans R, Black R, Loescher W, Fellows R: Osmotic relations of the drought‒tolerant shrub Artemisia tridentata in response to water stress. Plant Cell Environ 1992, 15(1):49-59.
  • [71]Ford C, Wilson J: Changes in levels of solutes during osmotic adjustment to water stress in leaves of four tropical pasture species. Funct Plant Biol 1981, 8(1):77-91.
  • [72]Jones M, Osmond C, Turner N: Accumulation of solutes in leaves of sorghum and sunflower in response to water deficits. Funct Plant Biol 1980, 7(2):193-205.
  • [73]Lee M, Choi Y, Burla B, Kim Y-Y, Jeon B, Maeshima M, Yoo J-Y, Martinoia E, Lee Y: The ABC transporter AtABCB14 is a malate importer and modulates stomatal response to CO2. Nat Cell Biol 2008, 10(10):1217-1223.
  • [74]Pinheiro C, Passarinho JA, Ricardo CP: Effect of drought and rewatering on the metabolism of < i > Lupinus albus organs. J Plant Physiol 2004, 161(11):1203-1210.
  • [75]Maxwell K, Johnson GN: Chlorophyll fluorescence—a practical guide. J Exp Bot 2000, 51(345):659-668.
  • [76]Thomas H: Accumulation and consumption of solutes in swards of Lolium perenne during drought and after rewatering. New Phytol 1991, 118(1):35-48.
  • [77]Amiard V, Morvan-Bertrand A, Billard J-P, Huault C, Keller F, Prud’homme M-P: Fructans, but not the sucrosyl-galactosides, raffinose and loliose, are affected by drought stress in perennial ryegrass. Plant Physiol 2003, 132(4):2218-2229.
  • [78]Stitt M, Gibon Y, Lunn JE, Piques M: Multilevel genomics analysis of carbon signalling during low carbon availability: coordinating the supply and utilisation of carbon in a fluctuating environment. Funct Plant Biol 2007, 34(6):526-549.
  • [79]Volaire F, Thomas H, Lelievre F: Survival and recovery of perennial forage grasses under prolonged Mediterranean drought: I. Growth, death, water relations and solute content in herbage and stubble. New Phytol 1998, 140(3):439-449.
  • [80]Behrman K, Kiniry J, Winchell M, Juenger T, Keitt T: Spatial forecasting of switchgrass yield under current and future climate change scenarios. Ecol Appl 2013, 23(1):73-85.
  • [81]Casler M, Vogel K, Taliaferro C, Ehlke N, Berdahl J, Brummer E, Kallenbach R, West C, Mitchell R: Latitudinal and longitudinal adaptation of switchgrass populations. Crop Sci 2007, 47(6):2249-2260.
  • [82]Casler M, Vogel K, Taliaferro C, Wynia R: Latitudinal adaptation of switchgrass populations. Crop Sci 2004, 44(1):293-303.
  • [83]Kiniry J, Anderson L, Johnson M-V, Behrman K, Brakie M, Burner D, Cordsiemon R, Fay P, Fritschi F, Houx J III: Perennial biomass grasses and the mason–dixon line: comparative productivity across latitudes in the southern great plains. BioEnergy Res 2013, 6(1):276-291.
  • [84]Lowry DB, Behrman KD, Grabowski P, Morris GP, Kiniry JR, Juenger TE: Adaptation between ecotypes and along environmental gradients in Panicum virgatum. Am Naturalist 2014, 183:682-692.
  文献评价指标  
  下载次数:78次 浏览次数:31次