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Isoprene emission protects photosynthesis in sunfleck exposed Grey poplar

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Abstract

In the present study, we combined transient temperature and light stress (sunfleck) and comparably analyzed photosynthetic gas exchange in Grey poplar which has been genetically modified in isoprene emission capacity. Overall, we demonstrate that for poplar leaves the ability to emit isoprene is crucial to maintain photosynthesis when exposed to sunflecks. Net CO2 assimilation and electron transport rates were strongly impaired in sunfleck-treated non-isoprene emitting poplars. Similar impairment was not detected when the leaves were exposed to high light (lightflecks) only. Within 10 h non-isoprene emitting poplars recovered from sunfleck-related impairment as indicated by chlorophyll fluorescence and microarray analysis. Unstressed leaves of non-isoprene emitting poplars had higher ascorbate contents, but also higher contents of malondialdehyde than wild-type. Microarray analyses revealed lipid and chlorophyll degradation processes in the non-isoprene emitting poplars. Thus, there is evidence for an adjustment of the antioxidative system in the non-isoprene emitting poplars even under normal growth conditions.

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Abbreviations

ASC:

Ascorbate

BHT:

Butylated hydroxytoluene

CHL:

Chlorophyllase

DHA:

Dehydroascorbate

DPS:

De-epoxidation status

ETR:

Electron transport rate

FIS:

Fast isoprene sensor

JA:

Jasmonate

LHCII:

Light harvesting complex II

MDA:

Malondialdehyde

MeJA:

Methyljasmonate

MEP:

Methylerythritol 4-phosphate

OPDA:

12-oxophytodienoic acid

PcISPS:

Populus × canescens isoprene synthase

PPFD:

Photosynthetic photon flux density

RNAi:

RNA interference

ROS:

Reactive oxygen species

TAG:

Triacylglyceride

TBA:

Thiobarbituric acid

TCA:

Trichloroacetic acid

WT:

Wild-type

References

  • Affek HP, Yakir D (2002) Protection by isoprene against singlet oxygen in leaves. Plant Physiol 129:269–277

    Article  CAS  PubMed  Google Scholar 

  • Behnke K, Ehlting B, Teuber M, Bauerfeind M, Louis S, Hänsch R, Polle A, Bohlmann J, Schnitzler JP (2007) Transgenic, non-isoprene emitting poplars don’t like it hot. Plant J 51:485–499

    Article  CAS  PubMed  Google Scholar 

  • Behnke K, Kleist E, Uerlings R, Wildt J, Rennenberg H, Schnitzler JP (2009) RNAi mediated suppression of isoprene biosynthesis impacts ozone tolerance. Tree Physiol 29:725–739

    Article  CAS  PubMed  Google Scholar 

  • Beigneux AP, Vergnes L, Qiao X, Quatela S, Davis R, Watkins SM, Coleman RA, Walzem AL, Philips M, Reue K, Young SG (2006) Agpat6—a novel lipid biosynthetic gene required for triacylglycerol production in mammary epithelium. J Lipid Res 47:734–744

    Article  CAS  PubMed  Google Scholar 

  • Biesenthal TA, Wu Q, Shepson PB, Wiebe HA, Anlauf KG, MacKay GI (1997) A study of relationship between isoprene, its oxidation products, and ozone, in the lower Fraser Valley. BC Atmos Environ 31:2049–2058

    Article  CAS  Google Scholar 

  • Brüggemann N, Schnitzler JP (2002) Comparison of isoprene emission, intercellular isoprene concentration and photosynthetic performance in water-limited oak (Quercus pubescens Willd. and Quercus robur L.) saplings. Plant Biol 4:456–463

    Article  Google Scholar 

  • Chazdon RL, Pearcy RW (1991) The importance of sunflecks for forest understory plants, photosynthetic machinery appears adapted to brief, unpredictable periods of radiation. Bioscience 41:760–766

    Article  Google Scholar 

  • Derwent RG, Simmonds PG, Seuring S, Dimmer C (1998) Observation and interpretation of the seasonal cycles in the surface concentrations of ozone and carbon monoxide at Mace Head, Ireland from 1990 to 1994. Atmos Environ 32:145–157

    Article  CAS  Google Scholar 

  • Dhondt S, Geoffroy P, Stelmach BA, Legrand M, Heitz T (2000) Soluble phospholipase A2 activity is induced before oxylipin accumulation in tobacco mosaic virus-infected tobacco leaves and is contributed by patatin-like enzymes. Plant J 23:431–440

    Article  CAS  PubMed  Google Scholar 

  • Du Z, Bramlage WJ (1992) Modified thiobarbituric acid assay for measuring lipid oxidation in sugar-rich plant tissue extracts. J Agric Food Chem 40:1566–1570

    Article  CAS  Google Scholar 

  • Ellenberg H (1963) Vegetation Mitteleuropas mit den Alpen in ökologischer. dynamischer und historischer Sicht. Ulmer, Stuttgart, Germany

    Google Scholar 

  • Evans GC (1956) An area survey method of investigating the distribution of light intensity in woodlands, with particular reference to sunflecks. J Ecol 44:391–428

    Article  Google Scholar 

  • Falcon S, Gentleman R (2007) Using GOstats to test gene lists for GO term association. Bioinformatics 23:257–258

    Article  CAS  PubMed  Google Scholar 

  • Haberer K, Herbinger K, Alexou M, Tausz M, Rennenberg H (2007) Antioxidative defense of old growth beech (Fagus sylvatica) under double ambient O3 concentrations in a free-air exposure system. Plant Biol 9:215–226

    Article  CAS  PubMed  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:180–198

    Google Scholar 

  • Hofer N, Alexou M, Heerdt C, Löw M, Werner H, Matyssek R, Rennenberg H, Haberer K (2008) Seasonal differences and within-canopy variations of antioxidants in mature spruce (Picea abies) trees under elevated ozone in a free-air exposure system. Environ Pollut 154:241–253

    Article  CAS  PubMed  Google Scholar 

  • Holk A, Rietz S, Zahn M, Quader H, Scherer GFE (2002) Molecular identification of cytosolic, patatin-related phospholipase A from Arabidopsis with potential functions in plant signal transduction. Plant Physiol 130:90–101

    Article  CAS  PubMed  Google Scholar 

  • Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4:249–264

    Article  PubMed  Google Scholar 

  • Jeffrey SW, Mantoura RFC, Bjørnland T (1997) Data for identification of 47 key phytoplankton pigments. In: Jeffrey SW, Mantoura RCF, Wright SW (eds) Phytoplankton pigments in oceanography: guidelines to modern methods. UNESCO Publishing, Paris, pp 239–260

    Google Scholar 

  • Kariola T, Brader G, Li J, Palva ET (2005) Chlorophyllase 1, a damage control enzyme, affects the balance between defense pathways in plants. Plant Cell Online 17:282–294

    Article  CAS  Google Scholar 

  • Kaup MT, Froese CD, Thompson JE (2002) A role for diacylglycerol acyltransferase during leaf senescence. Plant Physiol 129:1616–1626

    Article  CAS  PubMed  Google Scholar 

  • Kim K, Portis AR Jr (2005) Temperature dependence of photosynthesis in Arabidopsis plants with modifications in rubisco activase and membrane fluidity. Plant Cell Physiol 46:522–530

    Article  CAS  PubMed  Google Scholar 

  • Kirchgeßner H-P, Reichert K, Hauff K, Steinbrecher R, Schnitzler JP, Pfündel EE (2003) Light and temperature, but not UV radiation, affect chlorophylls and carotenoids in Norway spruce needles (Picea abies (L.) Karst.). Plant Cell Environ 26:1169–1179

    Article  Google Scholar 

  • Kotak S, Larkindale J, Lee U, von Koskull-Döring P, Vierling E, Scharf K-D (2007) Complexity of the heat stress response in plants. Curr Opin Plant Biol 10:310–316

    Article  CAS  PubMed  Google Scholar 

  • La Camera S, Geoffroy P, Samaha H, Ndiaye A, Rahim G, Legrand M, Heitz T (2005) A pathogen-inducible patatin-like lipid acyl hydrolase facilitates fungal and bacterial host colonization in Arabidopsis. Plant J 44:810–825

    Article  PubMed  Google Scholar 

  • La Camera S, Balagué C, Göbbel C, Geoffroy P, Legrand M, Feussner I, Roby D, Heitz T (2009) The Arabidopsis Patatin-Like Protein 2 (PLP2) plays an essential role in cell death execution and differentially affects biosynthesis of oxylipins and resistance to pathogens. Mol Plant Microbe Int 22:469–481

    Article  CAS  Google Scholar 

  • Leakey AD, Scholes JD, Press MC (2005) Physiological and ecological significance of sunflecks for dipterocarp seedlings. J Exp Bot 56:469–482

    Article  CAS  PubMed  Google Scholar 

  • Locato V, Gadaleta C, De Gara L, Concetta de Pinto M (2008) Production of reactive species and modulation of antioxidant network in response to heat shock: a critical balance for cell fate. Plant Cell Environ 31:1606–1619

    Article  CAS  PubMed  Google Scholar 

  • Loivamäki M, Gilmer F, Fischbach RJ, Sörgel C, Bachl A, Walter A, Schnitzler JP (2007) Arabidopsis, a model to study biological functions of isoprene emission? Plant Physiol 144:1–13

    Article  Google Scholar 

  • Loreto F, Velikova V (2001) Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiol 127:1781–1787

    Article  CAS  PubMed  Google Scholar 

  • Lösel DM (1978) Lipid metabolism of leaves of Poa pratensis during infection by Puccinia poarum. New Phytol 80:167–174

    Article  Google Scholar 

  • Matos AR, Pham-Thi A-T (2009) Lipid deacylating enzymes in plants: old activities, new genes. Plant Physiol Biochem 47:491–503

    Article  CAS  PubMed  Google Scholar 

  • Matos AR, Gigon A, Laffray D, Pêtres S, Zuily-Fodil Y, Pham-Thi A-T (2008) Effects of progressive drought stress on the expression of patatin-like lipid acyl hydrolase genes in Arabidopsis leaves. Physiol Plant 134:110–120

    Article  CAS  PubMed  Google Scholar 

  • Munné-Bosch S (2007) Alpha-tocopherol: a multifaceted molecule in plants. Vitam Horm 76:375–392

    Article  PubMed  Google Scholar 

  • Muraoka H, Koizumi H, Pearcy RW (2003) Leaf display and photosynthesis of tree seedlings in a cool-temperate deciduous broadleaf forest understorey. Oecologia 135:500–509

    PubMed  Google Scholar 

  • Niyogi KK (1999) Photoprotection revised: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50:333–359

    Article  CAS  PubMed  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Ann Rev Plant Physiol Plant Mol Biol 49:249–279

    Article  CAS  Google Scholar 

  • Nordby HE, Yelenosky G (1984) Effects of cold hardening on acyl lipids of citrus tissue. Phytochemistry 23:41–45

    Article  CAS  Google Scholar 

  • Padham AK, Hopkins MT, Wang T-W, McNamara LM, Lo M, Richardson LGL, Smith MD, Taylor CA, Thompson JE (2007) Characterization of a plastid triacylglycerol lipase from Arabidopsis. Plant Physiol 143:1372–1384

    Article  CAS  PubMed  Google Scholar 

  • Pastenes C, Horton P (1996) Effect of high temperature on photosynthesis in beans (I. Oxygen evolution and chlorophyll fluorescence). Plant Physiol 112:1245–1251

    CAS  PubMed  Google Scholar 

  • Pearcy RW (1990) Sunflecks and photosynthesis in plant canopies. Ann Rev Plant Phys Plant Mol Biol 41:421–453

    Article  CAS  Google Scholar 

  • Pompella A, Maellaro E, Casini AF, Ferrali M, Ciccoli L, Comport M (1987) Measurement of lipid peroxidation in vivo: a comparison of different procedures. Lipids 22:206–211

    Article  CAS  PubMed  Google Scholar 

  • Portis AR, Li C, Wang D, Salvucci ME (2008) Regulation of Rubisco activase and its interaction with Rubisco. J Exp Bot 59:1597–1604

    Article  CAS  PubMed  Google Scholar 

  • Qin D, Wu H, Peng H, Yao Y, Ni Z, Li Z, Zhou C, Sun Q (2008) Heat stress-responsive transcriptome analysis in heat susceptible and tolerant wheat (Triticum aestivum L.) by using Wheat Genome Array. BMC Genomics 9: 432. doi:10.1186/1471-2164-9-432

  • Rietz S, Holk A, Scherer GFE (2004) Expression of the patatin-related phospholipase A gene AtPLA IIA in Arabidopsis thaliana is upregulated by salicylic acid, wounding, ethylene, and iron and phosphate deficiency. Planta 219:743–753

    Article  CAS  PubMed  Google Scholar 

  • Roth U, von Roepenack-Lahaye E, Clemens S (2008) Proteome changes in Arabidopsis thaliana roots upon exposure to Cd2+. J Exp Bot 57:4003–4013

    Article  Google Scholar 

  • Sage RF, Kubien DS (2007) The temperature response of C(3) and C(4) photosynthesis. Plant Cell Environ 30:1086–1106

    Article  CAS  PubMed  Google Scholar 

  • Sakaki T, Saitol K, Kawaguchi A, Kondo N, Yamada M (1990) Conversion of monogalactosyldiacylglycerols to triacylglycerols in ozone-fumigated spinach leaves. Plant Physiol 94:766–772

    Article  CAS  PubMed  Google Scholar 

  • Salvucci ME, Osteryoung KW, Crafts-Brandner SJ, Vierling E (2001) Exceptional sensitivity of Rubisco activase to thermal denaturation in vitro and in vivo. Plant Physiol 127:1053–1064

    Article  CAS  PubMed  Google Scholar 

  • Schrader SM, Kleinbeck KR, Sharkey TD (2007) Rapid heating of intact leaves reveals initial effects of stromal oxidation on photosynthesis. Plant Cell Environ 30:671–678

    Article  CAS  PubMed  Google Scholar 

  • Schupp R, Rennenberg H (1988) Diurnal changes in the glutathione content of spruce needles (Picea abies L.). Plant Sci 57:113–117

    Article  CAS  Google Scholar 

  • Senthil-Kumar M, Kumar G, Srikanthbabu V, Udayakumar M (2007) Assessment of variability in acquired thermotolerance: potential option to study genotypic response and the relevance of stress genes. J Plant Physiol 164:111–125

    Article  CAS  PubMed  Google Scholar 

  • Sharkey TD, Singsaas EL (1995) Why plants emit isoprene. Nature 374:769

    Article  CAS  Google Scholar 

  • Sharkey TD, Chen X, Yeh S (2001) Isoprene increases thermotolerance of fosmidomycin-fed leaves. Plant Physiol 125:2001–2006

    Article  CAS  PubMed  Google Scholar 

  • Sharkey TD, Wiberley AE, Donohue AR (2008) Isoprene emission from plants: Why and how. Ann Bot 101:5–18

    Article  CAS  PubMed  Google Scholar 

  • Singsaas EL, Lerdau M, Winter K, Sharkey TD (1997) Isoprene increases thermotolerance of isoprene emitting leaves. Plant Physiol 115:1413–1420

    CAS  PubMed  Google Scholar 

  • Singsaas EL, Laporte MM, Shi J-Z, Monson RK, Bowling DR, Johnson K, Lerdau M, Jasentuliytana A, Sharkey TD (1999) Leaf temperature fluctuations affects isoprene emission from red oak (Quercus rubra) leaves. Tree Physiol 19:917–924

    CAS  PubMed  Google Scholar 

  • Sinnhuber RO, Yu TC (1958) Characterization of the red pigment formed in 2-thiobarbituric acid determination of oxidative rancidity. J Food Sci 23:626–633

    Article  CAS  Google Scholar 

  • Siwko ME, Marrink SJ, de Vries AH, Kozubek A, Uiterkamp AJMS, Mark A (2007) Does isoprene protect plant membranes from thermal shock? A molecular dynamics study. Biochim Biophys Acta 1768:198–206

    Article  CAS  PubMed  Google Scholar 

  • Tausz M, Sircelj H, Grill D (2004) The glutathione system as a stress marker in plant ecophysiology: is a stress-response concept valid? J Exp Bot 55:1955–1962

    Article  CAS  PubMed  Google Scholar 

  • Teramoto H, Nakamori A, Minagawa J, Ono T (2002) Light-intensity-dependent expression of Lhc gene family encoding light-harvesting chlorophyll-a/b proteins of photosystem II in Chlamydomonas reinhardtii. Plant Physiol 130:325–333

    Article  CAS  PubMed  Google Scholar 

  • Thompson AM (1992) The oxidizing capacity of the Earth’s atmosphere: probable past and future changes. Science 256:1157–1165

    Article  CAS  PubMed  Google Scholar 

  • Tsuchiya T, Ohta H, Okawa K, Iwamatsu A, Shimada H, Masuda T, Takamiya K (1999) Cloning of chlorophyllase, the key enzyme in chlorophyll degradation: finding of a lipase motif and the induction by methyl jasmonate. Proc Natl Acad Sci USA 96:15362–15367

    Article  CAS  PubMed  Google Scholar 

  • Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98:5116–5121

    Article  CAS  PubMed  Google Scholar 

  • Velikova V, Loreto F (2005) On the relationship between isoprene emission and thermotolerance in Phragmites australis leaves exposed to high temperatures and during the recovery from heat stress. Plant Cell Environ 28:318–327

    Article  CAS  Google Scholar 

  • Velikova V, Pinelli P, Pasqualini S, Reale L, Ferranti F, Loreto F (2005) Isoprene decreases the concentration of nitric oxide in leaves exposed to elevated ozone. New Phytol 166:419–426

    Article  CAS  PubMed  Google Scholar 

  • Vickers CE, Possell M, Cojocariu CI, Laothawornkitkul J, Ryan A, Mullineaux PM, Hewitt CN (2009a) Isoprene synthesis protects tobacco plants from oxidative stress. Plant Cell Environ 32:520–531

    Article  CAS  PubMed  Google Scholar 

  • Vickers CE, Gershenzon J, Lerdau MT, Loreto F (2009b) A unified mechanism of action for volatile isoprenoids in plant abiotic stress. Nat Biol Chem 5:283–291

    Article  CAS  Google Scholar 

  • Weis E (1981) Reversible heat-inactivation of the Calvin-cycle: a possible mechanism of temperature regulation of photosynthesis. Planta 151:33–39

    Article  CAS  Google Scholar 

  • Wiberley AE, Linskey AR, Falbel TG, Sharkey TD (2005) Development of the capacity for isoprene emission in kudzu. Plant Cell Environ 28:898–905

    Article  CAS  Google Scholar 

  • Yuan S, Liu W-J, Zhang N-H, Wang M-B, Liang H-G, Lin H-H (2005) Effects of water stress on major photosystem II gene expression and protein metabolism in barley leaves. Physiol Plant 125:464–473

    CAS  Google Scholar 

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Acknowledgements

We thank Ursula Scheerer (University of Freiburg) for ascorbate and glutathione analyses and Danielle Way (Duke University, Durham NC) for helpful comments on the manuscript. The work was supported by the German Science Foundation (DFG) (SCHN653/4 to J.-P.S.) within the German joint research group ‘Poplar—A Model to Address Tree-Specific Questions’ and by the European Commission in the frame of the Marie-Curie Research Training Network ‘ISONET’ (J.-P.S.).

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Authors and Affiliations

  1. Karlsruhe Institute of Technology, Institute for Meteorology and Climate Research (IMK-IFU), Kreuzeckbahnstr. 19, 82467, Garmisch-Partenkirchen, Germany

    Katja Behnke, Maaria Loivamäki, Ina Zimmer, Jörg-Peter Schnitzler & Sandrine Louis

  2. Institute for Forest Botany and Tree Physiology, Albert-Ludwigs-University Freiburg, 79110, Freiburg, Germany

    Heinz Rennenberg

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  1. Katja Behnke
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  2. Maaria Loivamäki
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  3. Ina Zimmer
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  4. Heinz Rennenberg
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  5. Jörg-Peter Schnitzler
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  6. Sandrine Louis
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Correspondence to Sandrine Louis.

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Katja Behnke and Maaria Loivamäki have contributed equally to the manuscript.

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Behnke, K., Loivamäki, M., Zimmer, I. et al. Isoprene emission protects photosynthesis in sunfleck exposed Grey poplar. Photosynth Res 104, 5–17 (2010). https://doi.org/10.1007/s11120-010-9528-x

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