Advertisement

Photosynthesis Research

, Volume 104, Issue 1, pp 5–17 | Cite as

Isoprene emission protects photosynthesis in sunfleck exposed Grey poplar

  • Katja Behnke
  • Maaria Loivamäki
  • Ina Zimmer
  • Heinz Rennenberg
  • Jörg-Peter Schnitzler
  • Sandrine Louis
Regular Paper

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.

Keywords

Isoprene Poplar Sunfleck Thermal stress Microarray Gas exchange 

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

Notes

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.).

Supplementary material

11120_2010_9528_MOESM1_ESM.pdf (50 kb)
Supplementary material 1 (PDF 51 kb)
11120_2010_9528_MOESM2_ESM.pdf (62 kb)
Supplementary material 2 (PDF 62 kb)
11120_2010_9528_MOESM3_ESM.pdf (53 kb)
Supplementary material 3 (PDF 54 kb)
11120_2010_9528_MOESM4_ESM.pdf (41 kb)
Supplementary material 4 (PDF 41 kb)

References

  1. Affek HP, Yakir D (2002) Protection by isoprene against singlet oxygen in leaves. Plant Physiol 129:269–277CrossRefPubMedGoogle Scholar
  2. 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 51:485–499CrossRefPubMedGoogle Scholar
  3. Behnke K, Kleist E, Uerlings R, Wildt J, Rennenberg H, Schnitzler JP (2009) RNAi mediated suppression of isoprene biosynthesis impacts ozone tolerance. Tree Physiol 29:725–739CrossRefPubMedGoogle Scholar
  4. 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 47:734–744CrossRefPubMedGoogle Scholar
  5. 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 31:2049–2058CrossRefGoogle Scholar
  6. 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 4:456–463CrossRefGoogle Scholar
  7. Chazdon RL, Pearcy RW (1991) The importance of sunflecks for forest understory plants, photosynthetic machinery appears adapted to brief, unpredictable periods of radiation. Bioscience 41:760–766CrossRefGoogle Scholar
  8. 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 32:145–157CrossRefGoogle Scholar
  9. 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 23:431–440CrossRefPubMedGoogle Scholar
  10. Du Z, Bramlage WJ (1992) Modified thiobarbituric acid assay for measuring lipid oxidation in sugar-rich plant tissue extracts. J Agric Food Chem 40:1566–1570CrossRefGoogle Scholar
  11. Ellenberg H (1963) Vegetation Mitteleuropas mit den Alpen in ökologischer. dynamischer und historischer Sicht. Ulmer, Stuttgart, GermanyGoogle Scholar
  12. Evans GC (1956) An area survey method of investigating the distribution of light intensity in woodlands, with particular reference to sunflecks. J Ecol 44:391–428CrossRefGoogle Scholar
  13. Falcon S, Gentleman R (2007) Using GOstats to test gene lists for GO term association. Bioinformatics 23:257–258CrossRefPubMedGoogle Scholar
  14. 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 9:215–226CrossRefPubMedGoogle Scholar
  15. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:180–198Google Scholar
  16. 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 154:241–253CrossRefPubMedGoogle Scholar
  17. 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 130:90–101CrossRefPubMedGoogle Scholar
  18. 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 4:249–264CrossRefPubMedGoogle Scholar
  19. 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 239–260Google Scholar
  20. 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 17:282–294CrossRefGoogle Scholar
  21. Kaup MT, Froese CD, Thompson JE (2002) A role for diacylglycerol acyltransferase during leaf senescence. Plant Physiol 129:1616–1626CrossRefPubMedGoogle Scholar
  22. Kim K, Portis AR Jr (2005) Temperature dependence of photosynthesis in Arabidopsis plants with modifications in rubisco activase and membrane fluidity. Plant Cell Physiol 46:522–530CrossRefPubMedGoogle Scholar
  23. 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 26:1169–1179CrossRefGoogle Scholar
  24. 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 10:310–316CrossRefPubMedGoogle Scholar
  25. 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 44:810–825CrossRefPubMedGoogle Scholar
  26. 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 22:469–481CrossRefGoogle Scholar
  27. Leakey AD, Scholes JD, Press MC (2005) Physiological and ecological significance of sunflecks for dipterocarp seedlings. J Exp Bot 56:469–482CrossRefPubMedGoogle Scholar
  28. 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 31:1606–1619CrossRefPubMedGoogle Scholar
  29. 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 144:1–13CrossRefGoogle Scholar
  30. 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 127:1781–1787CrossRefPubMedGoogle Scholar
  31. Lösel DM (1978) Lipid metabolism of leaves of Poa pratensis during infection by Puccinia poarum. New Phytol 80:167–174CrossRefGoogle Scholar
  32. Matos AR, Pham-Thi A-T (2009) Lipid deacylating enzymes in plants: old activities, new genes. Plant Physiol Biochem 47:491–503CrossRefPubMedGoogle Scholar
  33. 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 134:110–120CrossRefPubMedGoogle Scholar
  34. Munné-Bosch S (2007) Alpha-tocopherol: a multifaceted molecule in plants. Vitam Horm 76:375–392CrossRefPubMedGoogle Scholar
  35. Muraoka H, Koizumi H, Pearcy RW (2003) Leaf display and photosynthesis of tree seedlings in a cool-temperate deciduous broadleaf forest understorey. Oecologia 135:500–509PubMedGoogle Scholar
  36. Niyogi KK (1999) Photoprotection revised: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50:333–359CrossRefPubMedGoogle Scholar
  37. Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Ann Rev Plant Physiol Plant Mol Biol 49:249–279CrossRefGoogle Scholar
  38. Nordby HE, Yelenosky G (1984) Effects of cold hardening on acyl lipids of citrus tissue. Phytochemistry 23:41–45CrossRefGoogle Scholar
  39. 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 143:1372–1384CrossRefPubMedGoogle Scholar
  40. Pastenes C, Horton P (1996) Effect of high temperature on photosynthesis in beans (I. Oxygen evolution and chlorophyll fluorescence). Plant Physiol 112:1245–1251PubMedGoogle Scholar
  41. Pearcy RW (1990) Sunflecks and photosynthesis in plant canopies. Ann Rev Plant Phys Plant Mol Biol 41:421–453CrossRefGoogle Scholar
  42. 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 22:206–211CrossRefPubMedGoogle Scholar
  43. Portis AR, Li C, Wang D, Salvucci ME (2008) Regulation of Rubisco activase and its interaction with Rubisco. J Exp Bot 59:1597–1604CrossRefPubMedGoogle Scholar
  44. 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
  45. 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 219:743–753CrossRefPubMedGoogle Scholar
  46. Roth U, von Roepenack-Lahaye E, Clemens S (2008) Proteome changes in Arabidopsis thaliana roots upon exposure to Cd2+. J Exp Bot 57:4003–4013CrossRefGoogle Scholar
  47. Sage RF, Kubien DS (2007) The temperature response of C(3) and C(4) photosynthesis. Plant Cell Environ 30:1086–1106CrossRefPubMedGoogle Scholar
  48. Sakaki T, Saitol K, Kawaguchi A, Kondo N, Yamada M (1990) Conversion of monogalactosyldiacylglycerols to triacylglycerols in ozone-fumigated spinach leaves. Plant Physiol 94:766–772CrossRefPubMedGoogle Scholar
  49. 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 127:1053–1064CrossRefPubMedGoogle Scholar
  50. Schrader SM, Kleinbeck KR, Sharkey TD (2007) Rapid heating of intact leaves reveals initial effects of stromal oxidation on photosynthesis. Plant Cell Environ 30:671–678CrossRefPubMedGoogle Scholar
  51. Schupp R, Rennenberg H (1988) Diurnal changes in the glutathione content of spruce needles (Picea abies L.). Plant Sci 57:113–117CrossRefGoogle Scholar
  52. 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 164:111–125CrossRefPubMedGoogle Scholar
  53. Sharkey TD, Singsaas EL (1995) Why plants emit isoprene. Nature 374:769CrossRefGoogle Scholar
  54. Sharkey TD, Chen X, Yeh S (2001) Isoprene increases thermotolerance of fosmidomycin-fed leaves. Plant Physiol 125:2001–2006CrossRefPubMedGoogle Scholar
  55. Sharkey TD, Wiberley AE, Donohue AR (2008) Isoprene emission from plants: Why and how. Ann Bot 101:5–18CrossRefPubMedGoogle Scholar
  56. Singsaas EL, Lerdau M, Winter K, Sharkey TD (1997) Isoprene increases thermotolerance of isoprene emitting leaves. Plant Physiol 115:1413–1420PubMedGoogle Scholar
  57. 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 19:917–924PubMedGoogle Scholar
  58. Sinnhuber RO, Yu TC (1958) Characterization of the red pigment formed in 2-thiobarbituric acid determination of oxidative rancidity. J Food Sci 23:626–633CrossRefGoogle Scholar
  59. 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 1768:198–206CrossRefPubMedGoogle Scholar
  60. 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 55:1955–1962CrossRefPubMedGoogle Scholar
  61. 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 130:325–333CrossRefPubMedGoogle Scholar
  62. Thompson AM (1992) The oxidizing capacity of the Earth’s atmosphere: probable past and future changes. Science 256:1157–1165CrossRefPubMedGoogle Scholar
  63. 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 96:15362–15367CrossRefPubMedGoogle Scholar
  64. Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98:5116–5121CrossRefPubMedGoogle Scholar
  65. 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 28:318–327CrossRefGoogle Scholar
  66. 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 166:419–426CrossRefPubMedGoogle Scholar
  67. 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 32:520–531CrossRefPubMedGoogle Scholar
  68. Vickers CE, Gershenzon J, Lerdau MT, Loreto F (2009b) A unified mechanism of action for volatile isoprenoids in plant abiotic stress. Nat Biol Chem 5:283–291CrossRefGoogle Scholar
  69. Weis E (1981) Reversible heat-inactivation of the Calvin-cycle: a possible mechanism of temperature regulation of photosynthesis. Planta 151:33–39CrossRefGoogle Scholar
  70. Wiberley AE, Linskey AR, Falbel TG, Sharkey TD (2005) Development of the capacity for isoprene emission in kudzu. Plant Cell Environ 28:898–905CrossRefGoogle Scholar
  71. 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 125:464–473Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Katja Behnke
    • 1
  • Maaria Loivamäki
    • 1
  • Ina Zimmer
    • 1
  • Heinz Rennenberg
    • 2
  • Jörg-Peter Schnitzler
    • 1
  • Sandrine Louis
    • 1
  1. 1.Karlsruhe Institute of TechnologyInstitute for Meteorology and Climate Research (IMK-IFU)Garmisch-PartenkirchenGermany
  2. 2.Institute for Forest Botany and Tree PhysiologyAlbert-Ludwigs-University FreiburgFreiburgGermany

Personalised recommendations