Skip to main content
Log in

Effects of fosmidomycin on plant photosynthesis as measured by gas exchange and chlorophyll fluorescence

  • Regular Paper
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

In higher plants, many isoprenoids are synthesised via the chloroplastic 1-deoxy-d-xylulose 5-phosphate/2-C-methyl-d-erythritol 4-phosphate (MEP) pathway. Attempts to elucidate the function of individual isoprenoids have used the antibiotic/herbicidal compound fosmidomycin (3-[N-formyl-N-hydroxy amino] propyl phosphonic acid) to inhibit this pathway. Examination of the effect of fosmidomycin on the major components of photosynthesis in leaves of white poplar (Populus alba) and tobacco (Nicotiana tabacum) was made. Fosmidomycin reduced net photosynthesis in both species within 1 h of application, but only when photosynthesis was light-saturated. In P. alba, these reductions were confounded by high light and fosmidomycin inducing stomatal patchiness. In tobacco, this was caused by significant reductions in PSII chlorophyll fluorescence and reductions in V cmax and J max. Our data indicate that the diminution of photosynthesis is likely a complex effect resulting from the inhibition of multiple MEP pathway products, resulting in photoinhibition and photo-damage. These effects should be accounted for in experimental design and analysis when using fosmidomycin to avoid misinterpretation of results as measured by gas exchange and chlorophyll fluorescence.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

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

    Article  CAS  PubMed  Google Scholar 

  • Baker NR, Rosenqvist E (2004) Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot 55:1607–1621

    Article  CAS  PubMed  Google Scholar 

  • Baker NR, Harbinson J, Kramer DM (2007) Determining the limitations and regulation of photosynthetic energy transduction in leaves. Plant Cell Environ 30:1107–1125

    Article  CAS  PubMed  Google Scholar 

  • Barbagallo RP, Oxborough K, Pallett KE et al (2003) Rapid, non-invasive screening for perturbations of metabolism and plant growth using chlorophyll fluorescence imaging. Plant Physiol 132:485–493

    Article  CAS  PubMed  Google Scholar 

  • Barta C, Loreto F (2006) The relationship between the methyl-erythritol phosphate (MEP) pathway leading to emission of volatile isoprenoids and abscisic acid content in leaves. Plant Physiol 141:1676–1683

    Article  CAS  PubMed  Google Scholar 

  • Behnke K, Ehlting B, Teuber M et al (2007) Transgenic, non-isoprene emitting poplars don’t like it hot. Plant J 51:485–499

    Article  CAS  PubMed  Google Scholar 

  • Bernacchi CJ, Portis AR, Nakano H et al (2002) Temperature response of mesophyll conductance Implications for the determination of Rubisco enzyme kinetics and for limitations to photosynthesis in vivo. Plant Physiol 130:1992–1998

    Article  CAS  PubMed  Google Scholar 

  • Bro E, Meyer S, Genty B (1996) Heterogeneity of leaf CO2 assimilation during photosynthetic induction. Plant Cell Environ 19:1349–1358

    Article  CAS  Google Scholar 

  • Buckley TN, Farquhar GD, Mott KA (1997) Qualitative effects of patchy stomatal conductance distribution features on gas-exchange calculations. Plant Cell Environ 20:867–880

    Article  Google Scholar 

  • Claeys M, Graham B, Vas G et al (2004) Formation of secondary organic aerosols through photooxidation of isoprene. Science 303:1173–1176

    Article  CAS  PubMed  Google Scholar 

  • Cohen I, Knopf JA, Irihimovitch V et al (2005) A proposed mechanism for the inhibitory effects of oxidative stress on Rubisco assembly and its subunit expression. Plant Physiol 137:738–746

    Article  CAS  PubMed  Google Scholar 

  • Copolovici LO, Filella I, Llusia J et al (2005) The capacity for thermal protection of photosynthetic electron transport varies for different monoterpenes in Quercus ilex. Plant Physiol 139:485–496

    Article  CAS  PubMed  Google Scholar 

  • Cvejic JH, Rohmer M (2000) CO2 as main carbon source for isoprenoid biosynthesis via the mevalonate-independent methylerythritol 4-phosphate route in the marine diatoms Phaeodactylum tricornutum and Nitzschia ovalis. Phytochemistry 53:21–28

    Article  CAS  PubMed  Google Scholar 

  • Desimone M, Henke A, Wagner E (1996) Oxidative stress induces partial degradation of the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase in isolated chloroplasts of barley. Plant Physiol 111:789–796

    CAS  PubMed  Google Scholar 

  • Ethier GJ, Livingston NJ (2004) On the need to incorporate sensitivity to CO2 transfer conductance into the Farquhar-von Caemmerer-Berry leaf photosynthesis model. Plant Cell Environ 27:137–153

    Article  CAS  Google Scholar 

  • Farquhar GD (1989) Models of integrated photosynthesis of cells and leaves. Philos Trans R Soc B 323:357–367

    Article  CAS  Google Scholar 

  • Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90

    Article  CAS  Google Scholar 

  • Fraser TW, Mackender RO, Harvey BMR (1994) Ultrastructural evidence of damage to leaf stromal protein 4 hours after treatment with paraquat. J Exp Bot 45:1183–1186

    Article  CAS  Google Scholar 

  • Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron-transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92

    CAS  Google Scholar 

  • Guenther A, Hewitt CN, Erickson D et al (1995) A global-model of natural volatile organic-compound emissions. J Geophys Res 100:8873–8892

    Article  CAS  Google Scholar 

  • Guenther A, Karl T, Harley P et al (2006) Estimates of global terrestrial isoprene emissions using MEGAN (model of emissions of gases and aerosols from nature). Atmos Chem Phys 6:3181–3210

    Article  CAS  Google Scholar 

  • Jahnke S, Krewitt M (2002) Atmospheric CO2 concentration may directly affect leaf respiration measurement in tobacco, but not respiration itself. Plant Cell Environ 25:641–651

    Article  CAS  Google Scholar 

  • Koppisch AT, Fox DT, Blagg BSJ et al (2002) E. coli MEP synthase: steady-state kinetic analysis and substrate binding. Biochemistry 41:236–243

    Article  CAS  PubMed  Google Scholar 

  • Kuntz L, Tritsch D, Grosdemange-Billiard C et al (2005) Isoprenoid biosynthesis as a target for antibacterial and antiparasitic drugs: phosphonohydroxamic acids as inhibitors of deoxyxylulose phosphate reducto-isomerase. Biochem J 86:127–135

    Google Scholar 

  • Kuzuyama T, Shimizu T, Takahashi S et al (1998) Fosmidomycin, a specific inhibitor of 1-deoxy-d-xylulose 5-phosphate reductoisomerase in the nonmevalonate pathway for terpenoid biosynthesis. Tetrahedron Lett 39:7913–7916

    Article  CAS  Google Scholar 

  • Laothawornkitkul J, Paul ND, Vickers CE et al (2008) Isoprene emissions influence herbivore feeding decisions. Plant Cell Environ 31:1410–1415

    Article  CAS  PubMed  Google Scholar 

  • Lichtenthaler HK (1999) The 1-deoxy-d-xylulose-5-phosphate pathway of isoprenoid biosynthesis in plants. Annu Rev Plant Biol 50:47–65

    Article  CAS  Google Scholar 

  • Lichtenthaler HK (2000) Non-mevalonate isoprenoid biosynthesis: enzymes, genes and inhibitors. Biochem Soc Trans 28:785–789

    Article  CAS  PubMed  Google Scholar 

  • Lichtenthaler HK (2007) Biosynthesis, accumulation and emission of carotenoids, alpha-tocopherol, plastoquinone, and isoprene in leaves under high photosynthetic irradiance. Photosynth Res 92:163–179

    Article  CAS  PubMed  Google Scholar 

  • Lichtenthaler HK, Schwender J, Seemann M, Rohmer M (1995) Carotenoid biosynthesis in green algae proceeds via a novel biosynthetic pathway. In: Mathis P (ed) Photosynthesis: from light to biosphere. Kluwer, Amsterdam, pp 115–118

    Google Scholar 

  • Lichtenthaler HK, Schwender J, Disch A et al (1997) Biosynthesis of isoprenoids in higher plant chloroplasts proceeds via a mevalonate-independent pathway. FEBS Lett 400:271–274

    Article  CAS  PubMed  Google Scholar 

  • Loivamäki M, Mumm R, Dicke M et al (2008) Isoprene interferes with the attraction of bodyguards by herbaceous plants. Proc Natl Acad Sci USA 105:17430–17435

    Article  PubMed  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 

  • Loreto F, Pinelli P, Manes F et al (2004) Impact of ozone on monoterpene emissions and evidence for an isoprene-like antioxidant action of monoterpenes emitted by Quercus ilex leaves. Tree Physiol 24:361–367

    CAS  PubMed  Google Scholar 

  • Magel E, Mayrhofer S, Muller A, Zimmer I, Hampp R, Schnitzler JP (2006) Photosynthesis and substrate supply for isoprene biosynthesis in poplar leaves. Atmos Environ 40:S138–S151

    Article  CAS  Google Scholar 

  • Mott KA, Peak D (2007) Stomatal patchiness and task-performing networks. Ann Bot 99:219–226

    Article  PubMed  Google Scholar 

  • Okuhara M, Kuroda Y, Goto T et al (1980) Studies on new phosphonic acid antibiotics. 3. Isolation and characterization of Fr-31564, Fr-32863 and Fr-33289. J Antibiot 33:24–28

    CAS  PubMed  Google Scholar 

  • Ort DR, Baker NR (2002) A photoprotective role for O2 as an alternative electron sink in photosynthesis? Curr Opin Plant Biol 5:193–198

    Article  CAS  PubMed  Google Scholar 

  • Patterson DR (1987) Rohm and Haas Co. US Patent 4693742

  • Penuelas J, Llusia J, Asensio D et al (2005) Linking isoprene with plant thermotolerance, antioxidants and monoterpene emissions. Plant Cell Environ 28:278–286

    Article  CAS  Google Scholar 

  • Rodeghiero M, Niinemets U, Cescatti A (2007) Major diffusion leaks of clamp on leaf cuvettes still unaccounted: how erroneous are the estimates of the Farquhar et al. model parameters? Plant Cell Environ 30:1006–1022

    Article  CAS  PubMed  Google Scholar 

  • Rohmer M, Knani M, Simonin P et al (1993) Isoprenoid biosynthesis in bacteria—a novel pathway for the early steps leading to isopentenyl diphosphate. Biochem J 295:517–524

    CAS  PubMed  Google Scholar 

  • Ryan A, Cojocariu C, Possell M et al (2009) Defining hybrid poplar (Populus deltoides x Populus trichocarpa) tolerance to ozone: identifying key parameters. Plant Cell Environ 32:31–45

    Article  CAS  PubMed  Google Scholar 

  • Sanadze GA (2004) Biogenic isoprene (a review). Russ J Plant Physiol 51:729–741

    Article  CAS  Google Scholar 

  • Schreiber U, Klughammer C, Neubauer C (1988) Measuring P700 absorbance changes around 830 nm with a new type of pulse-modulation system. Z Naturforsch C 43:686–698

    CAS  Google Scholar 

  • Schwender J, Lichtenthaler HK, Seemann M, Rohmer M (1995) Biosynthesis of isoprenoid chains of chlorophylls and plastoquinone in Scenedesmus by a novel pathway. In: Mathis P (ed) Photosynthesis: from light to biosphere. Kluwer, Amsterdam, pp 1001–1004

    Google Scholar 

  • Schwender J, Seemann M, Lichtenthaler HK et al (1996) Biosynthesis of isoprenoids (carotenoids, sterols, prenyl side-chains of chlorophylls and plastoquinone) via a novel pyruvate/glyceraldehyde 3-phosphate non-mevalonate pathway in the green alga Scenedesmus obliquus. Biochem J 316:73–80

    CAS  PubMed  Google Scholar 

  • Schwender J, Zeidler J, Groner R et al (1997) Incorporation of 1-deoxy-d-xylulose into isoprene and phytol by higher plants and algae. FEBS Lett 414:129–134

    Article  CAS  PubMed  Google Scholar 

  • Shallcross DE, Monks PS (2000) New Directions: a role for isoprene in biosphere-climate-chemistry feedbacks. Atmos Environ 34:1659–1660

    Article  CAS  Google Scholar 

  • Shaner D, Stidham M, Muhitch M et al (1985) Mode of action of the imidazolinones. Proc Br Crop Prot Counc Conf Weeds 1:147–154

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Singh BK, Newhouse KE, Stidham MA (1989) Acetohydroxyacid synthase-imidazolinone interaction. In: Copping LC, Dalziel J, Dodge AD et al (eds) Prospects for amino acid biosynthesis inhibitors in crop protection and pharmaceutical chemistry. British Crop Protection Council monograph no. 42. British Crop Protection Council, Farnham, pp 87–95

  • Taipale R, Ruuskanen TM, Rinne J et al (2008) Technical note: quantitative long-term measurements of VOC concentrations by PTR-MS—measurement, calibration, and volume mixing ratio calculation methods. Atmos Chem Phys 8:6681–6698

    Article  CAS  Google Scholar 

  • Takahashi S, Kuzuyama T, Watanabe H et al (1998) A 1-deoxy-d-xylulose 5-phosphate reductoisomerase catalyzing the formation of 2-C-methyl-d-erythritol 4-phosphate in an alternative nonmevalonate pathway for terpenoid biosynthesis. Proc Natl Acad Sci USA 95:9879–9884

    Article  CAS  PubMed  Google Scholar 

  • Terashima I (1992) Anatomy of non uniform leaf photosynthesis. Photosynth Res 31:195–212

    Article  CAS  Google Scholar 

  • Terashima I, Wong SC, Osmond CB et al (1988) Characterization of non-uniform photosynthesis induced by abscisic-acid in leaves having different mesophyll anatomies. Plant Cell Physiol 29:385–394

    CAS  Google Scholar 

  • van Kraalingen DWG (1990) Implications of non-uniform stomatal closure on gas-exchange calculations. Plant Cell Environ 13:1001–1004

    Article  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 a heat stress. Plant Cell Environ 28:318–327

    Article  CAS  Google Scholar 

  • Velikova V, Edreva A, Loreto F (2004) Endogenous isoprene protects Phragmites australis leaves against singlet oxygen. Physiol Plant 122:219–225

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Velikova V, Pinelli P, Loreto F (2005b) Consequences of inhibition of isoprene synthesis in Phragmites australis leaves exposed to elevated temperatures. Agric Ecosyst Environ 106:209–217

    Article  CAS  Google Scholar 

  • Velikova V, Loreto F, Tsonev T et al (2006) Isoprene prevents the negative consequences of high temperature stress in Platanus orientalis leaves. Funct Plant Biol 33:931–940

    Article  CAS  Google Scholar 

  • Vickers CE, Possell M, Cojocariu CI et al (2009a) Isoprene synthesis protects transgenic tobacco plants from oxidative stress. Plant Cell Environ 32:520–531

    Article  CAS  PubMed  Google Scholar 

  • Vickers CE, Gershenzon J, Lerdau MT et al (2009b) A unified mechanism of action from volatile isoprenoids in plant abiotic stress. Nature Chem Biol 5:283–291

    Article  CAS  Google Scholar 

  • Wullschleger SD (1993) Biochemical limitations to carbon assimilation in C3 Plants—a retrospective analysis of the A/Ci curves from 109 species. J Exp Bot 44:907–920

    Article  CAS  Google Scholar 

  • Zeidler J, Lichtenthaler HK, May HU, Lichtenthaler FW (1997) Is isoprene emitted by plants synthesized via the novel isopentenyl pyrophosphate pathway? Z Naturforsch C 52:15–23

    CAS  Google Scholar 

  • Zeidler J, Schwender J, Müller C et al (1998) Inhibition of the non-mevalonate 1-deoxy-d-xylulose-5-phosphate pathway of plant isoprenoid biosynthesis by fosmidomycin. Z Naturforsch C 53:980–986

    CAS  Google Scholar 

Download references

Acknowledgements

This study was funded by the Biotechnology and Biological Sciences Research Council (award BBS/B/12172), and the NERC (studentship award NER/S/A/2005/13680 to AR). Additional support was provided by the European Science Foundation ‘VOCBAS’ programme, and the EC Marie Curie RTN ‘ISONET’.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Malcolm Possell.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Possell, M., Ryan, A., Vickers, C.E. et al. Effects of fosmidomycin on plant photosynthesis as measured by gas exchange and chlorophyll fluorescence. Photosynth Res 104, 49–59 (2010). https://doi.org/10.1007/s11120-009-9504-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-009-9504-5

Keywords

Navigation