Abstract
Infection of plants with pathogens leads not only to the induction of defence reactions but also to changes in carbohydrate metabolism. In this study, the effects of infection by a virulent and an avirulent strain of P. syringae on spatio-temporal changes in photosynthesis were compared using chlorophyll fluorescence imaging. The maximum PSII quantum yield, effective PSII quantum yield and nonphotochemical quenching were decreased in Arabidopsis leaves infected with either strain. At the same time, the quantum yield of nonregulated energy dissipation was increased. These changes could be detected by chlorophyll fluorescence imaging before symptoms were visible by eye. The effects were restricted to the vicinity of the infection site and did not spread to uninfected areas of the leaf. Qualitatively similar changes in photosynthetic parameters were observed in both interactions. Major differences between the responses to both strains were evident in the onset and time course of changes. A decrease in photosynthesis was detectable already at 3 h only after challenge with the avirulent strain while after 48 h the rate of photosynthesis was lower with the virulent strain. In contrast to photosynthesis, the regulation of marker genes for source/sink relations and the activities of invertase isoenzymes showed qualitative differences between both interactions. Inoculation of the virulent but not the avirulent strain resulted in downregulation of photosynthetic genes and upregulation of vacuolar invertases. The activity of vacuolar invertases transiently increased upon infection with the virulent strain but decreased with the avirulent strain while extracellular invertase activity was downregulated in both interactions.
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Abbreviations
- AOI:
-
Area of interest
- ETR:
-
Relative electron transport rate
- F v/F m :
-
Maximum photosystem II quantum yield
- HR:
-
Hypersensitive response
- PAR:
-
Photosynthetically active radiation
- PSII:
-
Photosystem II
- qN :
-
Nonphotochemical quenching
- Y(II):
-
Effective photosystem II quantum yield
References
Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639
Baker B, Zambryski P, Staskawicz B, Dinesh-Kumar SP (1997) Signaling in plant-microbe interactions. Science 276:726–733
Balachandran S, Osmond CB (1994a) Susceptibility of tobacco leaves to photoinhibition following infection with two strains of tobacco mosaic virus under different light and nitrogen nutrition regimes. Plant Physiol 104:1051–1057
Balachandran S, Osmond CB, Daley PF (1994b) Diagnosis of the earliest strain-specific interactions between tobacco mosaic virus and chloroplasts of tobacco leaves in vivo by means of chlorophyll fluorescence imaging. Plant Physiol 104:1059–1065
Berger S, Papadopoulos M, Schreiber U, Kaiser W, Roitsch T (2004) Complex regulation of gene expression, photosynthesis and sugar levels by pathogen infection in tomato. Physiol Plant 122:419–428
Buell CR, Joardar V, Lindeberg M, Selengut J, Paulsen IT, Gwinn ML, Dodson RJ, Deboy RT, Durkin A, Kolonay JF, Madupu R, Daugherty S, Brinkac L, Beanan MJ, Haft DH, Nelson WC, Davidsen T, Zafar N, Zhou L, Liu J, Yuan Q, Khouri H, Fedorova N, Tran B, Russel D, Berry K, Utterback T, van Aken SE, Feldblyum TV, D’Ascenzo M, Deng W, Ramos AR, Alfano JR, Cartinhour S, Chatterjee AK, Delaney TP, Lazarowitz SG, Martin GB, Schneider DJ, Tang X, Bender CL, White O, Fraser CM, Collmer A (2003) The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC 3000. Proc Natl Acad Sci USA 100:10181–10186
Cao H, Bowling SA, Gordon AS, Dong X (1994) Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6:1583–1592
Chou H, Bundock N, Rolfe SA, Scholes JD (2000) Infection of Arabidopsis thaliana leaves with Albugo candida (white blister rust) causes a reprogramming of host metabolism. Mol Plant Pathol 1:99–113
Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833
Dong X, Mindrinos M, Davis KR, Ausubel FM (1991) Induction of Arabidopsis defense genes by virulent Pseudomonas syringae strains and by a cloned avirulence gene. Plant Cell 3:61–72
Ehness R, Ecker M, Godt DE, Roitsch T (1997) Glucose and stress independently regulate source and sink metabolism and defense mechanisms via signal transduction pathways involving protein phosphorylation. Plant Cell 9:1825–1841
Fotopoulos V, Gilbert MJ, Pittman JK, Marvier AC, Buchanan AJ, Sauer N, Hall JL, Williams LE (2003) The monosaccharide transporter gene, AtSTP4, and the cell-wall invertase, Atßfruct1, are induced in Arabidopsis during infection with the fungal biotroph Erysiphe cichoracearum. Plant Physiol 132:821–829
Hammond-Kosack KE, Jones JDG (1996) Resistance gene-dependent plant defense responses. Plant Cell 8:1773–1791
Heath MC (2000) Hypersensitive response-related death. Plant Mol Biol 44:321–334
Herbers K, Meuwly P, Frommer WB, Metraux JP, Sonnewald U (1996) Systemic acquired resistance mediated by the ectopic expression of invertase: possible hexose sensing in the secretory pathway. Plant Cell 8:793–803
Jang JC, Sheen J (1994) Sugar sensing in higher plants. Plant Cell 6:1665–1679
Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. Photosynth Res 79:209–218
Lohaus G, Heldt HW, Osmond CB (2000) Infection with phloem limited Abutilon mosaic virus causes localized carbohydrate accumulation in leaves of Abutilon striatum: relationships to symptom development and effects on chlorophyll fluorescence quenching during photosynthetic induction. Plant Biol 2:161–167
Mouly A, Roby D (1988) Decrease in messenger RNA coding for the small subunit of ribulose-1,5-bisphosphate carboxylase in sunflower plants infected with Sclerotinia sclerotiorum. Plant Physiol Biochem 26:165–172
Nedbal L, Soukupova J, Whitmarsh J, Trtilek M (2000) Postharvest imaging of chlorophyll fluorescence from lemons can be used to predict fruit quality. Photosynthetica 38:571–579
Nedbal L, Whitmarsh J (2004) Chlorophyll fluorescence imaging of leaves and fruits. In: Papageorgiou G, Govindjee (eds) Chlorophyll a fluorescence. A signature of photosynthesis. Springer, Dordrecht, pp 389–407
Oxborough K (2004) Imaging of chlorophyll fluorescence: theoretical and practical aspects of an emerging technique for the monitoring of photosynthetic performance. J Exp Bot 55:1195–1205
Oxborough K, Baker N (1997) An instrument capable of imaging chlorophyll-a fluorescence from intact leaves at very low irradiance and at cellular and subcellular levels of organization. Plant Cell Environ 20:1473–1483
Penninckx IA, Thomma BP, Buchala A, Metraux JP, Broekaert WF (1998) Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell 10:2103–2113
Preston GM (2000) Pseudomonas syringae pv. tomato: the right pathogen, of the right plant, at the right time. Mol Plant Pathol 1:263–275
Roitsch T (1999) Source-sink regulation by sugar and stress. Curr Opin Plant Biol 2:198–206
Roitsch T, Balibrea ME, Hofmann M, Proels R, Sinha AK (2003) Extracellular invertase: key metabolic enzyme and PR protein. J Exp Bot 54:513–524
Roitsch T (2004) Plant response to stress: source-sink regulation by stress. In: Goodman RM (ed) Encyclopedia of plant and crop science. Marcel Dekker, New York, pp 1010–1013
Roitsch T, Gonzalez MC (2004) Function and regulation of plant invertases: sweet sensations. Trends Plant Sci 9:606–613
Scharte J, Schön H, Weis E (2005) Photosynthesis and carbohydrate metabolism in tobacco leaves during an incompatible interaction with Phytophthora nicotianae. Plant Cell Environ 28:1421–1435
Scholes JD, Rolfe SA (1996) Photosynthesis in localised regions of oat leaves infected with crown rust (Puccinia coronata): quantitative imaging of chlorophyll fluorescence. Planta 199:573–582
Schreiber U (2004) Pulse-amplitude-modulation (PAM) fluorometry and saturation pulse method: an overview. In: Papageorgiou G, Govindjee (eds) Chlorophyll a fluorescence. A signature of photosynthesis. Springer, Dordrecht, pp 279–319
Schreiber U, Bilger W, Neubauer C (1994) Chlorophyll fluorescence as a non-intrusive indicator for rapid assessment of in vivo photosynthesis. In: Schulze E-D, Caldwell MM (eds) Ecophysiology of photosynthesis. Series ecological studies, vol 100. Springer, Berlin Heidelberg New York, pp 49–70
Schreiber U, Neubauer C (1990) O2-dependent electron flow, membrane energization and the mechanism of non-photochemical quenching of chlorophyll fluorescence. Photosynth Res 25:279–293
Sinha AK, Hofmann MG, Romer U, Kockenberger W, Elling L, Roitsch T (2002) Metabolizable and non-metabolizable sugars activate different signal transduction pathways in tomato. Plant Physiol 128:1480–1489
Staskawicz BJ, Ausubel FM, Baker BJ, Ellis JG, Jones JDG (1995) Molecular genetics of plant disease resistance. Science 268:661–667
Sung S-JS, Xu D-P, Black CC (1989) Identification of actively filling sucrose sinks. Plant Physiol 89:1117–1121
Tao Y, Xie Z, Chen W, Glazebrook J, Chang HS, Han B, Zhu T, Zou G, Katagiri F (2003) Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15:317–330
The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815
Thomma BPHJ, Eggermont K, Penninckx IAMA, Mauch-Mani B, Vogelsang R, Cammue BPA, Broekaert WF (1998) Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Natl Acad Sci USA 95:15107–15111
Thomma BPHJ, Penninckx IA, Broekaert WF, Cammue BP (2001) The complexity of disease signaling in Arabidopsis. Curr Opin Immunol 13:63–68
Warabieda W, Borkowska B (2004) Chlorophyll a fluorescence as a diagnostic tool for assessment of apple resistance against two-spotted spider mite (Tetranychus urticae Koch.). EJPAU 7: Horticulture
Whalen MC, Innes RW, Bent AF, Staskawicz BJ (1991) Identification of Pseudomonas syringae pathogens of Arabidopsis and a bacterial locus determining avirulence on both Arabidopsis and soybean. Plant Cell 3:49–59
Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136:2621–2632
Acknowledgments
We are grateful to M. Rostas for statistical analyses and to W. Kaiser for sugar determinations. This work was supported by Bayerisches Staatsministerium für Umwelt, Gesundheit und Verbraucherschutz and the SFB 567.
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Bonfig, K.B., Schreiber, U., Gabler, A. et al. Infection with virulent and avirulent P. syringae strains differentially affects photosynthesis and sink metabolism in Arabidopsis leaves. Planta 225, 1–12 (2006). https://doi.org/10.1007/s00425-006-0303-3
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DOI: https://doi.org/10.1007/s00425-006-0303-3