Leaf stripe form of esca induces alteration of photosynthesis and defence reactions in presymptomatic leaves
Maryline Magnin-Robert A C , Patricia Letousey A C , Alessandro Spagnolo A , Fanja Rabenoelina A , Lucile Jacquens A , Laurence Mercier B , Christophe Clément A and Florence Fontaine A D
+ Author Affiliations
- Author Affiliations
A Université de Reims Champagne-Ardenne, URVVC-SE EA 2069, Laboratoire de Stress, Défenses et Reproduction des Plantes, UFR Sciences Exactes et Naturelles, Moulin de la Housse, BP 1039, 51687 Reims Cedex 2, France.
B Moët and Chandon, 20 Avenue de Champagne, 51200 Epernay, France.
C These authors contributed equally to this paper.
D Corresponding author. Email: florence.fontaine@univ-reims.fr
Functional Plant Biology 38(11) 856-866 https://doi.org/10.1071/FP11083
Submitted: 4 April 2011 Accepted: 2 August 2011 Published: 30 September 2011
Abstract
Esca is a destructive disease in grapevines (Vitis vinifera L.) caused by at least three fungi and characterised by two different external symptoms, the apoplectic and leaf stripe form. This latter form can be discerned as soon as symptoms become visible, but the preceding discrete signs during incubation are poorly or not understood. To further understand the development of the leaf stripe form, the period preceding and following the appearance of symptoms was investigated by studying physiological and molecular markers associated with photosynthetic mechanisms and stress response. No perturbation of any targeted metabolism was observed in asymptomatic leaves of asymptomatic canes from vines showing the leaf stripe form of esca. Conversely, drastic alterations of photosynthesis functions were registered in presymptomatic leaves, as revealed by the decrease of gas exchange and chlorophyll fluorescence, and the repression of photosynthesis-related genes. These alterations were amplified during symptom development. Expression of defence-related genes was affected and detected early in presymptomatic leaves and amplified during symptom expression. Our results suggest that grapevines may react precociously by reducing photosynthesis and triggering defence mechanisms in response to the leaf stripe form of esca.
Additional keywords: grapevine, pathogen, pathogenesis-related proteins, Vitis vinifera.
References
Abou-Mansour E, Couché E, Tabacchi R (2004) Do fungal naphthalenones have a role in the development of esca symptoms? Phytopathologia Mediterranea 43, 75–82.Alvarez ME, Pennell RI, Meijer P, Ishikawa A, Dixon RA, Lamb C (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92, 773–784.
| Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXit1KlsLg%3D&md5=c612b583659d8c02aefd61e16c521293CAS |
Amalfitano C, Evidente A, Surico G, Tegli S, Bertelli E, Mugnai L (2000) Phenols and stilbene polyphenols in the wood of esca-diseased grapevines. Phytopathologia Mediterranea 39, 178–183.
Berger S, Sinha AK, Roitsch T (2007) Plant physiology meets phytopathology: plant primary metabolism and plant–pathogen interactions. Journal of Experimental Botany 58, 4019–4026.
| Plant physiology meets phytopathology: plant primary metabolism and plant–pathogen interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXitlymtLg%3D&md5=0e8bb73b4f8206a3922dcdeda811a69aCAS |
Bertamini M, Nedunchezhian N, Tomasi F, Grando MS (2002) Phytoplasma [Stolbur-subgroup (Bois Noir-BN)] infection inhibits photosynthetic pigments, ribulose-1,5-bisphosphate carboxylase and photosynthetic activities in field grown grapevine (Vitis vinifera L. cv. Chardonnay) leaves. Physiological and Molecular Plant Pathology 61, 357–366.
| Phytoplasma [Stolbur-subgroup (Bois Noir-BN)] infection inhibits photosynthetic pigments, ribulose-1,5-bisphosphate carboxylase and photosynthetic activities in field grown grapevine (Vitis vinifera L. cv. Chardonnay) leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXktlKiu7o%3D&md5=69136e312b1c4f3d063a50ef81dcadfaCAS |
Bézier A, Lambert B, Baillieul F (2002) Study of defense-related gene expression in grapevine leaves and berries infected with Botrytis cinerea. European Journal of Plant Pathology 108, 111–120.
| Study of defense-related gene expression in grapevine leaves and berries infected with Botrytis cinerea.Crossref | GoogleScholarGoogle Scholar |
Bortolotti C, Murillo I, Fontanet P, Coca M, San Segundo B (2005) Long-distance transport of the maize pathogenesis-related PRms protein through the phloem in transgenic tobacco plants. Plant Science 168, 813–821.
| Long-distance transport of the maize pathogenesis-related PRms protein through the phloem in transgenic tobacco plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXosVGgsg%3D%3D&md5=deca6718b7c55a80289e5304ae3ad923CAS |
Bowler C, van Montagu M, Inzé D (1992) Superoxide dismutase and stress tolerance. Annual Review of Plant Physiology and Plant Molecular Biology 43, 83–116.
| Superoxide dismutase and stress tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XltVyjsb0%3D&md5=ba594bc1f31789b280dfe06d15dda5f9CAS |
Bruno G, Sparapano L, Graniti A (2007) Effects of three esca-associated fungi on Vitis vinifera L.: IV. Diffusion through the xylem of metabolites produced by tracheophilous fungi in the woody tissue of grapevine leads to esca-like symptoms on leaves and berries. Physiological and Molecular Plant Pathology 71, 106–124.
| Effects of three esca-associated fungi on Vitis vinifera L.: IV. Diffusion through the xylem of metabolites produced by tracheophilous fungi in the woody tissue of grapevine leads to esca-like symptoms on leaves and berries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjtlentLk%3D&md5=f17bf5357fcb442475459e483536dfbaCAS |
Calzarano F, D’Agostino V, Del Carlo M (2008) Trans-resveratrol extraction from grapevine: application to berries and leaves from vines affected by esca proper. Analytical Letters 41, 649–661.
| Trans-resveratrol extraction from grapevine: application to berries and leaves from vines affected by esca proper.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXktVCgs7o%3D&md5=e11b644821276f13a329f9e29e9560ffCAS |
Camps C, Kappel C, Lecomte P, Léon C, Gomès E, Coutos-Thévenot P, Delrot S (2010) A transcriptomic study of grapevine (Vitis vinifera cv. Cabernet-Sauvignon) interaction with the vascular ascomycete fungus Eutypa lata. Journal of Experimental Botany 61, 1719–1737.
| A transcriptomic study of grapevine (Vitis vinifera cv. Cabernet-Sauvignon) interaction with the vascular ascomycete fungus Eutypa lata.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXkvVOgs7k%3D&md5=d0ecf6341bbb8037df70c9520d8d3542CAS |
Chaumont M, Morot-Gaudry JF, Foyer C (1994) Seasonal and diurnal changes in photosynthesis and carbon partitioning in Vitis vinifera leaves in vines with and without fruit. Journal of Experimental Botany 45, 1235–1243.
| Seasonal and diurnal changes in photosynthesis and carbon partitioning in Vitis vinifera leaves in vines with and without fruit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXhtlartLc%3D&md5=b91fbac2a060a010fa570c391b2abc89CAS |
Cortesi P, Fischer M, Milgroom MG (2000) Identification and spread of Fomitiporia punctata associated with wood decay of grapevine showing symptoms of esca disease. Phytopathology 90, 967–972.
| Identification and spread of Fomitiporia punctata associated with wood decay of grapevine showing symptoms of esca disease.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cjjslyitQ%3D%3D&md5=b9099b89337331a9590895c078fd401eCAS |
Crous PW, Gams W (2000) Phaeomoniella chlamydospora gen. et comb. nov., a causal organism of Petri grapevine decline and esca. Phytopathologia Mediterranea 39, 112–118.
Crous PW, Gams W, Wingfield MJ, van Wyk PS (1996) Phaeoacremonium gen. nov. associated with wilt and decline disease of woody hosts and human infections. Mycologia 88, 786–796.
| Phaeoacremonium gen. nov. associated with wilt and decline disease of woody hosts and human infections.Crossref | GoogleScholarGoogle Scholar |
Dubos B (2002) Le syndrome de l’esca. In ‘Maladies cryptogamiques de la vigne’. (Ed. Feret Eds ) pp. 127–136. (Edition Féret: Bordeaux)
Feliciano AJ, Eskalen A, Gubler WD (2004) Differential susceptibility of three grapevine cultivars to Phaeoacremonium aleophilum and Phaeomoniella chlamydospora in California. Phytopathologia Mediterranea 43, 66–69.
Flexas J, Bota J, Escalona JM, Sampol B, Medrano H (2002) Effects of drought on photosynthesis in grapevines under field conditions: an evaluation of stomatal and mesophyll limitations. Functional Plant Biology 29, 461–471.
| Effects of drought on photosynthesis in grapevines under field conditions: an evaluation of stomatal and mesophyll limitations.Crossref | GoogleScholarGoogle Scholar |
Fourie PH, Halleen F (2002) Investigation of the occurrence of Phaeomoniella chlamydospora in canes of rootstock mother vines. Australasian Plant Pathology 31, 425–426.
| Investigation of the occurrence of Phaeomoniella chlamydospora in canes of rootstock mother vines.Crossref | GoogleScholarGoogle Scholar |
Freitas R, Rego C, Oliveira H, Ferreira RB (2009) Interactions among grapevine disease-causing fungi. The role of reactive oxygen species. Phytopathologia Mediterranea 48, 117–127.
Frick UB, Schaller A (2002) cDNA microarray analysis of fusicoccin-induced changes in gene expression in tomato plants. Planta 216, 83–94.
| cDNA microarray analysis of fusicoccin-induced changes in gene expression in tomato plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xps1eht7c%3D&md5=97ccb54eac2752ea8a04c3dbe6ea7182CAS |
Gechev TS, Gadjev IZ, Hille J (2004) An extensive microarray analysis of AAL-toxin-induced cell death in Arabidopsis thaliana brings new insights into the complexity of programmed cell death in plants. Cellular and Molecular Life Sciences 61, 1185–1197.
| An extensive microarray analysis of AAL-toxin-induced cell death in Arabidopsis thaliana brings new insights into the complexity of programmed cell death in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXls1aqsLo%3D&md5=2b036633d26e18a9fb4947568283bc72CAS |
Genty B, Briantais JM, Baker NR (1989) The relationship between quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990, 87–92.
Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual Review of Phytopathology 43, 205–227.
| Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVOksrrN&md5=24b1f4ae6d066cd8397bbb74846acb69CAS |
Hammerschmidt R (1999) Phytoalexins: what have we learned after 60 years? Annual Review of Phytopathology 37, 285–306.
| Phytoalexins: what have we learned after 60 years?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXnt1Wnt7o%3D&md5=ea5632a6a63561cb4b34436ee32ffaa0CAS |
Jeandet P, Douillet-Breuil AC, Bessis R, Debord S, Sbaghi M, Adrian M (2002) Phytoalexins from the Vitaceae: biosynthesis, phytoalexin gene expression in transgenic plants, antifungal activity, and metabolism. Journal of Agricultural and Food Chemistry 50, 2731–2741.
| Phytoalexins from the Vitaceae: biosynthesis, phytoalexin gene expression in transgenic plants, antifungal activity, and metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xis12gtbY%3D&md5=639941ecd6e272f0461be21cac4c1c5cCAS |
Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annual Review of Plant Physiology and Plant Molecular Biology 42, 313–349.
| Chlorophyll fluorescence and photosynthesis: the basics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXltFSmsrc%3D&md5=cdfa35428a0c7fbb342d6a1f597d8a97CAS |
Kuźniak E, Skłodowska M (2001) Ascorbate, glutathione and related enzymes in chloroplasts of tomato leaves infected by Botrytis cinerea. Plant Science 160, 723–731.
| Ascorbate, glutathione and related enzymes in chloroplasts of tomato leaves infected by Botrytis cinerea.Crossref | GoogleScholarGoogle Scholar |
Larignon P, Dubos B (1997) Fungi associated with esca disease in grapevine. European Journal of Plant Pathology 103, 147–157.
| Fungi associated with esca disease in grapevine.Crossref | GoogleScholarGoogle Scholar |
Letousey P, Baillieul F, Perrot G, Rabenoelina F, Boulay M, Vaillant-Gaveau N, Clément C, Fontaine F (2010) Early events prior to visual symptoms in the apoplectic form of grapevine esca disease. Phytopathology 100, 424–431.
| Early events prior to visual symptoms in the apoplectic form of grapevine esca disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmsVKiur8%3D&md5=bc375db6e802647d607f6f535ca8b67dCAS |
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology 148, 350–382.
| Chlorophylls and carotenoids: pigments of photosynthetic biomembranes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXhs1Cgu78%3D&md5=ec6cc395c9197f51bfa31290848109beCAS |
Lorenzini G, Guidi L, Nali C, Ciompi S, Soldatini GF (1997) Photosynthetic response of tomato plants to vascular wilt diseases. Plant Science 124, 143–152.
| Photosynthetic response of tomato plants to vascular wilt diseases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjsF2ru7w%3D&md5=adcf5788e3ce5f12510e4d52d26aee31CAS |
Lu C, Zhang J (2000) Photosynthetic CO2 assimilation, chlorophyll fluorescence and photoinhibition as affected by nitrogen deficiency in maize plants. Plant Science 151, 135–143.
| Photosynthetic CO2 assimilation, chlorophyll fluorescence and photoinhibition as affected by nitrogen deficiency in maize plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhtF2rt78%3D&md5=6d260bd41a0d1a6b508ac44c71970691CAS |
Manning VA, Chu AL, Steeves JE, Wolpert TJ, Ciuffetti LM (2009) A host-selective toxin of Pyrenophora tritici-repentis, Ptr ToxA, induces photosystem changes and reactive oxygen species accumulation in sensitive wheat. Molecular Plant-Microbe Interactions 22, 665–676.
| A host-selective toxin of Pyrenophora tritici-repentis, Ptr ToxA, induces photosystem changes and reactive oxygen species accumulation in sensitive wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtlGkt78%3D&md5=00e425812e78a1680b972929f635a565CAS |
Marrs KA (1996) The functions and regulation of glutathione S-transferases in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47, 127–158.
| The functions and regulation of glutathione S-transferases in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjtlWgsbo%3D&md5=0e7678df0c242d3ca63445410097e9b4CAS |
Martin N, Vesentini D, Rego C, Monteiro S, Oliveira H, Ferreira RB (2009) Phaeomoniella chlamydospora infection induces changes in phenolic compounds content in Vitis vinifera. Phytopathologia Mediterranea 48, 101–116.
Mauch F, Mauch-Mani B, Boller T (1988) Antifungal hydrolases in pea tissue: II. Inhibition of fungal growth by combinations of chitinase and β-1,3-glucanase. Plant Physiology 88, 936–942.
| Antifungal hydrolases in pea tissue: II. Inhibition of fungal growth by combinations of chitinase and β-1,3-glucanase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXkvVCr&md5=8e8b9086951096a1e8a5fd285e470299CAS |
Mazzullo A, Di Marco S, Osti F, Cesari A (2000) Bioassays on the activity of resveratrol, pterostilbene and phosphorous acid towards fungi associated with esca of grapevine. Phytopathologia Mediterranea 39, 357–365.
Moriondo M, Orlandini S, Giuntoli A, Bindi M (2005) The effect of downy and powdery mildew on grapevine (Vitis vinifera L.) leaf gas exchange. Journal of Phytopathology 153, 350–357.
| The effect of downy and powdery mildew on grapevine (Vitis vinifera L.) leaf gas exchange.Crossref | GoogleScholarGoogle Scholar |
Mugnai L, Graniti A, Surico G (1999) Esca (black measles) and brown wood-streaking: two old and elusive diseases of grapevines. Plant Disease 83, 404–418.
| Esca (black measles) and brown wood-streaking: two old and elusive diseases of grapevines.Crossref | GoogleScholarGoogle Scholar |
Nogués S, Cotxarrera L, Alegre L, Trillas MI (2002) Limitations to photosynthesis in tomato leaves induced by Fusarium wilt. New Phytologist 154, 461–470.
| Limitations to photosynthesis in tomato leaves induced by Fusarium wilt.Crossref | GoogleScholarGoogle Scholar |
Oxborough K (2004) Imaging of chlorophyll a fluorescence: theoretical and practical aspects of an emerging technique for the monitoring of photosynthetic performance. Journal of Experimental Botany 55, 1195–1205.
| Imaging of chlorophyll a fluorescence: theoretical and practical aspects of an emerging technique for the monitoring of photosynthetic performance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXksVagsrc%3D&md5=9e001e2459348fa4bfaeb9171ec1b869CAS |
Petit A-N, Vaillant N, Boulay M, Clément C, Fontaine F (2006) Alteration of photosynthesis in grapevines affected by esca. Phytopathology 96, 1060–1066.
| Alteration of photosynthesis in grapevines affected by esca.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFChtLjL&md5=6c0795a04b1b109228c8151fa2be89b5CAS |
Petit A-N, Wojnarowiez G, Panon M-L, Baillieul F, Clément C, Fontaine F, Vaillant-Gaveau N (2009) Botryticides affect grapevine leaf photosynthesis without inducing defense mechanisms. Planta 229, 497–506.
| Botryticides affect grapevine leaf photosynthesis without inducing defense mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFSmsrw%3D&md5=f366e951ee43d1f7e5a2ad73438cabf8CAS |
Raines CA (2003) The Calvin cycle revisited. Photosynthesis Research 75, 1–10.
| The Calvin cycle revisited.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXht1Kru7o%3D&md5=b05abfb0e9088dfc63b0f81faee0d8d1CAS |
Retief E, McLeod A, Fourie PH (2006) Potential inoculum sources of Phaeomoniella chlamydospora in South African grapevine nurseries. European Journal of Plant Pathology 115, 331–339.
| Potential inoculum sources of Phaeomoniella chlamydospora in South African grapevine nurseries.Crossref | GoogleScholarGoogle Scholar |
Sparapano L, Bruno G, Graniti A (2001) Three-year observation of grapevines cross-inoculated with esca-associated fungi. Phytopathologia Mediterranea 40, S376–S386.
Stoev K, Slavtcheva T (1982) La photosynthèse nette chez la vigne (V. vinifera L.) et les facteurs écologiques. Connaissance de la Vigne et du Vin 16, 171–185.
Surico G, Mugnai L, Marchi G (2008) The esca disease complex. In ‘Integrated management of diseases caused by fungi, phytoplasma and bacteria.’ (Eds A Ciancio, KG Mukerji) pp. 119–136. (Springer: Heidelberg)
Terrier N, Glissant D, Grimplet J, Barrieu F, Abbal P, Couture C, Ageorges A, Atanassova R, Léon C, Renaudin JP, Dédaldéchamp F, Romieu C, Delrot S, Hamdi S (2005) Isogene specific oligo arrays reveal multifaceted changes in gene expression during grape berry (Vitis vinifera L.) development. Planta 222, 832–847.
| Isogene specific oligo arrays reveal multifaceted changes in gene expression during grape berry (Vitis vinifera L.) development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1emsrzL&md5=8423f8dbdd1139901ba63dad8e44ee22CAS |
Valtaud C, Foyer CH, Fleurat-Lessard P, Bourbouloux A (2009) Systemic effects on leaf glutathione metabolism and defence protein expression caused by esca infection in grapevines. Functional Plant Biology 36, 260–279.
| Systemic effects on leaf glutathione metabolism and defence protein expression caused by esca infection in grapevines.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXisFSqur4%3D&md5=e12c321c4aa895c98bd0e4d95a1e8b5cCAS |
van Kooten O, Snel JFH (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynthesis Research 25, 147–150.
| The use of chlorophyll fluorescence nomenclature in plant stress physiology.Crossref | GoogleScholarGoogle Scholar |
van Loon LC, van Strien EA (1999) The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiological and Molecular Plant Pathology 55, 85–97.
| The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXltVahurk%3D&md5=78acbbfeed1a49c6c4fca310be14a801CAS |
