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Mechanism of Powdery Mildew Infection in Grapevines

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Mechanism of Powdery Mildew Infection in Grapevines Mechanism of powdery mildew infection in grapevines FINAL REPORT to GRAPE AND WINE RESEARCH & DEVELOPMENT CORPORATION Project Number: CRV 02/07N Principal Investigator: Dr Ian B. Dry Research Organisation: Cooperative Research Centre for Viticulture Date: 29th June 2006 Project Title: Mechanism of powdery mildew infection in grapevines CRCV Project Number: 3.1.5 Period Report Covers: July 2002 – June 2006 Author Details: Dr Ian Dry CSIRO Plant Industry Postal address: PO Box 350, Glen Osmond, SA 5064, Australia Phone: 08 83038632 Fax: 08 83038601 Mobile: Email: [email protected] Date report completed: June 2006 Publisher: Cooperative Research Centre for Viticulture ISBN OR ISSN: Copyright: © Copyright in the content of this guide is owned by the Cooperative Research Centre for Viticulture. Disclaimer: The information contained in this report is a guide only. It is not intended to be comprehensive, nor does it constitute advice. The Cooperative Research Centre for Viticulture accepts no responsibility for the consequences of the use of this information. You should seek expert advice in order to determine whether application of any of the information provided in this guide would be useful in your circumstances. The Cooperative Research Centre for Viticulture is a joint venture between the following core participants, working with a wide range of supporting participants. Table of Contents Abstract ……………………………………….… 2 Executive summary ……………………………………....…. 3 Copy of Matt Hayes PhD thesis Appendix 1: Communication Appendix 2: Intellectual Property Appendix 3: References Appendix 4: Staff Appendix 5: Publications Appendix 6: Budget reconciliation Abstract This study has provided new insights into the molecular and biochemical processes associated with the powdery mildew:grapevine interaction. Our results indicate that powdery mildew infection of grapevine epidermal cells leads to the modification of specific host genes involved in carbohydrate metabolism and transport which results in increased supply of hexoses to the pathogen to support growth and development. It is not known if these changes in host gene expression are manipulated directly by the invading pathogen or are a consequence of fungal colonisation. However, there is good evidence to indicate that the plant hormone ABA has an important role in regulating these changes in host gene expression. Potentially, modification of the expression of host genes associated with carbohydrate metabolism could provide an alternative way to engineer resistance to this pathogen in grapevine. 2 Executive summary Powdery mildew is the most economically important grapevine disease worldwide. Complete crop loss occurs in vineyards of unsprayed highly susceptible cultivars and frequent yield losses of 20% or more occur where fungicides are applied after the disease is well established. The effect of fungal infection of the fruit causes significant losses to both the wine and table grapes industries. Costs of disease management and yield losses in Australia are estimated at 5% the value of total grape production. Current control of the disease can only be achieved by the use of fungicides. However, powdery mildew strains resistant to DMI fungicides have recently been reported and there is world-wide pressure to reduce the use of "hard" chemicals to control plant pathogens on crops grown for human consumption. These problems could be overcome by the development of grapevine cultivars with enhanced resistance to powdery mildew. The major focus of our CRCV research on powdery mildew resistance genes is targeted towards the isolation of resistance genes from the American grape Muscadinia rotundifolia (CRCV Project 3.1.1). While our research indicates that the Run1 gene confers complete resistance to powdery mildew isolates present in France and Australia, there can be no guarantee that new powdery mildew isolates, which are able to overcome the Run1 resistance, may not arise by natural mutation in the field or through accidental importation into this country. This is especially pertinent when one considers the length of time that individual vines are expected to remain in the field. Thus, the current approach of most research programs involved in developing disease resistant crops is to “pyramid” multiple resistance genes or strategies within the one plant as it is extremely unlikely that a single mutation in the pathogen would be able to overcome two different resistance mechanisms simultaneously. The aim of this project, therefore, was to provide us with a better understanding of the biochemical and genetic basis of the powdery mildew: grapevine interaction with the aim of devising alternative resistance strategies which will act in combination with the Run1 gene to provide long term resistance in the field. Grapevine powdery mildew, caused by Erysiphe necator, is a biotrophic pathogen that forms a stable association with host cells without directly causing cell death, and take up nutrients such as sugars, amino acids etc from host epidermal cells via a feeding structure called a haustorium. There is evidence from research on other biotrophic fungal pathogens, such as rust, to suggest that pathogen infection results in changes in the expression of host genes involved in nutrient supply and transport which increases the availability of nutrients to, and hence, growth of the pathogen. It is not known if these changes in host gene expression are manipulated directly by the invading pathogen or are a consequence of fungal colonisation. This project set out to investigate whether similar processes are operating in the powdery mildew: grapevine interaction. To identify host genes that may mediate nutrient delivery to powdery mildew infected tissues and therefore may contribute to disease susceptibility, a candidate gene approach using degenerate and RT-PCR, and a non-targeted approach using microarray analysis was instigated. In addition to genes encoding pathogenesis and stress-related proteins, microarray analysis revealed that transcript levels of a putative metal transporter and a cell wall structural protein were elevated in infected berry skin, while aquaporin water channels and genes associated with photosynthesis were generally repressed. Degenerate PCR was used to isolated new cell wall invertase, monosaccharide and amino acid transporter genes and initial RT-PCR revealed that expression of genes involved in sugar mobilisation were the most significantly modulated by powdery mildew infection. Previously unreported hexose transporters (HTs), (VvHT3, VvHT4 and VvHT5) and a cwINV (VvcwINV) were isolated from cDNA prepared from powdery mildew infected grapevine leaves. Full length clones of grapevine HTs and cwINV were obtained by RACE PCR. Heterologous expression of the three new HTs in yeast confirmed that VvHT4 and VvHT5 mediated glucose uptake, while VvHT3 did not function in the yeast system. However, transient expression of a 3 translational fusion of the VvHT3 protein with green florescence protein in onion epidermal cells indicated that it is targeted to the plasma membrane of plant cells. Quantitative RT- PCR analysis of these new genes, together with previously reported grapevine HTs and cytoplasmic and vacuolar invertases, indicated that expression of VvcwINV and VvHT5, were significantly up-regulated by PM infection, while a vacuolar invertase was strongly down-regulated by PM infection. Invertase activity assays were in agreement with these findings, showing elevated sucrolytic activity in insoluble fractions and reduced sucrolytic activity in soluble fractions. These results suggest that apoplasmic phloem unloading of sucrose in the infected leaf is elevated and that VvHT5 is induced to recover the additional hexoses from the apoplasm. Basic localisation studies indicated that VvHT5 and VvcwINV are not induced specifically in powdery mildew infected leaf regions, but are induced in a more diffuse distribution within infected leaves. To determine if induction of VvHT5 and VvcwINV is specific to PM infection or if other stimuli may also mediate these responses, leaves were inoculated with downy mildew or stressed by wounding. Transcript levels of VvHT5 and VvcwINV were elevated by wounding and downy mildew infection, suggesting that the induction of these genes may be part of a general stress response. To explore the signalling pathways that may underlie these responses, leaves were treated with the plant growth regulators ethylene, jasmonate and abscisic acid. Exogenous application of ethylene and methyl jasmonate only marginally affected the expression of the genes studied, however foliar application of abscisic acid (ABA) induced gene expression changes similar to those observed in response to powdery mildew infection and wounding. Promoter sequences of VvHT3, VvHT4, VvHT5 and VvcwINV were isolated and analysed for the presence of regulatory elements. Compared with the promoters of VvHTs that were not induced by pathogen infection or wounding, the VvHT5 and VvcwINV promoters contained numerous motifs associated with induction by ABA including ABRE, Myc and Myb binding elements. The path of sugar loading into the mesocarp of grape berries during ripening is still poorly understood and few molecular components associated with this process have been described. Quantitative RT-PCR was used to monitor the expression of five HTs and VvcwINV during Cabernet sauvignon and Shiraz berry development and ripening. Of the three new HTs reported here, the expression of VvHT3 is most consistent
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