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First published online November 9, 2007; 10.1104/pp.107.108712 Plant Physiology 146:236-249 (2008) © 2008 American Society of Plant Biologists OPEN ACCESS ARTICLE
Powdery Mildew Induces Defense-Oriented Reprogramming of the Transcriptome in a Susceptible But Not in a Resistant Grapevine1,[W],[OA]Department of Agriculture, Missouri State University, Mountain Grove, Missouri 65711 (R.W.M.F., C.F., L.G.K., Y.H., W.Q.); Departamento de Investigación Trigo, Nidera S.A., (7607) Miramar, Provincia de Buenos Aires, Argentina (M.G.); Donald Danforth Plant Science Center, St. Louis, Missouri 63132 (E.M., D.P.S.); and Department of Molecular Genetics and Microbiology and Department of Statistics, University of Florida, Gainesville, Florida 32611 (L.M.M.)
Grapevines exhibit a wide spectrum of resistance to the powdery mildew fungus (PM), Erysiphe necator (Schw.) Burr., but little is known about the transcriptional basis of the defense to PM. Our microscopic observations showed that PM produced less hyphal growth and induced more brown-colored epidermal cells on leaves of PM-resistant Vitis aestivalis ‘Norton’ than on leaves of PM-susceptible Vitis vinifera ‘Cabernet sauvignon’. We found that endogenous salicylic acid levels were higher in V. aestivalis than in V. vinifera in the absence of the fungus and that salicylic acid levels increased in V. vinifera at 120 h postinoculation with PM. To test the hypothesis that gene expression differences would be apparent when V. aestivalis and V. vinifera were mounting a response to PM, we conducted a comprehensive Vitis GeneChip analysis. We examined the transcriptome at 0, 4, 8, 12, 24, and 48 h postinoculation with PM. We found only three PM-responsive transcripts in V. aestivalis and 625 in V. vinifera. There was a significant increase in the abundance of transcripts encoding ENHANCED DISEASE SUSCEPTIBILITY1, mitogen-activated protein kinase kinase, WRKY, PATHOGENESIS-RELATED1, PATHOGENESIS-RELATED10, and stilbene synthase in PM-infected V. vinifera, suggesting an induction of the basal defense response. The overall changes in the PM-responsive V. vinifera transcriptome also indicated a possible reprogramming of metabolism toward the increased synthesis of the secondary metabolites. These results suggested that resistance to PM in V. aestivalis was not associated with overall reprogramming of the transcriptome. However, PM induced defense-oriented transcriptional changes in V. vinifera.
Powdery mildew caused by an obligate biotrophic fungus, Erysiphe necator (synonym Uncinula necator [Schw.] Burr.), is an economically important disease of grapevines. The powdery mildew fungus (PM) infects green tissues of vines and causes significant losses in yield and reduction in berry quality. Most widely grown grape cultivars are highly susceptible to E. necator, because they are derived from Vitis vinifera, a species that was not exposed to this pathogen during its evolution (Mullins et al., 1992  ). In contrast, other grapevine species such as Vitis labrasca, Vitis rupestris (Doster and Schnathorst, 1985a), Vitis aestivalis (Giannakis et al., 1998), and Muscadinia rotundifolia (Olmo, 1971) co-evolved with E. necator on the North American continent and possess various levels of resistance to the pathogen (Mullins et al., 1992). Resistance to PM in grapevines is determined by either a single locus or quantitative trait loci (QTL). For example, resistance to PM in M. rotundifolia was traced back to Resistance against U. necator1 (Run1), a single dominant locus that contains two families of resistance gene analogs (Pauquet et al., 2001; Donald et al., 2002; Barker et al., 2005). The Run1-mediated resistance is believed to be mediated through a hypersensitive response (Donald et al., 2002). Resistance to PM in grapevines can also be linked with QTLs (Dalbo et al., 2000; Regner et al., 2003; Fischer et al., 2004). The constitutive expression of pathogenesis-related (PR) genes, such as genes encoding β-1,3-glucanases (PR-2) and chitinases (PR-3) in disease-resistant North American grapevine species (Robinson et al., 1997; Tattersall et al., 1997; Giannakis et al., 1998; Fung et al., 2007), may represent one type of QTL-mediated cumulative effects. In addition, physical barriers that block the penetration of the fungus may act as a passive defense mechanism (Doster and Schnathorst, 1985b; Heintz and Blaich, 1989; Ficke et al., 2004). Thus, it is apparent that the genetic basis of resistance to PM is complex in grapevine. While we have gained some understanding of the genetic basis of the grapevine's resistance to PM, little is known about the molecular processes and gene regulation during compatible and incompatible PM-grapevine interactions.
Upon contact with an epidermal cell, an E. necator conidiospore germinates to form a penetration peg that breaches the cuticle and the cell wall. Subsequently, an infection structure, termed a haustorium, is formed within the epidermal cell through which a dynamic exchange of signals and metabolites occurs between the pathogen and the host cell (Heintz and Blaich, 1990
A plant's resistance to a pathogen can be executed at different levels and to differing degrees through reinforcing cell walls and mounting biochemical defenses (Glazebrook, 2005
Large-scale transcriptional profiling in response to pathogens has revealed novel aspects in compatible and incompatible interactions between plants and their pathogens (Mysore et al., 2002
Epidermal Cells of V. aestivalis and V. vinifera Respond Differently to Conidiospores To compare the characteristics of PM-induced symptoms in the two grapevine genotypes, we conducted a microscopy study of conidiospore germination and hyphal development during a 6-d time period. Microscopic images of 24, 48, and 120 hpi are presented in Figure 1 . Conidiospores produced appressoria and secondary hyphae on both V. vinifera and V. aestivalis leaves at 24 hpi. In V. aestivalis leaves, most epidermal cells invaded by the conidiospores exhibited brown coloration, which was visible after tissue was cleared of chlorophyll (Fig. 1). This browning appeared more intense in the region of the cell wall. Brown-colored cells were also observed beneath appressoria that developed from secondary hyphae on V. aestivalis leaves at 120 hpi. The infection led to the formation of colonies with dense secondary hyphae on V. vinifera leaves but only small colonies with sparse hyphae on V. aestivalis leaves by 120 hpi.
SA Is Present at Elevated Levels in PM-Infected V. vinifera and in Mock-Inoculated V. aestivalis
It is known that SA is a signal molecule in the induction of host defense responses, including hypersensitive response and systemic acquired resistance, and that the increase of endogenous SA levels is associated with the activation of PR gene expression (Shah, 2003
Our earlier results from the analysis of genotype-specific transcriptome changes demonstrated that representative PR genes including PR-2 and PR-3 were transcribed constitutively at higher levels in V. aestivalis than in V. vinifera (Fung et al., 2007 ). It is possible that higher expression of PR genes is a result of elevated SA levels in V. aestivalis. To test this possibility, we compared the levels of endogenous SA between the two grapevine genotypes under mock-inoculation conditions. We found that the endogenous SA content in V. aestivalis was significantly higher than in V. vinifera in the absence of the fungus (Fig. 2).
In a previous study, we found that transcriptome changes can be reliably measured in both V. aestivalis and V. vinifera by using the Vitis GeneChip (Fung et al., 2007 For the genes that were significantly different between PM- and mock-inoculated samples for at least one time point, we classified the differences at each time point as up-regulated, down-regulated, or the same based upon the nominal P value for the contrast between PM- and mock-inoculated samples at that time point and the direction of difference (Supplemental Table S1). We observed that the number of PM-responsive transcripts increased as PM developed in V. vinifera (Fig. 3 ). The total number of up- and down-regulated transcripts during the early infection stage (0–8 hpi) was around 100 to 150 and then increased to over 250 at 12 hpi and 350 at 48 hpi (Fig. 3). Further analysis of the 625 PM-responsive transcripts indicated that they represented 598 genes (510 UniGenes and 88 singletons) based on the UniGene assignment in the National Center for Biotechnology Information (NCBI). Twenty of the 510 UniGenes were represented by more than one probe set. In total, 240 genes (175 UniGenes and 65 singletons) were up-regulated and 345 genes (323 UniGenes and 22 singletons) were down-regulated in at least one time point, while four genes (UniGenes) were both up- and down-regulated during some of the time points. Expression of 12 of the genes (11 UniGenes and one singleton) was significant only for the initial test but not in the individual time-point test.
We hypothesized that a possible reason for the low number of PM-responsive transcripts in V. aestivalis was that many of the 625 PM-responsive transcripts were constitutively expressed at a higher or lower level in V. aestivalis than in V. vinifera even prior to PM infection. To test this hypothesis, we compared the transcript levels of the two genotypes for the 625 PM-responsive transcripts of V. vinifera. We first tested whether the two genotypes were different at any time point at an FDR of 0.05. The nominal P value for the contrast at an individual time point, together with the direction of the observed difference, was used to classify the difference between genotypes at that time point as higher, lower, or the same. We found that 508 out of 625 PM-responsive transcripts showed higher or lower expression in V. aestivalis in comparison with V. vinifera for at least one individual time point. Of these 508 transcripts, 83 transcripts were expressed at a higher level and 219 were expressed at a lower level in V. aestivalis in all six time points under the mock-inoculation condition. We also tested whether our findings were consistent with differential treatment response directly by testing the interaction of treatment and variety across all time points. Of the 625 transcripts identified, 533 showed evidence for an interaction between treatment and variety (FDR 0.20).
We performed quantitative real-time PCR (qRT-PCR) assays on a subset of genes to verify differential expression measured in the microarray analysis. Thirteen genes were selected from the 598 PM-responsive genes in V. vinifera (FDR threshold P value < 0.05). Two of the three that were differentially regulated in V. aestivalis in response to PM infection were also analyzed by qRT-PCR. The degree of change in transcript abundance of each gene determined by the microarray and by the qRT-PCR assay was compared by using the difference in natural log values between PM- and mock-inoculated samples for each of the six time points (Supplemental Table S2). For 13 of the 15 genes, the results between the qRT-PCR and microarray were in agreement. The correlation between the microarray and qRT-PCR estimates was positive in all cases and significantly different from zero (Supplemental Table S2; Supplemental Fig. S1). The lowest observed correlation was 0.61 at 0 hpi and the highest was 0.90 at 24 and 48 hpi. For two of the 15 genes (1611550_at and 1611058_at), concordance at the 0 and 12 hpi time points was poor. It appeared that these two genes showed absolute differences in expression levels between the two platforms and, on this basis, were eliminated from comparisons for the remaining time points.
To acquire a global overview of the PM-responsive transcriptome, we performed a nonlinear cluster analysis on the difference between PM- and mock-inoculated samples of the 14,571 informative transcripts in V. vinifera that were detected in at least one sample (Qu and Xu, 2006
Key Defense Genes Change in PM-Inoculated V. vinifera
We found that the expression level of genes encoding PR-2 (β-1,3-glucanases), PR-3 (chitinases), and PR-5 (thaumatin-like protein) increased upon the PM infection across the course of the infection process (Supplemental Table S1), confirming previous reports that these genes are associated with grapevine defense against pathogens (Derckel et al., 1996
Primary Metabolism Is Affected in PM-Inoculated V. vinifera
We analyzed the expression patterns of genes that are involved in primary and secondary metabolism and presented the results in Supplemental Figure S3. Genes in tetrapyrrole synthesis, light harvesting, the Calvin cycle, and photorespiration were mostly down-regulated, suggesting the overall down-regulation of photosynthesis genes (Supplemental Fig. S3A). Genes for pyruvate metabolism involving the conversion of pyruvate to acetyl-CoA were down-regulated together with genes for glycolysis (Supplemental Fig. S3B). The redistribution of carbon reserves was evident based on the up-regulation of genes encoding invertase and
In combating pathogens, a range of secondary metabolites were synthesized, leading to antimicrobial compounds and to lignins, which reinforce cell walls (Nicholson and Hammerschmidt, 1992 Within the isoprenoid biosynthetic pathway, there were two key genes up-regulated, hydroxymethylglutaryl-CoA (HMG CoA) synthase and HMG CoA reductase, that convert acetyl-CoA into HMG CoA and then to mevalonate, the precursor for isopentenyl pyrophosphate and the various terpene, carotenoid, or sterol compounds (Supplemental Fig. S3E). The HMG CoA reductase gene was also one of four genes that was significantly up-regulated in V. aestivalis during PM infection (Fig. 5). The up-regulation of these two genes suggested a tight coordination between the up-regulation of the isoprenoid pathway and the metabolism of acetyl-CoA via β-oxidation of fatty acid (Supplemental Fig. S3C). In particular, the transcript of HMG CoA synthase was expressed at a significantly higher level in V. aestivalis under both mock- and PM-inoculation conditions (Fig. 5; Supplemental Fig. S3E). An overview of the transcriptome changes in metabolic pathways in response to PM infection and possible consequences from mobilization of carbon reserves to secondary metabolites is presented in Figure 6 .
PM-Induced Defense Response in V. aestivalis ‘Norton’
Based on previous findings in other plant-pathogen interactions (Mysore et al., 2002
Among the transcripts present at elevated levels in the mock-inoculated V. aestivalis leaves was EDS1 (Fig. 5), a key regulator of defense that is required for the pathogen-induced accumulation of SA (Parker et al., 1996
In apple (Malus domestica), the association of elevated defense gene expression with resistance to the apple scab fungal pathogen (Venturia ineaqualis) was recently reported (Degenhardt et al., 2005
Accumulating evidence supports the hypothesis that in compatible interactions leading to susceptibility, obligate biotrophic pathogens inactivate host defense responses to sustain their interaction with living host cells (Bushnell and Rowell, 1981
The reprogramming of metabolic pathways is considered to be one of the defense strategies that plants utilize to generate antimicrobial compounds and signal molecules for restraining the growth of pathogens (La Camera et al., 2004
Stilbene synthase, which is a key enzyme in the synthesis of trans-resveratrol and stilbene phytoalexins, is induced in response to fungal elicitors, the oomycete Plasmopara viticola, and the necrotrophic fungal pathogens Botrytis cinerea and Phomopsis viticola in V. vinifera (Melchior and Kindl, 1991
At the transcriptional level, disease-resistant V. aestivalis ‘Norton’ responded weakly to PM. In contrast, in disease-susceptible V. vinifera ‘Cabernet sauvignon’, genes encoding key defense components were significantly up-regulated in response to PM. Endogenous SA content was significantly higher in V. aestivalis ‘Norton’ than in V. vinifera ‘Cabernet sauvignon’. Although it is not clear if these genotype-specific differences in transcript abundance of defense-related genes and higher SA content contribute to PM resistance in V. aestivalis ‘Norton’, these new discoveries point toward future experiments that can uncover the mechanisms responsible for fungal resistance in V. aestivalis ‘Norton’ and for fungal susceptibility in V. vinifera ‘Cabernet sauvignon’.
Full MIAME/Plant compliant descriptions of sources of the PM and grapevines, experiment design, plant samples, RNA extraction, array hybridization, and statistical analysis are included in the Supplemental Data.
Fully expanded leaves at the third or fourth positions from the shoot tip were chosen for inoculation, the inoculated area of each leaf was marked with India ink, and the area was excised at 24-h intervals for light microscopic observation. Removal of chlorophyll and fixation of leaf tissue followed a previous protocol (Vanacker et al., 2000
In the SA assays of Vitis aestivalis and Vitis vinifera with PM or mock inoculation, four leaves were randomly collected from each vine and pooled to form one biological replicate. In the comparative SA analysis of the two genotypes, five leaves were randomly chosen from each vine and pooled to form one biological replicate. Three independent biological replicates were sampled. Leaf samples were immediately frozen and ground in liquid nitrogen. One-half gram of leaf tissues was extracted for measuring acid-hydrolyzed SA by a procedure modified from previous protocols (Gaffney et al., 1993
In each time point, the mean of the normalized expression level for the mock-inoculation treatment was subtracted from the mean of the normalized expression level for PM-inoculation treatment. The differences were analyzed using the method developed by Qu and Xu (2006)
Total RNAs for qRT-PCR were from the same samples as used for GeneChip hybridization. Total RNA were treated with TURBO DNA-free DNase I (Ambion) and purified using RNeasy MinElute Cleanup kit (Qiagen). RNA quantity and quality were assessed by GeneQuant pro spectrophotometer (GE Healthcare) and by Agilent 2100 Bioanalyzer (Agilent). Two micrograms of DNase I-treated RNA from three biological replicate samples at each time point were pooled. Complementary DNA was synthesized from the RNA samples by MultiScribe reverse transcriptase with random hexamer oligonucleotide provided in the Taqman Reverse Transcription Reagent kit (Applied Biosystems). The amounts of transcripts of a selected gene in PM-inoculated versus mock-inoculated grapevine leaf tissues were compared by using actin as control. PCRs were performed in the MX3005P system (Stratagene) using SYBR Green. Reaction was set up following the protocol in the SYBR Green RT-PCR reagent kit (Applied Biosystems). Each reaction was run in triplicates in reaction volume of 20 µL. Cycling parameters were 95°C for 10 min, 50 cycles of 95°C for 15 s, and 60°C for 30 s. Data were analyzed in the MxPro-Mx3005P v3.00 QPCR software (Stratagene) according to the manufacturer's instructions. The differences in CT (threshold cycle) values for actin across all V. vinifera and V. aestivalis cDNA samples series were 1.73 and 1.2, respectively. PCR efficiency (E) was calculated from the exponential phase of each individual amplification plot and the equation (1 + E) = 10slope based on a previous method (Peirson et al., 2003
For each Affymetrix probe set, component sequence with longer coding region and 3' poly(A) tail was identified in the NCBI UniGene database. Then the closest homolog was identified through BLASTX searches (NCBI). The closest Arabidopsis (Arabidopsis thaliana) homolog was also identified by BLAST (NCBI) and cross checked with The Arabidopsis Information Resource. Affymetrix data of this study have been deposited in the Gene Expression Omnibus. The accession number is GSE6404.
The following materials are available in the online version of this article.
We thank Kari Huppert, Karen McPherson, and Nan Li for their outstanding technical support and Susanne Howard, Clayton Dennis, and Lisa Bono for their assistance with data management. We thank James Schoelz for insightful discussion and Walter Gassmann and Shauna Somerville for the critical reviewing of the manuscript. We also thank Don Baldwin of the University of Pennsylvania Microarray Core Facility for the excellent microarray processing services and Sunridge Nurseries for their generous gift of V. vinifera propagation material. Received September 5, 2007; accepted November 1, 2007; published November 9, 2007.
1 This work was supported by the U.S. Department of Agriculture Cooperative State Research, Education, and Extension Service (grant nos. 2004–38901–02138 and 2006–38901–02138). 
2 Present address: Department of General and Environmental Microbiology, Faculty of Science, University of Pecs, 7601 Pecs, Hungary.
3 Present address: Department of Plant Molecular and Cellular Biology, University of Florida, Gainesville, FL 32611. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Wenping Qiu (wenpingqiu{at}missouristate.edu).
[W] The online version of this article contains Web-only data.
[OA] Open Access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.107.108712 * Corresponding author; e-mail wenpingqiu{at}missouristate.edu.
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ABSTRACT
RESULTS
ijkm was assumed normal with error variance 
2N for residuals associated with V. aestivalis observations and 
amylase, which function to convert Suc and starch into Fru and Glc (Supplemental Fig. S3B). In addition, the up-regulation of genes for Glc-6-P dehydrogenase and chorismate mutase suggested the involvement of shikimate pathway in the synthesis of flavonoid secondary metabolites (Supplemental Fig. S3B). Lipid metabolism was also strongly affected with the down-regulation of genes in the fatty acid synthesis pathway as well as the up-regulation of genes in the fatty acid degradation pathway (Supplemental Fig. S3C). These transcriptional changes indicated a possible remobilization of fatty acid carbon reserves back to the key precursor, acetyl-CoA, which was correlated with the up-regulation of isoprenoid biosynthesis during PM infection (Supplemental Fig. S3E). In addition, it was found that many of the PM-responsive genes involved in primary metabolism were expressed at a higher level in V. vinifera than in V. aestivalis under mock-inoculation conditions (Supplemental Fig. S3, A and B). 
