JXB Advance Access originally published online on November 15, 2004
Journal of Experimental Botany 2005 56(412):567-575; doi:10.1093/jxb/eri030
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RESEARCH PAPER |
Induction of a sunflower CC-NBS-LRR resistance gene analogue during incompatible interaction with Plasmopara halstedii
UMR 1095 INRA-UBP ‘Amélioration et Santé des Plantes’, Université Blaise Pascal, 24 avenue des Landais, F-63177 Aubière cedex, France
* To whom correspondence should be addressed. Fax: +33 4 73407914. E-mail: m-fouad.bouzidi{at}univ-bpclermont.fr
Received 2 July 2004; Accepted 15 September 2004
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Abstract |
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Downy mildew caused by Plasmopara halstedii is one of the main diseases causing economic losses in cultivated sunflower. Resistance in this host is conferred by major genes denoted Pl. The inbred sunflower line QIR8, which contains the Pl8 locus and is resistant to all known downy mildew races, was used to isolate a full-length resistance gene analogue (RGA) belonging to the CC-NBC-LRR class of plant resistance genes. The genetically incompatible combination involving downy mildew races 300 and sunflower line QIR8 was characterized by a hypersensitive-like reaction. Semi-quantitative RT-PCR analysis showed that the transcript of Ha-NTIR11g RGA was specifically induced during the incompatible reaction. The transcript was induced
3 d post-infection (dpi), and then decreased by 9 dpi. The high level of transcriptional expression of this RGA coincides with a transcript accumulation of the hsr203J gene which is a marker of the hypersensitive reaction. Treatment with signalling molecules, including salicylic acid and methyl jasmonate, did not activate transcription of the Ha-NTIR11g gene, indicating that Ha-NTIR11g expression is not regulated by defence signalling pathways triggered by these molecules. Ha-NTIR11g was not induced by treatment with hydrogen peroxide or wounding. These results suggest that Ha-NTIR11g RGA may play a critical role in protecting sunflower cells against P. halstedii. The transcript accumulation of R gene-mediated signalling components was also examined. Key words: Helianthus annuus, plant resistance, Plasmopara halstedii, resistance gene analogue
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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The success of a pathogen in infecting a host plant depends on how rapidly the plant recognizes the pathogen and activates appropriate defence reactions. If the pathogen carries an avr (avirulence) gene whose product is specifically recognized by the product of the corresponding R (resistance) gene in the plant, resistance mechanisms are triggered rapidly, resulting in disease resistance. If either the avr or the R gene is absent, the pathogen is not recognized rapidly, the defence responses are activated slowly, and disease ensues (Dangl and Jones, 2001
).
During an incompatible plant–pathogen interaction, recognition of a potential pathogen often results in a hypersensitive reaction (HR) and the activation of programmed cell death of cells at the site of the attack, designed to stop the spread of the pathogen. This HR response is characterized by numerous physiological and molecular changes, i.e. an oxidative burst and nitric oxide production, an oxidative cross-linking of various cell wall compounds, the production of antibiotics (phytoalexins and terpenoids) and ‘pathogenesis-related’ (PR) proteins, and ultimately a reactive oxygen species-dependent collapse and electrolyte leakage leading to HR cell death (Atkinson et al., 1985; Apostol et al., 1989; Lamb et al., 1989; Bowles, 1990; Bradley et al., 1992; Delledonne et al., 1998; Desikan et al., 2001; Concetta de Pinto et al., 2002; Shadle et al., 2003).
Most plant R genes that have been isolated to date encode proteins which share structural similarities in that they have a nucleotide-binding site (NBS) and a leucine-rich repeat (LRR). The NBS region is preceded by either a coiled-coil (CC) domain or a so-called TIR domain that is defined by its homology with the intracellular effector domains of Drosophila Toll and human interleukin-1 receptors. At present, three different R-gene-mediated signalling pathways have been described in Arabidopsis thaliana. The first involves the TIR-NBS-LRR type of R genes (e.g. RPP1 and RPP5) and requires EDS1 (Enhanced Disease Susceptibility) and PAD4 (Phytoalexin Deficient) functions to attain full resistance. The second involves a subgroup of the CC-NBS-LRR type of R genes (e.g. RPM1 and RPS2) and requires functional NDR1 (Non-race-specific Disease Resistance) and PBS2 (avrPphB susceptible 2). The third pathway involves the remaining CC-NBS-LRR type R genes (e.g. RPP7, RPP8, and RPP13) and is independent of the function of EDS1, PAD4, NDR1, and PBS2 (Aarts et al., 1998; Feys and Parker, 2000; McDowell et al., 2000; Bittner-Eddy and Beynon, 2001; Glazebrook, 2001; Dodds and Schwechheimer, 2002; Peart et al., 2002).
Downy mildew caused by the oomycete Plasmopara halstedii (Farl.) Berl. de Toni, is one of the principal diseases causing economic losses in cultivated sunflower (Helianthus annuus L.). The major dominant genes denoted by Pl confer resistance against this disease. In a previous study (Radwan et al., 2004), a complete RGA was isolated from sunflower line QIR8 and named Ha-NTIR11g; it belongs to the CC-NBS-LRR class of plant resistance genes. Genetic studies have shown that this RGA is linked to resistance to Plasmopara halstedii race 300 (Radwan et al., 2003, 2004). Whereas most findings in the literature concerning plant resistance genes emphasize the identification of new R gene sequences and the evolution of this large family, very little is known about regulation of their expression. The aim of the present study was therefore to compare the transcriptional expression of Ha-NTIR11g RGA along with different defence-related genes during compatible and incompatible reactions with sunflower downy mildew race 300, and following treatment with signalling molecules such as salicylic acid (SA), methyl-jasmonic acid (MeJA), and hydrogen peroxide (H2O2), or after wounding.
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Materials and methods |
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Sunflower genotypes and infection procedure
Infections were performed on sunflower lines QIR8 (resistant) and CAY (susceptible). Their genotypes and phenotypic segregation for resistance to downy mildew have been described previously (Radwan et al., 2003
). The procedures for infection with Plasmopara halstedii (race 300) and the conditions for plant growth were as described elsewhere by Mouzeyar et al. (1993).
Treatment with plant hormones, H2O2, and wounding
Treatment with signalling molecules was carried out by spraying 12-d-old sunflower leaves with either SA (2 mM) or MeJA (100 µM) in sterile water. For the H2O2 treatment, 12-d-old sunflower leaves were sprayed with H2O2 (10 µM) in sterile water. Control plants were sprayed with sterile water only. To achieve wounding, the leaves of sunflower plants were scratched with sterile forceps.
Microscopic procedures
To enable microscopic observations, the sunflower seedlings were fixed in FAA (formalin:acetic acid:ethanol; 5:5:90 by vol.). Free-hand sections of infected and non-infected plants were mounted on glass slides and observed without any further treatment. Photographs were taken using an Axio cam HRC, Zeiss digital camera.
DNA and RNA manipulations
DNA was isolated using the CTAB method as described by Saghai Maroof et al. (1984). RNA was extracted using the method described by Bogorad et al. (1983) with slight adjustments for small samples (0.5 g). For northern blot analysis, poly (A)+ mRNA was isolated using the PolyAtract mRNA Isolation system (Promega, France).
Southern and northern blots
DNA digestion and Southern hybridization were performed as described previously (Gentzbittel et al., 1999) on 10 µg of genomic DNA using the BamHI, EcoRI, EcoRV, and HindIII restriction enzymes (100 units of each). Genomic DNA fragments were separated on 0.8% agarose gel and then transferred to a Hybond N+ (Amersham) membrane. For northern blot preparation, 7 µg of poly (A)+ extracted from QIR8 and CAY were separated under denaturing conditions on 1.5% agarose gel containing formaldehyde, and then transferred to a Hybond N+ membrane (Amersham) in accordance with standard techniques (Sambrook et al., 1982). The complete cDNA corresponding to Ha-NTIR11g (Radwan et al., 2004) was labelled with [
-32P]dCTP using Amersham megaprime DNA labelling. The wash procedures for the Southern and northern blots were carried out at 65 °C and 42 °C, respectively. The blots were washed twice with a 2x SCC/0.1% SDS solution for 15 min then with a 1x SCC/0.1% SDS solution for 15 min and finally with a 0.1x SCC/0.1% solution for 15 min. X-ray films were then exposed to the filters at –80 °C.
RT-PCR procedures
Total RNA was treated with DNase I to remove any genomic DNA contamination. Thereafter, 2 µg of DNase-treated RNA were reverse transcribed using the SuperScript First-Strand Synthesis System for an RT-PCR Kit (Invitrogen, France). A ‘minus’ reverse transcriptase PCR reaction, where no reverse transcriptase enzyme was added during the cDNA synthesis reaction, was used to test each mRNA sample for genomic DNA contamination.
Primer design for RT-PCR reactions
Specific primers were designed using sequences obtained from sunflower line QIR8. Some of these sequences have been described in previous papers, the others were cloned during this study.
To detect the expression of Ha-NTIR11g in the resistant line QIR8 and the susceptible line CAY, the full-length sequence of Ha-NTIR11g from the resistant line (accession number AY490793) was used to design a primer pair which was used to amplify a unique band both in the resistant and the susceptible lines using DNA as template. To ensure that the amplified bands correspond to the resistant and susceptible alleles, they were cloned and sequenced and the corresponding sequences were aligned. The primers used in this experiment match perfectly both resistant (accession number AY490793) and susceptible (accession number AY645207) alleles. Thus, this primer pair was used subsequently in the RT-PCR experiments, considering that it amplifies the same gene in both sunflower lines.
For PR-5, accession number AAM21199 (Hu et al., 2003) was used to design the primers. The sunflower elongation factor EF-1 sequence (accession number AM19764) was used as an internal standard. In order to check for the presence of the oomycete within sunflower tissues during the time-course of RT-PCR analysis, specific primers targeting the P. halstedii elongation factor Ph-TEF1 (accession number CB174619) were used.
Because the sunflower defence-related genes described here were being cloned for the first time, degenerate primers derived from conserved regions within homologous sequences in other plant species were used, following multiple sequence alignments using CLUSTAL-X (Thompson et al., 1997).
Degenerate primers were designed for the hsr203J gene [forward 5'-CGC(TC)TAGCGCG(ATGC)GTGGC(ATCG)AACGC-3'; reverse 5'-(TG)A(ATGC)GTT(ATGC)CCGCCGGAGC(ATGC)GTCTCC-3'], EDS1 [forward 5'-GT(AGCT)CCTCGGAT(AGCT)ATGCTTGCTC-3'; reverse 5'-CA(AGCT)GCAG(AGCT)ATAACTTGCAACAG-3'], and EDR1 [forward 5'-GA(AG)T(AT)TCT(GT)CC(AT)AG(AGCT)GGAAGC-3'; reverse 5'-CC(AGCT)AAATCAC(AGCT)(AG)ACCTT(AGCT)ACA(AGCT)TCCA-3']. QIR8 cDNA was used as the template, the resulting PCR products being purified using the GFX PCR purification system kit (Amersham-Pharmacia-Biotech, France), sub-cloned in the pGEMT-easy vector according to the manufacturer's protocol (Promega), and sequenced by Genome express (Grenoble, France). Specific primers were then designed for RT-PCR analysis. Table 1 shows the sequences of these specific primers, together with the RT-PCR conditions (Tm and total PCR cycles).
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RGA and defence gene expression
The transcriptional expression of each gene was analysed using semi-quantitative PCR. Reverse transcribed cDNA was diluted 1/6, and then 2 µl was used in 40 µl of a PCR mix containing 0.3 U (0.3 µl) of Taq DNA polymerase (Advantage 2, Clontech, France), 1x Taq polymerase buffer, 0.1 mM of each dNTP, and 0.75 mM of each primer. PCR was carried out in a Bio-rad thermocycler under the following conditions: initial denaturation at 94 °C for 3 min followed by 25–36 cycles (depending on the experiments; see Table 1) of 15 s at 94 °C, 15 s at Tm °C (Table 1) and 20 s at 72 °C. PCR products were separated using 3% Tris–acetic acid–EDTA–agarose gels, except for the CC-NBS-LRR products for which 1.5% Tris–acetic acid–EDTA–agarose gels were used. Gels were stained with ethidium bromide (0.5 mg ml–1). To ensure that the observed bands all corresponded to the expected sequences, all RT-PCR products were cloned and completely sequenced (Genome Express Grenoble, France). The experiment was repeated three times, with similar results being obtained.
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Results |
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Genomic organization of the Ha-NTIR11g gene
Southern blot analysis of resistant and susceptible sunflower genomic DNA was performed to determine the presence of CC-NBS-LRR homologous sequences. Genomic DNA of sunflower was digested with BamHI, EcoRI, EcoRV, and HindIII, and hybridized with a 32P-labelled probe generated from a full-length cDNA of Ha-NTIR11g. Several bands were observed for each of the restriction endonucleases tested, which suggests that both the resistant and susceptible sunflower genomes have several copies of Ha-NTIR11g homologous genes (Fig. 1A). These results indicate that Ha-NTIR11g belongs to a complex, multigene family. All polymorphic fragments were mapped to the Pl8 locus (data not shown). To test whether the same complex diagram exists at the transcript level, northern analysis was carried out using the resistant and susceptible sunflower lines. An RNA gel blot containing 7 µg of poly (A)+ RNA isolated from healthy hypocotyls of QIR8 and CAY were hybridized with the complete cDNA of Ha-NTIR11g. Transcripts of
5 kb were detected in QIR8 and CAY sunflower hypocotyls (Fig. 1B). The transcript length observed was consistent with the transcript length of Ha-NTIR11g. For the susceptible line, no major band was observed even after 15 d of exposure. It should be noted that the transcription level of this RGA was very weak and could not be seen before at least 15 d of exposure. For this reason, the more sensitive RT-PCR method was used to specifically monitor the expression level of Ha-NTIR11g during the infection process.
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Analysis of Ha-NTIR11g gene expression
One primer pair was used (Table 1) to amplify 514 bp from infected and uninfected hypocotyls of the resistant (QIR8) and susceptible (CAY) parents. The four PCR fragments obtained using these combinations were then cloned, and five clones of each were sequenced. Sequence comparisons indicated no difference between the sequence of infected and non-infected hypocotyls in either of the parents used during this study. However, there was a 31% difference between the sequence of the resistant parent (accession number AY490793) and the susceptible parent (accession number AY645207). The sequences of the former (PR-CC) and the latter (PS-CC) shared 100% and 69% identity, respectively, with the Ha-NTIR11g RGA sequence. In addition, the sequence of the primers used in this study was 100% identical in both lines. Thus, these data suggest that, by using these primers, the differences in expression levels observed could conceivably be attributable to the Ha-NTIR11g RGA clone.
Expression of the Ha-NTIR11g gene of sunflowers infected by P. halstedii
The transcript level of the Ha-NTIR11g gene in resistant and susceptible lines of sunflower was determined after infection with P. halstedii by semi-quantitative RT-PCR analysis. Total RNA was isolated from hypocotyls 1.5, 3, 6, 9, 12, and 15 d after infection (dpi), as well as from non-infected plants. Figure 2 shows that the transcript of Ha-NTIR11g was detected at a low level in the hypocotyls of control plants grown in the absence of infection, but was induced about 3 dpi, declining after 9 d. The peak transcriptional expression of this gene (6 dpi) coincided with activation of a transcript accumulation of the hsr203J gene, which is a physiological marker of the hypersensitive reaction (Pontier et al., 1994). In the susceptible line, the transcription level was too low and undetectable after 33 amplification cycles; this number was therefore raised to 36. Under these conditions, no significant induction of either transcript was observed after infection.
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By comparison, an accumulation of PR-5 transcripts was observed in resistant hypocotyls 6 d after infection, reaching its highest level at 9 d and then declining 12 d after infection (Fig. 2). The high level of transcriptional expression of PR-5 (9 dpi) coincided with a decrease in CC-NBS-LRR transcripts. These results suggest that Ha-NTIR11g RGA was induced earlier than the defence gene expression of PR-5. In contrast, the expression of genes involved in signalling pathways, such as EDS1 and EDR1, was not induced after infection in either compatible or incompatible combinations (Fig. 2).
Effect of abiotic stimuli on accumulation of Ha-NTIR11g transcript
To test whether the Ha-NTIR11g gene could be induced by stimuli other than pathogen infection, the effect of various signalling molecules, hydrogen peroxide, and wounding was evaluated by semi-quantitative RT-PCR analysis (Figs 3, 4). A transcript accumulation of the Ha-NTIR11g gene was not induced by treatment with either SA (2 mM) or MeJA (100 µM). Significant activation of PR-5 transcription was observed in response to SA (Fig. 4). These results suggest that Ha-NTIR11g gene expression is not responsive to the defence signal transduction pathways mediated by SA and MeJA. Ha-NTIR11g transcript did not accumulate after treatment with H2O2 or wounding (Fig. 4).
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Hypersensitive-like reaction
To test whether the transcriptional activation of Ha-NTIR11g could be associated with the hypersensitive reaction, microscopic observations were performed during the same experiment. In both genetically compatible and incompatible combinations, and 3 dpi, intercellular hyphae and haustoria were visible in the hypocotyl base area. No microscopic differences were observed between the two combinations.
By 6 dpi, in the case of the compatible combination, the pathogen had spread halfway along the hypocotyls. Cells containing haustoria had a normal appearance and there was no evidence of hypersensitive cell death (Fig. 5A). On the other hand, in the case of the genetically incompatible combination, parenchymal cells that were in contact with the pathogen or close to it, exhibited some modifications: the cytoplasm appeared granular with a red coloration and seemed to undergo a hypersensitive-like reaction (Fig. 5B). By 9 dpi, in the genetically compatible reaction, the hypocotyls were systemically invaded by hyphae (Fig. 5C) and the pathogen was present in the cotyledons. With the genetically incompatible combination, the cells around the pathogen or close to it collapsed, and the remaining compacted cell walls formed layers, encircling the pathogen structures (Fig. 5D). These necrotic regions were also observed in cotyledons (data not shown).
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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One resistant (QIR8) and one susceptible (CAY) line in the sunflower were used to study the resistance conferred by the Pl8 locus which appears to contain sequences belonging to the CC-NBS-LRR class of plant resistance genes (Radwan et al., 2003
, 2004). Using the RACE-PCR procedure, Radwan et al. (2004) had previously isolated full-length cDNA and genomic sequences of 5154 bp and 6726 bp in length, respectively, which were all mapped to the Pl8 locus. Homology searches have shown that this RGA shares similarities with other resistance genes such as the RPP13-like protein encoded by the Arabidopsis downy mildew resistance gene from Arabidopsis thaliana (Sato et al., 2000), the I2C family from the tomato wilt disease resistance locus I2 (Ori et al., 1997; Simons et al., 1998), and the resistance candidate (RGC 1b) from Lactuca sativa (Shen et al., 1998). Obviously, sequence comparisons with other genes cloned from various plant species can provide interesting information about the possible role of this RGA, but experimental data are also required. Therefore, in order to investigate whether this RGA is expressed and if the level of its transcript accumulation may vary during the infection process, the same experimental protocol was employed to analyse infected and non-infected plants using both semi-quantitative RT-PCR and microscopic observations.
Differential expression of Ha-NTIR11g RGA
The function of R gene products as receptors interacting with pathogen elicitors in a setting of defence signalling has been suggested both by direct and indirect evidence (Baker et al., 1997; Jia et al., 2000; Jones, 2001; Nimchuk et al., 2001). Structural analysis of R genes that have many features in common suggests that they are active in signalling cascade(s) that co-ordinate initial plant defence responses in order to impair pathogen growth (Ellis and Jones, 1998; Hammond-Kosack and Jones, 1997). While avirulence genes probably play a role in the fitness or pathogenicity of the pathogen (Leach and White, 1996; Vivian and Gibbon, 1997), R-gene products may have a function in plant development and therefore be expressed in healthy, unchallenged plants, ready to detect any attack (Hammond-Kosack and Jones, 1997).
The Ha-NTIR11g gene is constitutively expressed at low levels in the healthy hypocotyls and cotyledons of the resistant genotype, whereas it was not detected in the present conditions in both tissues in the susceptible genotype. After infection, levels of the Ha-NTIR11g gene are induced only in the incompatible combination. Similar constitutive expression has been observed for RPS2, RPM1, RPP5, M1, Pto, Prf, Xa21, Cf-9, XaI, and Hs1pro–1 R genes (Grant et al., 1995; Hammond-Kosack and Jones, 1997; Milligan et al., 1998; Parker et al., 1997; Salmeron et al., 1996; Song et al., 1995; Yoshimura et al., 1998; Thurau et al., 2003). However, very few R genes exhibit the ability to be activated during pathogen infection, i.e. XaI, a bacterial resistance gene in rice (Yoshimura et al., 1998), the pib rice blast resistance gene (Wang et al., 1999; 2001), and Hs1pr°–1, a nematode-resistant gene in sugar beet (Thurau et al., 2003). In soybean, of six clustered TIR-NBS-LRR resistance genes, three are constitutively expressed and three others may be differentially expressed (Graham et al., 2002). In the present pathological system, the transient increase in steady-state levels of Ha-NTIR11g transcript found with the incompatible combination coincided with the onset of a hypersensitive-like reaction (cell collapse, activation of an hsr203J homologue), suggesting a correlation between the hypersensitive reaction and activation of this gene. Few studies on resistance genes such as Xa1, Xa21, pib, Hs1pr°–1, RPW8.1, and RPW8-2 have demonstrated that they are transcriptionally regulated by either pathogen infection, wounding, or treatment with certain chemicals (Yoshimura et al., 1998; Century et al., 1999; Wang et al., 2001; Thurau et al., 2003; Xiao et al., 2003). Furthermore, enhanced expression of a resistance gene such as RPW8-1 or RPW8-2 may directly control the onset of a spontaneous hypersensitive-like reaction (Xiao et al., 2003). Similarly, the over-expression of Pto, a tomato disease resistance gene which determines race-specific resistance to the bacterial pathogen Pseudomonas syringae pv. tomato, activates defence responses in the absence of the Pto–AvrPto interaction and confers broad disease resistance (Tang et al., 1999). Interestingly, the observation reported in these studies concerned monocots, dicots, and a wide range of structurally unrelated resistance genes, suggesting that the transcriptional activation of resistance genes may be a phenomenon which is common to several plant–pathogen systems.
Neither wounding nor the treatment of sunflower leaves with SA or other substances such as MeJA and H2O2 managed to induce significantly an accumulation of Ha-NTIR11g transcript, indicating that the activation of this gene is specifically associated with the infection by P. halstedii. Enhanced transcription of the Ha-NTIR11g gene appeared to co-localize with the area of P. halstedii containment (see hypocotyls). Similar observations were reported by Mes et al. (2000), who analysed the GUS activity driven by the Fusarium resistance gene I-2 promoter and showed that I-2 expression was restricted to the infected site in the resistant plant. However, these authors failed to detect any enhanced activity of the I-2 gene. Taken together, these results suggest that the CC-NBS-LRR analogue gene Ha-NTIR11g is locally activated in resistant sunflower during infection by P. halstedii, independently of any signal transduction pathways mediated by SA and MeJA.
The EDS1 gene, which encodes lipase-like protein (Falk et al., 1999), has been induced by Plasmopara infection. This finding was in line with other results suggesting that only resistance genes belonging to the TIR-NBS-LRR class require EDS1 and PAD4 function to ensure full resistance (Aarts et al., 1998; Feys and Parker, 2000; McDowell et al., 2000; Bittner-Eddy and Beynon, 2001; Glazebrook, 2001; Dodds and Schwechheimer, 2002; Peart et al., 2002).
In conclusion, a sunflower RGA belonging to the CC-NBS-LRR class of plant resistance genes was cloned, and it was shown that it was transcripionally activated in the incompatible interaction. However, the role of this gene in sunflower resistance to P. halstedii needs to be verified by both transforming a susceptible sunflower line and analysing its complete promoter.
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Acknowledgements |
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We would like to thank the Egyptian Ministry of Higher Education for awarding a Doctoral Scholarship to OR, and PROMOSOL for its financial support.
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References |
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