| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
|
First published online April 13, 2007; 10.1104/pp.106.094318 Plant Physiology 144:1093-1103 (2007) © 2007 American Society of Plant Biologists OPEN ACCESS ARTICLE
Mutations in LACS2, a Long-Chain Acyl-Coenzyme A Synthetase, Enhance Susceptibility to Avirulent Pseudomonas syringae But Confer Resistance to Botrytis cinerea in Arabidopsis1,[OA]Department of Biology, Indiana University, Bloomington, Indiana 47405
We identified an Arabidopsis (Arabidopsis thaliana) mutant, sma4 (symptoms to multiple avr genotypes4), that displays severe disease symptoms when inoculated with avirulent strains of Pseudomonas syringae pv tomato, although bacterial growth is only moderately enhanced compared to wild-type plants. The sma4 mutant showed a normal susceptible phenotype to the biotrophic fungal pathogen Erysiphe cichoracearum. Significantly, the sma4 mutant was highly resistant to a necrotrophic fungal pathogen, Botrytis cinerea. Germination of B. cinerea spores on sma4 mutant leaves was inhibited, and penetration by those that did germinate was rare. The sma4 mutant also showed several pleiotropic phenotypes, including increased sensitivity to lower humidity and salt stress. Isolation of SMA4 by positional cloning revealed that it encodes LACS2, a member of the long-chain acyl-CoA synthetases. LACS2 has previously been shown to be involved in cutin biosynthesis. We therefore tested three additional cutin-defective mutants for resistance to B. cinerea: att1 (for aberrant induction of type three genes), bodyguard, and lacerata. All three displayed an enhanced resistance to B. cinerea. Our results indicate that plant cutin or cuticle structure may play a crucial role in tolerance to biotic and abiotic stress and in the pathogenesis of B. cinerea.
Disease resistance in plants is mediated by both preformed and induced defenses. Examples of preformed defenses include physical barriers such as the cutin layer on leaf and stem surfaces; antimicrobial enzymes stored in the tonoplast that are released upon cell damage; and secondary metabolites that are often present at low constitutive levels, but whose levels are increased during pathogen attack (Morrissey and Osbourn, 1999  ). Induced defenses include production of reactive oxygen species, secretion of antimicrobial proteins, cross-linking of cell walls, production of additional secondary metabolites, and the hypersensitive response (HR; a type of programmed cell death; Glazebrook, 2005). Rapid induction of defenses is usually mediated by disease resistance (R) genes, which encode proteins that detect specific pathogen virulence proteins (Jones and Dangl, 2006). The hallmark of R gene-mediated resistance is specificity. Most R proteins detect only one or two virulence proteins. However, different R genes activate very similar responses, suggesting that there are convergent points in R protein signaling. Despite this seeming convergence, we have a very poor understanding of what proteins function downstream of R proteins to activate the HR and other defense responses.
A large number of R genes from plants and their cognate virulence genes from pathogens have been cloned. In Arabidopsis (Arabidopsis thaliana), the R genes RPM1 and RPS2 have been intensively studied (Bent et al., 1994
We expected to identify several classes of mutants from this screen. The first class of mutants was expected to contain mutations in downstream signaling components that are shared by both RPM1 and RPS2, such as positive regulators of defense responses, including transcription factors and regulators of the HR. A second class of mutants was expected to be in genes required for assembly and/or stability of R protein complexes such as SGT1 and RAR1 (Tornero et al., 2002
As described below, we uncovered mutations in the first and third class. In this article, we describe characterization and cloning of enhanced susceptibility mutant sma4 (symptoms to multiple avr genotypes4), which appears to belong to the third class. The sma4 mutant displayed severe disease symptoms after infection with Pst DC3000 carrying avrRpt2 and avrB, either together or individually. Interestingly, this mutant was highly resistant to the necrotrophic fungal pathogen Botrytis cinerea. We cloned the SMA4 gene by map-based cloning, and found that SMA4 encodes a member of the long-chain acyl-CoA synthetase (LACS) family, LACS2, which has previously been shown to function in cutin synthesis (Schnurr et al., 2004
Identification of Arabidopsis Mutants Susceptible to a P. syringae Strain Expressing Both avrB and avrRpt2
Approximately 16,600 ethylmethanesulfonate, diepoxybutane, and fast neutron-mutagenized M2 plants were screened for disease symptoms following inoculation with DC3000 harboring both avrB and avrRpt2 on separate plasmids. Nine putative mutants that displayed strong symptoms were selected. M3 progeny of these nine mutants were dip inoculated with strain DC3000 expressing avrB or avrRpt2 individually. Three of the mutants retained resistance to DC3000(avrB) but appeared fully susceptible to DC3000(avrRpt2). Allelism tests revealed that these mutations were in fact in RPS2. Although this was an unexpected result at the time, we now know that AvrRpt2 affects RPM1 function by eliminating RIN4 (Axtell and Staskawicz, 2003
M3 progeny of the remaining six mutants displayed disease symptoms when inoculated with either DC3000(avrB) or DC3000(avrRpt2). Allelism tests of these six mutants indicated that three of the mutations were allelic to ndr1 (Century et al., 1997 The remaining three mutations were not allelic to ndr1 or each other. We designated these mutants sma1, sma3, and sma4. Here, we describe characterization of the sma4 mutant and the cloning of the SMA4 gene. The other two mutants remain to be fully characterized.
Varying degrees of necrotic collapse were consistently observed on sma4 plants relative to wild-type Col-0 by 3 to 4 d after dip inoculation with strain DC3000 carrying avrRpt2, avrB (Fig. 1, A and B ), or avrPphB (data not shown). These observations suggested that the DC3000 avirulent genotypes were at least partially virulent on sma4 mutant plants.
The symptoms of necrotic leaf collapse in response to each of the Pst DC3000 avr genotypes were very atypical compared to those observed when virulent DC3000 was allowed to infect wild-type Col-0 plants. The sma4 symptoms in response to infection by strain DC3000(avrRpt2) were the most severe. Typically, some necrotic collapse was observed as early as 48 h after dip inoculation at 1.5 x 108 cfu/mL. By late day 3 and early day 4 after infection, most of the older, outer rosette leaves were observed to be entirely collapsed and dead. In contrast, a virulent Pst DC3000 infection on wild-type Col-0 plants typically produces chlorosis, large water-soaked lesions, and pin-point necrotic pits over the surface of Arabidopsis leaves (Whalen et al., 1991 ). Rarely is whole leaf collapse and death observed in a virulent Pst DC3000 interaction at an inoculum concentration of 1.5 x 108 cfu/mL. Strains of DC3000 carrying avrB, avrRpm1, and avrPphB induced a phenotype on sma4 plants similar to that induced by DC3000(avrRpt2). However, these responses were consistently less severe (Fig. 1; data not shown).
Examination of sma4 plants inoculated with the same concentration of the virulent control strain DC3000(avrB::
The sma4 phenotype of necrotic collapse more closely resembled a HR than true susceptibility. The HR is strongly associated with cessation of bacterial growth and other resistant responses in the infected plant (Klement, 1982
We normally use a low (1 x 105 cfu/mL) concentration of pathogen carried in a solution of 10 mM MgCl2 with 0.001% L-77 wetting agent as the method of inoculation for monitoring in planta pathogen growth. However, we noted that sma4 plants rapidly (within 2 h) exhibited severe necrotic leaf collapse after vacuum infiltrating pathogen cells suspended in a 10 mM MgCl2 solution. Vacuum infiltration causes the leaves to become saturated with the infiltrated solution in the intercellular leaf spaces. The plants are allowed to shed the excess water by drying out slowly over a period of a few hours. This drying is occasionally observed to damage some wild-type leaves along their margins, where some necrosis may develop. However, sma4 plants consistently developed extensive tissue collapse on more than 50% of their leaves or were entirely killed by the drying process. The collapse developed too quickly to be explained by a pathogen-induced effect such as HR induction, which normally takes at least 12 h to become visible. We assessed whether the vacuum infiltration process, the subsequent leaf drying, or the buffer components were the cause of this sma4 phenotype. Vacuum infiltration of sterile 10 mM MgC12 and 0.001% L-77 caused the same degree of sma4 tissue collapse as was seen with the pathogen inoculations. Vacuum infiltration with the pathogen carried in distilled water plus 0.001% L-77 did not cause any more sma4 leaf collapse than collapse of wild-type Col-0 leaves within 2 h of the infiltration. Finally, sma4 leaves vacuum infiltrated with distilled water plus L-77 and no pathogen also did not display collapse. These observations suggested that the 10 mM MgCl2 was responsible for the leaf collapse. We therefore used distilled water instead of 10 mM MgCl2 to generate the bacterial growth curve data shown in Figure 1. To ascertain whether this effect was limited to salt exposure or reflected a general osmotic sensitivity conferred by the sma4 mutation, we repeated the vacuum infiltrations with sterile 15 mM NaC1, 15 mM MgSO4, sterile 20 mM Glc, and sterile 20 mM mannitol plus 0.001% L-77 wetting agent. The NaCl and MgSO4 treatments produced a response similar to the MgCl2 treatments in severity, while the Glc and mannitol treatments responded similar to infiltration with water. We also noted that we could block the observed collapse by loosely sealing the salt-infiltrated sma4 plants under plastic covers, which kept the surrounding humidity relatively high. However, these covers did not allow the leaves to dry by shedding the excess water from their intercellular spaces. These results suggested that the rapid tissue collapse (within 2 h) was triggered by salt exposure, but also required the drying process after salt exposure. The phenotype was not attributable to a general osmotic sensitivity of the sma4 leaf cells.
We routinely germinated our Arabidopsis seeds in soil-filled pots under clear plastic domes, which provided an environment of near 100% relative humidity. Approximately 1 to 2 weeks after germinating, when the first true leaves become visible, we removed the domes, which resulted in a rapid drop in humidity from about 100% to about 60%. Although wild-type seedlings tolerated this sudden humidity drop without visible effects, sma4 seedlings were observed to undergo a high rate of necrosis and death (Fig. 2 ), presumably due to desiccation of the seedlings. Mutant sma4 seedlings up to 2.5 weeks postgermination consistently suffered leaf collapse within 2 h after removal of the humidity cover. The sma4 leaf collapse could be blocked by leaving the seedlings under the humidity cover for an additional 1.5 to 2 weeks. At this age, removal of the humidity cover still resulted in some rapidly appearing necrosis on sma4 leaf margins, but leaf death rarely occurred.
sma4 Leaf Cells Leak Ions Faster Than Wild-Type Col-0 Cells during the HR and after Salt Exposure To further assess the relationship of the sma4 mutation to pathogen susceptibility, salt stress, and desiccation sensitivity, we compared the rate and amount of ion leakage from sma4 and Col-0 cells as a possible indicator of cell integrity during the HR and after vacuum infiltration of 10 mM MgC12 and MgSO4. We inoculated individual leaves of sma4 mutant and wild-type Col-0 plants with P. syringae pv glycinea Race 4 (avrRpt2) [PsgR4(avrRpt2)] at a cell density of 5 x 107 cfu/mL suspended in distilled water. We assayed the amount of ion leakage every 5 h for 25 h by measuring the conductivity of fluid eluted from sampled leaves. Figure 3A indicates that by 12 h after inoculation, sma4 leaf cells had leaked a significantly greater amount of ions than the Col-0 leaf cells. By 24 h, the point at which a visible HR is plainly visible on both sma4 and Col-0 leaves, the difference was even more dramatic. We repeated this experiment with strain Pst DC3000(avrRpt2) infiltrated at a concentration of 1 x 107 cfu/mL and obtained a similar result (data not shown). These results suggested that, while sma4 plants develop an HR that is visibly and microscopically similar to Col-0 plants, the sma4 leaves appear to leak cell contents faster than Col-0 leaves in response to an HR-inducing bacterial strain.
We also assessed the effect of vacuum infiltration of 10 mM MgC12 and 10 mM MgSO4 on ion leakage (Fig. 3B). The rapid collapse of sma4 leaves correlated with a greater degree of ion leakage from sma4 leaves after salt treatment compared to Col-0 leaves (Fig. 3B).
Because sma4 mutant plants appeared to be more prone to leaf collapse after both biotic and abiotic stresses, we hypothesized that the mutant would display enhanced sensitivity to a necrotrophic pathogen such as B. cinerea, which actively kills infected leaves and grows on the dead tissue. Wild-type Col-0 plants are moderately susceptible to this pathogen, and growth of B. cinerea can be enhanced by induction of an HR (Thomma et al., 1998
In addition to B. cinerea, we also tested a biotrophic fungal pathogen, Erysiphe cichoracearum strain UCSC, which is virulent on wild-type Col-0 plants (Adam and Somerville, 1996 ), and another necrotrophic fungal pathogen, Alternaria brassicicola. We observed no significant difference between Col-0 wild type and the sma4 mutants in their response to these pathogens (data not shown).
Resistance to necrotrophic pathogens is often dependent on jasmonic acid (JA) and ethylene signaling pathways (Glazebrook, 2005
Genetic Mapping and Identification of SMA4 To characterize the genetic basis of sma4-mediated responses to pathogens, the mutant was backcrossed to wild-type Col-0. The Fl progeny were resistant to dip inoculation with DC3000(avrRpm1), which indicated that sma4 was a recessive mutation. Consistent with this, the F2 progeny segregated 3:1 wild-type:sma4 mutant phenotypes. To verify that partial susceptibility to multiple avr genotypes was indeed conferred by a single mutation, several F3 families from the sma4 x Col-0 F2 progeny were tested for symptoms after dip inoculation with DC3000(avrRpm1), DC3000(avrB), and DC3000(avrRpt2). These F3 families displayed symptoms of partial susceptibility to each of the different avr genotypes, indicating that the sma4 phenotype was conferred by a single mutant locus. Using PCR-based molecular markers, we mapped the sma4 mutation to an 88-kb interval on chromosome I (see "Materials and Methods"). We then amplified and sequenced open reading frames from the sma4 mutant from most of the predicted genes in this region, except for pseudogenes and genes encoding tRNA, or ribosomal RNA. In total, 15 genes were sequenced and a T-to-A mutation was found in At1g49430. No mutation was found in the other genes sequenced in this region. The point mutation in the sma4 mutant was located in the left border of intron 4 of At1g49430 according to the annotated sequence of this gene (Fig. 6A ). To examine whether this mutation affected the splicing of At1g49430, we performed reverse transcription (RT)-PCR, followed by direct sequencing of the cDNA of this gene from both sma4 and Col-0 plants. These analyses revealed that intron 4 was retained in the sma4 cDNA, resulting in a 145-base insertion. This insertion caused a premature stop codon, which would prevent translation of the last 15 exons of SMA4 (Fig. 6A); thus, the sma4 mutation likely causes a complete loss of function.
To further confirm that SMA4 is At1g49430, we complemented the sma4 mutant with a 6.8-kb genomic DNA sequence containing the full-length At1g49430 gene including 1.5 kb of upstream promoter region and 0.8 kb of downstream sequences. Figure 6, B and C, shows that this genomic DNA fragment rescued sma4-mediated disease phenotypes. These data demonstrated that At1g49430 is the SMA4 gene.
At1g49430 has previously been shown to encode a LACS, of which there are nine family members in Arabidopsis (Shockey et al., 2002
It should be noted that the lacs2-1 mutant has been reported to display a strong dwarfed phenotype with small wrinkled leaves (Schnurr et al., 2004
To gain more insight into the role of plant cuticle structure in resistance to B. cinerea, we tested three additional cutin-defective mutants for resistance to B. cinerea: att1 (for aberrant induction of type three genes), bodyguard (bdg), and lacerata (lcr; Wellesen et al., 2001
We have shown that loss of LACS2 function makes Arabidopsis more susceptible to avirulent strains of the Arabidopsis bacterial pathogen Pst DC3000, but more resistant to a virulent strain of the necrotrophic fungus B. cinerea. Why does loss of LACS2 function cause these phenotypes? LACS2 encodes a LACS (Schnurr et al., 2004 ). LACS enzymes activate free fatty acids to acyl-CoAs, a key step for the utilization of fatty acids by most lipid metabolic enzymes (Shockey et al., 2002). LACS2 is expressed in the epidermal cell layer of Arabidopsis leaves and the T-DNA insertion mutant lacs2-1 has a thinner cuticle layer compared to wild-type plants. A preferred substrate of the LACS2 enzyme is  -hydroxypalmitic acid; thus, Schnurr and colleagues concluded that LACS2 catalyzes the synthesis of -hydroxy fatty acid-CoA intermediates required for cutin synthesis (Schnurr et al., 2004). Leaves of a lacs2-1 null mutant release chlorophyll faster than wild-type leaves when immersed in 80% ethanol and support pollen germination, which indicates that the cuticular barrier on lacs2-1 plants is more permeable (Schnurr et al., 2004). We propose that it is this increased permeability that causes the enhanced tissue collapse upon infiltration of dilute salt solutions or avirulent pathogens, and that causes enhanced resistance to B. cinerea.
Support for this hypothesis comes from work on ATT1, which encodes an Arabidopsis Cyt P450 monooxygenase (CYP86A2) that is required for proper cuticle development. Loss-of-function att1 mutants have lower cutin content, loose cuticle ultrastructure, and increased rates of water vapor transmission (Xiao et al., 2004 An increase in cuticle permeability to water vapor in the sma4 mutant is consistent with our observation that sma4 seedlings are quite sensitive to rapid decreases in humidity (Fig. 2). An increase in cuticle permeability would also explain the observed increase in ion leakage after bacterial infection or salt exposure (Fig. 3).
The most interesting phenotype of sma4, however, is its resistance to the necrotrophic fungus B. cinerea. Given that sma4 leaves collapse and die more rapidly when infected with P. syringae, an increased resistance to a necrotroph was unexpected. One possible explanation for the enhanced resistance is that B. cinerea may rely on specific physical and/or chemical queues on the leaf surface to promote germination and penetration. Host surface structure has been implicated in the pathogenesis of other necrotrophic pathogens. For example, in the interaction between Colletotrichum trifolii and alfalfa (Medicago sativa), the host surface chemistry appears to be important for induction of the fungal gene expression required for pathogenic development (Dickman et al., 2003
If the inhibition hypothesis is correct, it is plausible that the permeability of the cuticle enhances export of an antifungal compound to the leaf surface or, alternatively, enhances import of a fungal elicitor that triggers production of an antifungal compound. Evidence that export of antifungal compounds to the leaf surface is important comes from recent work on the Arabidopsis PEN3 gene. PEN3 encodes a plasma membrane-localized ATP-binding cassette transporter that localizes around fungal penetration sites (Stein et al., 2006
It has recently been reported that a transgenic Arabidopsis line that expresses a fungal cutinase displays enhanced resistance to B. cinerea (Chassot and Métraux, 2005
Plant Growth Conditions and Mutant Screening
Arabidopsis (Arabidopsis thaliana) plants were grown in growth rooms under a 9-h-light/15-h-dark cycle at 23°C as described previously (Frye and Innes, 1998
Inoculation of Arabidopsis plants with Pst DC3000 and measurement of bacterial growth within leaves was performed as described previously using vacuum infiltration of 6-week-old plants (Simonich and Innes, 1995
Intact leaves were entirely infiltrated with a bacterial density of 5 x 107 cfu/mL in deionized water. At 0, 5, 10, 15, 20, and 25 h after infiltration, a random sample of inoculated leaves was excised from the plants and five leaf discs, each 7 mm in diameter, were cut from the excised leaves with a cork borer and immediately floated, abaxial side down, in 6 mL of 0.001% L-77 surfactant (Union Carbide) in water. The sampling was done in triplicate for each time point. Leaf discs were floated for 4 h, after which conductivity measurements of the bathing solution were made with a Radiometer Copenhagen CDM2f conductivity meter and Radiometer Copenhagen CDC104 detector (The London Company).
F2 progeny of a sma4 cross to Landsberg erecta were used to genetically map the SMA4 gene. The F2 plants were inoculated with Pst DC3000(avrRpt2) and scored 3 d after inoculation. Plants displaying a sma4 phenotype were used for mapping. Initially, the sma4 mutation was mapped to chromosome I between SSLP markers T27K12 and CIW1. To further localize the SMA4 gene, we developed new markers at intervals between these two markers using Monsanto Col-0 and Landsberg erecta polymorphism data (marker data available upon request). A total of 556 susceptible F2 plants representing 1,112 meioses were scored, which enabled us to localize sma4 between two markers at positions 29 kb and 117 kb of the bacterial artificial chromosome (BAC) clone F13F21 (GenBank accession no. AC007504), defining an 88-kb region that cosegregated with the sma4 mutation.
Candidate genes were amplified by PCR from genomic DNA isolated from the sma4 mutant and from wild-type plants and directly sequenced. All sequencing reactions were performed using BigDye Terminator kits (Applied Biosystems) and separated on an ABI 3730 automated DNA sequencer. In total, 15 genes were amplified from the sma4 mutant by PCR and directly sequenced. To obtain the SMA4 cDNA sequence, RNA was isolated and first-strand cDNA synthesis was performed as described previously (Tang et al., 2005
A full-length SMA4 genomic sequence, including the promoter region and 3' untranslated region, was amplified from BAC F13F21 using the following primers: 5'-AACCGCTAGCTTCCTTATAAAAAGTTAAAGAAAAAG-3' and 5'-AATTGGGCCCCGTATGAGAATGATTAGTTTAGTTGA-3'. The PCR product was digested with ApaI and NheI and ligated with the binary vector pGreen0029 digested with ApaI and XbaI (Hellens et al., 2000
The pGreen0029:At1g49430 construct was transformed into Agrobacterium tumefaciens strain GV3101 by electroporation and selected on LB plates containing 50 µg/mL kanamycin sulfate (Sigma). Arabidopsis plants were transformed using the floral dip method (Clough and Bent, 1998
Double mutants were created by standard genetic crosses. The ein2-1 mutation was in the Col-0 background (Alonso et al., 1999
We thank J. Browse for providing lacs2-1 seeds, J. Turner for providing coi1-1 seeds, J. Ecker for providing ein2-1 seeds, J. Zhou for providing att1 seeds, A. Yephremov for providing bdg and lcr seeds, F.M. Ausubel for providing the B. cinerea strain, and T. Mengiste for providing an A. brassicicola strain. We also thank the Arabidopsis Biological Resource Center at The Ohio State University for providing BAC clone F13F21. Received December 7, 2006; accepted April 2, 2007; published April 13, 2007.
1 This work was supported by the National Institutes of Health (NIH; grant nos. R01 GM63761 and R01 GM046451 to R.W.I.). M.T.S. was supported by an NIH training grant in genetics (GM 07757). 
2 Present address: State Key Laboratory of Plant Cell and Chromosome Engineering, Institute Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China.
3 Present address: Linus Pauling Institute, Oregon State University, Corvallis, OR 97331–6512. 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: Dingzhong Tang (dztang{at}genetics.ac.cn).
[OA] Open Access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.106.094318 * Corresponding author; e-mail dztang{at}genetics.ac.cn; fax 86–10–6484–7489.
Adam L, Somerville SC (1996) Genetic characterization of five powdery mildew disease resistance loci in Arabidopsis thaliana. Plant J 9: 341–356[CrossRef][Web of Science][Medline] Alonso JM, Hirayama T, Roman G, Nourizadeh S, Ecker JR (1999) EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 284: 2148–2152 Axtell MJ, Staskawicz BJ (2003) Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112: 369–377[CrossRef][Web of Science][Medline] Bent AF, Kunkel BN, Dahlbeck D, Brown KL, Schmidt R, Giraudat J, Leung J, Staskawicz BJ (1994) RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. Science 265: 1856–1860 Bessire M, Chassot C, Jacquat A-C, Humphry M, Borel S, Petétot JM-C, Métraux J-P, Nawrath C (2007) A permeable cuticle in Arabidopsis leads to a strong resistance to Botrytis cinerea. EMBO J 26: 2158–2168[CrossRef][Medline] Bisgrove SR, Simonich MT, Smith NM, Sattler A, Innes RW (1994) A disease resistance gene in Arabidopsis with specificity for two different pathogen avirulence genes. Plant Cell 6: 927–933[Abstract] Century KS, Holub EB, Staskawicz BJ (1995) NDR1, a locus of Arabidopsis thaliana that is required for disease resistance to both a bacterial and a fungal pathogen. Proc Natl Acad Sci USA 92: 6597–6601 Century KS, Shapiro AD, Repetti PP, Dahlbeck D, Holub E, Staskawicz BJ (1997) NDR1, a pathogen-induced component required for Arabidopsis disease resistance. Science 278: 1963–1965 Chassot C, Métraux J-P (2005) The cuticle as source of signals for plant defense. Plant Biosyst 139: 28–31 Chassot C, Nawrath C, Metraux JP (2007) Cuticular defects lead to full immunity to a major plant pathogen. Plant J 49: 972–980[Web of Science][Medline] Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735–743[CrossRef][Web of Science][Medline] Dickman MB, Ha YS, Yang Z, Adams B, Huang C (2003) A protein kinase from Colletotrichum trifolii is induced by plant cutin and is required for appressorium formation. Mol Plant Microbe Interact 16: 411–421[CrossRef][Web of Science][Medline] Ferrari S, Plotnikova JM, De Lorenzo G, Ausubel FM (2003) Arabidopsis local resistance to Botrytis cinerea involves salicylic acid and camalexin and requires EDS4 and PAD2, but not SID2, EDS5 or PAD4. Plant J 35: 193–205[CrossRef][Web of Science][Medline] Frye CA, Innes RW (1998) An Arabidopsis mutant with enhanced resistance to powdery mildew. Plant Cell 10: 947–956 Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43: 205–227[CrossRef][Web of Science][Medline] Govrin EM, Levine A (2000) The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr Biol 10: 751–757[CrossRef][Web of Science][Medline] Grant MR, Godiard L, Straube E, Ashfield T, Lewald J, Sattler A, Innes RW, Dangl JL (1995) Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science 269: 843–846 Hellens RP, Edwards EA, Leyland NR, Bean S, Mullineaux PM (2000) pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol Biol 42: 819–832[CrossRef][Web of Science][Medline] Jones JD, Dangl JL (2006) The plant immune system. Nature 444: 323–329[CrossRef][Medline] Klement Z (1982) Hypersensitivity. In MS Mount, GH Lacy, eds, Phytopathogenic Procaryotes, Vol 2. Academic Press, New York, pp 149–177 Kunkel BN, Bent AF, Dahlbeck D, Innes RW, Staskawicz BJ (1993) RPS2, an Arabidopsis disease resistance locus specifying recognition of Pseudomonas syringae strains expressing the avirulence gene avrRpt2. Plant Cell 5: 865–875 Kunkel BN, Brooks DM (2002) Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol 5: 325–331[CrossRef][Web of Science][Medline] Kurdyukov S, Faust A, Nawrath C, Bar S, Voisin D, Efremova N, Franke R, Schreiber L, Saedler H, Metraux JP, et al (2006) The epidermis-specific extracellular BODYGUARD controls cuticle development and morphogenesis in Arabidopsis. Plant Cell 18: 321–339 Mackey D, Belkhadir Y, Alonso JM, Ecker JR, Dangl JL (2003) Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112: 379–389[CrossRef][Web of Science][Medline] Mackey D, Holt BF, Wiig A, Dangl JL (2002) RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108: 743–754[CrossRef][Web of Science][Medline] Morrissey JP, Osbourn AE (1999) Fungal resistance to plant antibiotics as a mechanism of pathogenesis. Microbiol Mol Biol Rev 63: 708–724 Schnurr J, Shockey J, Browse J (2004) The acyl-CoA synthetase encoded by LACS2 is essential for normal cuticle development in Arabidopsis. Plant Cell 16: 629–642 Shockey JM, Fulda MS, Browse JA (2002) Arabidopsis contains nine long-chain acyl-coenzyme A synthetase genes that participate in fatty acid and glycerolipid metabolism. Plant Physiol 129: 1710–1722 Sieber P, Schorderet M, Ryser U, Buchala A, Kolattukudy P, Metraux JP, Nawrath C (2000) Transgenic Arabidopsis plants expressing a fungal cutinase show alterations in the structure and properties of the cuticle and postgenital organ fusions. Plant Cell 12: 721–738 Simonich MT, Innes RW (1995) A disease resistance gene in Arabidopsis with specificity for the avrPph3 gene of Pseudomonas syringae pv. phaseolicola. Mol Plant Microbe Interact 8: 637–640[Web of Science][Medline] Stein M, Dittgen J, Sanchez-Rodriguez C, Hou BH, Molina A, Schulze-Lefert P, Lipka V, Somerville S (2006) Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 18: 731–746 Tang D, Ade J, Frye CA, Innes RW (2005) Regulation of plant defense responses in Arabidopsis by EDR2, a PH and START domain-containing protein. Plant J 44: 245–257[CrossRef][Web of Science][Medline] Tang D, Innes RW (2002) Overexpression of a kinase-deficient form of the EDR1 gene enhances powdery mildew resistance and ethylene-induced senescence in Arabidopsis. Plant J 32: 975–983[CrossRef][Web of Science][Medline] Thomma B, Eggermont K, Penninckx I, 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 Tornero P, Merritt P, Sadanandom A, Shirasu K, Innes RW, Dangl JL (2002) RAR1 and NDR1 contribute quantitatively to disease resistance in Arabidopsis, and their relative contributions are dependent on the R gene assayed. Plant Cell 14: 1005–1015 Warren RF, Henk A, Mowery P, Holub E, Innes RW (1998) A mutation within the leucine-rich repeat domain of the Arabidopsis disease resistance gene RPS5 partially suppresses multiple bacterial and downy mildew resistance genes. Plant Cell 10: 1439–1452 Wellesen K, Durst F, Pinot F, Benveniste I, Nettesheim K, Wisman E, Steiner-Lange S, Saedler H, Yephremov A (2001) Functional analysis of the LACERATA gene of Arabidopsis provides evidence for different roles of fatty acid omega-hydroxylation in development. Proc Natl Acad Sci USA 98: 9694–9699 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 Wright CA, Beattie GA (2004) Pseudomonas syringae pv. tomato cells encounter inhibitory levels of water stress during the hypersensitive response of Arabidopsis thaliana. Proc Natl Acad Sci USA 101: 3269–3274 Xiao F, Goodwin SM, Xiao Y, Sun Z, Baker D, Tang X, Jenks MA, Zhou JM (2004) Arabidopsis CYP86A2 represses Pseudomonas syringae type III genes and is required for cuticle development. EMBO J 23: 2903–2913[CrossRef][Web of Science][Medline] Xie DX, Feys BF, James S, Nieto-Rostro M, Turner JG (1998) COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280: 1091–1094 This article has been cited by other articles:
|
|||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| ASPB Publications | PLANT PHYSIOLOGY® | THE PLANT CELL | |
|---|---|---|---|
TOP
ABSTRACT
RESULTS
) (Simonich and Innes, 1995
