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First published online July 17, 2003; 10.1104/pp.103.025312 Plant Physiology 132:2230-2239 (2003) © 2003 American Society of Plant Biologists Molecular Characterization of a Novel Lipase-Like Pathogen-Inducible Gene Family of Arabidopsis1University of Fribourg, Department of Biology, Plant Biology, Route Albert-Gockel 3, 1700 Fribourg, Switzerland (G.J., A.M., J.-P.M.); Stanford University, Carnegie Institution of Washington, Department of Plant Biology, 260 Panama Street, Stanford, California 94305 (L.Z.); and University of Neuchâtel, Institute of Botany, Biochemistry, Rue Emile-Argand 9, Case Postale 2, CH–2007 Neuchâtel, Switzerland (B.M.-M.)
In a differential screening between Arabidopsis plants pretreated with the resistance-inducer  -aminobutyric acid and untreated control plants, we
have identified a gene encoding a novel lipase-like protein, PRLIP1.
The abundance of PRLIP1 mRNAs in Arabidopsis leaves was up-regulated
by application of -aminobutyric acid, salicylic acid (SA), and ethylene
as well as by various pathogens. Induction of PRLIP1 depended on a
functioning SA and ethylene signal transduction pathway but was independent of
jasmonate signaling. This novel pathogenesis-related (PR) gene of
Arabidopsis belongs to a gene family consisting of six (PRLIP1, PRLIP2,
PRLIP4, PRLIP5, PRLIP6, and PRLIP7) closely related members in
tandem position on chromosome 5. Among these genes, PRLIP2 also was
induced in leaves by SA and infections by pathogens but on a much lower level
than PRLIP1. The PRLIP1 family showed a tissue-specific
expression pattern. Both PRLIP1 and PRLIP2 were specifically
expressed in leaves and siliques, PRLIP1 additionally in stems and
flowers. The expression of PRLIP6 and PRLIP4 was root
specific, whereas mRNA of PRLIP5 and PRLIP7 were not
detected in any of these tissues. The more distantly related genes PRLIP3,
PRLIP9, and PRLIP8 were found on chromosomes 2, 4, and 5,
respectively. The expression level of PRLIP3 was checked and found
constitutive during the different stress conditions tested. The
PRLIP1 gene was overexpressed in Escherichia coli, and the
resulting PRLIP1 protein showed esterase activity on
p-nitrophenyl-butyrate and allowed the growth of the bacteria on
lipidic substrates such as Tween20 or Tween80.
During evolution, plants have developed various mechanisms to cope with numerous biotic and abiotic stresses. Beside constitutive barriers, plants can recognize a microbial invader early in the interaction and activate adequate defense responses. Rapid recognition of a pathogen is based on the presence of resistance (R) genes in the host, the products of which are presumed to interact with the products of avirulence (Avr) genes of the pathogen. This activates multiple signal transduction pathways finally leading to the induction of plant defenses (Dangl and Jones, 2001  ). At the cellular level, the result of pathogen
recognition often becomes apparent as a necrosis localized at the site of
attack, called the hypersensitive response, that is accompanied by various
cellular changes such as an oxidative burst leading to the release of active
oxygen species (ROI), a rise in salicylic acid (SA) levels, and the induction
of defense genes such as those coding for pathogenesis-related (PR) proteins
(Doke et al., 1996;
Mittler and Lam, 1996;
Dempsey et al., 1999;
van Loon and van Strien,
1999). Such a localized induced defense response often leads to
the activation of systemic resistance mechanisms effective against a large
number of pathogens (Sticher et al.,
1997). This type of resistance can be achieved by a pretreatment
with either necrotizing pathogens or chemical inducers of resistance (systemic
acquired resistance [SAR]; Ryals et al.,
1996) as well as by nonpathogenic rhizobacteria (induced systemic
resistance [ISR]; van Loon et al.,
1998). SAR and ISR can be distinguished with respect to the signal
transduction pathway required for the induction of defense. SAR is
SA-dependent leading to the induction of PR genes, whereas ISR
functions via a jasmonate (JA)/ethylene (ET)-dependent pathway
(Pieterse et al., 1998). The
latter pathway is also necessary for the induction of defense genes such as
plant defensins (Penninckx et al.,
1996).
Recently, genes with homology to lipases were found to be required for
SA-dependent induction of defense responses. For instance, the enhanced
disease susceptibility 1 (EDS1) gene encodes a protein that has
homology to the catalytic site of eukaryotic lipases
(Falk et al., 1999
In addition to SA, JA and ET also play important roles as signal molecules
mediating disease resistance, especially in response to necrotrophic fungal
pathogens (Penninckx et al.,
1996
Arabidopsis plants pretreated with the non-protein amino acid
Here, we describe the isolation by subtraction suppression hybridization of
a BABA-inducible gene, PRLIP1, and the biological and biochemical
characterization of this gene and its product. The predicted PRLIP1 amino acid
sequence has regions of similarity to Ser hydrolases (eukaryotic lipases and
esterases) similar to PAD4 (Jirage et al.,
1999
Description of the Gene Family
Subtractive suppression hybridization was used to detect changes in gene
expression after treatment with BABA, an inducer of resistance to pathogens
(Zimmerli et al., 2000
The catalytic triad typical for the esterase and lipase activity, which includes the amino acids Ser, Asp, and His, is conserved among all the PRLIPs (Fig. 2), strongly suggesting that these proteins have esterase or lipase activity. Comparison of PRLIPs with other known or predicted Ser hydrolases and lipases placed them in a separated branch of the phylogenetic tree (data not shown), indicating that PRLIPs are representing a novel protein family.
The gene structure of the PRLIPs is also characteristic for each subgroup. The first intron of the coding region is always present and has a conserved position (Fig. 2) not only in Arabidopsis but also in the rice orthologs. The second intron, however, has a subgroup-specific characteristic. In all subgroup I genes, it has been observed in a conserved position of a variable region of the PRLIP proteins (Fig. 2). Subgroup II or III genes have no second intron in both Arabidopsis and rice with the only exception of PRLIP9 (Fig. 2).
Increased expression of PRLIP1 and PRLIP2 genes after
BABA and BTH treatments was found in northern blots
(Fig. 3A) using
sequence-specific probes (Fig.
3B). The mRNA levels of PRLIP4, PRLIP5, PRLIP6, and
PRLIP7 in Arabidopsis leaves were too low to be detected.
PRLIP1 had a basal overall mRNA level in non-treated leaves of both
Arabidopsis accessions WS and Columbia (Col-0). Its expression was further
induced by BTH in both accessions and additionally by BABA in WS. In Col-0 the
mRNA of the PRLIP1 gene appeared to be longer. Besides a
19-nucleotide changes between the coding regions of the two accessions,
sequence analysis revealed the presence of an additional intron in the
3'-untranslated region of Col-0 where the acceptor site was mutated (AG
The expression pattern of the related gene from subgroup II, PRLIP3, localized at another genetic locus was tested and showed a constitutive expression level (Fig. 3A). Therefore further expression studies have been focused on the closely related genes of subgroup I. The induction of these PRLIP genes in Arabidopsis (Col-0) leaves after treatments with BABA, BTH, SA, ET, and methyl jasmonate (MeJA) was further investigated using real-time PCR to avoid the difficulties due to high sequence homologies and low mRNA levels (Fig. 4). The expression of PRLIP1 was induced by BTH, SA, and ET but not MeJA whereas PRLIP2 gene showed induction by BTH and SA only. A strong induction of both genes was observed after UV treatment but wounding had no effect (data not shown). PRLIP6 was induced by both ET and MeJA but not by SA and BTH (Fig. 4). Neither PRLIP4 nor PRLIP5 nor PRLIP7 mRNA was detected after these treatments.
Real-time PCR was also used to determine the constitutive expression of the PRLIP genes in various organs of Arabidopsis plants (Fig. 5). Both PRLIP1 and PRLIP2 were expressed in 2-week-old Arabidopsis seedlings as well as in leaves and in siliques, and PRLIP1 was also highly expressed in stems. The expression level of PRLIP2 was always lower than PRLIP1; it was very weak in stems and flowers, and similarly to PRLIP1, it remained undetected in roots. In contrast, PRLIP6 was only weakly expressed in seedlings, leaves, stems, flowers, and siliques, but was highly expressed in cultured roots. The expression of the PRLIP4 gene was above detection level in root tissues only, whereas PRLIP5 and PRLIP7 were below detection level in all organs (data not shown). Thus, the expression of both PRLIP1 and PRLIP2 presented predominance in green tissues with a stronger overall expression of PRLIP1, whereas PRLIP4 and PRLIP6 showed root preference in their expression. Therefore, PRLIP1 and PRLIP2 were retained for further analyses, because both were induced in leaves.
Inoculation of Arabidopsis (Col-0) with the avirulent Peronospora parasitica isolate EMWA led to a strong increase in the expression of PRLIP1 and PR1 that was detectable as early as 1 d after inoculation, whereas no change was observed in PRLIP2 expression (Fig. 6A). During the compatible interaction with P. parasitica isolate NOCO, an increase in expression of the three genes was only detected 3 to 5 d after inoculation (Fig. 6A). Infection with the virulent bacteria Pseudomonas syringae pv tomato (Pst) DC3000 induced PRLIP1 and PRLIP2 between 12 and 16 h postinoculation (hpi), whereas the expression of PR-1 was enhanced only 24 hpi (Fig. 6B).
Inoculation with the avirulent bacteria Pst avrRpt2 led to an
induction of PRLIP1 as early as 4 hpi, whereas the effect on
PR-1 expression was apparent only after 12 hpi
(Fig. 7). The response to
avirulent bacteria was abolished in Arabidopsis overexpressing the
NahG gene (Delaney et al.,
1994
To study the enzymatic activity of PRLIP proteins, PRLIP1 was selected from
this lipase-like gene family based on its expression pattern in response to
various inducers. Its cDNA isolated from Arabidopsis (Col-0) was inserted into
the multiple cloning site of the pGEX vector and expressed as a fusion protein
with glutathione S-transferase (GST). Escherichia coli cells
harboring this plasmid expressed a GST-PRLIP1 fusion protein of about 65 kD as
shown by the presence of a band of the predicted Mr in
homogenates of transformed bacteria (data not shown). To test for esterase
activity, the potential of transformed bacteria to grow on Tween20 or Tween80
was compared between GST-PRLIP1-expressing cells and control cells expressing
only GST (Hong et al., 2000
Plants respond to the different biotic stresses by a local and systemic induction of various novel proteins referred to as PR proteins (van Loon and van Strien, 1999 ). Some PR proteins may be effective in inhibiting pathogen
growth, multiplication and/or spread, whereas others may be responsible for
maintenance of SAR (Ryals et al.,
1996). Most PR proteins often are members of gene families and
exist in both basic and acidic isoforms
(Samac et al., 1990;
Brederode et al., 1991). Acidic
PR proteins are predominantly extracellular, and their expression is
characteristically induced after the accumulation of SA
(Malamy et al., 1990;
Métraux et al.,
1990).
In contrast to their acidic counterparts, many basic PR proteins do not
accumulate in response to SA or during the establishment of SAR. The
expression of basic PR proteins can be triggered by ET
(Brederode et al., 1991
First of all, the expression of PRLIP1 and PRLIP2 was
induced in Arabidopsis leaves infected with P. parasitica, P.
syringae pv tomato DC3000
(Fig. 6), and Phytophthora
brassicae (data not shown), whereas no induction was observed after
Botrytis cinerea infection (data not shown). The expression of
PRLIP1 but not PRLIP2 was induced during the incompatible
interaction with by P. syringae pv tomato avrRpt2, and the
accumulation of mRNA preceded that of PR-1
(Fig. 7), a widely used marker
for the SA pathway (Sticher et al.,
1997
Like other PRs, the PRLIP genes were also induced in
Arabidopsis upon ectopic treatments with various plant defense signals such as
SA, ET, or JA. For instance, PRLIP1 and PRLIP2 were induced
by SA in leaves, whereas PRLIP6 was induced in the same tissue by ET
and MeJA (Fig. 4). The
expression pattern of PRLIP1 placed this gene among the few ones
known to be influenced by both SA and ET
(Gu et al. 2000
The lipase-like proteins EDS1 and PAD4 have been shown to be important in
pathogen-induced accumulation of SA (Falk
et al., 1999
More is known about the role of lipases in JA-dependent defense signaling.
JA is produced through the octadecanoid pathway and is initiated by the
addition of molecular oxygen to linolenic acid
(Schaller, 2001
Recently, a phospholipase A1, defective in anther dehiscence1 (DAD1) was
identified and shown to be involved in JA biosynthesis
(Ishiguro et al., 2001
An ET-inducible gene has been reported recently in carnation encoding a
protein capable of deesterifying fatty acids from p-nitrophenyl
palmitate, tri-linolein, soybean phospholipids, and Tween
(Hong et al., 2000
Recent studies suggest that cross-talk between SA-, JA- and ET-dependent
signaling pathways fine-tunes plant defense responses
(Glazebrook, 2001
Biological Material
Arabidopsis mutants npr1, cpr1, jar1, and
etr1 (all in Col-0 background) were obtained from X. Dong (Duke
University, Durham, NC), P.E. Staswick (University of Nebraska, Lincoln), and
the Nottingham Arabidopsis Stock Center (UK), respectively. A transgenic line
of Arabidopsis (Col-0) harboring the NahG gene
(Delaney et al., 1994
Strain DC 3000 of Pseudomonas syringae pv tomato and the
isogenic strain carrying the Avr gene avrRpt2 were cultivated at
28°C, 235 rpm in King's medium B containing rifampicin for selection as
described earlier (Zimmerli et al.,
2000 For bacterial inoculation, cells were collected by centrifugation, resuspended in 10 mM MgCl2 to an approximate concentration of 105 colony forming units mL-1. Three leaves per plant were infiltrated using a 1-mL syringe without needle. Tissue samples were harvested from inoculated leaves at the indicated time points, flash frozen in liquid N2, and kept at -80°C until further use. Plants were inoculated with Peronospora parasitica by spraying with a suspension of 105 conidia mL-1 water until shortly before run-off occurred. Inoculated plants were kept at 20°C in a 12-h/12-h light/dark cycle and during the 1st d of the growth cycle at 100% relative humidity to ensure infection. To produce new inoculum, 6 d after inoculation, plants were placed back to 100% relative humidity for 1 d to induce sporulation.
BABA (Fluka, Buchs, Switzerland) and BTH (Novartis) were dissolved in water
(300 µM) and applied as soil drench as described earlier
(Zimmerli et al. 2000
RNA was isolated from frozen tissue samples as described previously
(Zimmerli et al., 2000
The PCR-Select cDNA Subtraction kit (BD Biosciences Clontech, Palo Alto, CA) was used according to manufacturer's instructions. The obtained PCR products were separated on sequencing PAGE, and the bands were stained by silver. The selected bands showing differential expression were excised and incubated in 100 µL of TE buffer overnight. The redissolved DNA was than reamplified using the same primer pair it was obtained with.
The ABI Prism 7700 Sequence Detection System (Applied Biosystems, Foster
City, CA) was used according to the manufacturer's instructions. The reverse
transcription reactions were performed using 2 µg of total RNA,
oligo(dT)18 primer, and the Omniscript kit (Qiagen, Hilden,
Germany). The resulting cDNA solution was then diluted with water up to 1 mL.
In the PCR reactions, 10 µL of this cDNA solution, 300 nM of
each primers, and SYBR Green PCR Master Mix (Applied Biosystems) were used in
a 50-µL final volume. The
For heterologous expression of the GST-PRLIP1 fusion protein in E. coli, the pGEX-5X-1 vector (Amersham Biosciences, Uppsala) was used. The full-length coding region of PRLIP1 cDNA was obtained by PCR amplification using a 1:1 mixture of the Pfu and TaqDNA polymerases (Promega, Madison, WI) and the primers PRLIP1/5'Bam: 5'-CGGATCCACGAAAATTGGAAGGAGG and PRLIP1/3'Bam: 5'-CGGATCCTTAACAAATTATTCAGTTGACAAG. The fragment was inserted at the BamHI site of the vector and the construct was verified by sequencing (Microsynth, Balgach, Switzerland). To obtain 6x-His-tagged PRLIP1 protein, the cDNA was reinserted into the BamHI site of the pQE-30 vector (Qiagen).
E. coli BL-21 cells were transformed with these
constructs, and protein was extracted from the sonicated bacteria by B-PER
Bacterial Protein Extraction Reagent (Pierce, Rockford, IL). To purify the
6x-His-PRLIP1, protein inclusion bodies were solubilized using B-PER
supplemented with 8 M urea. The 6x-His-tagged protein was then
bound on a TALON Resin column (BD Biosciences Clontech) in the same buffer.
The refolding of the denatured protein was done on the column by stepwise
reduction of the concentration of urea to 0 M. The folded protein
was eluted with 100 mM imidazole in 0.1 M phosphate
buffer, pH 7. Protein concentrations were measured according to Bradford
(1976
SDS-PAGE was performed according to Laemmli
(1970
Bacteria were grown in M9 minimal medium
(Sambrook et al., 1989
Triacylglycerol lipase activity was tested according to MacKenzie et al.
(1967
We thank J. Ryals (Novartis) for the cDNA of PR-1, and we are grateful to C. Nawrath (University of Fribourg, Switzerland) for the organ-specific RNA samples of Arabidopsis. We thank L. Sticher and F. Mauch (University of Fribourg, Switzerland) for the critical reading of this manuscript. Received April 11, 2003; returned for revision May 14, 2003; accepted May 14, 2003.
1 This work was supported by the Swiss National Foundation (grant nos. 3100–049279.96 to B.M.M. and 3100–055662.98 to J.-P.M.).  * Corresponding author; e-mail brigitte.mauch{at}unine.ch; fax 41–32–718–2201.
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12920-12925 This article has been cited by other articles:
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TOP
ABSTRACT
RESULTS
-helix around the S residue are indicated with a line above the
sequence. The position of introns are indicated by lowercase letters. The
first intron is present in position a in all genes except in PRLIP8
where it is shifted downstream to position b; the second intron of
PRLIP9 is in position c; whereas all genes of subgroup I have the
second intron in position d. PRLIP3 and PRLIP8 have no
second intron.
GG), thus impairing its splicing (data not shown). The PRLIP2
gene had no detectable basal expression and was also inducible by BTH (both WS
and Col-0) and BABA (WS; 
1 and lysoPL1 are
specifically upregulated during gene-for-gene interactions and upon SA
treatment. 
