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Plant Physiol. (1998) 116: 1037-1042
Differential Expression of a Novel Gene in Response to
Coronatine, Methyl Jasmonate, and Wounding in the Coi1
Mutant of Arabidopsis1
Celso E. Benedetti*,
Cinthia L. Costa,
Silvia R. Turcinelli, and
Paulo Arruda
Centro de Biologia Molecular e Engenharia
Genética-Universidade Estadual de Campinas, Campinas,
São Paulo 13083-970, Brazil (C.E.B., C.L.C., S.R.T., P.A.); and Departamento de Genética e Evolução, Instituto
de Biologia, Universidade Estadual de Campinas, 13083-970, Campinas,
São Paulo, Brazil (P.A.)
 |
ABSTRACT |
Coronatine is a phytotoxin produced
by some plant-pathogenic bacteria. It has been shown that coronatine
mimics the action of methyl jasmonate (MeJA) in plants. MeJA is a
plant-signaling molecule involved in stress responses such as wounding
and pathogen attack. In Arabidopsis thaliana, MeJA is
essential for pollen grain development. The coi1 (for
coronatine-insensitive) mutant of Arabidopsis,
which is insensitive to coronatine and MeJA, produces sterile male
flowers and shows an altered response to wounding. When the
differential display technique was used, a message that was rapidly
induced by coronatine in wild-type plants but not in
coi1 was identified and the corresponding cDNA was
cloned. The coronatine-induced gene ATHCOR1 (for
A. thaliana coronatine-induced) is expressed in seedlings, mature
leaves, flowers, and siliques but was not detected in roots. The
expression of this gene was dramatically reduced in coi1
plants, indicating that COI1 affects its expression.
ATHCOR1 was rapidly induced by MeJA and wounding in
wild-type plants. The sequence of ATHCOR1 shows no
strong homology to known proteins. However, the predicted polypeptide
contains a conserved amino acid sequence present in several bacterial,
animal, and plant hydrolases and includes a potential
ATP/GTP-binding-site motif (P-loop).
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INTRODUCTION |
JA and its methyl ester, MeJA, and related compounds derived from
linolenic acid are recognized as signaling molecules synthesized by
plants in response to wounding and herbivore and pathogen attack (Creelman et al., 1992 ; Farmer and Ryan, 1992; Mueller et al., 1993).
These substances can activate the expression of several genes, leading
to the accumulation of their products, which are referred to as
jasmonate-induced proteins. The best-studied jasmonate-induced proteins
include proteinase inhibitors, thionins, vegetative storage proteins,
lipoxygenases, ribosome-inactivating proteins, enzymes of
phenylpropanoid metabolism, and others (Koda, 1992; for review, see
Reinbothe et al., 1994). The jasmonates can also repress the expression
of genes related to photosynthesis at the transcriptional and
translational levels (Reinbothe et al., 1994). It has been demonstrated
that MeJA induces a shift in the length of the plastid rbcL
transcript in barley, thus impairing translation initiation (Reinbothe
et al., 1993). However, little is known about the mechanisms by which
jasmonates control gene expression and the signal cascade that mediates
this response. New evidence suggests that protein phosphorylation is
required for the activation of certain wound-inducible genes that
respond to JA (Damman et al., 1997).
Coronatine is a phytotoxin produced by several pathovars of
Pseudomonas syringae (Ichihara et al., 1977; Mitchell and
Young, 1978; Mitchell, 1982). Its biological effects include induction of leaf chlorosis and inhibition of root growth (Nishiyama et al.,
1976; Ferguson and Mitchell, 1985; Kenyon and Turner, 1990), and it has
been suggested to play a role in disease development as a virulence
factor produced by the bacteria during infection. Mutations that
abolished coronatine production in P. syringae pv
tomato reduced the capacity of this pathogen to produce
necrotic lesions on tomato (Lycopersicon esculentum) leaves
(Bender et al., 1987). Moreover, coronatine production was required for
the successful infection of Arabidopsis leaves by P. syringae pv tomato, and this was attributed to the
suppression of defense-related genes by the toxin (Mittal and Davis,
1995).
Coronatine acts as a mimic of MeJA in plants (Weiler et al., 1994), and
the Arabidopsis thaliana mutant insensitive to coronatine (coi1) is also insensitive to MeJA and is male sterile (Feys
et al., 1994; Benedetti et al., 1995). In addition, coi1
plants are more sensitive to wounding than are the wild type, but they
are resistant to P. syringae infection (Feys et al., 1994).
These findings suggest that both coronatine and MeJA may interact with a common receptor and that MeJA is required for pollen development and
mediates at least part of the wound response. However, there is
evidence that one of the MeJA responses in Arabidopsis is needed to
induce the symptoms caused by a coronatine-producing strain of P. syringae (Feys et al., 1994). This apparent paradox remains to be
clarified, since MeJA is suggested to play a role in plant-defense responses (Coehn et al., 1993; Mueller et al., 1993; Reinbothe et al.,
1994). Nevertheless, no correlation could be found between jasmonates
and defense responses in plant-pathogen interactions (Schweizer et al.,
1993; Kogel et al., 1995; Schweizer et al., 1997). How coronatine could
function as a virulence factor by mimicking MeJA in a bacteria-plant
interaction is an open question.
In an attempt to clarify this issue we are studying coronatine and MeJA
responses in Arabidopsis by identifying genes that are rapidly
activated by coronatine, MeJA, or wounding. To detect and clone such
genes we are using the mRNA differential display technique (Liang and
Pardee, 1992). We present here the initial characterization of a novel
Arabidopsis gene that is induced by coronatine, MeJA, and wounding, the
expression of which is affected by the COI1 gene.
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MATERIALS AND METHODS |
Biological Material and Chemicals
Wild-type Arabidopsis thaliana ecotype
Columbia (Col-0) was used. The coi1 mutant was described
previously (Feys et al., 1994) and was donated by Dr. John G. Turner
(University of East Anglia, UK). Coronatine and MeJA were obtained as
previously described (Feys et al., 1994).
Plant Growth
Seeds of wild-type Arabidopsis were germinated in MS medium
(Murashige and Skoog, 1962), whereas coi1 seeds from an
F2 population segregating for the Coi phenotype
were first germinated in MS containing 1 µm coronatine to
select for homozygous coi1 plants. Seedlings were grown in
white light (70 µE m 2
s1) for 1 week in a growth cabinet with a 16-h
day/8-h night photoperiod at 22°C, after which they were transferred
to fresh MS and grown for another 1 week. Seedlings were then either
transferred to fresh MS for coronatine and MeJA treatments or moved to
soil to grow to maturity.
Coronatine and MeJA Treatments
Two-week-old seedlings were transferred to MS (control seedlings)
or MS containing either 1 µm coronatine or 10 µm MeJA. After different periods of incubation, they were
frozen in liquid nitrogen and total RNA was extracted.
Wounding
For the wounding experiment, seeds were germinated in MS and grown
for 2 weeks under short-day conditions (9-h day/15-h night at 22°C).
Seedlings were then transferred to soil and grown for 2 weeks. Leaves
of individual plants were wounded once with scissors. After the
treatment, plants were returned to the growth cabinet, and wounded
leaves were collected at different times, frozen in liquid nitrogen,
and stored at  70°C for RNA extraction.
RNA Extraction and Differential Display
Total RNA from roots, seedlings, leaves, flowers, siliques, and
wounded leaves was extracted according to the method of Verwoerd et al.
(1989).
Differential display of mRNA was performed according to the method of
Liang and Pardee (1992), with minor modifications. Total RNA (1 µg)
from control and coronatine-treated seedlings of wild-type and
coi1 plants were reverse transcribed with 100 units of
reverse transcriptase in the presence of 2.5 µm
T12VN as anchored primers and 20 µm
dNTPs for 10 min at 25°C, followed by a 50-min incubation at 37°C.
Two microliters of the reaction was then added to 18 µL of the PCR
mixture consisting of 1× PCR buffer, 1.25 mm
MgCl2, 1 µm anchored primer
(T12VN), 1 µm arbitrary primer
(10-mer from Operon, Alameda, CA), 2.0 µm dNTPs, 10 µCi
[ -33P]ATP, and 1.5 units of Taq
polymerase. PCR conditions were 40 cycles of 94°C for 30 s,
40°C for 2 min, and 72°C for 30 s, followed by 5 min of
elongation at 72°C. PCR products were analyzed on a 6% acrylamide
denaturing DNA-sequencing gel. Gels were dried at 80°C for 2 h,
and radiographic films were aligned to them and exposed overnight at
70°C. Differentially displayed bands were cut off and eluted in 200 µL of water at 95°C for 15 min. DNA was ethanol precipitated to
remove urea and reamplified by PCR using the same conditions as above,
except that the final concentration of dNTPs was 20 µm.
Reamplified DNA was analyzed on agarose gels, and bands of the expected
size were purified and cloned into pMOSBlue vector (Amersham). Cloned
fragments were sequenced and used to probe RNA blots and to screen a
cDNA library of Arabidopsis flowers.
Northern Analysis
Total RNA (20 µg of each sample) was electrophoresed on
formaldehyde-agarose gels (Sambrook et al., 1989), transferred onto nylon membranes (Hybond N+, Amersham) by capillary blot,
and fixed by UV cross-linking according to the manufacturer's
instructions. Blots were hybridized using the cloned fragments obtained
from the display gels or fragments of the full-length cDNA clones as
probes. Membranes were washed twice with 2.0× SSC containing 0.1% SDS
for 10 min at 42°C and twice with 0.2× SSC containing 0.1% SDS for
10 min at 42°C.
cDNA Library Screening
A cDNA library of Arabidopsis (ecotype Landsberg erecta) flowers
constructed in Lambda Zap II cloning vector (Stratagene) was kindly
donated by Dr. Elliot M. Meyerowitz (California Institute of
Technology, Pasadena). The library was screened following the manufacturer's protocols using the cloned fragments that showed differential expression as probes on northern analysis.
RACE
The 5 end of the isolated cDNA was cloned by RACE according to
the method of Frohman et al. (1988). Total RNA from wild-type flowers
and from MeJA- and coronatine-treated seedlings was reverse transcribed
using the P1 primer (5-CCATTCTTACACATACAACC-3). First-strand cDNA was
purified and amplified by PCR using P1 and the
(dT17)-adaptor primer (Frohman et al., 1988).
After 20 PCR cycles (94°C for 30 s, 45°C for 1 min, and 72°C
for 1 min), an aliquot was reamplified using the internal P2 primer
(5-CGTGATGGATGGGTCTAATG-3) and the adapter primer in 20 PCR cycles of
94°C for 30 s, 55°C for 1 min, and 72°C for 1 min (Frohman
et al., 1988). PCR fragments were gel purified, cloned into pMOSBlue
vector (Amersham), and sequenced.
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RESULTS |
A DNA fragment of about 280 bp was detected by differential
display in wild-type but not coi1 seedlings upon induction
with coronatine (not shown). DNA from the corresponding region of the display gel was reamplified, cloned, and sequenced.
This clone, TGCOPP9-280, was used to probe a northern blot of total
RNA extracted from seedlings and flowers of wild-type and
coi1 mutant plants (Fig. 1).
The probe confirmed the differential expression of a major transcript
of approximately 1.3 kb that was induced by coronatine in wild-type but
not in coi1 seedlings. Apparently, two transcripts of
similar molecular weight were also detected in lower levels in
untreated wild-type seedlings and flowers but not in male sterile
flowers of coi1 (Fig. 1).
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| Figure 1.
Northern analysis of total RNA extracted from
flowers and seedlings of wild-type (wt) and coi1 mutant
seedlings (coi) growing in MS or in MS containing 1 µm
coronatine (Cor) for 4 h, hybridized with TGCOPP9-280. The
display probe detected a major transcript of about 1.3 kb that is
induced by coronatine in wild-type but not coi1
seedlings. Transcripts of similar molecular weight are observed in
lower levels in seedlings and flowers of the wild type but not in
male-sterile flowers of coi1. The position of the
16S ribosomal band is indicated.
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The clone TGCOPP9-280 was used to screen a cDNA library from
Arabidopsis flowers. Five independent cDNA clones were isolated and
sequenced. The sequences of all clones were identical and contained the
entire sequence of TGCOPP9-280. However, unexpectedly, we found that
the anchored primer T12GC did not prime at the
poly(A+) tail of the mRNA but within the gene in
an A-rich region. In addition, all of the isolated cDNAs were truncated
at their 5 ends. To obtain a full-length clone, the 5 end of the gene
was generated by RACE from mRNAs extracted from flowers or seedlings treated with either coronatine or MeJA. The sequences of these different RACE products were identical, indicating that the transcripts induced by coronatine or MeJA and those expressed in flowers were the
same. The RACE products were also identical to the corresponding 5 end
of the cDNAs isolated from the library, except they contained an extra
50 bp in their 5 ends (Fig. 2). A
full-length cDNA clone was then obtained by ligating the 5 end of the
RACE product to the original cDNA isolated from the library using a
SacI site upstream of the P2 primer (not shown). The
resulting clone, ATHCOR1 (Arabidopsis
thaliana
coronatine-induced gene 1, accession no. AF021244), was
chosen for further analysis.
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| Figure 2.
Sequence of ATHCOR1 cDNA (AF021244) and its
predicted protein. The 5 end of the untranslated sequence obtained
from mRNAs by RACE is underlined. The first guanosine residue was not
found in the genomic clone (not shown) and was interpreted as the mRNA cap. Amino acids in bold represent a possible
N-glycosylation site and the bold, underlined sequence
represents a potential ATP-/GTP-binding site motif A (P-loop).
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The sequence of ATHCOR1 cDNA has 1172 bp and may encode a novel protein
of 324 amino acids with a molecular mass of 34.8 kD (Fig. 2). The
predicted polypeptide has no significant homology to other proteins in
the database, except in two small and conserved domains (A and B) found
in microbial, plant, and mammalian hydrolases. These include the
Synechocystis sp. dienelactone hydrolase,
Moraxela sp. haloacetate dehalogenase, guinea pig
platelet-activating factor acetylhydrolase, and epoxide hydrolases from
soybean, potato, and Arabidopsis (Fig.
3). In the literature, no biochemical
function has been attributed to domain A in these different hydrolases; however, domain B is a potential ATP-/GTP-binding site known as the
P-loop, which is common to many ATP-/GTP-binding proteins (Saraste et
al., 1990).
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| Figure 3.
Protein alignments between regions of the
translated peptide from ATHCOR1 with two conserved domains (A and B)
found in different hydrolases. SHAF, Similar to human-activating factor
acetylhydrolase from C. elegans, U64598; PAF,
platelet-activating factor acetylhydrolase from Cavia
porcellus, JC5021; HDH, haloacetate dehalogenase from Moraxella sp., A44856; Mtu, unknown Mycobacterium
tuberculosis Z95389; AtsEH, Arabidopsis epoxide hydrolase,
D16628; GlyEH, soybean epoxide hydrolase, D63781; and DLH, dienelactone
hydrolase from Synechocystis sp. dienelactone hydrolase,
D90904. Black boxes indicate conserved amino acids at the minimum of
50%. Gray boxes indicate changes by similar residues. The percentage
of similarity between ATHCOR1 and each of the sequences is presented.
The consensus for the putative ATP-/GTP-binding site described in the
literature (Saraste et al., 1990) is indicated by an asterisk.
Sequences were aligned by the CLUSTAL W program (Thompson et al., 1994) and shaded by the BOXSHADE program (used at the Bioinformatics Group
WWW site at the Swiss Institute for Experimental Cancer Research,
Lousanne, Switzerland).
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Northern blots using ATHCOR1 as a probe confirmed the same pattern of
coronatine induction observed with the TGCOPP9-280 probe shown in
Figure 1, except that the cDNA detected a single, approximately 1.3-kb
band on northern analysis. To determine whether this gene was also
induced by MeJA, wild-type and coi1 seedlings were grown in
the presence of 10 µm MeJA, which produces the same
phenotype as 1 µm coronatine (e.g. inhibition of root
growth and anthocyanin accumulation; Feys et al., 1994). Figure
4 shows that the gene is rapidly induced
by MeJA and that high levels of the transcript accumulate in the first
4 h of treatment. A similar pattern of induction was observed with
1 µm coronatine; however, the toxin was apparently a less
efficient inducer of the gene in comparison with MeJA (Fig. 4).
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| Figure 4.
Time-course induction of total RNA extracted from
seedlings of wild-type Arabidopsis growing in MS medium (Control) or MS containing 1 µm coronatine (Cor) or 10 µm
MeJA. ATHCOR1 was rapidly induced by MeJA after 30 min
of induction. A weaker induction of ATHCOR1 was observed
with coronatine treatment. A background hybridization with the
28S ribosomal band is shown.
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ATHCOR1 was used to probe northern blots of total RNA extracted from
different plant organs (Fig. 5). The
coronatine-/MeJA-induced gene was normally expressed in low levels in
young and mature leaves and was apparently expressed in higher levels
in flowers, but not detected at all in roots. Its expression was
dramatically reduced in all tissues of coi1 plants (Fig. 5).
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| Figure 5.
A, Northern analysis of total RNA extracted from
different organs of wild-type (wt) and coi1
(coi1) mutant plants. ATHCOR1 is normally
expressed in seedlings (S), young (L) and mature (M) leaves, flowers
(F), and siliques (Si), but it could not be detected in roots (R). Very
low levels of the corresponding transcript were detected in
coi1 tissues. B, Total RNA stained with ethidium bromide
before being transferred onto the membrane.
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Wounding of wild-type leaves produced a rapid induction of
ATHCOR1 (Fig. 6). Its
expression peaked about 30 min after wounding and returned to basal
levels in the following 4 h. Wounded leaves of coi1
showed a similar pattern of induction, but transcripts accumulated at
much lower levels (Fig. 6).
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| Figure 6.
A, Northern analysis of total RNA extracted from
leaves of wild-type (wt) and coi1
(coi1) mutant plants after wounding.
ATHCOR1 was highly induced in wild-type leaves by
wounding. Its expression peaked about 30 min after leaves were injured
and decreased to normal levels after the first 4 h. The same
pattern of induction was observed in the leaves of coi1,
although at much lower levels. B, Total RNA stained with ethidium
bromide before being transferred onto the membrane.
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DISCUSSION |
The coi1 mutant of Arabidopsis has proved to be an
excellent model for the identification and analysis of coronatine- and MeJA-responsive genes. By means of differential display we have successfully identified ATHCOR1, a novel Arabidopsis gene
that is induced by the phytotoxin coronatine in wild-type plants but not in the coi1 mutant. ATHCOR1 is expressed in
leaves, flowers, and siliques, but it could not be detected in roots.
Treatment with MeJA or wounding also increased its expression in
wild-type but not in coi1 plants. However, the time-course
induction of ATHCOR1 by exogenously applied MeJA was
different from that of wounding, which seems to follow a transient
stimulus.
ATHCOR1 has no strong similarities to other proteins, except in two
conserved domains present in several hydrolases, including the
dienelactone hydrolase, haloacetate dehalogenase, epoxide hydrolase,
and acetylhydrolase. Epoxide hydrolase is the only one that has been
described in plants. The microbial dienelactone hydrolase hydrolyzes
dienelactone to maleylacetate and has esterase activity toward other
substrates (Pathak et al., 1991; Beveridge and Ollis, 1995).
Haloacetate dehalogenase acts specifically on halogenated acetates to
yield glycolate as a carbon source in microorganisms (Kawasaki et al.,
1992). Epoxide hydrolase catalyzes the conversion of epoxides to diols.
In plants epoxide hydrolase has been suggested to play a role in the
biosynthesis of monomers of cutin, a polymer that accumulates in the
cell wall of wounded tissues (Kolattukudy, 1984; Blée and
Schuber, 1993).
An epoxide hydrolase from A. thaliana (AtsEH) has been
cloned (Kiyosue et al., 1994). AtsEH is only 20% similar to ATHCOR1 and is not expressed in flowers (Kiyosue et al., 1994). However, an
epoxide hydrolase from potato, which is highly homologous to AtsEH, is
induced by MeJA and wounding (Stapleton et al., 1994). Since
ATHCOR1 is rapidly expressed in response to wounding, and because its expression is significantly reduced in coi1
plants, which are more sensitive to wounding, we speculate that this
gene may be important in the process of healing injured tissue. It is
possible that ATHCOR1 belongs to a family of related enzymes involved
in the biosynthesis/hydrolysis of plant cell wall components. ATHCOR1 may also function during anther development, since
male sterile-flowers of coi1 have much lower levels of its
transcripts.
It is interesting to note that the predicted protein of
ATHCOR1 has a potential ATP-/GTP-binding site. This would
suggest that the protein could hydrolyze ATP or GTP to exert its
function or it could simply be modulated by the binding of nucleotides in a regulatory fashion. We are currently investigating these possibilities. Further characterization of ATHCOR1 will be
necessary to understand its function and regulation by MeJA, as well as its possible role in the wounding response and perhaps in disease development of Arabidopsis infected by coronatine-producing strains of
P. syringae.
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FOOTNOTES |
1
This work was supported by grant no. 95/6662-5
from Fundação de Amparo à Pesquisa do Estado de
São Paulo. C.E.B. received a fellowship from Conselho Nacional de
Desenvolvimento Cientifico e Tecnológico (no. 300764/95-2) and
Fundação de Amparo à Pesquisa do Estado de São
Paulo (no. 97/0917-7). C.L.C. received a fellowship from
Fundação de Amparo à Pesquisa do Estado de São
Paulo (96/10274-3).
*
Corresponding author; e-mail benedett{at}turing.unicamp.br; fax
55-19-788-2193.
Received September 2, 1997;
accepted November 19, 1997.
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ABBREVIATIONS |
Abbreviations:
dNTP, deoxyribonucleotide triphosphate.
JA, jasmonic acid.
MeJA, methyl jasmonate.
MS, Murashige-Skoog.
RACE, rapid
amplification of cDNA ends.
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ACKNOWLEDGMENTS |
We wish to thank Dr. John G. Turner for donating the
coi1 mutant and Dr. Elliot M. Meyerowitz for providing the
Arabidopsis cDNA library. We also thank Dr. Adilson Leite and Dr. Ivan
Maia for their helpful discussions.
| |
LITERATURE CITED |
Bender CL,
Stone HE,
Sims JJ,
Cookey DA
(1987)
Reduced pathogen fitness of Pseudomonas syringae pv tomato Tn5 mutants defective in coronatine production.
Physiol Mol Plant Pathol
30:
273-283
Benedetti CE,
Xie D,
Turner JG
(1995)
COI1-dependent expression of an Arabidopsis vegetative storage protein in flowers and siliques and in response to coronatine and methyl jasmonate.
Plant Physiol
109:
567-572
[Abstract]
Beveridge AJ,
Ollis DL
(1995)
A theoretical study of substrate-induced activation of dienelactone hydrolase.
Protein Eng
8:
135-142
[Abstract/Free Full Text]
Blée E,
Schuber F
(1993)
Biosynthesis of cutin monomers: involvement of a lipoxygenase/peroxygenase pathway.
Plant J
4:
113-123
Coehn Y,
Gisi U,
Niderman T
(1993)
Local and systemic protection against Phytophthora infestans induced in potato and tomato plants by jasmonic acid and jasmonic methyl ester.
Phytopathology
83:
1054-1062
Creelman RA,
Tierney ML,
Mullet JE
(1992)
Jasmonic acid/methyl jasmonate accumulate in wounded soybean hypocotyls and modulate wound gene expression.
Proc Natl Acad Sci USA
89:
4938-4941
[Abstract/Free Full Text]
Damman C,
Rojo E,
Sánches-Serrano JJ
(1997)
Abscisic acid and jasmonic acid activate wound-inducible genes in potato through separate, organ-specific signal transduction pathways.
Plant J
11:
773-782
[CrossRef][Web of Science][Medline]
Farmer EE,
Ryan CA
(1992)
Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase inhibitors.
Plant Cell
4:
129-134
[Abstract/Free Full Text]
Ferguson IB,
Mitchell RE
(1985)
Stimulation of ethylene production in bean leaf discs by the pseudomonad phytotoxin coronatine.
Plant Physiol
77:
969-973
[Abstract/Free Full Text]
Feys BJ,
Benedetti CE,
Penfold CN,
Turner JG
(1994)
Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen.
Plant Cell
6:
751-759
[Abstract/Free Full Text]
Frohman MA,
Dush MK,
Martin GR
(1988)
Rapid production of full-length cDNAs from rare transcripts: amplification using single gene-specific oligonucleotide primer.
Proc Natl Acad Sci USA
85:
8998-9002
[Abstract/Free Full Text]
Ichihara A,
Shiraishi K,
Sato H,
Sakamura K,
Nishiyama K,
Sakai R,
Furusaki A,
Matsumoto T
(1977)
The structure of coronatine.
J Am Chem Soc
99:
636-637
[CrossRef]
Kawasaki H,
Tsuda K,
Matsushita I,
Tonomura K
(1992)
Lack of homology between two haloacetate dehalogenase genes encoded on a plasmid from Moraxella sp. strain B.
J Gen Microbiol
138:
1317-1323
[Abstract/Free Full Text]
Kenyon JS,
Turner JG
(1990)
Physiological changes in Nicotiana tabacum leaves during development of chlorosis caused by coronatine.
Physiol Mol Plant Pathol
37:
463-477
Kiyosue T,
Beetham JK,
Pinot F,
Hammock BD,
Yamaguchi-Shinozaki K,
Shinozaki K
(1994)
Characterization of an Arabidopsis cDNA for a soluble epoxide hydrolase gene that is induced by auxin and water stress.
Plant J
6:
259-269
[CrossRef][Web of Science][Medline]
Koda Y
(1992)
The role of jasmonic acid and related compounds in the regulation of plant development.
Int Rev Cytol
135:
155-199
[Web of Science][Medline]
Kogel KH,
Ortel B,
Jarosch B,
Atzorn R,
Schiffer R,
Wasternack C
(1995)
Resistance in barley against the powdery mildew fungus (Erysiphe graminis f. sp. hordei) is not associated with enhanced levels of endogenous jasmonates.
Eur J Plant Pathol
101:
319-332
Kolattukudy PE
(1984)
Biochemistry and function of cutin and suberin.
Can J Bot
62:
2918-2933
Liang P,
Pardee AB
(1992)
Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction.
Science
257:
967-971
[Abstract/Free Full Text]
Mitchell RE
(1982)
Coronatine production by some phytopathogenic pseudomonads.
Physiol Mol Plant Pathol
20:
83-89
Mitchell RE,
Young H
(1978)
Identification of a chlorosis-inducing toxin of Pseudomonas glycinea as coronatine.
Phytochemistry
17:
2028-2029
[CrossRef]
Mittal S,
Davis KR
(1995)
Mol Plant-Microbe Interact
8:
165-171
[Medline]
Mueller MJ,
Brodschelm W,
Spannagl E,
Zenk MH
(1993)
Signaling in the elicitation process is mediated through the octadenoid pathway leading to jasmonic acid.
Proc Natl Acad Sci USA
90:
7490-7494
[Abstract/Free Full Text]
Murashige T,
Skoog F
(1962)
A revised medium for rapid growth and bioassays with tobacco tissue culture.
Physiol Plant
15:
493-497
Nishiyama K,
Sakai R,
Ezuka A,
Ichihara A,
Shiraishi K,
Ogosawara M,
Sato H,
Mamura S
(1976)
Phytotoxic effect of coronatine produced by Pseudomonas coronafaciens var. atropurpurea on leaves of Italian ryegrass.
Ann Phytopathol Soc Jpn
42:
613-614
Pathak D,
Ashley G,
Ollis D
(1991)
Thiol protease-like active site found in the enzyme dienolactone hydrolase: localization using biochemical, genetic, and structural tools.
Proteins
9:
267-279
[CrossRef][Medline]
Reinbothe S,
Mollenhauer B,
Reinbothe C
(1994)
JIPs and RIPs: the regulation of plant gene expression by jasmonates in response to environmental cues and pathogens.
Plant Cell
6:
1197-1209
[CrossRef][Web of Science][Medline]
Reinbothe S,
Reinbothe C,
Heintzen C,
Seidenbecher C,
Parthier B
(1993)
A methyl jasmonate-induced shift in the length of the 5 untranslated region impairs translation of the plastid rbcL transcript in barley.
EMBO J
12:
1505-1512
[Web of Science][Medline]
Sambrook J,
Fritsch EF,
Maniatis T
(1989)
Molecular Cloning: A Laboratory Manual, Ed 2.
Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
Saraste M,
Sibbald PR,
Wittinghofer A
(1990)
The P-loop a common motif in ATP- and GTP-binding proteins.
Trends Biochem Sci
15:
430-434
[CrossRef][Web of Science][Medline]
Schweizer P,
Buchala A,
Silverman P,
Seskar M,
Raskin I,
Métraux J-P
(1997)
Jasmonate-inducible genes are activated in rice by pathogen attack without a concomitant increase in endogenous jasmonic acid levels.
Plant Physiol
114:
79-88
[Abstract]
Schweizer P,
Gees R,
Mösinger E
(1993)
Effects of jasmonic acid on the interaction of barley (Hordeum vulgare L.) with the powdery mildew Erysiphe graminis f. sp. hordei.
Plant Physiol
102:
503-511
[Abstract]
Stapleton A,
Beetham JK,
Pinot F,
Garbarino JE,
Friedman M,
Hammock BD,
Belknap WR
(1994)
Cloning and expression of soluble epoxide hydrolase from potato.
Plant J
6:
251-258
[CrossRef][Web of Science][Medline]
Thompson JD,
Higgins DG,
Gibson TJ
(1994)
CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and matrix choice.
Nucleic Acids Res
22:
4673-4680
[Abstract/Free Full Text]
Verwoerd TC,
Dekker BMM,
Hoekema A
(1989)
A small-scale procedure for the rapid isolation of plant RNAs.
Nucleic Acids Res
17:
2362
[Free Full Text]
Weiler EW,
Kutchan TM,
Gorba T,
Brodschelm W,
Niesel U,
Bublitz F
(1994)
The Pseudomonas phytotoxin coronatine mimics octadenoid signaling molecules of higher plants.
FEBS Lett
345:
9-13
[CrossRef][Web of Science][Medline]
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Top
Abstract
Introduction