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First published online June 5, 2003; 10.1104/pp.102.019273 Plant Physiology 132:1415-1423 (2003) © 2003 American Society of Plant Biologists Integration of Wounding and Osmotic Stress Signals Determines the Expression of the AtMYB102 Transcription Factor Gene1Department of Molecular Plant Physiology, Utrecht University, Padualaan 8, 3584CH Utrecht, The Netherlands
Transcript levels of the Arabidopsis R2R3-AtMYB102 transcription factor gene, previously named AtM4, are rapidly induced by osmotic stress or abscisic acid (ABA) treatment. Reporter gene expression studies revealed that in addition, wounding is required for full induction of the gene. Histochemical analysis showed a local  -glucuronidase induction
around the wounding site, especially in veins. In ABA-treated plants,
wounding-induced -glucuronidase activity could be mimicked by the wound
signaling compound methyl jasmonate. In silico studies of the
AtMYB102 promoter sequence and its close homolog AtMYB74
demonstrated several conserved putative stress regulatory elements such as an
ABA-responsive element, its coupling element 1 (CE1), and a W box.
Interestingly, further studies showed that the 5'-untranslated region is
essential for the osmotic stress and wounding induced expression of the
AtMYB102 gene. This 5'-untranslated region contains putative
conserved regulatory elements such as a second W box and an overlapping
MYB-binding element. These studies suggest that AtMYB102 expression
depends on and integrates signals derived from both wounding and osmotic
stress.
Abscisic acid (ABA) is the major plant hormone in water stress signaling. ABA regulates plant water balance and osmotic stress tolerance. The role of ABA in the osmotic stress responses has been studied extensively, and the availability of ABA-deficient and -insensitive mutants especially has been most helpful in these studies (Koornneef et al., 1998  ). Several of these mutants show severe wilting even
upon a mild water stress treatments, supporting the role of ABA under stress
conditions. ABA levels increase in wilting leaves due to the de novo synthesis
of the carotenoid cleavage enzyme 9-cis-epoxycarotenoid dioxygenase (NCED),
VP14 in maize (Zea mays). This enzyme catalyzes what appears to be
the rate-limiting step in ABA biosynthesis
(Tan et al., 1997). A clear
correlation in Phaseolus vulgaris was found between NCED
(PvNCED1) mRNA expression, NCED protein levels, and ABA levels in
dehydrated leaves and roots, indicating the important role of NCED in stress
ABA biosynthesis. Moreover, overexpression of the Arabidopsis AtNCED3
results in the accumulation of ABA (Iuchi
et al., 2001).
Two separate groups of stress-responsive genes are induced during osmotic
stress: the "early response genes" and the "delayed-response
genes" (Kiyosue et al.,
1994
Wounding is another stress factor that often is closely related to osmotic
stress. Tissue damage is usually associated with decompartmentalization,
release of cellular contents, and a loss of water. Such damage induces local
osmotic stress responses similar to those occurring in water-stressed intact
plants (Reymond et al., 2000
In several Solanaceous plants, both JA and ABA can activate the expression
of wound-responsive genes through the systemin-activated signaling system
(Hildmann et al., 1992 It is of interest to unravel the regulatory connections between wound-activated signaling pathways and signal transduction pathways triggered by other stress factors such as osmotic stress. Here, the expression analysis of a putative Arabidopsis transcription factor of the R2R3 MYB class is presented. This AtMYB102 gene is responsive to osmotic stress and wounding. Dehydration, osmotic or salinity stress, and ABA application enhance AtMYB102 transcript levels. Also, methyl jasmonate (MeJa) enhances expression synergistically in combination with ABA, whereas MeJa alone has a limited effect. It is proposed that AtMYB102 is a regulatory component, which integrates osmotic stress and wounding signaling pathways in Arabidopsis.
AtMYB102 mRNA Levels Respond to Osmotic Stress and ABA
Previously, it was reported that Arabidopsis ecotype Columbia-0 (Col-0)
AtMYB102 mRNA levels are induced by dehydration stress in leaves
(Kranz et al., 1998
The Arabidopsis Col-0 ecotype was transformed with a construct containing a
2-kb AtMYB102 promoter fragment including the mRNA 5' leader
sequence and the first three amino acids of the mature protein fused in frame
to the
The combination of osmotic stress and wounding and its effect on mRNA levels and GUS enzyme activity was further investigated in the Col-0 ecotype. Pots with 3-week-old transgenic plants were treated with hormones known to be important in osmotic stress and wound signaling. Endogenous AtMYB102 and GUS transcript levels were determined by realtime PCR with Actin2 as the endogenous reference. ABA treatment induces transcript levels as expected. However, GUS mRNA level seems less responsive compared with the endogenous transcript (2- over 10-fold, respectively), as was found for all other treatments (Fig. 4, A and B). Possibly, GUS transcript stability differs from that of the endogenous AtMYB102 transcripts. Alternatively, this might be due to a less efficient PCR with the GUS primers. However, the expression patterns of the GUS and the AtMYB102 transcripts are nearly identical over the treatments as was observed in a number of experiments with similar treatments (data not shown). The wound signaling hormone jasmonate enhances AtMYB102 transcript levels approximately 2-fold compared with a 10-fold induction by ABA (Fig. 4A). Combined application of these compounds induced the transcript abundance 13-fold. Interestingly, GUS activity was not altered compared with the control treatment for both separate treatments, but the activity increased when both ABA and jasmonate were applied (Fig. 4C). Wounding in combination with ABA further enhances GUS enzymatic activity (Fig. 4C). Wounding disrupts tissues and is accompanied by osmotic stress. This combination boosts transcript levels and GUS activity. These results suggest that AtMYB102 functions in a wound response pathway that may involve jasmonate and that is integrated with an osmotic stress and ABA response pathway.
Ethylene is a plant hormone that is induced locally upon wounding.
Therefore, the effect of this hormone on the wounding response was tested.
ACC, a precursor of ethylene, was applied to 3-week-old wounded and
ABA-treated plants. Ethylene in combination with wounding has a small but
consistent inhibitory effect on transcript levels and GUS activity
(Fig. 4). No effect was found
in combination with ABA alone. Ethylene has been proposed as an inhibitory
compound of the local jasmonate-dependent wound response pathway
(Rojo et al., 1999
Experiments with the GUS reporter construct revealed that ABA induces GUS transcript levels, but GUS activity is not enhanced (Fig. 4, B and C). This observation suggests a posttranscriptional regulatory mechanism of the AtMYB102 gene. The AtMYB102 promoter-GUS construct includes the 5'-UTR of 108 nucleotides (see "Materials and Methods"). Such 5'-UTR regions are often involved in translation regulation, and this possibility was investigated using an AtMYB102 promoter-GUS construct lacking the 108-bp 5'-UTR. Six independent hygromycin-resistant Col-0 lines showing different expression levels were analyzed for GUS mRNA levels and GUS enzymatic activity. Surprisingly, the endogenous AtMYB102 transcript levels and the GUS transcript levels were differentially regulated by salt stress (Fig. 5A). This indicates that the 5'-UTR is essential for the stress response. The GUS transcript levels basically are in agreement with GUS enzymatic activity as observed in the independent lines (Fig. 5B). Moreover, in the lines transformed with the construct lacking the 5'-UTR, wounding does not enhance GUS activity as it does in lines with the intact constructs.
AtMYB102 Is Responsive to Osmotic Stress and ABA
The AtMYB102 was identified previously as a light-regulated gene
(AtM4) expressed in seedlings
(Quaedvlieg et al., 1996
Analyzing GUS reporter gene constructs in the Col-0 and C24 ecotypes provided additional information on regulation and location of AtMYB102 gene expression. Some enhancement of GUS activity was observed in plants of both ecotypes exposed to salinity stress or ABA. This enhancement was only observed with sensitive enzymatic assays but not in histochemical experiments. Surprisingly, GUS activity was strongly induced by wounding in combination with either osmotic stress or ABA treatment (Figs. 3 and 4). Thus, wounding is important for full expression of the GUS reporter gene. Jasmonate is a well-known hormone involved in wounding responses. Applying MeJa in combination with ABA to 3-week-old Col-0 transgenic plants tested its possible involvement. ABA, and to a lesser extent MeJa, enhance AtMYB102 transcript levels but fail to induce GUS activity (Fig. 4), suggesting a posttranscriptional regulatory mechanism. Only the combined application of MeJa and ABA significantly induced GUS activity. These results indicate that jasmonate signaling is required for expression of AtMYB102, but this needs further investigation. Wounding is more effective in combination with ABA than with jasmonate in inducing transcript levels and GUS activity (Fig. 4). Perhaps wounding is more effective than jasmonate due to the locally induced osmotic stress at the wounding site.
Ethylene might be another factor involved in the observed expression
because it is synthesized locally after wounding. Studies on
jasmonate-responsive genes like JR1 and JR2 suggest that
ethylene inhibits the local jasmonate-dependent signaling pathway
(Rojo et al., 1999
Full expression of AtMYB102 requires both osmotic stress- and
wounding-induced signaling pathways. Most likely, in Arabidopsis the AtMYB102
protein is produced after local wounding with its associated osmotic stress.
This allows as of yet unknown target genes to be regulated accordingly in a
wounding-dependent manner. Prolonged osmotic stress induces ABA accumulation
and a further enhancement of the response in time. In tomato, ABA and
jasmonate can activate proteinase inhibitor genes through a common signal
transduction pathway (Hildmann et al.,
1992 The 5'-UTR sequence could be important for a posttranscriptional regulatory mechanism as suggested by experiments where ABA induces GUS mRNA levels but not enzymatic activity in the promoter-GUS transgenic lines. This notion was tested using a leaderless AtMYB102 promoter-GUS construct, but, surprisingly, these experiments showed the presence of essential stress-responsive elements in the 5'-UTR. Steady-state GUS transcript levels in the lines lacking the 5'-UTR remain unchanged during exposure to salt stress alone or combined with wounding (Fig. 5). The GUS transcripts levels were representative for the observed GUS activity, and wounding did not enhance GUS activity in these lines (Fig. 5).
The closest homolog of AtMYB102 in the genome of Arabidopsis is
AtMYB74. This AtMYB74 revealed considerable sequence
conservation with AtMYB102 and has a similar expression pattern
(Kranz et al., 1998
The 5'-UTR is essential for stress-induced expression of
AtMYB102. This region contains overlapping putative MYB and W-box
elements that are conserved in the 5'-UTRs of AtMYB102 and
AtMYB74 (Fig. 6). Another conserved element in the 5'-UTR is a pyrimidine-rich tract
(Fig. 6). The RNA-binding
protein, polypyrimidine tract-binding protein, is known to interact with such
tracts and regulates the utilization of premessenger and mRNA in association
with other proteins involved in splicing and translation initiation
(Shav-Tal and Zipori, 2002 In conclusion, osmotic stress in combination with wounding is needed for full expression of AtMYB102. Thus, AtMYB102 seems to integrate signals from these separate signal transduction pathways. It will be interesting to identify the expression mechanisms involved and the downstream processes controlled by AtMYB102. Moreover, overexpression of the gene in combination with phenotypic and metabolic analyses are underway and hopefully will shed light on its function.
Plant Material Arabidopsis ecotype Col-0 seeds were sown on soil in 5-cm pots, moistened, and placed for 3 to 5 d in a cold room at 4°C in the dark to synchronize germination. The pots were transferred to a climate room to allow growth to rosette stage with an 8-h photoperiod at 22°C. The plants were sprayed with solutions containing 100 µM ABA (mixed isomers, Sigma-Aldrich Chemie, Steinheim, Germany), 10 µM MeJa (Duchefa, Haarlem, The Netherlands), or 10 µM ACC (Sigma-Aldrich Chemie) and water was used as control. All solutions contained 0.01% (v/v) Silwet L77 (Van Meeuwen Chemicals, Weesp, The Netherlands). About 5 mL of the solution was sprayed on five rosette stage plants. The plants were returned to the climate room at 22°C, 70% relative humidity until harvesting. For salinity stress, the soil was saturated with 200 mM NaCl solution, and about 1 L of the solution was poured on the soil surface of 10 plants and allowed to drain. Wounding of the plants was performed using scalpel or forceps.
RNAse Protection and RT-PCR Analyses The first strand cDNA for RT-PCR analysis was synthesized with oligo(dT) primers on 1 to 2.5 µg of total RNA using SUPERSCRIPT II (Invitrogen, Carlsbad, CA) as described by the manufacturer. All RNA was pretreated with DNAse I using the DNA free kit (Ambion) according to the protocol. Amplification reactions contained 2 µL of the 2-fold diluted cDNA pool, 1x polymerase buffer (Roche Diagnostics), 2.5 mM of each dNTP, 10 pmol of each primer, and 2.5 units of Taq DNA polymerase. PCR was performed with denaturation at 94°C for 3 min, followed by 25 cycles of denaturation at 94°C for 30 s, annealing at 55°C for 30 s, and extension at 72°C for 1 min. A final extension at 72°C for 10 min was performed to complete the reaction. The primers used were: AtMYB102, FS102cDNA 5'-TAAACAATCAATGGCAAGGTCAC-3' and 5RACE102C 5'-CTGTGAGTCACTGGATCAATCC-3'; and Tubuline 4, F-B-TUBULIN4 5'-GCTTACGAATCCGAGGGTGCC-3' and R-B-TUBULIN4 5'-GTCCAGTGTCTGTGATATTGCACC-3'. PCR products (5 µL) were fractionated on a 1% (w/v) agarose gel, transferred onto Hybond N+ membranes (Amersham, Buckinghamshire, UK), and hybridized with 32P-labeled fragments generated with the PCR primers specified. Hybridization signals were visualized using a PhosphorImager (Molecular Dynamics, Sunnyvale, CA).
Real-Time PCR The primer probe combination of AtMYB102 was: probe, FAM 5'-AGAACTCCAATCTTCCATGCCACCATTCC-'3 Tamra; forward primer, 5'-AACCAATATTTCGAGAACACGATTACT-'3; and reverse primer, 5'-TGTTGTTAAACTGACGAGCTTCATT-'3. The primer probe combination of the Promoter::GUS fusion construct was: probe, FAM 5'-CGGCCGCCTGCAGCAGCCAA-'3 Tamra; forward primer, 5'-CAATGGCAAGGTCACAATCACT-'3; and reverse primer, 5'-TAAACTAGTCAGATCTACAGCGCTAAG-'3. The primer probe combination of Actin2 was: probe, FAM 5'-AAGTCTTGTTCCAGCCCTCGTTTGTGG-'3 Tamra; forward primer, 5'-GCTGAGAGATTCAGATGCCCA-'3; and reverse primer, 5'-GTGGATTCCAGCAGCTTCCAT-'3.
Total RNA was prepared as mentioned for RT-PCR analyses from leaves of rosette stage plants exposed to dehydration stress for 4 h and reverse transcribed as above using 2.5 µg of total RNA and 1.5 pmol gene-specific primer 5'RACE102A (5'-GCTGATGACGACGATTAGTATCC-3') in a 12-µL reaction mix. The reaction was stopped by heating at 70°C for 15 min and treated with 1 µL of RNAse H (Promega) at 37°C for 30 min. The gene-specific cDNA was purified over a spin column Qiaquick PCR purification kit (Qiagen, Hilden, Germany) and eluted in 19 µL of 10 mM Tris buffer (pH 8.0). The cDNA was C tailed by adding 2.5 µL of One-Phor-All buffer (Amersham-Pharmacia Biotech, Uppsala) and 2.5 µL of 2 mM dCTP. The mixture was heated at 94°C for 3 min, transferred to ice for 5 min, 25 units of terminal deoxynucleotidyl transferase (Amersham-Pharmacia Biotech) was added, and C tailing was performed at 37°C for 10 min and terminated at 70°C for 5 min. PCR was performed on 5 µL of the C-tailed gene-specific cDNA using 20 pmol 5RACE-AP (5'-GGCCACGCGTCGACTAGTACGGGIIGGGIIGGGIIG-3') and 20 pmol 5RACE102B (5'-GACATGTTCATGTGATGTGAAG-3') under RT-PCR conditions as described before with a melting temperature of 55°C and for 35 cycles. The PCR products were separated on a 1% (w/v) agarose gel along a size marker. Visible bands were isolated from the gel using Qiaex II gel extraction kit (Qiagen) and eluted in 20 µL of 10 mM Tris buffer (pH 8.0). A second identical PCR was performed on 5 µL of 1:250 (v/v) diluted gel-isolated fragments with 20 pmol 5RACE-AUAP (5'-GGC-CACGCGTCGACTAGTAC-3') and 20 pmol 5RACE102C (5'-CTGT-GAGTCACTGGATCAATCC-3'). The obtained fragment was cloned in a pGEM-T vector (Promega) according to the protocol and sequenced. The transcription initiation site could be located 108 bp upstream of the ATG codon.
For GUS histochemistry, plant material was stained overnight at 37°C in
a 1 mM 5-bromo-4-chloro-3-indolyl Plant material for microscopy was infiltrated and embedded in a Technovit 7100 (Kulzer, Heraus, Germany) as instructed by the manufacturer. Sections of 4 µm were made on a Reichert-Jung 1140 rotary microtome (Hanau, Germany) carrying a disposable Adams steel knife. Sections were stained with 0.1% (w/v) Ruthenium red (Sigma-Aldrich Chemie) in distilled water for 2 to 5 min at room temperature and fixed under a glass slide cover.
Relative GUS-activity was measured using the GUS-Light, Chemiluminescent
Reporter Gene Assay (Tropix, Inc., Bedford, MA) as described by the
manufacturer. Proteins were extracted from samples containing at most 3
cm2 leaf tissue in a buffer containing 50 mM sodium
phosphate (pH 7.0), 10 mM EDTA, 0.1% (w/v) sodium lauryl sarcosine,
0.1% (v/v) Triton X-100, and 10 mM
For the AtMYB102 promoter-GUS construct in C24, the plasmid pM4.1
harboring the promoter was digested with SalI and BstEII and
made blunt with Klenow (Amersham-Pharmacia Biotech). The fragment was cloned
in the binary vector pBi101.2 using the SalI/SmaI sites,
obtaining a translational fusion including the first three gene-specific amino
acids. The construct was transformed to C24 ecotype via a root transformation
procedure mediated by Agrobacterium tumefaciens
(Valvekens et al., 1988 Using a PCR-based cloning strategy, a 2-kb promoter fragment was fused to the GUS reporter gene in pCAMBIA3381Xa. The primers F102LDR (5'-AATGCGCTCCCCTTTCTC-3') and R102LDR (5'-GTGACCTTGCCATTGATTGTTTA-3') were used to amplify the 2-kb promoter region of the AtMYB102 gene on Col-0 ecotype DNA. The proofreading DNA polymerase Pfu was used with Taq DNA polymerase in a 1:80 (v/v) unit ratio. The fragment was cloned in a pGEM-T vector (Promega) and sequenced. A construct with the 5'-end of the AtMYB102 promoter at the vector T7 promoter site was digested with SphI and made blunt with T4 DNA polymerase (Amersham-Pharmacia Biotech) and with PstI. The fragment was cloned into the SmaI and PstI sites of pCAMBIA3381Xa. The translational fusion with the GUS coding region includes three amino acids of the AtMYB102 protein.
The constructs were transformed into Col-0 ecotype by an A.
tumefaciens (C58C1)-mediated floral dip method
(Clough and Bent, 1998 Received December 23, 2002; returned for revision February 12, 2003; accepted April 18, 2003.
Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.102.019273.
1 This work was supported by the European Commission (REGIA EU contract no.
QLG2–1999–00876). * Corresponding author; e-mail J.C.M.Smeekens{at}bio.uu.nl; fax 31–0–302513655.
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