Journal of Experimental Botany, Vol. 52, No. 359, pp. 1331-1338,
June 1, 2001
© 2001 Oxford University Press
Original Papers |
14-3-3 gene family in hybrid poplar and its involvement in tree defence against pathogens1
Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, 1055 du PEPS, Sainte-Foy, Québec, Canada G1V 4C7
Received 10 November 2000; Accepted 26 January 2001
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Abstract |
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In ongoing investigations of the role of the signal transduction pathway in tree–pathogen interactions, four complete and two partial 14-3-3 cDNAs have been isolated which are members of a gene family. Comparisons of DNA sequences reveal a high degree of identity among the cDNAs, and, in some cases, higher than 75% sequence similarity with previously published sequences. Sequence analysis at the amino acid level uncovered potential phosphorylation sites, some of which were identical among the proteins, and some of which varied. Treatment of trees with chitosan, jasmonates or by wounding of leaves, caused increases in the levels of 14-3-3 mRNA transcripts. Since jasmonates and chitosan are signal transducers of defence reactions in plants, these results suggest a possible role for 14-3-3 proteins in the pathogen defence response of deciduous trees. Effects of elicitors on transcription of the pal gene were also monitored. Pal is a well-characterized, pathogen response-related gene.
Key words: 14-3-3, chitosan, jasmonates, wounding, defence mechanism.
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Introduction |
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TopAbstractIntroductionMaterials and methodsResults and discussionReferences |
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14-3-3 proteins are one of several groups of proteins that occur as a protein family; the 14-3-3 family is found in all eukaryotes. These proteins have been widely studied in mammals following the original study (Moore and Perez, 1967
). Since then, 14-3-3s have been found in plants, Drosophila, yeasts, amoeba, and mammals (reviewed in Aitken, 1995; Ferl, 1996). They are highly conserved, but occur as distinct isoforms (Ferl, 1996). Phylogenetic-tree analyses (Wu et al., 1997) demonstrate that some isoforms of the 14-3-3 protein family in Arabidopsis thaliana display a different evolutionary course from that of mammals. Significant divergence was found between the genomic structure of plant and mammalian 14-3-3 genes.
A number of potential activities and functions have been attributed to 14-3-3 proteins. Some isoforms are induced by pathogens (Brandt et al., 1992) and by low temperatures (Jarillo et al., 1994; Kidou et al., 1993), and some are down-regulated by high salt concentrations (Chen et al., 1994). These results suggest the involvement of the 14-3-3 protein family in the signal transduction pathways which are related to stress response. In fact, recent studies have shown that activation of plasma membrane H+-ATPase by fusicoccin is modulated by 14-3-3s (Baunsgaard et al., 1998) and that specific members of 14-3-3 subset families were induced both after treatment with fusicoccin, and also during a gene-for-gene resistance response (Roberts and Bowles, 1999). Similarly, a 14-3-3 transcript was up-regulated during a race-specific hypersensitive response of soybean inoculated with Pseudomonas syringae pv. glycinea (Seehaus and Tenhaken, 1998). Divergent roles for 14-3-3 proteins have been suggested for the regulation of nitrate reductase and sucrose phosphate synthase (reviewed in Chung et al., 1999; Sehnke and Ferl, 1996). Finally, interactions of 14-3-3 with enzymes with potential roles in defence responses, including ascorbate peroxidase (Zhang et al., 1997b) and caffeate O-methyl transferase (Zhang et al., 1997a) have been also demonstrated. These observations clearly link 14-3-3 proteins with cellular regulators of plant metabolism.
Plant 14-3-3 proteins have been found associated with transcription factor complexes binding to G-box elements in the promoters of genes activated by various stresses (de Vetten et al., 1992; Ferl, 1996; Lu et al., 1992); the 14-3-3s do not bind directly to DNA but to the G-box binding factors. Both G-box binding factors and 14-3-3s can be phosphorylated, and phosphorylation of some G-box binding factors stimulates DNA binding (Dröge-Laser et al., 1997; Klimczak et al., 1992). Similarly, several components of the core transcriptional complex of the abscisic acid-inducible Em gene bind 14-3-3 proteins in vitro suggesting a complex transcriptional regulation involving several 14-3-3 isoforms (Finnie et al., 1999). Moreover, direct interaction between 14-3-3s and the core transcriptional complex proteins TBP and TFII B suggest an activation role for these proteins (Pan et al., 1999). On numerous occasions, 14-3-3s have been reported to interact with other proteins and protein kinases (Ferl, 1996; Morrison, 1994; Reuther et al., 1994). Recently, 14-3-3 proteins have been shown to bind and activate a plant calcium-dependent protein kinase (CDPK) (Camoni et al., 1998). Similarly, it has been demonstrated that binding of 14-3-3 proteins to a cauliflower CDPK has a functional influence over nitrate reductase (Moorhead et al., 1999). This influence, in fact, includes an increased sensitivity of nitrate reductase to inhibition by 14-3-3s. Overall, many biological roles for plant 14-3-3 proteins have been suggested, including regulation of metabolism, assembly of transcription factor complexes and organellar protein trafficking (reviewed in Roberts, 2000).
The aim of the present research was to study 14-3-3s in poplar trees, a woody species that serves as a model for plant molecular biologists. First, the presence of a 14-3-3 gene family was confirmed and corresponding cDNA sequences were isolated. Subsequently, sequences were analysed both at the nucleic acid and at the amino acid level in order to draw comparisons with previously documented sequences, and to identify potential phosphorylation sites in these 14-3-3 proteins. Furthermore, experiments were performed to examine the induction of 14-3-3s in poplar leaves in response to ‘simulated’ pathogen attacks. Chemical elicitors including chitosan and jasmonates were used in order to facilitate the experimental design and to circumvent variability inherent in a biological system, such as the fungal inoculation of plants (Creelman and Mullet, 1997b; Ebel and Cosio, 1994).
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Materials and methods |
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Plant material
The plant material used was Populus tremulaxP. alba clone INRA717-1-B4. Poplar trees were grown either in vitro in 0.5xMSG medium (Leplé et al., 1992
) or in Pro-Mix soil (Premier Tech). In vitro-grown trees were kept in controlled growth chambers (25 °C, 16/8 h light/dark). The trees in soil were kept in a greenhouse at 25 °C under 16 h lighting.
cDNA synthesis
Poplar leaves (clone INRA717-1-B4) were detached from the plant and wounded by cutting with a scalpel several times. The leaves were then placed on wet filter paper in a Petri dish and incubated for 6 h in a growth chamber and harvested. Total RNA was extracted from wounded detached poplar leaves as follows. A small aliquot (1.5 ml) of 65 °C extraction buffer (Chang et al., 1993) was mixed with 0.2 g of plant material which had been ground in liquid nitrogen. The mixture was incubated on ice for 1 h. Samples were heated at 55 °C for 2 min and centrifuged at 14 000 g in a microfuge at room temperature. A 0.5 vol. of 95% ethanol was added to the supernatant, and this solution was loaded onto a Qiagen RNeasy column and processed as per the manufacturer's protocol, except that one extra wash was added at each wash step.
A cDNA pool was synthesized using an AMV reverse transcriptase kit from Roche Molecular Biochemicals. The second strand of the cDNA was synthesized during the first cycle of the touch down PCR (see next section) using the primer RTd(T)15+(5'CTCGAGCGGCCGCTTTTTTTTTTTTTTT 3').
Primer design, touch down PCR, cloning, and sequencing
Oligonucleotides were constructed following an alignment of known amino acid sequences from GenBank to obtain the least degeneracy. Sequences from human, yeast, nematode, and plant 14-3-3s were used in the comparisons. Primers 14-3-3-A (5' GCNGARCARGCNGARMGNTAYGA 3') and 14-3-3-B (5' GTCCANARNGTNARRTTRTC 3') were used to amplify 14-3-3 fragments from the poplar cDNA pool (mentioned above) using a touch down PCR technique (Don et al., 1991). Annealing temperatures varied from 60 °C to 50 °C in the first round of amplification. A second round of amplification was necessary to obtain single amplified fragments (Ausubel et al., 1987). The annealing temperature for the second amplification was 65 °C.
The resulting fragments were cloned into plasmid PCR2.1 using a TA cloning kit (Invitrogen), and then sequenced using the dideoxy chain termination method (Sanger et al., 1977) with an ABI373 automated DNA sequencer. Preliminary analyses of partial sequences were performed using comparisons with the GenBank databases, search programs in NCBI, and alignment programs in GCG (Devereux et al., 1984).
cDNA library construction, screening, and clone analyses
A cDNA library was constructed from a pool of leaves from in vitro plants of Populus tremulaxP. alba clone INRA717-1-B4 that had been separately subjected to different inductions. Solutions of elicitors (chitosan [5 ml of a 2 mg ml-1 solution], salicylic acid [5 ml of 2 mM solution], and jasmonic acid [5 µl of a 1 M solution]) had been applied directly to the surface of the solid medium in the magenta container, followed by a 21 h incubation under full lighting. RNA isolation, library construction and screening, and sequencing of positive clones were done as previously described (Richard et al., 2000).
Sequence alignments were performed using the ClustalW method (Higgins et al., 1996). A motif/pattern search was performed using SMART (Schultz et al., 2000) and PFAM (Bateman et al., 2000). Protein structure prediction methods used were HNN (see internet address: http://pbil.ibcp.fr) and PREDATOR (Frishman and Argos, 1996).
Genomic DNA isolation and Southern blot analysis
Poplar genomic DNA was isolated from in vitro plants using Qiagen Genomic-tips and the Qiagen protocol for its use with plants. DNA was digested overnight, precipitated, separated electrophoretically on a 0.8% agarose gel, and transferred to Zetaprobe (Bio-Rad) membrane using a LKB 2016 Vacugene apparatus. The DNA was fixed to the membrane by UV-cross-linking. Prehybridization was performed in Church buffer (Church and Gilbert, 1984) at 65 °C for a minimum of 30 min. A PCR probe (32P-dCTP, using primers 14-3-3A and 14-3-3B with fragment 14-3-3P20-5) was then added to the prehybridization buffer for an overnight hybridization at 60 °C in Church buffer.
Plant treatments for gene induction experiments
Trees were subjected to chitosan, wounding treatment, jasmonic acid or methyl jasmonate for subsequent Northern blot analysis. Three plants were used per treatment, and in all cases leaves were harvested as follows. At each time point a leaf of the same age/stage was cut from each tree. For example, leaf number 9 (counting from the top) was harvested at time 0 h, then leaf 8 at time 2 h and so on. Chitosan, 1 mg ml-1, was applied with a soft cotton swab to the abaxial and adaxial face of the poplar leaf blades. Control plants were swabbed with water and kept under the same conditions. Wounding of poplar leaves was done (at time 0 h) by piercing small holes through all the leaf blades to be harvested. Control plants were kept under the same conditions. Jasmonic acid (80 µM with 0.05% Tween 20, pH 7.0) was sprayed on the abaxial and adaxial face of the leaf blades every hour for 5 h. Control plants were sprayed with 0.05% Tween 20. Methyl jasmonate was used in a confined environment: 10 µl was applied to a cotton ball that was placed at the foot of the plant, and the plant was placed in a sealed bag. Control plants were also placed in a sealed bag.
RNA isolation and Northern blot analysis
RNA isolation was performed as previously described (Chang et al., 1993). Formaldehyde agarose gel electrophoresis of total RNA (10 µg well-1) was performed as described earlier (Ausubel et al., 1987). RNA was transferred onto a nylon membrane (Zeta-Probe) overnight using a gravitational/capillary system with 10xSSC. Hybridization was performed as in Southern hybridization except that the overnight hybridization temperature was 65 °C. Membranes were exposed to pre-flashed X-OMATTM AR Scientific Imaging Film (Kodak) for 12–36 h. Quantification of transcript accumulation was evaluated by densitometric measurement of autoradiograms using the Sigmagel program (Jandel). Results were normalized for an equal loading quantity using ethidium bromide staining of ribosomal RNA. The histogram represents scanning values of the most representative hybridization experiment (shown) and is a mean of duplicate densitometry scan analyses of replicate induction experiments. In the analyses, a difference of magnitude of transcript accumulation of 2-fold or greater was considered to be significant.
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Results and discussion |
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TopAbstractIntroductionMaterials and methodsResults and discussionReferences |
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Sequence comparisons
The presence of 14-3-3s in many organisms has been well documented (Ferl, 1996
). They are ubiquitous and accomplish a wide variety of functions involved in cell processes. In aligning amino acid sequences of nematode, yeast, plant, and human, a high degree of similarity was found (data not shown). In designing the primers for PCR the least degeneracy obtained was 35%. Six partial sequences were found using PCR amplification with a wound-induced cDNA pool. And when a cDNA library from multiply elicited poplar was screened, four complete cDNAs were isolated and these cDNAs corresponded to four of the six partial sequences. The sequences are available in the GenBank database (accession numbers AF272572, AF121194, AF272573, AF121195 for the complete cDNAs designated 14-3-3P20-1, P20-2, P20-4, and P20-5, respectively; as well, accession numbers AF121193 and AF121196 for partial cDNAs designated 14-3-3P20-7 and P20-8, respectively). To date, complete cDNAs have not been recovered for clones P20-7 and P20-8. These partial sequences hybridized with many other 14-3-3 sequences (see also Fig. 2, Southern hybridization). This result is, to some degree, expected considering the sequence similarities among the complete 14-3-3 cDNAs. In addition, this result may be a reflection of the relative abundance of different members of the 14-3-3 family in elicited poplar. Specifically this result suggests that the 14-3-3 cDNAs represented by the partial sequences, P20-7 and P20-8, are present in a lower quantity in this study's stress-induced cDNA library.
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Figure 1 is a sequence alignment (Clustal W) of the four complete cDNAs from poplar and the zeta isoform 14-3-3 protein of Bos taurus (accession number 4557913), crystallized by Liu et al. (Liu et al., 1995
). This study found nine antiparallel alpha-helices, and a dimeric structure which forms a groove for potential interaction with a substrate. Note the similarity in amino acid content between the poplar 14-3-3s and the crystallized 14-3-3 in the alpha-helical regions indicated (Fig. 1). By further testing with methods of structure prediction (such as HNN and PREDATOR) it is predicted that our 14-3-3 proteins have a similar three-dimensional conformation to the zeta isoform of Bos taurus.
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1 to Further analysis using motif search engines reveals the presence of several motifs, patterns, and signatures in poplar 14-3-3 proteins. In all four proteins signature 1, R-N-L-[LIV]-S-[VG]-[GA]-Y-[KN]-N-[IVA] (Prosite database PS00796) is located at the N-terminus and signature 2, Y-K-[DE]-S-T-L-I-[IM]-Q-L-[LF]-[RHC]-D-N-[LF]-T-[LS]-W-[TAN]-[SAD] (PS00797) at the C-terminus. These two regions are highly similar among all 14-3-3 proteins. A motif/pattern search (PFAM and SMART) revealed a cAMP- and cGMP-dependent protein kinase phosphorylation site ([RK] (2)-X-[ST]; PS00004), protein kinase C phosphorylation sites ([ST]-X-{RK]; PS00005), a potential tyrosine kinase phosphorylation site ([RK]-X-(2,3)-[DE]-X(2,3)-Y; PS00007), and a casein kinase II phosphorylation site ([ST]-X(2)-[DE]; PS00006). Most of the motifs found through our analyses lay within helices 3, 5, and 8. The latter finding corroborates previously published work that identified features in these helices which are specific to the binding of target proteins (Liu et al., 1995
; Xiao et al., 1995; Petosa et al., 1998; Ichimura et al., 1997).
To date many studies have demonstrated that the dimeric structure of 14-3-3 proteins contains many potential protein-binding sites, and that these sites can be specific to its target's phosphorylation status. For example, it was shown that the region spanning helices 7 and 8 (Fig. 1
) can bind the phosphorylated tryptophan hydroxylase (Ichimura et al., 1997). As well, Rittinger et al. solved a high-resolution X-ray structure of 14-3-3 phosphoserine peptide complexes, identifying several binding sites for the 14-3-3-substrate interaction (Rittinger et al., 1999). Two distinct but overlapping ligand binding sites have been identified in a 14-3-3 (Petosa et al., 1998). This group went on to suggest that 14-3-3 proteins act in signal transduction by inducing the formation of homo- or heterodimers in their bound peptides. Further research in this laboratory will include the identification and characterization of substrates which bind with poplar 14-3-3 proteins.
Southern blot analysis
Southern blot analysis (Fig. 2) demonstrates that the probe used hybridized with more than one of the fragments of the digested poplar genomic DNA. This corroborates the other findings (Wu et al., 1997) which reported multiplicity of 14-3-3 genes in Arabidopsis, and suggested that the 14-3-3 gene family of poplar is extensive. To test this hypothesis the banding patterns of Southerns of several 14-3-3 gene fragments were compared with two different poplar hybrids (data not shown), one from the Leuce Section (Populus tremulaxP. alba clone INRA717-1-B4), and one from the Aigeiros Section (Populus nigraxP. maximowiczii NM1) (Eckenwalder, 1996). Considerable variation was seen between Southern blots, despite the high degree of similarity among the probe sequences, hence the data were inconclusive with regard to gene multiplicity.
Induction of mRNA accumulation by chitosan, wounding, jasmonic acid, and methyl jasmonate
Accumulation of 14-3-3 mRNA following specific challenges by either a compatible pathogen, or by treatment with an elicitor such as fusicoccin was previously demonstrated in crop plants (Seehaus and Tenhaken, 1998; Roberts and Bowles, 1999). A similar increase in 14-3-3 mRNA accumulation was observed following chitosan treatment. Figure 3 shows that 14-3-3 mRNA levels are increased at 2 h, an induction that increases to reach a plateau at 4–8 h and then decreases at 24 h post-treatment. Existing evidence indicates that the defence responses induced by chitosan are similar to those caused by pathogen attack (Benhamou, 1996; Côté and Hahn, 1994), and that the phenylalanine ammonia lyase (pal) gene transcription is also induced in plants following a pathogen attack (Dixon and Paiva, 1995; Smith, 1996). In all induction experiments, the efficacy of defence-response induction by probing was confirmed, in parallel, for expression of pal (gene fragment kindly provided by Dr C Douglas, UBC, Vancouver, BC, Canada). In Fig. 3 the pal mRNA level was clearly increased at 4 h and 8 h post-treatment, and more so at 24 h. Although these results are, in general, as would be expected, the variability of the level of induction could also be due to the relative uptake of chitosan, as well as the fact that it was applied only once, at time 0.
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Similar experiments were conducted for wounding and methyl jasmonate (MeJa) treatments. Following wounding, a clear induction of 14-3-3 mRNA levels was observed (Fig. 4
). By 2 h post-treatment, 14-3-3 transcript accumulation was perceptible and by 4 h post-treatment, mRNA levels reached a plateau for the remainder of the test period. Parallel probing for pal demonstrated induction of this gene by 4 h post-wounding. This result is comparable to that previously published (Ellard-Ivey and Douglas, 1996) in which pal transcription in parsley plants was inducible by both wounding and MeJa. In a similar study in poplar cell suspensions, an experimental system that could be considered more comparable to this present study, the elicitor PGA lyase also induced pal-gene transcription (Moniz de Sa et al., 1992).
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Results of induction by both jasmonic acid (JA) and MeJa (Figs 5, 6), were similar to those with wounding. However, there was a variation between the response to the two different forms of jasmonate application. Repetitive spraying of JA caused a more rapid increase in levels of 14-3-3 transcripts than constant exposure to MeJa. Significant increases in the levels of transcripts were at 8 h and 24 h post-treatment for JA and MeJa, respectively. In Figs 5 and 6, the levels of transcription of the pal gene were also observed in response to the two different jasmonate treatments. Briefly, a strong induction was observed at 8 h after spraying with JA, and a weaker induction was observed at 24 h in response to continuous exposure to MeJa. These findings are consistent with those in parsley mentioned previously (Ellard-Ivey and Douglas, 1996
), and also corroborate the evidence for the role of jasmonates in the wounding response. JA not only accumulates in wounded plants (Creelman and Mullet, 1997a), but it is also a modulator of plant responses to wounding (Wasternack and Parthier, 1997). Therefore, although some similarities would be expected between plant responses to jasmonates and wounding, some differences would also be expected in that there are additional factors at play in the wounding response.
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The 14-3-3 genes that have been characterized here are clearly induced by elicitors and this observation is supported by work done on 14-3-3 genes isolated from tomato (Roberts and Bowles, 1999
). In this specific study at least ten 14-3-3 genes were found and these exhibited differential patterns of expression in leaves following various elicitor treatments. However many of these 14-3-3 genes were already expressed at high levels in healthy leaves. Thus, we have to keep in mind that transcriptional control of 14-3-3 gene expression would not necessarily be the unique controlling event and that pre-existing 14-3-3 isoforms could also play an important role in an immediate response mechanism. Since this cloning strategy was based on using stress-induced poplar leaves, isoforms were probably isolated that are transcriptionally induced after wounding or elicitor treatments. Since many 14-3-3s have been associated with signal transduction pathways, the authors are now conducting experiments to identify the relationship between their 14-3-3s and pal as well as other potential pathogen response-related genes. Furthermore, in characterizing the roles of the 14-3-3 gene family, it is hoped we will gain a better overall understanding of the tree-defence response to pathogen attack.
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Acknowledgments |
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We thank Dr N Brisson (Université de Montréal) and Dr R Hamelin (Canadian Forest Service, Sainte-Foy, Québec, Canada) for revision of the manuscript. We thank Dr N Benhamou (Université Laval, Sainte-Foy, Québec, Canada) for her help in the use and preparation of chitosan and the knowledgeable anonymous reviewers for the constructive criticism on an earlier version of this manuscript. Also, we thank Dr C Douglas for providing the pal cDNA. This research was supported by a grant from the Natural Sciences and Engineering Research Council (NSERC) of Canada and the National Biotechnology Strategy of Canada to AS. GL and MC were supported by an NSERC Post-doctoral Fellowship and student Fellowship, respectively.
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Notes |
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1 The nucleotide sequence data reported will appear in the GenBank Nucleotide Sequence Database under the accession numbers AF121193 (14-3-3P20-7), AF121194 (14-3-3P20-2), AF121195 (14-3-3P20-5), AF121196 (14-3-3P20-8), AF272572 (14-3-3P20-1), AF272573 (14-3-3P20-4).
2 To whom correspondence should be addressed. Fax: +1 418 648 5849. E-mail: seguin{at}cfl.forestry.ca
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