Journal of Experimental Botany, Vol. 53, No. 367, pp. 225-232,
February 1, 2002
© 2002 Oxford University Press
Original Papers |
Characterization of the V-type H(+)-ATPase in the resurrection plant Tortula ruralis: accumulation and polysomal recruitment of the proteolipid c subunit in response to salt-stress1
2 Department of Plant Biology, Southern Illinois University-Carbondale, Carbondale, IL 62901-6509, USA
3 Department of Agronomy and Range Science, University of California, Davis, CA 95616-8515, USA
Received 8 May 2001; Accepted 24 September 2001
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Abstract |
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Tortula ruralis is an important experimental system for the study of plant vegetative desiccation tolerance. EST gene discovery efforts utilizing desiccated gametophytes have identified a cDNA Vac1 encoding a predicted polypeptide with significant similarity to the vacuolar H+-ATPase c subunit. VAC1, the 167 amino acid deduced polypeptide, has a predicted molecular mass of 16.9 kDa, and a predicted pI of 9.7. Phylogenetic analysis demonstrated that previously characterized proteolipid polypeptide sequences could be reproducibly grouped into two major clades and that VAC1 forms a discrete evolutionary group. RNA blot and Western blot hybridizations were used to analyse expression of Vac1 and accumulation of VAC1 in response to (1) desiccation and rehydration, (2) increased NaCl concentration, and (3) NaCl-shock. During a desiccation–rehydration cycle, Vac1 transcripts are expressed in both the total and polysomal RNA fractions in approximately equal amounts, and the steady-state transcript levels are unchanged. However, Vac1 transcript levels increased in response to both elevated NaCl concentration and NaCl-shock. There is a preferential accumulation of Vac1 transcripts within the polysomal RNA fraction in response to salt stress, and these data suggest that T. ruralis possesses a salinity-stress-dependent and desiccation-stress-independent mechanism for post-transcriptional gene control. Using a cotton anti-c subunit polyclonal antibody raised against the C-terminal domain, it was shown that the amount of Tortula 16 kDa proteolipid in the tonoplast protein fraction was unaffected by any stress treatment.
Key words: Desiccation, moss, salinity, V-ATPase.
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Introduction |
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The moss Tortula ruralis is an important experimental system for the study of vegetative desiccation-tolerance, organelle repair and recovery, and post-transcriptional gene control in plants (Oliver and Wood, 1997
). The proposed mechanisms of desiccation tolerance differ between bryophytes and tracheophytes. T. ruralis employs a constitutive protection system and an active rehydration-induced recovery mechanism (Oliver et al., 2000). This is in contrast to the strategy proposed for the angiosperm Craterostigma plantagineum which utilizes a drying-induced elevation of abscisic acid to trigger the accumulation of gene products that mediate the establishment of a cellular protection system prior to desiccation (Ingram and Bartels, 1996). Unlike many plant stress responses, the alteration in gene expression within T. ruralis gametophytes elicited by desiccation stress is primarily regulated at the post-transcriptional level as a result of differential selection and/or recruitment of rehydrin mRNAs from a qualitatively constant mRNA pool (Oliver, 1991).
Using desiccated T. ruralis gametophytes, EST analysis was employed to discover genes that control vegetative desiccation tolerance, and components of the moss vacuolar H+-ATPase (V-ATPase) have been identified (Wood et al., 1999). The plant vacuole plays a central role in a variety of physiological and metabolic processes including cellular expansion, ion homeostasis, nutrient acquisition and storage, regulation of cytoplasmic pH, and the molecular adaptation to high salinity (Hasegawa et al., 2000; Martinoia et al., 2000; Ratajczak and Wilkins, 2000; Schumacher et al., 1999; Smart et al., 1998; Wilkins and Jernstedt, 1999). The V-ATPase (EC 3.6.1.34) is a primary-active transport enzyme associated with the tonoplast membrane and various endomembranes such as the Golgi apparatus, Golgi-derived vesicles, ER and provacuoles (Ratajczak, 2000). The V-ATPase acidifies intracellular compartments (including the vacuolar lumen) and contributes to a proton motive force capable of driving the secondary transport of numerous ions and metabolites across these membranes (Sze et al., 1999; Ratajczak and Wilkins, 2000).
The V-ATPase holoenzyme is comprised of two major functional domains, the V1 membrane peripheral domain and the V0 membrane integral domain (Ratajczak, 2000). On a stoichiometric basis, the most abundant peptides are subunit A (63–72 kDa), subunit B (52–60 kDa) and subunit c (16–20 kDa) (Ward and Sze, 1992). Subunit A is the substrate-binding catalytic subunit and subunit B is the substrate-binding non-catalytic subunit of the V1 peripheral domain. Subunit c is the primary constituent of the V0 integral domain and requires at least 6 c subunits to form the proton pore. Additional c subunits (i.e. c' and c'') have been identified in yeast although their role in pore formation and/or proton movement is unclear (Ratajczak, 2000). Subunit c is a 16–20 kDa hydrophobic protein also known as the proteolipid subunit containing four conserved transmembrane domains (Lai et al., 1991; Hasenfratz et al., 1995). In yeast, amino acid residue 137Glu within transmembrane domain IV of subunit c has been demonstrated by site-directed mutagenesis to be essential to V-ATPase activity (Nuomi et al., 1991) and is postulated to function in proton translocation across the lipid bilayer. N,N'-dicyclohexylcarbodiimide (DCCD) inhibits V-ATPase activity by covalently binding to 137Glu (Kaestner et al., 1988).
The environmental response of V-ATPase to salinity-stress has been extensively studied at the transcript, protein and enzymatic levels (Ratajczak, 2000; Ratajczak and Wilkins, 2000). Subunit c-encoding cDNAs have been identified and characterized from a number of angiosperm species including Avena sativa (Lai et al., 1991), Mesembryanthemum crystallinum (Tsiantis et al., 1996), Daucus carota (Löw and Rausch, 1996), Beta vulgaris (Kirsch et al., 1996) and Arabidopsis thaliana (Perera et al., 1995). In general, salinity increases c subunit steady-state transcript levels 2–4-fold with a concomitant, but variable, effect upon the abundance of V-ATPase subunits. D. carota proteolipid transcript levels showed a modest and transient increase in response to 100 mM NaCl applied for 48 h with no concomitant increase in the c subunit peptide (Löw and Rausch, 1996). In the halotolerant plant B. vulgaris, proteolipid transcript levels increased in response to 400 mM NaCl applied for 48 h (Kirsch et al., 1996). Similarly, in the halophyte M. crystallinum proteolipid transcript levels increased in response to incremental increases of NaCl over an 8 d period to a final concentration of 400 mM (Tsiantis et al., 1996).
It is postulated that cellular and biochemical processes mediated by the plant vacuole, and the activity of the V-ATPase, play a fundamental role in the ability of resurrection plants to survive complete drying of their vegetative structures. In order to pursue this hypothesis at the molecular level, and to investigate the relationship between salinity-stress and desiccation-stress in T. ruralis, a cDNA Vac1 encoding a predicted polypeptide with significant similarity to the V-ATPase c subunit was isolated and characterized.
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Materials and methods |
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Plant material
Gametophytes of Tortula ruralis [Hedw.] Gaerten., Meyer & Scherb. were collected, harvested, desiccated, and rehydrated as described previously (Wood et al., 1999
). Hydrated moss was obtained after a 24 h rehydration period. Desiccated moss was obtained by placing cut hydrated gametophytes on a filter paper disc over activated silica gel (rapid-dried, RD) or a stirred saturated solution of sodium nitrite at 20 °C (RH 66%) for 24 h (slow-dried, SD). The air-dried weight is achieved in 1 h for rapid-dried and 6 h for slow-dried gametophytes. Rehydrated moss was obtained by the addition of ddH2O to desiccated moss. Salt-treated moss was obtained by the step-wise addition of NaCl (50 mM 2 h, 50 mM+50 mM 2 h, and 100 mM+50 mM 2 h; 6 h total application) or by incubation in 50 mM, 100 mM or 150 mM for 6 h. Voucher specimens are kept at the Jepson and University Herbarium (University of California, Berkeley, CA, USA).
cDNA clone isolation and DNA sequence analysis
The EST clone RNP10 (AI305045) was previously isolated from a T. ruralis cDNA expression library cDNA derived from the polysomal, mRNP fraction of desiccated gametophytes (Wood et al., 1999). The truncated cDNA has significant similarity to subunit c of the vacuolar-type H+-ATPase as determined by BLASTN, and a full-length cDNA clone was obtained by 5' random amplification of cDNA ends (5'-RACE) using the gene specific primers EST10A (5'-CCAACTCTACATATACAA-3') and EST10B (5'-CGAGAAAACGAGATATGTA-3') (Zeng and Wood, 2000). DNA sequence was determined by the Plant Biotechnology and Genome Center (Southern Illinois University) using an automated sequencer (ABI model 377; Applied Biosystems, Foster City, CA). Multiple alignments of the deduced amino acid sequence for VAC1 and related vacuolar-type H+-ATPase c subunits were created using CLUSTAL-V (Higgins et al., 1991) and phylogenetic trees were constructed using the Neighbor–Joining algorithm. Prediction of transmembrane helices was determined using TMHMM (ver. 1.0) (www.expasy.ch/). The data set consisted of the following predicted amino acid sequences: Oryza sativa (Q40635), Avena sativa (M73232), M. crystallinum (Q39437), Dendrobium crumenatum (AAF04597), Vigna radiata (O22552), A. thaliana (Q39039), Gossypium hirsutum (Q43434), Pleurochrysis carterae (Q43362), Neurospora crassa (P31413), Porphyra yezoensis (BAA87944), Saccharomyces cerevisiae (P25515), Drosophila melanogaster (P23380), and Mus musculus (NP_033859).
RNA isolation and RNA blot hybridizations
Total RNA was isolated using the RNeasy kit (Qiagen, Valencia, CA, USA) as described by the manufacturer. Polysomes were extracted from gametophytic tissue using a low salt extraction buffer (Wood and Oliver, 1999). The 27000 g supernatant was layered over a sucrose pad and centrifuged at 100000 g for 90 min in a 50TI ultracentrifuge rotor (Beckman Scientific, Fullerton, CA, USA). The polysomal pellet (100000 g pellet) was solubilized in polysome-resuspension buffer. RNA blot analysis was performed using standard techniques as described previously (Duff et al., 1999). The 439 bp 5'-RACE product of RNP 10 used as probe was labelled with [
32P]-dCTP (NEN-DuPont) using the random prime labelling kit (Decaprime II Kit, Ambion, Austin, TX, USA). Membranes were prehybridized and hybridized at 42 °C using ULTRAhybTM (Ambion) as described by the manufacturer. Membranes were washed at 42 °C (2x5 min in 2x SSC, 0.1% SDS followed by 2x15 min in 0.1x SSC, 0.1% SDS). Blots were stripped and reprobed with rRNA-DNA to demonstrate equal loading.
Protein analysis
Microsomal membrane fractions were prepared from gametophytic tissue essentially as described earlier (Schumacher et al., 1999). 0.5 g of tissue was homogenized in extraction buffer (350 mM sucrose, 70 mM TRIS-Cl pH 8.0, 10% (v/v) glycerol, 3 mM Na2EDTA, 0.15% (w/v) BSA, 5.0% (v/v) Triton X-100, and 4 mM DTT). The supernatant was filtered and centrifuged at 15000 g for 15 min at 4 °C. The 15000 g supernatant was centrifuged at 100000 g for 90 min in a 50TI ultracentrifuge rotor (Beckman Scientific, Fullerton, CA) and the microsomal pellet was solubilized in resuspension buffer (350 mM sucrose, 10 mM MES pH 7.0, 2 mM DTT). Microsomal protein was quantified using the Bio-Rad protein assay kit (Melville, NY) using BSA as a standard. Electrophoresis on denaturing polyacrylamide gels was performed on slab gels (Laemmli, 1970) with a 4% (w/v) stacking gel and a 12.5% (w/v) resolving gel. Proteins were fixed and electrotransferred for 1 h onto supported nitrocellulose (Schleicher and Schuell, Keene, NH) in a buffer containing 25 mM Gly and 20% (v/v) methanol at a constant current of 64 mA. Blots were blocked with 2% (w/v) dry milk in TRIS-buffered saline, incubated with rabbit anti-proteolipid polyclonal antibody raised against synthetic peptides corresponding to either the carboxy-terminal domain (SSRAGQSRAE) or amino-terminal domain (MSTTFSGDETA) of the cotton c subunit (Hasenfratz et al., 1995) (1:800) followed by a goat anti-rabbit IgG alkaline phosphatase conjugate that was detected using 4-nitroblue-tetrazolium chloride and 5-bromo 4-chloro 3-indoyl-phosphate (Bio-Rad).
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Results |
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Characterization of Vac1
A Tortula ruralis EST (RNP10, AF303372) with significant similarity to the V-ATPase c subunit (Lai et al., 1991
) was isolated from a cDNA expression library derived from the polysomal fraction of desiccated gametophytes (Wood et al., 1999). The full-length cDNA was obtained using 5'-RACE and named Vac1 (Vacuolar ATPase c-subunit gene number 1). The Vac1 cDNA was 831 bp in length and contained a single, continuous open reading frame from nucleotide 109 to 612 (data not shown). The ORF encodes a polypeptide of 167 amino acids with a predicted molecular mass of 16.9 kDa and predicted pI of 9.7. The deduced Tortula polypeptide VAC1 is 90–91% identical to c subunit paralogues from Arabidopsis, cotton, ice plant, and rice (Fig. 1A). Conserved amino acid substitutions are dispersed throughout the length of the polypeptide. The Tortula N-terminal domain is longer and shows the greatest divergence relative to the higher plant subunits. VAC1 is predicted to contain four transmembrane helices: residues 13–35 (Helix I), 59–81 (Helix II), 94–116 (Helix III), and 135–157 (Helix IV) (Fig. 1B). The DCCD-binding site is postulated to be a glutamate residue (142Glu) within transmembrane domain IV.
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Phylogenetic analysis of VAC1
To examine the structural relationship between the predicted polypeptide VAC1 and similar vacuolar-type H+-ATPase c subunits, the deduced polypeptide sequences were analysed. The phylogenetic tree, assembled from the pairwise alignment of these deduced polypeptide sequences, is depicted in Fig. 2. As far as is known, VAC1 is the first c subunit to be characterized in bryophytes and this analysis demonstrates its evolutionary relationship to other c subunit sequences. The proteolipid sequences could be reproducibly grouped into two major clades, one for plants and algae, and one for animals and fungi. T. ruralis VAC1 is distinct from animals, fungi and tracheophytes, and forms a discrete evolutionary group.
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Expression of Vac1 in T. ruralis gametophytes
The accumulation of T. ruralis Vac1 steady-state mRNA transcripts was analysed by RNA blot hybridization in response to stress induced by a desiccation–rehydration cycle (Fig. 3) or NaCl treatment (Fig. 4). Total and polysomal RNA was isolated from hydrated (control) (C), slow-dried (SD), rapid-dried (RD), rehydrated (Re) rapid-dried rehydrated (RDR) or salt-treated gametophytic tissues as described (see Materials and methods). To enable normalization of the hybridization signals to account for loading anomalies, the membrane was reprobed after the initial analysis using a plant 18S nuclear rRNA probe. T. ruralis Vac1 hybridized to a single mRNA species of approximately 900 bp (Figs 3, 4).
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Vac1 transcripts are present within both the total and polysomal RNA fractions in approximately equal amounts (C, SD, Re lanes in Fig. 3
) and the steady-state transcript levels are unchanged by a desiccation–rehydration cycle. These findings clearly demonstrate that Vac1 transcripts are retained within the polysomal fractions of both desiccated and rehydrated gametophytes. Previously, three distinct classes of T. ruralis cDNA clones were identified based upon the relative recruitment of their corresponding transcripts into the polysomal fraction of rapid-dried (RD), and RD-rehydrated (RDR) gametophytes (Scott and Oliver, 1994). These classes included constitutive cDNAs, cDNAs representing hydrin transcripts and cDNAs representing rehydrin transcripts. Hydrins are transcripts that are lost from polysomal fractions during rehydration, rehydrins are transcripts that are preferentially found in rehydrating polysomal fractions, and constitutive clones are transcripts found within each polysomal fraction in similar amounts. According to the authors' prior cDNA classification scheme Vac1 is a constitutive clone (i.e. transcripts are equally distributed between the RD and RDR polysomal fractions).
NaCl-treated moss was obtained in increments by the step-wise addition of NaCl (50 mM 2 h, 50 mM+50 mM 2 h, and 100 mM+50 mM 2 h; 6 h total application) or by shock treatment by incubation in 50 mM, 100 mM or 150 mM for 6 h (Fig. 4). Initial salt treatments resulted in an increase in Vac1 transcripts of 2–4-fold relative to controls. In the total RNA fraction, Vac1 steady-state transcript levels declined during sustained exposure to 150 mM NaCl, and the decline is more pronounced under shock treatment than in the incremental increase in NaCl-treatments, which allows for acclimation to increasing salt concentrations. The decrease in Vac1 transcripts in the total RNA fractions under high salt conditions (Fig. 4A) was not observed under similar salt-stress conditions in the polysomal RNA fraction (Fig. 4B). In sharp contrast to a desiccation–rehydration cycle, Vac1 steady-state mRNA levels increased in response to salinity, and are preferentially recruited to the polysomal RNA fraction.
Accumulation of VAC1 in T. ruralis gametophytes
To determine the response of VAC1 protein expression in response to salinity, microsomal proteins were separated by SDS-PAGE and subjected to immunoblotting using polyclonal antibody raised against synthetic peptides corresponding to the N- or C-terminal domains of the cotton c subunit (Schumacher et al., 1999) (Fig. 5). Compared to the deduced cotton peptide, Tortula VAC1 N-terminal and C-terminal domains share 60% (6/10) and 90% (9/10) amino acid identity, respectively (Fig. 1A). Despite the divergence in the terminal domains, a 16 kDa protein of the expected molecular weight for the V-ATPase proteolipid subunit was recognized by both the cotton C-terminal (Fig. 5) and N-terminal (data not shown) polyclonal antibodies. The relative amount of the 16 kDa peptide was unchanged in response to desiccation and rehydration (data not shown), or increasing salt exposure or salt shock (Fig. 5).
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Discussion |
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The analysis of ESTs has been a powerful analytical technique for the discovery of new genes in mosses including Physcomitrella patens (Reski et al., 1998
; Machuka et al., 1999) and T. ruralis (Wood et al., 1999). In this paper, the isolation and characterization of the EST-derived T. ruralis cDNA Vac1 encoding a predicted polypeptide with significant similarity to the V-ATPase c subunit is described. Vac1 steady-state transcript levels were unchanged in either the total or polysomal RNA fractions relative to controls during a desiccation–rehydration cycle (Fig. 3), nor did the abundance of VAC1 protein change in response to salt stress (Fig. 5). In response to salinity-stress in T. ruralis Vac1, steady-state transcript levels increased within total RNA under moderate salt stress, but preferentially accumulated within the polysomal RNA fraction under increasing salt concentrations (Fig. 4) although no concomitant increase in VAC1 protein was detected (Fig. 5). Previous research using T. ruralis has demonstrated that during rehydration mRNAs are differentially selected from a qualitatively identical mRNA pool (Oliver, 1991), and that mRNA preferentially accumulate within the polysomal RNA fraction during a desiccation–rehydration cycle (Scott and Oliver, 1994). It was subsequently demonstrated that a variety of mRNA transcripts are stably maintained within the polysomal RNA fractions of desiccated gametophytes (Duff et al., 1999; Zeng and Wood, 2000; Wood et al., 2000a) and that Tr288 transcripts are conserved in association with proteins as mRNPs (Wood and Oliver, 1999). In the case of desiccation, it was hypothesized that differential recruitment of mRNAs to the polysomal fraction is mediated by mRNPs and that those genes stably maintained within the polysomal RNA fractions are essential to the maintenance of the constitutive tolerance protection system(s) (Wood and Oliver, 1999; Oliver et al., 2000; Wood et al., 2000a). However, in the case of Vac1, mRNA transcripts preferentially accumulate within the polysomal RNA fraction in response to salinity rather than desiccation (Fig. 4). The present data suggest that T. ruralis employs a similar strategy for the post-transcriptional control of genes involved in the adaption to salinity-stress as it does for the control of genes involved in adaption to desiccation-stress.
Anatomically, T. ruralis gametophytes are a leafy shoot comprised of an axial conducting core (i.e. xylem-like water-conducting tissues) with leaves that are one cell thick except at the multi-stratose mid-vein (Oliver and Bewley, 1984). Like all mosses, T. ruralis gametophytes lack stomata and cannot regulate their intracellular water status by modulating the gas exchange properties of the leaf tissue. Terminally differentiated bryophyte cells generally contain a single vacuole (Paolillo and Reighard, 1967). However, a number of moss species, including the desiccation-tolerant species T. ruralis (Oliver and Bewley, 1984) and Pleurozium schreberi (Noailles, 1978) contain several vacuoles of moderate volume. During a desiccation–rehydration cycle in T. ruralis (Tucker et al., 1976) and P. schreberi (Noailles, 1978) the multiple vacuoles divide into several smaller vacuole-derived vesicles which fuse upon rehydration to re-form the vacuole. Vacuolar fragmentation and reformation during a desiccation–rehydration cycle is also seen within the desiccation-tolerant angiosperms Craterostigma wilmsii, Myrothamnus flabellifolius, and Xerophyta humilis (Farrant, 2000). The vacuole in desiccation-tolerant plants is a dynamic structure and it is postulated that any gene product that mediates vacuolar fragmentation and reformation must play a fundamental role in the ability of resurrection plants to survive complete drying of their vegetative structures. The V0 domain, of which subunit c is the primary constituent, is postulated to mediate fusion of intracellular membranes, such as the vacuole (Peters et al., 2001). In yeast, calmodulin has been shown to bind to the c subunit and is thought to induce a large conformational change upon the V0 domain (i.e. increase the pore opening by radial expansion of the central hydrophilic cavity). Further, V0 domains from opposing membranes are capable of forming a trans-complex in a calmodulin- and GTP-dependent manner and the V0 trans-complexes are postulated to form a continuous proteolipid-lined pore at the membrane fusion site. Peters et al. propose that radial expansion of V0 trans-complexes may provide a central mechanism for intracellular membrane fusion (Peters et al., 2001).
Gene discovery efforts have identified V-ATPase components in other resurrection plants: subunit A from Sporobolus stapfianus (Blomstedt et al., 1998), and subunit c from M. flabellifolius (S Mundree, University of Cape Town, South Africa, personal communication). The Physcomitrella EST Program (http://www.moss.leeds.ac.uk) has identified two subunit c ESTs in the moss P. patens and the authors' research group is in the process of obtaining full-length P. patens c subunit cDNAs (AJ Wood, unpublished results). Efficient targeted gene disruption (i.e. homologous recombination) is a well-established tool in P. patens (Schaefer and Zryd, 1997). This capability is at present unique amongst all plants and represents an extremely powerful technique for the functional analysis of plant genes (Wood et al., 2000b). Mosses such as T. ruralis and P. patens will be key experimental systems for the study of V-ATPase function in vivo, and will provide greater insight to the role which V0 plays in tonoplast and endomembrane fusion, adaption to elevated NaCl concentration, desiccation-tolerance, and to stress-inducible post-transcriptional gene control.
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Acknowledgments |
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The authors thank Barbara Crandall-Stotler (Southern Illinois University, Carbondale, IL) for helpful discussions. This work was supported in part by a grant to AJW (USDA NRI No. 9735100).
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Notes |
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1 The nucleotide sequence data appear in EMBL, GenBank and DDBJ Nucleotide Sequence Databases under the accession number AF303372.
4 To whom correspondence should be addressed. Fax: +1 618 453 3441. E-mail: wood{at}plant.siu.edu
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Abbreviations |
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DCCD, N,N'-dicyclohexylcarbodiimide; mRNP, messenger ribonucleoprotein particle..
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Wood AJ, Duff RJ, Oliver MJ. 2000a. The translational apparatus of Tortula ruralis: polysomal retention of transcripts encoding the ribosomal proteins RPS14, RPS16 and RPL23 in desiccated and rehydrated gametophytes. Journal Experimental Botany 51, 1655–1662.
Wood AJ, Oliver MJ, Cove DJ. 2000b. Frontiers in bryological and lichenological research. I. Bryophytes as model systems. The Bryologist 103, 128–133.
Zeng Q, Wood AJ. 2000. A cDNA encoding ribosomal protein RPL15 from the desiccation-tolerant bryophyte Tortula ruralis: mRNA transcripts are stably maintained in desiccated and rehydrated gametophytes. Bioscience Biotechnology Biochemistry 64, 2221–2224.
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