Journal of Experimental Botany, Vol. 51, No. 351, pp. 1655-1662,
October 2000
© 2000 Oxford University Press
Original Papers |
The translational apparatus of Tortula ruralis: polysomal retention of transcripts encoding the ribosomal proteins RPS14, RPS16 and RPL23 in desiccated and rehydrated gametophytes
1 Department of Plant Biology, Southern Illinois University-Carbondale, Carbondale, IL 62901–6509, USA
2 Plant Stress and Water Conservation Laboratory, Plant Stress and Genome Development Unit, 3810 Fourth Street, Lubbock, TX 79415, USA
Received 18 December 1999; Accepted 20 May 2000
 |
Abstract |
|---|
 Top Abstract IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Tortula ruralis (Syntrichia ruralis) is an important model system for the study of plant vegetative desiccation tolerance. One of the most intriguing aspects of desiccation-tolerant plants is the maintenance of key cellular components in stable and viable forms in the desiccated state, particularly those related to the translational apparatus (i.e. ribosomes and ribosomal RNAs). This study investigated the third integral component of the translational apparatus, the ribosomal proteins. Three T. ruralis cDNAs encoding predicted polypeptides with significant similarity to ribosomal proteins were isolated from a cDNA expression library derived from the polysomal, messenger ribonucleoprotein particle (mRNP) fraction of desiccated gametophytes; Rps14 and Rps16 encode the small-subunit ribosomal proteins RPS14 and RPS16, respectively, and Rpl23 encodes the large-subunit ribosomal protein RPL23. RPS14, RPS16 and RPL23, the deduced polypeptides, have predicted molecular masses of 14.4 kDa, 16.2 kDa and 14.9 kDa and predicted pI's of 11.08, 10.34 and 10.67, respectively. Phylogenetic analysis of the deduced amino acid sequences demonstrated that each of the T. ruralis proteins is most similar to ribosomal proteins from higher plants even though RPS14 and RPL23 show high divergence from their other plant counterparts. RNA blot hybridizations of RNAs present within the polysomal mRNP fraction (i.e. the 100 Kxg pellet) demonstrated that Rps14, Rps16 and Rpl23 are expressed in moss gametophytes during a desiccation–rehydration cycle and, according to the prior cDNA classification scheme in T. ruralis, are constitutive clones. These findings clearly demonstrated that Rps14, Rps16 and Rpl23 transcripts are retained within the polysomal fractions of desiccated gametophytes.
Key words: Desiccation, moss, ribosomal protein, Tortula ruralis, translation.
|
Introduction |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Desiccation-tolerant plants, commonly known as resurrection plants, possess the unique ability to survive severe water deficit and revive from the air-dried state (Bewley, 1979
). Most plants are capable of producing desiccation-tolerant tissues, in particular seeds and pollen, but few can survive the drying of their vegetative structures (Oliver and Bewley, 1997). Although uncommon, vegetative desiccation-tolerance is widely distributed throughout the plant kingdom ranging from bryophytes and pteridophytes to angiosperms (Bewley and Krochko, 1982; Ingram and Bartels, 1996; Oliver and Bewley, 1997; Farrant et al., 1999). One of the most intriguing aspects of desiccation-tolerant plants is the maintenance of key cellular components in stable and viable forms in the desiccated state.
The bryophyte Tortula ruralis (Syntrichia ruralis) is an important model system for the study of plant vegetative desiccation-tolerance and post-transcriptional gene control (reviewed in Oliver and Bewley, 1997; Oliver and Wood, 1997; Oliver et al., 1997, 1998; Wood et al., 2000b). T. ruralis gametophytes can be rapidly dried to extremely low relative water contents (i.e. 1 h over activated silica gel) or at speeds that resemble field rates for Tortula clumps (i.e. 6 h at 67% RH in a closed atmosphere) and the gametophytes fully recover normal activity upon rehydration. The ability for cells to conduct protein synthesis rapidly declines as T. ruralis gametophytic tissues desiccate (Bewley, 1972, 1973b). This loss of protein synthetic capacity is manifested in a loss of polysomes that result from the run-off of ribosomes from mRNAs coupled with a failure in the initiation machinery (see Bewley, 1979, for a review). Protein and RNA synthesis recover rapidly upon rehydration of desiccation-tolerant mosses (Bewley, 1973a, b; Gwozdz et al., 1974; Oliver and Bewley, 1984a). The rate of recovery to control levels is dependent upon the rate of prior desiccation, the slower the rate of drying the faster the recovery (Gwozdz et al., 1974; Oliver and Bewley, 1984a). It has been postulated (Wood and Oliver, 1999) that transcripts which are maintained in the slow-dried state and can be isolated in the polysomal fraction (i.e. the 100 Kxg pellet) are conserved in association with proteins as messenger ribonucleoprotein particles (mRNPs) (Spirin et al., 1964).
In sharp contrast to desiccation-intolerant angiosperms, T. ruralis maintains the integrity of the translational apparatus when cells experience severe water-deficits (Bewley, 1972). Both ribosomes and ribosomal RNAs are stable during desiccation. Upon rehydration, both the conserved and newly synthesized pools of these components swiftly embark on the formation of new polysomes (Oliver and Bewley, 1984b, c). The plant ribosome is composed of both the large (60S) and small (40S) ribosomal subunits, and a cadre of ribosomal proteins (r-proteins) (Bailey-Serres, 1998). Small- or large-ribosomal proteins are key structural components of a functional ribosome and contribute to the proper and efficient translation of mRNAs (Moore, 1998). Plant r-proteins are categorized using a unified system of nomenclature that is based upon rat r-protein designations (Wool et al., 1991; Bailey-Serres, 1998). There are estimated to be 78 r-proteins in rat, all with an apparent molecular mass less than 50 kDa and the majority with a pI greater than 8.5 (Wool et al., 1995). Plant r-proteins have similar biophysical properties; however, due to the lack of a systematic study within a single model plant, the number of r-proteins in angiosperms is estimated to range from 75 to 92 polypeptides (Bailey-Serres, 1998).
The re-establishment of translational efficiency within rehydrated T. ruralis requires the formation of a functional ribosome, including a myriad of r-proteins. The rapid recovery of protein synthesis is indicative of a stable population of r-proteins (either as a pool of conserved peptide and/or mRNA, or as newly synthesized gene products or as part of stable and intact ribosomes) available for incorporation into a polyribosomal complex (Bewley, 1973a, b; Gwozdz et al., 1974; Oliver and Bewley, 1984a, c). We postulate that genes essential to recovery and cellular repair (such as r-proteins) are preferentially expressed upon rehydration of desiccated gametophytes, and genes that are essential to limiting cellular damage are expressed under hydrated and rehydrated conditions (Oliver and Wood, 1997; Wood and Oliver, 1999; Wood et al., 1999). In this report, the isolation and mRNA accumulation of three T. ruralis cDNAs encoding predicted polypeptides with significant similarity to the ribosomal proteins RPS14, RPS16 and RPL23 are described (Bailey-Serres, 1998).
|
Materials and methods |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Plant material
Gametophytes of Tortula ruralis [Hedw.] Gaerten., Meyer & Scherb. were collected, harvested, desiccated and rehydrated as described previously (Wood et al., 1999
). Voucher specimens are kept at the Jepson and University Herbarium (UC; University of California, Berkeley, CA, USA). Hydrated moss was obtained after a 24 h rehydration period and rapid-dried moss was obtained by placing cut hydrated gametophytes on a filter paper disc over activated silica gel in a glass Petri dish. The air-dried weight (c. 20% of the original fresh weight) is achieved in 1 h for rapid-dried gametophytes. Rehydrated moss was obtained by the addition of ddH2O to desiccated moss.
Isolation of cDNA clones, DNA sequencing and DNA analysis
A directionally cloned (EcoRI/XhoI) cDNA library of 1.5x106 primary transformants was constructed in phage lambda (Uni-ZAP XR, Stratagene, LaJolla, CA, USA) by the unidirectional insertion of oligo-dT-primed cDNA derived from the polysomal, mRNP fraction (i.e. the 100 Kxg pellet) of desiccated gametophytes (Wood et al., 1999). The amplified phage library was converted to a plasmid library by mass excision to release the phagemid vector. 152 individual clones were picked at random from the plasmid library and manual single-pass sequencing of the 3' ends was performed. Plasmid DNA was isolated following the alkali lysis protocol and sequenced directly with the T7-, T3-universal or M13 reverse primers. The dideoxy chain termination method (Sanger, 1981) was employed using [35S]-dATP and SequiTherm Excel II (Epicentre Technologies Corp., Madison WI, USA) following the manufacturer's protocol for non-cycle sequencing. Resulting DNA fragments were electrophoresed on 6% acrylamide gels, fixed, and exposed to film using standard techniques. Sequences were then read into Vector NTI (InforMax, North Bethesda, MD, USA) which was used for sequence assembly, analysis and homology searches. Similarity of the T. ruralis sequences to nucleotide sequences in GenBank, EMBL, DDBJ, and PDB databases were determined using the FASTA and BLASTN server (as described by Wood et al., 1999). MW and pI prediction, identification of targeting sequences, and alignment of deduced amino acid sequences were performed using software available on the ExPASy molecular biology server (www.expasy.ch/).
Three separate data sets, corresponding to RPS14, RPS16 or RPL23, were used for phylogenetic analyses. Each data set included the newly generated T. ruralis deduced amino acid sequence and deduced amino acid sequences from additional taxa, obtained from GenBank, previously identified as RPS14, RPS16 or RPL23 homologues. RPS14 data set: Caenorhabditis elegans (P48150), Cricetulus griseus (M11241), Drosophila melanogaster (M21045), Homo sapiens (NP005608), Kluyveromyces marxianus (S53438), Lupinus luteus (AF026079), Mus musculus (Y08307), Nicotiana tabacum (U66262), Podocoryne carnea (X71384), Rattus norvegicus (X15040), Trypanosoma brucei (M36124), and Zea mays (P19950). RPS16 data set: Arabidopsis thaliana (Q42340), C. elegans (Q22054), Fritillaria agrestis (AF031546), Gossypium hirsutum (X75954), H. sapiens (M60854), Lupinus polyphyllus (X51766), M. musculus (P14131), Oryza sativa (L36313), Rattus rattus (X17665), and Schizosaccharomyces pombe (AB017604). RPL23 data set: Brugia malayi (U66218), C. elegans (P48158), D. melanogaster (M85295), H. sapiens (X52839), Leishmania infantum (AF097022), N. tabacum (L18915), O. sativa (D10404), Picea mariana (AF051229), R. rattus (X58200), Saccharomyces cerevisiae (X01694), and Trypanosoma cruzi (D87216). Amino acid sequences were aligned manually with the SeqApp program (Gilbert, 1993). In each case it was not possible unambiguously to align portions of the extreme amino and carboxyl termini of the sequences. These portions, therefore, were eliminated from subsequent phylogenetic analyses. Distance matrices were calculated from the amino acid data and phylogenetic trees were constructed using the Neighbor-Joining algorithm as implemented in PAUP* Version 4.0 b2a (Swofford, 1998). The amount of support for each node of the resultant trees was examined with 100 bootstrap replicates (Felsenstein, 1985) with the random addition option using Neighbor joining.
RNA isolation and RNA blot hybridizations
Polysomal RNA was isolated and RNA blot analysis performed using standard techniques (as described by Duff et al., 1999). Polysomes were extracted from gametophytic tissue using a low salt extraction buffer (200 mM sucrose, 200 mM TRIS-HCl pH 8.5, 60 mM KCl, 50 mM magnesium acetate, 5 mM DTT, 5 mM EGTA, 1% (v/v) NP-40, 0.5% (v/v) deoxycholate, 100 mg ml–1 heparin, 50 µg ml–1 cycloheximide, and 10 mM ribonucleoside–vanadyl complex) (Wood and Oliver, 1999). The 27000 g supernatant was layered over a sucrose pad (1.5 M sucrose, 40 mM TRIS-HCl pH 8.5, 20 mM KCl, 10 mM magnesium acetate, 5 mM DTT, 100 mg ml–1 heparin) and centrifuged at 100 000 g for 90 min in a 50TI ultracentrifuge rotor (Beckman Scientific, Fullerton, CA, USA). The polysomal pellet (100 Kxg pellet) was solubilized in polysome-resuspension buffer (10 mM TRIS-Cl pH 7.5, 1 mM EDTA, 200 mM KCl).
After transfer of the RNA, hybridizations were accomplished by incubating membranes overnight at 62 °C in prehybridization buffer (0.5 M NaPO4, pH 7.1, 1% SDS, 1% BSA, and 100 µg ml–1 of sonicated salmon sperm DNA). The probe used in the analysis was the full cDNA insert from the appropriate plasmid (i.e. RNP20, RNP37 or RNP47). The isolated insert was labeled with [
32P]-dCTP (Amersham Pharmacia, Piscataway, NJ, USA) using the Decaprime II kit (Ambion, Austin, TX, USA). DNA probe was boiled for 5 min and added directly to the prehybridization solution. Membranes were initially washed at 42 °C followed by a 62 °C in wash buffer (40 mM NaPO4, pH 7.1, 0.1% SDS) until the membrane gave near background readings on a hand-held monitor. Blots were stripped and re-probed with rRNA-DNA to demonstrate equal loading.
|
Results |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Characterization of Rps14, Rps16 and Rpl23
A cDNA expression library was constructed from the polysomal, mRNP fraction (i.e. the 100 Kxg pellet) of desiccated T. ruralis gametophytes (Oliver and Wood, 1997
) and more than 150 expressed sequence tags (ESTs) were characterized (Duff et al., 1999; Wood et al., 1999, 2000a). The complete DNA sequence was determined for three full-length EST clones RNP20, RNP37 and RNP47 (see Materials and methods). Sequence similarity of the RNP20 (accession number AI305056), RNP37 (accession number AI305072) and RNP47 (accession number AI305082) nucleotide sequences to nucleotide sequences in GenBank, EMBL, DDBJ, and PDB databases was determined using the BLASTN server. The RNP20 and RNP37 nucleotide sequences were shown to have significant identity to the rat small-subunit ribosomal proteins RPS14 (Paz et al., 1989) and RPS16 (Chan et al., 1990), respectively (Fig. 1A, B). The RNP47 nucleotide sequence was shown to have significant identity to the rat large-subunit ribosomal protein L23 (Chan et al., 1991) (Fig. 1C). In keeping with the nomenclature conventions established for ribosomal protein genes in plants (Wool et al., 1991; Bailley-Serres, 1998), these T. ruralis genes (i.e. RNP20, RNP37 and RNP47) have been named Rps14, Rps16 and Rpl23, and the encoded polypeptides RPS14, RPS16 and RPL23, respectively.
|
Rps14 was 585 bp in length and contained a single, continuous open reading frame from nucleotide 63 to 469 flanked by a 62 bp 5' UTR, a 116 bp 3' UTR and a poly (A) tail comprised of 18 adenylate residues (data not shown). The ORF encodes a polypeptide of 134 amino acids with a predicted molecular mass of 14.4 kDa and predicted pI of 11.08 (Fig. 1A
; Table 1). Rps16 was 585 bp in length and contained a single, continuous open reading frame from nucleotide 34 to 462 flanked by a 33 bp 5' UTR, a 123 bp 3' UTR and a poly (A) tail comprised of 30 adenylate residues (data not shown). The ORF encodes a polypeptide of 142 amino acids with a predicted molecular mass of 16.2 kDa and predicted pI of 10.34 (Fig. 1B; Table 1). Rpl23 was 529 bp in length and contained a single, continuous open reading frame from nucleotide 35 to 452 flanked by a 34 bp 5' UTR, a 77 bp 3' UTR and a poly (A) tail comprised of 14 adenylate residues (data not shown). The ORF encodes a polypeptide of 248 amino acids with a predicted molecular mass of 14.9 kDa and predicted pI of 10.67 (Fig. 1C; Table 1). In each case, the initiation and termination sequences conformed to the known consensus sequences in plants (Lutcke et al., 1987), and each cDNA contained putative polyadenylation signal sequences (data not shown). Rps14, Rps16 and Rpl23 each contained the highly conserved far-upstream element which has been designated as the UUG-core motif (Wood et al., 2000a). Rps14 (AAUUAA, nucleotide 539), Rps16 (AAUGUA, nucleotide 507) and Rpl23 (AUGAUA, nucleotide 492) also contained putative near-upstream polyadenylation signals similar to the plant consensus polyadenylation motifs (AAUAAA or AUGAAA) (Wood et al., 2000a).
|
Predicted cellular localization of RPS14, RPS16 and RPL23
Ribosome biogenesis occurs primarily within the nucleolus (Bailey-Serres, 1998). The majority of r-proteins are therefore nuclear localized and become associated with nuclear pre-ribosomes, although some r-proteins are added after transport to the cytoplasm (Scharf and Nover, 1987). T. ruralis RPS16 and RPL23 are both strongly predicted to be nuclear localized by PSORT (see Materials and methods) (Table 1) and each contains a version of the bipartite nuclear sequence (residues 12–28 and 72–88, respectively) (Fig. 1B, C; Table 1). The bipartite nuclear sequence (BNS) was initially characterized in Xenopus and is comprised of two interdependent basic domains that are postulated to interact with a receptor molecule in the transport process (Robbins et al., 1991). RPS14 is not predicted by PSORT to be targeted to the nucleus and contains no known nuclear localization signal (Table 1).
Phylogenetic analysis of RPS14, RPS16 and RPL23
To examine the structural relationship between the predicted polypeptides RPS14, RPS16 and RPL23 and similar r-proteins, the deduced amino acid sequences were analysed by the Neighbor-Joining method. Three separate phylogenetic trees, assembled from the pairwise alignment of these deduced polypeptide sequences, are depicted in Fig. 2. In each case the Tortula sequence groups with other plant sequences even though the deduced Rps14 and Rpl23 sequences are shown to be significantly divergent from their angiosperm counterparts. In contrast, the deduced polypeptide sequence of Rps16 is shown to be as similar to the angiosperm Fritillaria as the included angiosperms are to one another.
|
Expression of Rps14, Rps16 and Rpl23 in T. ruralis gametophytes
The steady-state mRNA accumulation of T. ruralis Rps14, Rps16 and Rpl23 transcripts were analysed by RNA blot hybridization using polysomal mRNA fractions of treated gametophytes (Fig. 3A, B, C). Polysomal RNA was isolated from hydrated, rapid-dried (RD) and rapid-dried rehydrated tissues as described in the Materials and methods. To enable normalization of the hybridization signals to account for loading anomalies, the membrane was re-probed after the initial analysis using a plant 18S nuclear rRNA probe. T. ruralis Rps14, Rps16 and Rpl23 each hybridized to a single mRNA species of approximately 1, 1.5 and 2.0 kb, respectively. T. ruralis Rps14, Rps16 and Rpl23 transcript are present within control (i.e. hydrated) rapid-dried, and RD rehydrated RNA fractions (Fig. 3A, B, C).
|
|
Discussion |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
The isolation and characterization of three Tortula ruralis cDNAs from a desiccated gametophyte cDNA library encoding polypeptides with significant similarity to ribosomal proteins RPS14, RPS16 and RPL23 have been described. These findings clearly demonstrate that Rps14, Rps16 and Rpl23 transcripts are retained within the polysomal fractions of desiccated and rehydrated gametophytes (Fig. 3
). Previously, three distinct classes of cDNA clones in T. ruralis had been identified based upon the relative recruitment of their corresponding transcripts into the polysomal fraction of hydrated, and rapid-dried (RD) rehydrated 2 h gametophytes (Oliver, 1991). These classes included constitutive cDNAs, cDNAs representing hydrin transcripts and cDNAs representing rehydrin transcripts (Scott and Oliver, 1994). 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 prior cDNA classification scheme Rps14, Rps16 and Rpl23 are constitutive clones. It has been hypothesised that genes essential to recovery and cellular repair are preferentially expressed upon rehydration of desiccated gametophytes, i.e. the rehydrins (Oliver and Bewley, 1997; Wood and Oliver, 1999; Duff et al., 1999). It has also been postulated that constitutive transcripts consist of both important housekeeping genes and those genes that maintain the constitutive desiccation-tolerance protection system(s). In this scenario RPS14, RPS16 and RPL23 could fit into either category of constitutive gene products.
The defining character of r-proteins is their interaction with the ribosome (Moore, 1998). However, extraribosomal enzymatic activity has been identified for numerous r-proteins and this activity is increasingly recognized as biologically significant (Wool, 1996). Mutant analysis within A. thaliana has clearly demonstrated the existence of ‘multipurpose’ r-proteins. RPS18 has been identified as pfl, a nuclear recessive mutation that causes pointed first leaves (Van Lijsebettens et al., 1994) and RPS27 has been identified as ars27A, a T-DNA insertional mutant that is sensitive to methyl methane sulphate (Revenkova et al., 1999). Studies on animal systems further the concept of ‘multipurpose’ r-proteins. H. sapiens RPS19 is associated with Diamond-Blackfan anaemia, a chronic constitutional aregenerative anaemia (Draptchinskaia et al., 1999). Murine r-protein S3 has activity indistinguishable from UV endonuclease III and is implicated in DNA damage processing (Kim et al., 1995). D. melanogaster RPS3 has been shown to possess both apurinic/apyrimidinic lyase and deoxyribophosphodiesterase activities and has been postulated to play a key role in the eukaryotic DNA base excision repair pathway (Sandrigursky et al., 1997).
Stored r-protein mRNAs, encoding RPS4 and RPS6, have been characterized in desiccated embryo axes of maize (Beltrana-Pena et al., 1995) and are predicted to be actively translated upon rehydration and germination. RPS14 homologues have been identified as a stress-inducible gene in an EST study of the desiccation-tolerant angiosperm Craterostigma plantagineum (Bockel et al., 1998) and by a functional cloning screen for genes that elicit the hypersensitive response in tobacco leaves (Karrer et al., 1998). Empirical evidence is accumulating which suggests r-proteins are not only central to translational efficiency, but have important pleiotropic effects.
Earlier analyses demonstrated that slow drying of T. ruralis gametophytes results in a rapid decline in protein synthesis that is manifested in a complete loss of polysomes (Oliver and Bewley, 1997). It has been postulated (Wood and Oliver, 1999) that transcripts which are maintained in the slow-dried state and can be isolated in the 100 Kxg pellet, such as Rps14, Rps16 and Rpl23 (Fig. 3), are conserved in association with proteins as mRNPs (Spirin et al., 1964; Pramanik et al., 1992). The 100 Kxg pellet used for RNA blot analysis, and to generate the cDNA library, contains most of the cytosolic translational machinery, such as RNA-protein complexes and ribosomes, as well as other cellular constituents which have sufficient mass to pellet through a 1.5 M sucrose pad at 100 000 g over 90 min. It has been demonstrated that mRNP formation in response to desiccation does occur in T. ruralis for at least one mRNA transcript (i.e. the rehydrin Tr288) (Wood and Oliver, 1999). As a general phenomenon, it is hypothesized that the formation of mRNPs in response to desiccation, and their possible roles in mRNA storage and protection, has important consequences for the study of vegetative desiccation-tolerance. The capability to store key components during a stress event that are needed for recovery offers a sensitive and flexible response to environmental stresses. It is postulated that post-transcriptional gene control allows a more rapid return to growth than does the relatively slower activation and transcription of specific stress or stress-recovery response genes. Even in plants where gene activation is a common response to water loss, it is possible that certain transcripts required for the recovery process are stored in mRNPs during drying. The polysomal retention of Rps3a (Duff et al., 1999) and Rps14, Rps16 and Rpl23 transcripts in desiccated gametophytes indicates that not all transcripts made in response to a stress event are required for immediate use but may be synthesized and stored for the recovery period.
|
Acknowledgments |
|---|
This work was supported in part by grants to AJW (USDA, NRI-CGP grant number 9735100) and MJO (CRIS project 6208-21000-008-00D). The authors thank Youngkoo Cho and Qin Zeng (Southern Illinois University, Carbondale, IL, USA) for reviewing the manuscript, and Marie Syapin for technical assistance. Mention of a trademark or proprietary product does not constitute a guarantee or warranty of the product by the United States Department of Agriculture, and does not imply its approval to the exclusion of other products that may also be suitable. The nucleotide sequence data appear in EMBL, GenBank and DDBJ Nucleotide Sequence Databases under the accession numbers AF108724, AF108725 and AF108726.
|
Notes |
|---|
3 To whom correspondence should be addressed. Fax: +1 618 453 3441. E-mail: wood{at}plant.siu.edu
4 Present address: Department of Biology, University of Akron, Akron, OH 44325-3908, USA.
|
Abbreviations |
|---|
EST, expressed sequence tag; ORF, open reading frame.
|
References |
|---|
|
TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Bailey-Serres J.1998. Cytoplasmic ribosomes of higher plants. In: Bailley-Serres J, Gallie DR, eds. A look beyond transcription: mechanisms determining mRNA stability and translation in plants. Rockville, MD, USA: American Society of Plant Physiologists, 125–144.
Beltrana-Pena E, Ortiz-Lopez A, Sanchez de Jimenez E.1995. Synthesis of ribosomal proteins from stored mRNAs early in seed germination. Plant Molecular Biology 28, 327–336.[Web of Science][Medline]
Bewley JD.1972. The conservation of polyribosomes in the moss Tortula ruralis during total desiccation. Journal of Experimental Botany 2, 692–698.
Bewley JD.1973a. Polyribosomes conserved during desiccation of the moss Tortula ruralis are active. Plant Physiology 51, 285–288.
Bewley JD.1973b. Desiccation and protein synthesis in the moss Tortula ruralis. Canadian Journal of Botany 51, 203–206.
Bewley JD.1979. Physiological aspects of desiccation-tolerance. Annual Review of Plant Physiology 30, 195–238.[Web of Science]
Bewley JD, Krochko J.1982. Desiccation-tolerance. In: Lange OL, Nobel PS, Osmond CB, Ziegler H, eds. Encyclopedia of plant physiology, Vol. 12B. Physiological ecology II. Berlin: Springer-Verlag, 325–378.
Bockel C, Salamini F, Bartels D.1998. Isolation and characterization of genes expressed during early events of the dehydration process in the resurrection plant Craterostigma plantagineum. Journal of Plant Physiology 152, 158–166.
Chan YL, Paz V, Olvera J, Wool IG.1990. The primary structure of rat ribosomal protein S16. FEBS Letters 263, 85–88.[Web of Science][Medline]
Chan YL, Paz V, Wool IG.1991. The primary structure of rat ribosomal protein L23. Biochemical and Biophysical Research Communications 178, 1153–1159.[Web of Science][Medline]
Draptchinskaia N, Gustavsson P, Andersson B, et al.1999. The gene encoding ribosomal protein S19 is mutated in Diamond-Blackfan anemia. Nature Genetics 21, 169–175.[Web of Science][Medline]
Duff RJ, Oliver MJ, Wood AJ.1999. A Tortula ruralis cDNA encoding small-subunit ribosomal protein S3a: polysomal retention of transcript in response to desiccation and rehydration. The Bryologist 102, 418–425.
Farrant JM, Cooper K, Kruger LA, Sherwin HW.1999. The effect of drying rate on the survival of three desiccation-tolerant angiosperm species. Annals of Botany 84,371–379.
Felsenstein E.1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.[Web of Science]
Gilbert DG.1993. SeqApp, version 1.9a157. Bloomington, IN: Biocomputing Office, Biology Department, Indiana University.
Gwozdz EA, Bewley JD, Tucker EB.1974. Studies on protein synthesis in Tortula ruralis: polyribosome reformation following desiccation. Journal of Experimental Botany 25, 599–608.
Ingram J, Bartels D.1996. The molecular basis of dehydration tolerance in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47, 377–403.[Web of Science][Medline]
Karrer EE, Beachy RN, Holt CA.1998. Cloning of tobacco genes that elicit the hypersensitive response. Plant Molecular Biology 36, 681–690.[Web of Science][Medline]
Kim J, Chubatsu LS, Admon A, Stahl J, Fellous R, Linn S.1995. Implication of mammalian ribosomal protein S3 in the process of DNA damage. Journal of Biological Chemistry 270, 13620–13629.
Lutcke HA, Chow KC, Mickel FS, Moss KA, Kern HF, Scheele GA.1987. Selection of AUG initiation codons differs in plants and animals. EMBO Journal 6, 43–48.[Web of Science][Medline]
Moore PB.1998. The three-dimensional structure of the ribosome and its components. Annual Review of Biomolecular Structure 27, 35–58.[Web of Science][Medline]
Oliver MJ.1991. Influence of protoplasmic water loss on the control of protein synthesis in the desiccation-tolerant moss Tortula ruralis: ramifications for a repair-based mechanism of desiccation-tolerance. Plant Physiology 97, 1501–1511.
Oliver MJ, Bewley JD.1984a. Plant desiccation and protein synthesis. IV. RNA synthesis, stability, and recruitment of RNA into protein synthesis upon rehydration of the desiccation-tolerant moss Tortula ruralis. Plant Physiology 74, 21–25.
Oliver MJ, Bewley JD.1984b. Plant desiccation and protein synthesis. V. Stability of poly(A)– and poly(A)+ RNA during desiccation and their synthesis upon rehydration in the desiccation-tolerant moss Tortula ruralis and the intolerant moss Crateneuron filicinum. Plant Physiology 74, 917–922.
Oliver MJ, Bewley JD.1984c. Plant desiccation and protein synthesis. VI. Changes in protein synthesis elicited by desiccation of the moss Tortula ruralis are effected at the translational level. Plant Physiology 74, 923–927.
Oliver MJ, Bewley JD.1997. Desiccation-tolerance of plant tissues: a mechanistic overview. Horticulture Reviews 18, 171–212.
Oliver MJ, Wood AJ.1997. Desiccation-tolerance of mosses. In: Koval T, eds. Stress-inducible processes in higher eukaryotic cells. New York: Plenum Publishing Corporation, 1–26.
Oliver MJ, Wood AJ, O'Mahony P.1997. How some plants recover from vegetative desiccation: a repair based strategy. Acta Physiologia Plantarum 19,419–425.
Oliver MJ, Wood AJ, O'Mahony P.1998. ‘To dryness and beyond’—preparation for the dried state and rehydration in vegetative desiccation-tolerant plants. Plant Growth Regulation 24, 193–201.
Paz V, Chan YL, Gluck A, Wool IG.1989. The primary structure of rat ribosomal protein S14. Nucleic Acids Research 17, 9484.
Pramanik SK, Krochko JE, Bewley JD.1992. Distribution of cytosolic mRNAs between polysomal and ribonucleoprotein complex fractions in alfalfa embryos. Plant Physiology 99, 1590–1596.
Revenkova E, Masson J, Koncz C, Afsar K, Jakovleva L, Paszkowski J.1999. Involvement of Arabidopsis thaliana ribosomal protein S27 in mRNA degradation triggered by genotoxic stress. EMBO Journal 18, 490–499.[Web of Science][Medline]
Robbins J, Dilworth SM, Laskey RA, Dingwall C.1991. Two independent basic domains in nucleoplasmin nuclear targeting sequence: identification of a class of bipartite nuclear targeting sequence. Cell 64, 615–623.[Web of Science][Medline]
Sanger F.1981. Determination of nucleotide sequences in DNA. Science 214, 1205–1210.
Sandrigursky M, Yacoub A, Kelley MR, Deutsch WA, Franklin WA.1997. The Drosophila ribosomal protein S3 contains a DNA deoxyribophosphodiesterase (dRpase) activity. Journal of Biological Chemistry 272, 17480–17484.
Scharf K-D, Nover L.1987. Control of ribosome biosynthesis in plant cell cultures under heat shock conditions. II. Ribosomal proteins. Biochimica et Biophysica Acta 909, 44–57.
Scott II HB, Oliver MJ.1994. Accumulation and polysomal recruitment of transcripts in response to desiccation and rehydration of the moss Tortula ruralis. Journal of Experimental Botany 45, 577–583.
Swofford DL.1998. PAUP*, Phylogenetic Analysis Using Parsimony (*and other methods), Version 4. Sunderland, Massachusetts: Sinauer Associates.
Spirin AS, Belitsina NV, Ajtkhozhin MA.1964. Messenger RNA in early embryogenesis. Zhurnal Obshchei Biologii 25, 321–338.[Medline]
Van Lijsebettens M, Vanderhaeghen R, De Block M, Bauw G, Villarroel R, Van Montagu M.1994. An S18 ribosomal protein gene copy at the Arabidopsis PFL locus affects plant development by its specific expression in meristems. EMBO Journal 13,3378–3388.[Web of Science][Medline]
Wood AJ, Duff RJ, Oliver MJ.1999. Expressed Sequence Tags (ESTs) from desiccated Tortula ruralis identify a large number of novel plant genes. Plant and Cell Physiology 40, 361–368.
Wood AJ, Duff RJ, Zeng Q, Oliver MJ.2000a. Molecular architecture of Bryophyte genes: putative polyadenylation signals in cDNA 3'-ends of Tortula ruralis. The Bryologist 103, 44–51.
Wood AJ, Oliver MJ.1999. Translational control in plant stress: characterization of messenger ribonucleoprotein particles (mRNPs) in desiccated Tortula ruralis. The Plant Journal 18,359–370.
Wood AJ, Oliver MJ, Cove DJ.2000b. Frontiers in Bryological and Lichenological research. I. Bryophytes as model systems. The Bryologist 103, 128–133.
Wool IG.1996. Extraribosomal functions of ribosomal proteins. Trends in Biological Sciences 21, 164–165.
Wool IG, Chan Y-L, Gluck A.1995. Structure and evolution of mammalian ribosomal proteins. Biochemistry and Cell Biology 73, 933–947.[Web of Science][Medline]
Wool IG, Chan Y-L, Gluck A, Suzuki K.1991. The primary structure of rat ribosomal proteins P0, P1 and P2 and a proposal for a uniform nomenclature for mammalian and yeast ribosomal proteins. Biochemie 73, 861–870.[Medline]
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  K. M. Fisher Bayesian reconstruction of ancestral expression of the LEA gene families reveals propagule-derived desiccation tolerance in resurrection plants Am. J. Botany, April 1, 2008; 95(4): 506 - 515. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Q. Zeng, X. Chen, and A. J. Wood Two early light-inducible protein (ELIP) cDNAs from the resurrection plant Tortula ruralis are differentially expressed in response to desiccation, rehydration, salinity, and high light J. Exp. Bot., May 1, 2002; 53(371): 1197 - 1205. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||