Comparative genomic analysis of 1047 completely sequenced cDNAs from an Arabidopsis-related model halophyte, Thellungiella halophila
© Taji et al; licensee BioMed Central Ltd. 2010
Received: 30 July 2010
Accepted: 24 November 2010
Published: 24 November 2010
Thellungiella halophila (also known as T. salsuginea) is a model halophyte with a small size, short life cycle, and small genome. Thellungiella genes exhibit a high degree of sequence identity with Arabidopsis genes (90% at the cDNA level). We previously generated a full-length enriched cDNA library of T. halophila from various tissues and from whole plants treated with salinity, chilling, freezing stress, or ABA. We determined the DNA sequences of 20 000 cDNAs at both the 5'- and 3' ends, and identified 9569 distinct genes.
Here, we completely sequenced 1047 Thellungiella full-length cDNAs representing abiotic-stress-related genes, transcription factor genes, and protein phosphatase 2C genes. The predicted coding sequences, 5'-UTRs, and 3'-UTRs were compared with those of orthologous genes from Arabidopsis for length, sequence similarity, and structure. The 5'-UTR sequences of Thellungiella and Arabidopsis orthologs shared a significant level of similarity, although the motifs were rearranged. While examining the stress-related Thellungiella coding sequences, we found a short splicing variant of T. halophila salt overly sensitive 1 (ThSOS1), designated ThSOS1S. ThSOS1S contains the transmembrane domain of ThSOS1 but lacks the C-terminal hydrophilic region. The expression level of ThSOS1S under normal growth conditions was higher than that of ThSOS1. We also compared the expression levels of Na+-transport-system genes between Thellungiella and Arabidopsis by using full-length cDNAs from each species as probes. Several genes that play essential roles in Na+ excretion, compartmentation, and diffusion (SOS1, SOS2, NHX1, and HKT1) were expressed at higher levels in Thellungiella than in Arabidopsis.
The full-length cDNA sequences obtained in this study will be essential for the ongoing annotation of the Thellungiella genome, especially for further improvement of gene prediction. Moreover, they will enable us to find splicing variants such as ThSOS1S (AB562331).
Thellungiella halophila (also known as T. salsuginea) is used as a model system for understanding abiotic stress tolerance. It shows tolerance not only to extreme salinity stress, but also to chilling, freezing, and ozone stresses [1–10]. Thellungiella is closely related to Arabidopsis, with 90% cDNA sequence identity between the two species, and it can be easily transformed by using the floral dipping method [1, 11]. Thellungiella has a number of other features useful for genetic research, such as small size, short life cycle, high seed number, and self-compatibility.
The Arabidopsis genome sequence and other genetic resources, including collections of full-length cDNAs, have provided powerful tools for comparative genomics to understand the biology and evolution of other plants [3, 5, 12]. In particular, highly accurate full-length cDNA sequences that span the entire protein-coding region of a given gene can advance comparative, functional, and structural genome analyses. The accurate prediction of protein-coding regions in genome sequences is limited by the difficulty of finding islands of coding sequences within an ocean of noncoding DNA, and by the complexity of individual genes that may code for multiple peptides through alternative splicing. The sequence data from full-length cDNAs has contributed to the accuracy of annotation and to improving gene prediction in Arabidopsis [13–15]. For these reasons, we have been working to collect similar data for Thellungiella.
We previously reported construction of a full-length cDNA library of Thellungiella derived from various tissues and from whole seedlings subjected to environmental stress treatments, including high salinity, chilling, freezing, and abscisic acid (ABA). We obtained a total of 35 171 sequences from 20 000 clones, and named them RIKEN Thellungiella Full-length (RTFL) cDNA clones. These sequences were assembled by using the CAP3 method and were clustered into 9569 nonredundant cDNA groups .
Thellungiella has an effective system for suppressing Na+ influx and for excreting Na+ . It also exhibits high potassium/sodium selectivity, according to electrophysiological analysis of instantaneous current . This implies that Thellungiella has ion channels with specific features that lead to superior sodium/potassium homeostasis. Membrane transporters have been shown to be important components of salt tolerance mechanisms in other species on account of their regulation of ion homeostasis. For example, the SALT OVERLY SENSITIVE (SOS) pathway is a well-defined pathway in Arabidopsis for the regulation of sodium ion homeostasis during plant growth under salinity stress [17, 18]. In this pathway, a calcium-binding protein, SOS3, perceives a change in intracellular calcium concentration induced by salt stress and then binds to and activates SOS2, a serine/threonine protein kinase. The SOS3-SOS2 complex increases the expression and activity of SOS1, which encodes a plasma membrane Na+/H+ exchanger (antiporter) [19, 20]. Activated SOS1 transports cytosolic sodium out of the cell, reducing the cellular build-up of toxic levels of sodium . The Thellungiella SOS1 gene, ThSOS1, has a conserved amino acid sequence and protein structure with orthologous genes from Arabidopsis and other plants . Transgenic Thellungiella plants in which ThSOS1 transcript levels were reduced by RNA interference (RNAi) showed lower salt tolerance than wild-type plants, suggesting that SOS1 is critical for salt tolerance in halophytic species as well as in glycophytic species such as Arabidopsis . Recently, a 193-kb Thellungiella BAC clone containing the putative SOS1 locus was sequenced, annotated, and compared with the sequence in the orthologous 146-kb region of the Arabidopsis genome on chromosome 2 .
Here, we selected 1047 cDNAs for genes related to salt stress, transcription factors, transporters, and protein phosphatase 2Cs from 9569 individual RTFL clones, and determined the complete sequences. We then predicted the coding sequence (CDS), 5'-UTR, and 3'-UTR for each of the cDNAs and compared them with the corresponding regions from the orthologous Arabidopsis genes. We also compared the expression levels of Thellungiella and Arabidopsis Na+-transport system genes by using full-length cDNAs to probe Northern blots under equal conditions of hybridization and detection.
Results and Discussion
Selection and complete sequencing of 1047 full-length cDNAs
Classification of 1250 full-sequenced cDNAs
number of cDNAs
433 salt stress related genes
Thellungiella salt stress inducible genes
Taji et al., 2004 Plant Physiol
Gong et al., 2005 Plant J.
Wong et al., 2005 Plant Mol Biol.
Taji et al., unpublished data
salt stress inducible genes in Thellungiella and Arabidopsis
constitutive high-expressed genes in Thellungiella compared with Arabidopsis
genes encoding Na+ transporter
overlapping genes in EST libraries of abiotic stressed plants from Thellungiella
response to abiotic or biotic stress classified by Gene Ontology a
Taji et al., 2009 BMC Plant Biol.
transcription factor classified by Gene Ontology a
Taji et al., 2009 BMC Plant Biol.
protein phosphatase 2C
Taji et al., 2009 BMC Plant Biol.
total after elimination of overlapped cDNAs
Comparison of CDS, 5'-UTR, and 3'-UTR sequences between orthologous genes inThellungiella and Arabidopsis
Comparison of structure of UTR regions between Thellungiella and Arabidopsis
Structural comparison of ThSOS1 and splicing variant ThSOS1S
The transmembrane portion of ThSOS1/ThSOS1S has sequence similarities with plasma membrane Na+/H+ exchangers of animal, bacterial, and fungal cells . In animal cells, Na+/H+ exchanger 1 (NHE1) functions as a Na+/H+ antiporter to maintain pH homeostasis . NHE1 has a C-terminal tail of ~300 aa, which is important in regulating the Na+/H+ antiporter activity through phosphorylation or binding of regulatory proteins . The Synechocystis Na+/H+ antiporter SynNhaP also has a long hydrophilic C-terminal tail (100 aa). In SynNhaP, the deletion of a 56-aa hydrophilic terminal region partially inhibited the antiporter activity, and replacement of the long C-terminal tail with the orthologous region from the halotolerant cyanobacterium Aphanothece halophytica, ApNhaP, altered its ion specificity . Arabidopsis Na+/H+ antiporter SOS1 has 12 predicted transmembrane domains in the N-terminal region and a long cytoplasmic tail of ~700 aa at the C-terminus . The predicted cytoplasmic tail of SOS1 interacts with radical-induced cell death 1 (RCD1), a regulator of oxidative stress responses under salt or oxidative stress. Like rcd1 mutants, sos1 mutants show an altered sensitivity to oxidative stresses . These results suggest that the long C-terminal tail mediates not only the regulation of transport activity with a variety of intracellular regulatory proteins, but also the ion specificity and the cross-talk with other stress tolerance mechanisms.
The N-terminal transmembrane region of SOS1 shows high similarity among various organisms (Figure 4A), whereas there is no significant similarity among the C-terminal regions . The C-terminal sequence variation may result in different functions for this region among different organisms. In particular, NhaP, a Na+/H+ antiporter of Pseudomonas aeruginosa, is highly homologous to SOS1, NHE1, SynNhaP, and ApNha1 (Figure 4A), but it does not have the C-terminal long tail . ThSOS1S is similar to NhaP in that it contains only a Na+/H+-exchanger domain in the transmembrane domain. It is possible that ThSOS1S functions as an Na+/H+ antiporter whereas ThSOS1 functions not only in salt stress response (via the N-terminal Na+/H+ antiporter), but also in response to other abiotic stresses (via the long C-terminal tail).
Expression levels of ThSOS1 and ThSOS1S
Expression profiles of Na+transport genes of Thellungiella and Arabidopsis
It is difficult to understand the relationship between HKT1 expression and salinity tolerance. On the one hand, the overexpression of AtHKT1 increased sensitivity to NaCl (but not to LiCl or KCl) compared with wild-type plants . On the other hand, the ectopic production of wheat HKT1 containing specific amino acid substitutions (A240V, Q270L, or N365S) enhanced NaCl tolerance in yeast . We compared the deduced amino acid sequences of HKT1 among Arabidopsis, Thellungiella, and wheat to search for point mutations inducing higher salt tolerance in Thellungiella HKT1. However, none of the mutations that gave high salt tolerance in the wheat HKT1 experiment was found in Thellungiella HKT1 (data not shown). It remains unknown whether other differences in the HKT1 sequences between Thellungiella and Arabidopsis confer salinity tolerance to Thellungiella. Arabidopsis HKT1 transports only Na+, not K+, because in the K+ channel motif GYG, which is critical for K+ selectivity, the first glycine is replaced with serine (Ser-68) . The same position in the Thellungiella HKT1 ortholog is also serine (Ser-68), suggesting that Thellungiella HKT1 also transports only Na+.
We sequenced 1047 Thellungiella cDNAs and used this information to compare the responses of Thellungiella and Arabidopsis to high-salinity conditions. The full-length cDNA sequences will contribute to annotation of the Thellungiella genome and will improve gene predictions. Moreover, these fully sequenced cDNAs will enable finding splicing variants such as ThSOS1S. RNA blot analysis indicated that the extreme salt tolerance of Thellungiella might be attributable to the constitutively higher expression of genes functioning in the Na+ transport system.
Sequences from this study have been deposited in NCBI GenBank under accession numbers [GenBank: AK352512] to [GenBank: AK353558]. The RTFL clones are available for distribution from the RIKEN Bioresource Center http://www.brc.riken.go.jp/lab/epd/Eng/.
Determination of CDSs, 5'-UTRs, and 3'-UTRs of full-length cDNAs
The locations of CDSs were determined with the EMBOSS getorf program (ver. 6 ), which identifies the longest stretch of uninterrupted sequence between a start codon (ATG) and stop codon (TGA, TAG, TAA) in the 5'- to 3' direction as the predicted CDS. The sequences before and after each predicted CDS were designated as the 5'- and 3'-UTRs, respectively. The 3' poly(A)-tail lengths were not included when determining the UTR lengths.
Identification of orthologous genes in Arabidopsis and Thellungiella
The CDS data set of 1047 Thellungiella cDNAs was compared with the gene sequences in The Arabidopsis Information Resource (TAIR8) by using BLAST searches (ver. 2.2.17 ). The top hit in each BLAST search was assumed to be the Arabidopsis ortholog.
Plant materials and growth conditions
Seeds of Thellungiella halophila (Shang Dong ecotype) and Arabidopsis thaliana (Columbia-0 ecotype) were sown on MS agar plates containing full-strength MS, 0.8% (w/v) agar, and 1% sucrose with vitamin mixture (10 mg L-1 myoinositol, 200 μg L-1 glycine, 50 μg L-1 nicotinic acid, 50 μg L-1 pyridoxine hydrochloride, 10 μg L-1 thiamin hydrochloride, pH 5.7) and the plates were sealed with surgical tape. The seeds were stratified at 4°C for 7 days and then transferred to 80 μmol m-2s-1 irradiance under an 8/16-h day/night cycle at 22°C for germination and growth.
Three-week-old Arabidopsis and Thellungiella plants that had been grown on 1/2 MS plates were soaked in 250 mM NaCl solution for 1, 2, 5, or 10 h. Total RNA was extracted by using RNAiso reagent (TaKaRa, Japan). Total RNA (10 μg) was fractionated in 1% agarose gel containing formaldehyde and blotted onto a nylon membrane using 20× SSC. DNA fragments of the full-length cNDAs for AtSOS1 (RAFL09-06-M16), AtSOS2 (RAFL09-61-G03), AtNHX1 (RAFL09-87-C17), AtNHX2 (RAFL07-95-G07), AtNHX5 (RAFL09-15-L23), AtHKT1 (RAFL15-31-F16), ThSOS1 (RTFL01-052_J19), ThSOS2 (RTFL01-012_C03), ThNHX1 (RTFL01-029_F03), ThNHX2 (RTFL01-047_K14), ThNHX5 (RTFL01-046_D22) and ThHKT1 (RTFL01-044_N15) were used as probes. Probes were labeled with [32P]dCTP using a DNA Labeling Kit ver. 2 (TaKaRa, Japan), and membranes were hybridized with 32P-labeled fragments at 65°C overnight. The membranes were washed 3 times with 1× SSC, 1% SDS for 3 min at room temperature; then once with 1× SSC, 1% SDS for 15 min at room temperature; then twice with 0.1× SSC, 0.1% SDS for 15 min at 65°C.
Semiquantitative or quantitative RT-PCR
For cDNA synthesis, 1 μg of total RNA was first treated with DNaseI (Sigma-Aldrich, USA) for 15 min at room temperature, and the enzyme was inactivated by heating at 70°C for 10 min. Reverse transcription was performed with the ThermoScript RT-PCR system (Invitrogen, USA) according to the manufacturer's instructions. Synthesized cDNAs were purified using the Gel Extraction kit. Semiquantitative RT-PCR analysis for ThSOS1 and AtSOS1 expression was performed using 1 μl of the cDNA, primer sets (ThSOS1; Exon13-14 forward 5'-CCGAGACAGGAACAATGTTTAT-3' and Exon15-16 reverse 5'-AGTAAGCTGCCTGAACACCAT-3', AtSOS1; Exon13-14 forward 5'-AGGAGACTGGAACATTGTTTCT-3' and Exon15-16 reverse 5'-AGTAAGTTGCTTGCACACCATT-3') and BioTaq polymerase with the supplied buffer and dNTP (BIOLINE, UK). The PCR conditions were as follows: 30 cycles of 95°C for 30 s, 55°C for 30 s and 72°C for 30 s. A 10 μl aliquot of each PCR reaction was separated on an agarose gel. The comparative expression analysis of ThSOS1 and ThSOS1S was performed by quantitative PCR with LightCycler Systems for Real-Time PCR (Roche Applied Science, Japan) using the LightCycler-FastStart DNA Master SYBR Green I kit (Roche Applied Science, Japan) and the primer sets (ThSOS1; Exon14-15 forward 5'- CGGTTTACCAGCCTCAAAGATACGAA-3' and reverse 5'- AAACGCTTGTAAGGCCTTATTCAGCAT-3', ThSOS1S; Exon14-15 forward 5'- TTTACCAGCCTCAAAGGGAAACTGTG-3' and ThSOS1S specific reverse 5'- CACCTAACTATGCCCGCTCAAGGA-3' and Actin2; forward 5'- AGTGGTCGTACAACCGGTATTGT-3' and reverse 5'- GATGGCATGAGGAAGAGAGAAAC-3') according to the manufacturer's instructions. The PCR conditions were as follows: 40 cycles of 95°C for 10 s, 55°C for 10 s and 72°C for 10 s. The relative expressions were calculated using the Second Derivative Maximum Method on LightCycler Data Analysis software (Roche Applied Science, Japan). The Actin2 (At3g18730) co-orthologous gene was used to normalize ThSOS1 and ThSOS1S expressions.
Measurement of plant Na+content
Two-week-old Arabidopsis and Thellungiella plants grown on 1/2 MS agar plates were transferred to plates containing 1/2 MS agar medium plus 250 mM NaCl. Plants were harvested at 1, 3, 5, 7, 10, 14, 21, and 28 days after transfer. For each sample, five plants were pooled and soaked in 5 mL sterile distilled water. The leaf-water mixture was boiled for 15 min, filtered through a 0.2-μm filter (Toyo Roshi Kaisha, Ltd.), and diluted 20-fold. The solution was analyzed by using a Shim-pack IC-C3/C3 (S) column (Shimadzu, Japan) on a Shimadzu PIA-1000 Personal Ion Analyzer (Shimadzu, Japan).
We are grateful for the technical support provided by Kousuke Sugahara and Tatsuya Murata of the Faculty of Applied Bioscience, Tokyo University of Agriculture. The Arabidopsis accessions used in this study are maintained and provided by the RIKEN BRC through the National Bio-Resource Project of the MEXT, Japan. Characterization of full-length sequence of RTFL clones was supported by the National Bio-Resource Project of the MEXT, Japan. This work was supported by a Grant-in-aid for Young Scientists from the Ministry of Education, Culture, Sports, Science and Technology of Japan (T. T.), and by the Advanced Research Project of Tokyo University of Agriculture.
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