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Structure, phylogeny, allelic haplotypes and expression of sucrose transporter gene families in Saccharum.

ABSTRACT: Sugarcane is an economically important crop contributing to about 80% of the world sugar production. Increasing efforts in molecular biological studies have been performed for improving the sugar yield and other relevant important agronomic traits. However, due to sugarcane's complicated genomes, it is still challenging to study the genetic basis of traits, such as sucrose accumulation. Sucrose transporters (SUTs) are critical for both phloem loading in source tissue and sucrose uptaking in sink tissue, and are considered to be the control points for regulating sucrose storage. However, no genomic study for sugarcane sucrose transporter (SsSUT) families has been reported up to date.By using comparative genomics and bacterial artificial chromosomes (BACs), six SUT genes were identified and characterized in S. spontaenum. Phylogenetic analyses revealed that the two pairs SsSUTs (SsSUT1/SsSUT3 and SsSUT5/SsSUT6) could be clustered together into two separate monocot specific SUT groups, while SsSUT2 and SsSUT4 were separated into the other two groups, with members from both dicot and monocot species. Gene structure comparison demonstrated that the number and position of exons/introns in SUTs were highly conserved among the close orthologs; in contrast, there were variations among the paralogous SUTs in Sacchuarm. Though with the high polyploidy level, gene allelic haplotype comparative analysis showed that the examined four SsSUT members exhibited conservations of gene structures and amino acid sequences among the allelic haplotypes accompanied by variations of intron sizes. Gene expression analyses were performed for tissues from seedlings under drought stress and mature plants of three Saccharum species (S.officinarnum, S.spotaneum and S.robustum). Both SUT1 and SUT4 expressed abundantly at different conditions. SUT2 had similar expression level in all of the examined tissues, but SUT3 was undetectable. Both of SUT5 and SUT6 had lower expression level than other gene member, and expressed stronger in source leaves and are likely to play roles in phloem loading. In the seeding plant leave under water stress, four genes SUT1, SUT2, SUT4 and SUT5 were detectable. In these detectable genes, SUT1 and SUT4 were down regulated, while, SUT2 and SUT5 were up regulated.In this study, we presented the first comprehensive genomic study for a whole gene family, the SUT family, in Saccharum. We speculated that there were six SUT members in the S. spotaneum genome. Out of the six members, SsSUTs, SsSUT5 and SsSUT6 were recent duplication genes accompanied by rapid evolution, while, SsSUT2 and SsSUT4 were the ancient members in the families. Despite the high polypoidy genome, functional redundancy may not exist among the SUTs allelic haplotypes supported by the evidence of strong purifying selection of the gene allele. SUT3 could be a low active member in the family because it is undetectable in our study, but it might not be a pseudogene because it harbored integrated gene structure. SUT1 and SUT4 were the main members for the sucrose transporter, while, these SUTs had sub-functional divergence in response to sucrose accumulation and plant development in Saccharum.

SUBMITTER: Zhang Q

PROVIDER: S-EPMC4736615 | biostudies-literature | 2016 Feb

REPOSITORIES: biostudies-literature

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Project description:Main conclusionProvide an evolutionary and an empirical molecular genetic foundation of the Sus gene family in tobacco and will be beneficial for further investigations of Sus gene functions Sucrose synthase (Sus) has been well characterized as the key enzyme participating in sucrose metabolism, and the gene family encoding different Sus isozymes has been cloned and characterized in several plant species. However, scant information about this gene family is available to date in tobacco. Here, we identified 14, 6, and 7 Sus genes in the genomes of Nicotiana tabacum, N. sylvestris and N. tomentosiformis, respectively. These tobacco Sus family members shared high levels of similarity in their nucleotide and amino acid sequences. Phylogenetic analysis revealed distinct evolutionary paths for the tobacco Sus genes. Sus1-4, Sus5, and Sus6-7 originated from three Sus precursors, respectively, which were generated by duplication before the split of monocots and eudicots. There were two additional duplications, before and after the differentiation of the Solanaceae, which separately gave rise to Sus3/4 and Sus1/2. Gene exon/intron structure analysis showed that the tobacco Sus genes contain varying numbers of conserved introns, resulting from intron loss under different selection pressures during the course of evolution. The expression patterns of the NtSus genes differed from each other in various tobacco tissues. Transcripts of Ntab0259170 and Ntab0259180 were detected in leaves at all tested developmental stages, suggesting that these two genes play a predominant role in sucrose metabolism during leaf development. Expression of Ntab0288750 and Ntab0234340 were conspicuously induced by low temperature and virus treatment, indicating that these two isozymes are important in meeting the increased glycolytic demand that occurs during abiotic stress. Our results provide an evolutionary and an empirical molecular genetic foundation of the Sus gene family in tobacco, and will be beneficial for further investigations of Sus gene functions in the processes of tobacco leaf development and tobacco resistance to environmental stresses.

Project description:BackgroundSugarcane served as the model plant for discovery of the C4 photosynthetic pathway. Magnesium is the central atom of chlorophyll, and thus is considered as a critical nutrient for plant development and photosynthesis. In plants, the magnesium transporter (MGT) family is composed of a number of membrane proteins, which play crucial roles in maintaining Mg homeostasis. However, to date there is no information available on the genomics of MGTs in sugarcane due to the complexity of the Saccharum genome.ResultsHere, we identified 10 MGTs from the Saccharum spontaneum genome. Phylogenetic analysis of MGTs suggested that the MGTs contained at least 5 last common ancestors before the origin of angiosperms. Gene structure analysis suggested that MGTs family of dicotyledon may be accompanied by intron loss and pseudoexon phenomena during evolution. The pairwise synonymous substitution rates corresponding to a divergence time ranged from 142.3 to 236.6 Mya, demonstrating that the MGTs are an ancient gene family in plants. Both the phylogeny and Ks analyses indicated that SsMGT1/SsMGT2 originated from the recent ρWGD, and SsMGT7/SsMGT8 originated from the recent σ WGD. These 4 recently duplicated genes were shown low expression levels and assumed to be functionally redundant. MGT6, MGT9 and MGT10 weredominant genes in the MGT family and werepredicted to be located inthe chloroplast. Of the 3 dominant MGTs, SsMGT6 expression levels were found to be induced in the light period, while SsMGT9 and SsMTG10 displayed high expression levels in the dark period. These results suggested that SsMGT6 may have a function complementary to SsMGT9 and SsMTG10 that follows thecircadian clock for MGT in the leaf tissues of S. spontaneum. MGT3, MGT7 and MGT10 had higher expression levels Insaccharum officinarum than in S. spontaneum, suggesting their functional divergence after the split of S. spontaneum and S. officinarum.ConclusionsThis study of gene evolution and expression of MGTs in S. spontaneum provided basis for the comprehensive genomic study of the entire MGT genes family in Saccharum. The results are valuable for further functional analyses of MGT genes and utilization of the MGTs for Saccharum genetic improvement.

Project description:BACKGROUND:Sucrose phosphate synthase (SPS) genes play vital roles in sucrose production across various plant species. Modern sugarcane cultivar is derived from the hybridization between the high sugar content species Saccharum officinarum and the high stress tolerance species Saccharum spontaneum, generating one of the most complex genomes among all crops. The genomics of sugarcane SPS remains under-studied despite its profound impact on sugar yield. RESULTS:In the present study, 8 and 6 gene sequences for SPS were identified from the BAC libraries of S. officinarum and S. spontaneum, respectively. Phylogenetic analysis showed that SPSD was newly evolved in the lineage of Poaceae species with recently duplicated genes emerging from the SPSA clade. Molecular evolution analysis based on Ka/Ks ratios suggested that polyploidy reduced the selection pressure of SPS genes in Saccharum species. To explore the potential gene functions, the SPS expression patterns were analyzed based on RNA-seq and proteome dataset, and the sugar content was detected using metabolomics analysis. All the SPS members presented the trend of increasing expression in the sink-source transition along the developmental gradient of leaves, suggesting that the SPSs are involved in the photosynthesis in both Saccharum species as their function in dicots. Moreover, SPSs showed the higher expression in S. spontaneum and presented expressional preference between stem (SPSA) and leaf (SPSB) tissue, speculating they might be involved in the differentia of carbohydrate metabolism in these two Saccharum species, which required further verification from experiments. CONCLUSIONS:SPSA and SPSB genes presented relatively high expression and differential expression patterns between the two Saccharum species, indicating these two SPSs are important in the formation of regulatory networks and sucrose traits in the two Saccharum species. SPSB was suggested to be a major contributor to the sugar accumulation because it presented the highest expressional level and its expression positively correlated with sugar content. The recently duplicated SPSD2 presented divergent expression levels between the two Saccharum species and the relative protein content levels were highest in stem, supporting the neofunctionalization of the SPSD subfamily in Saccharum.

Project description:BackgroundSugarcane is an economically important crop contributing about 80% and 40% to the world sugar and ethanol production, respectively. The complicated genetics consequential to its complex polyploid genome, however, have impeded efforts to improve sugar yield and related important agronomic traits. Modern sugarcane cultivars are complex hybrids derived mainly from crosses among its progenitor species, S. officinarum and S. spontanuem, and to a lesser degree, S. robustom. Atypical of higher plants, sugarcane stores its photoassimilates as sucrose rather than as starch in its parenchymous stalk cells. In the sugar biosynthesis pathway, sucrose synthase (SuSy, UDP-glucose: D-fructose 2-a-D-glucosyltransferase, EC 2.4.1.13) is a key enzyme in the regulation of sucrose accumulation and partitioning by catalyzing the reversible conversion of sucrose and UDP into UDP-glucose and fructose. However, little is known about the sugarcane SuSy gene family members and hence no definitive studies have been reported regarding allelic diversity of SuSy gene families in Saccharum species.ResultsWe identified and characterized a total of five sucrose synthase genes in the three sugarcane progenitor species through gene annotation and PCR haplotype analysis by analyzing 70 to 119 PCR fragments amplified from intron-containing target regions. We detected all but one (i.e. ScSuSy5) of ScSuSy transcripts in five tissue types of three Saccharum species. The average SNP frequency was one SNP per 108 bp, 81 bp, and 72 bp in S. officinarum, S. robustom, and S. spontanuem respectively. The average shared SNP is 15 between S. officinarum and S. robustom, 7 between S. officinarum and S. spontanuem , and 11 between S. robustom and S. spontanuem. We identified 27, 35, and 32 haplotypes from the five ScSuSy genes in S. officinarum, S. robustom, and S. spontanuem respectively. Also, 12, 11, and 9 protein sequences were translated from the haplotypes in S. officinarum, S. robustom, S. spontanuem, respectively. Phylogenetic analysis showed three separate clusters composed of SbSuSy1 and SbSuSy2, SbSuSy3 and SbSuSy5, and SbSuSy4.ConclusionsThe five members of the SuSy gene family evolved before the divergence of the genera in the tribe Andropogoneae at least 12 MYA. Each ScSuSy gene showed at least one non-synonymous substitution in SNP haplotypes. The SNP frequency is the lowest in S. officinarum, intermediate in S. robustum, and the highest in S. spontaneum, which may reflect the timing of the two rounds of whole genome duplication in these octoploids. The higher rate of shared SNP frequency between S. officinarum and S. robustum than between S. officinarum and in S. spontaneum confirmed that the speciation event separating S. officinarum and S. robustum occurred after their common ancestor diverged from S. spontaneum. The SNP and haplotype frequencies in three Saccharum species provide fundamental information for designing strategies to sequence these autopolyploid genomes.

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Structure, phylogeny, allelic haplotypes and expression of sucrose transporter gene families in Saccharum.

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