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Comparative analysis of sucrose phosphate synthase (SPS) gene family between Saccharum officinarum and Saccharum spontaneum.

ABSTRACT: 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.

SUBMITTER: Ma P

PROVIDER: S-EPMC7488781 | biostudies-literature | 2020 Sep

REPOSITORIES: biostudies-literature

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Comparative analysis of sucrose phosphate synthase (SPS) gene family between Saccharum officinarum and Saccharum spontaneum.

Ma Panpan P Zhang Xingtan X Chen Lanping L Zhao Qian Q Zhang Qing Q Hua Xiuting X Wang Zhengchao Z Tang Haibao H Yu Qingyi Q Zhang Muqing M Ming Ray R Zhang Jisen J

BMC plant biology 20200914 1

<h4>Background</h4>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.<h4>Results</h4>In the present study, ...[more]

PMID: 32928111

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Project description:BackgroundSugarcane is a major sugar and biofuel crop, but genomic research and molecular breeding have lagged behind other major crops due to the complexity of auto-allopolyploid genomes. Sugarcane cultivars are frequently aneuploid with chromosome number ranging from 100 to 130, consisting of 70-80 % S. officinarum, 10-20 % S. spontaneum, and 10 % recombinants between these two species. Analysis of a genomic region in the progenitor autoploid genomes of sugarcane hybrid cultivars will reveal the nature and divergence of homologous chromosomes.ResultsTo investigate the origin and evolution of haplotypes in the Bru1 genomic regions in sugarcane cultivars, we identified two BAC clones from S. spontaneum and four from S. officinarum and compared to seven haplotype sequences from sugarcane hybrid R570. The results clarified the origin of seven homologous haplotypes in R570, four haplotypes originated from S. officinarum, two from S. spontaneum and one recombinant.. Retrotransposon insertions and sequences variations among the homologous haplotypes sequence divergence ranged from 18.2 % to 60.5 % with an average of 33.7 %. Gene content and gene structure were relatively well conserved among the homologous haplotypes. Exon splitting occurred in haplotypes of the hybrid genome but not in its progenitor genomes. Tajima's D analysis revealed that S. spontaneum hapotypes in the Bru1 genomic regions were under strong directional selection. Numerous inversions, deletions, insertions and translocations were found between haplotypes within each genome.ConclusionsThis is the first comparison among haplotypes of a modern sugarcane hybrid and its two progenitors. Tajima's D results emphasized the crucial role of this fungal disease resistance gene for enhancing the fitness of this species and indicating that the brown rust resistance gene in R570 is from S. spontaneum. Species-specific InDel, sequences similarity and phylogenetic analysis of homologous genes can be used for identifying the origin of S. spontaneum and S. officinarum haplotype in Saccharum hybrids. Comparison of exon splitting among the homologous haplotypes suggested that the genome rearrangements in Saccharum hybrids after hybridization. The combined minimum difference at 19.5 % among homologous chromosomes in S. officinarum would be sufficient for proper genome assembly of this autopolyploid genome. Retrotransposon insertions and sequences variations among the homologous haplotypes sequence divergence may allow sequencing and assembling the autopolyploid Saccharum genomes and the auto-allopolyploid hybrid genomes using whole genome shotgun sequencing.

Project description:Sugarcane (Saccharum spp. hybrids) is an economically important crop widely grown in tropical and subtropical regions for sugar and ethanol production. However, the large genome size, high ploidy level, interspecific hybridization and aneuploidy make sugarcane one of the most complex genomes and have long hampered genome research in sugarcane. Modern sugarcane cultivars are derived from interspecific hybridization between S. officinarum and S. spontaneum with 80-90% of the genome from S. officinarum and 10-20% of the genome from S. spontaneum. We constructed bacterial artificial chromosome (BAC) libraries of S. officinarum variety LA Purple (2n = 8x = 80) and S. spontaneum haploid clone AP85-441 (2n = 4x = 32), and selected and sequenced 97 BAC clones from the two Saccharum BAC libraries. A total of 5,847,280 bp sequence from S. officinarum and 5,011,570 bp from S. spontaneum were assembled and 749 gene models were annotated in these BACs. A relatively higher gene density and lower repeat content were observed in S. spontaneum BACs than in S. officinarum BACs. Comparative analysis of syntenic regions revealed a high degree of collinearity in genic regions between Saccharum and Sorghum bicolor and between S. officinarum and S. spontaneum. In the syntenic regions, S. spontaneum showed expansion relative to S. officinarum, and both S. officinarum and S. spontaneum showed expansion relative to sorghum. Among the 75 full-length LTR retrotransposons identified in the Saccharum BACs, none of them are older than 2.6 mys and no full-length LTR elements are shared between S. officinarum and S. spontaneum. In addition, divergence time estimated using a LTR junction marker and a syntenic gene shared by 3 S. officinarum and 1 S. spontaneum BACs revealed that the S. spontaneum intergenic region was distant to those from the 3 homologous regions in S. officinarum. Our results suggested that S. officinarum and S. spontaneum experienced at least two rounds of independent polyploidization in each lineage after their divergence from a common ancestor.

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.

Project description:Polyploid Saccharum with complex genomes hindered the progress of sugarcane improvement, while their chloroplast genomes are much smaller and simpler. Chloroplast (cp), the vital organelle, is the site of plant photosynthesis, which also evolves other functions, such as tolerance to environmental stresses. In this study, the cp genome of two sugarcane ancestors Saccharum officinarum and S. spontaneum were sequenced, and genome comparative analysis between these two species was carried out, together with the photosynthetic ability. The length is 141,187 bp for S. officinarum and that is 7 bp longer than S. spontaneum, with the same GC content (38.44%) and annotated gene number (134), 13 with introns among them. There is a typical tetrad structure, including LSC, SSC, IRb and IRa. Of them, LSC and IRa/IRb are 18 bp longer and 6 bp shorter than those in S. spontaneum (83,047 bp and 22,795 bp), respectively, while the size of SSC is same (12,544 bp). Five genes exhibit contraction and expansion at the IR junctions, but only one gene ndhF with 29 bp expansion at the border of IRb/SSC. Nucleotide diversity (Pi) based on sliding window analysis showed that the single copy and noncoding regions were more divergent than IR- and coding regions, and the variant hotspots trnG-trnM, psbM-petN, trnR-rps14, ndhC-trnV and petA-psbJ in the LSC and trnL-ccsA in the SSC regions were detected, and petA-psbJ with the highest divergent value of 0.01500. Genetic distances of 65 protein genes vary from 0.00000 to 0.00288 between two species, and the selective pressure on them indicated that only petB was subjected to positive selection, while more genes including rpoC2, rps3, ccsA, ndhA, ndhA, psbI, atpH and psaC were subjected to purifying or very strong purifying selection. There are larger number of codons in S. spontaneum than that in S. officinarum, while both species have obvious codon preference and the codons with highest-(AUG) and lowest frequency (AUA) are same. Whilst, the most abundant amino acid is leucine in both S. officinarum and S. spontaneum, with number of 2175 (10.88% of total) and 2228 (10.90% of total) codons, respectively, and the lowest number is cysteine, with only 221 (1.105%) and 224 (1.096%), respectively. Protein collinearity analysis showed the high collinearity though several divergences were present in cp genomes, and identification of simple sequence repeats (SSRs) were included in this study. In addition, in order to compare cold tolerance and explore the expanding function of this environmental stress, the chlorophyll relative content (SPAD) and chlorophyll fluorescence Fv/Fm were measured. The significantly higher SPAD were observed in S. spontaneum than those in S. officinarum, no matter what the control conditions, exposure to low temperature or during recovery, and so was for Fv/Fm under exposure to low temperature, together with higher level of SPAD in S. spontaneum in each measurement. Aforementioned results suggest much stronger photosynthetic ability and cold tolerance in S. spontaneum. Our findings build a foundation to investigate the biological mechanism of two sugarcane ancestor chloroplasts and retrieve reliable molecular resources for phylogenetic and evolutionary studies, and will be conducive to genetic improvement of photosynthetic ability and cold resistance in modern sugarcane.

Dataset Information

Comparative analysis of sucrose phosphate synthase (SPS) gene family between Saccharum officinarum and Saccharum spontaneum.

Publications

Comparative analysis of sucrose phosphate synthase (SPS) gene family between Saccharum officinarum and Saccharum spontaneum.

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