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Evolution and expression of the fructokinase gene family in Saccharum.

ABSTRACT: Sugarcane is an important sugar crop contributing up to about 80% of the world sugar production. Efforts to characterize the genes involved in sugar metabolism at the molecular level are growing since increasing sugar content is a major goal in the breeding of new sugarcane varieties. Fructokinases (FRK) are the main fructose phosphorylating enzymes with high substrate specificity and affinity.In this study, by combining comparative genomics approaches with BAC resources, seven fructokinase genes were identified in S. spontaneum. Phylogenetic analysis based on representative monocotyledon and dicotyledon plant species suggested that the FRK gene family is ancient and its evolutionary history can be traced in duplicated descending order: SsFRK4, SsFRK6/SsFRK7,SsFRK5, SsFRK3 and SsFRK1/SsFRK2. Among the close orthologs, the number and position of exons in FRKs were conserved; in contrast, the size of introns varied among the paralogous FRKs in Saccharum. Genomic constraints were analyzed within the gene alleles and between S. spontaneum and Sorghum bicolor, and gene expression analysis was performed under drought stress and with exogenous applications of plant hormones. FRK1, which was under strong functional constraint selection, was conserved among the gene allelic haplotypes, and displayed dominant expression levels among the gene families in the control conditions, suggesting that FRK1 plays a major role in the phosphorylation of fructose. FRK3 and FRK5 were dramatically induced under drought stress, and FRK5 was also found to increase its expression levels in the mature stage of Saccharum. Similarly, FRK3 and FRK5 were induced in response to drought stress in Saccharum. FRK2 and FRK7 displayed lower expression levels than the other FRK family members; FRK2 was under strong genomic selection constraints whereas FRK7 was under neutral selection. FRK7 may have become functionally redundant in Saccharum through pseudogenization. FRK4 and FRK6 shared the most similar expression pattern: FRK4 was revealed to have higher expression levels in mature tissues than in premature tissues of Saccharum, and FRK6 presented a slight increase under drought stress.Our study presents a comprehensive genomic study of the entire FRK gene family in Saccharum, providing the foundations for approaches to characterize the molecular mechanism regulated by the SsFRK family in sugarcane.

SUBMITTER: Chen Y

PROVIDER: S-EPMC5319016 | biostudies-literature | 2017 Feb

REPOSITORIES: biostudies-literature

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Evolution and expression of the fructokinase gene family in Saccharum.

Chen Yihong Y Zhang Qing Q Hu Weichang W Zhang Xingtan X Wang Liming L Hua Xiuting X Yu Qingyi Q Ming Ray R Zhang Jisen J

BMC genomics 20170221 1

<h4>Background</h4>Sugarcane is an important sugar crop contributing up to about 80% of the world sugar production. Efforts to characterize the genes involved in sugar metabolism at the molecular level are growing since increasing sugar content is a major goal in the breeding of new sugarcane varieties. Fructokinases (FRK) are the main fructose phosphorylating enzymes with high substrate specificity and affinity.<h4>Results</h4>In this study, by combining comparative genomics approaches with BAC ...[more]

PMID: 28222695

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Project description:BackgroundCalcineurin B-like protein (CBL)-interacting protein kinases (CIPKs) are the primary components of calcium sensors, and play crucial roles in plant developmental processes, hormone signaling transduction, and in the response to exogenous stresses.ResultsIn this study, 48 CIPK genes (SsCIPKs) were identified from the genome of Saccharum spontaneum. Phylogenetic reconstruction suggested that the SsCIPK gene family may have undergone six gene duplication events from the last common ancestor (LCA) of SsCIPKs. Whole-genome duplications (WGDs) served as the driving force for the amplification of SsCIPKs. The Nonsynonymous to synonymous substitution ratio (Ka/Ks) analysis showed that the duplicated genes were possibly under strong purifying selection pressure. The divergence time of these duplicated genes had an average duplication time of approximately 35.66 Mya, suggesting that these duplication events occurred after the divergence of the monocots and eudicots (165 Mya). The evolution of gene structure analysis showed that the SsCIPK family genes may involve intron losses. Ten ScCIPK genes were amplified from sugarcane (Saccharum spp. hybrids). The results of real-time quantitative polymerase chain reaction (qRT-PCR) demonstrated that these ten ScCIPK genes had different expression patterns under abscisic acid (ABA), polyethylene glycol (PEG), and sodium chloride (NaCl) stresses. Prokaryotic expression implied that the recombinant proteins of ScCIPK3, - 15 and - 17 could only slightly enhance growth under salinity stress conditions, but the ScCIPK21 did not. Transient N. benthamiana plants overexpressing ScCIPKs demonstrated that the ScCIPK genes were involved in responding to external stressors through the ethylene synthesis pathway as well as to bacterial infections.ConclusionsIn generally, a comprehensive genome-wide analysis of evolutionary relationship, gene structure, motif composition, and gene duplications of SsCIPK family genes were performed in S. spontaneum. The functional study of expression patterns in sugarcane and allogenic expressions in E. coli and N. benthamiana showed that ScCIPKs played various roles in response to different stresses. Thus, these results improve our understanding of the evolution of the CIPK gene family in sugarcane as well as provide a basis for in-depth functional studies of CIPK genes in sugarcane.

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.

Project description:BACKGROUND: Proteins of the mammalian PYHIN (IFI200/HIN-200) family are involved in defence against infection through recognition of foreign DNA. The family member absent in melanoma 2 (AIM2) binds cytosolic DNA via its HIN domain and initiates inflammasome formation via its pyrin domain. AIM2 lies within a cluster of related genes, many of which are uncharacterised in mouse. To better understand the evolution, orthology and function of these genes, we have documented the range of PYHIN genes present in representative mammalian species, and undertaken phylogenetic and expression analyses. RESULTS: No PYHIN genes are evident in non-mammals or monotremes, with a single member found in each of three marsupial genomes. Placental mammals show variable family expansions, from one gene in cow to four in human and 14 in mouse. A single HIN domain appears to have evolved in the common ancestor of marsupials and placental mammals, and duplicated to give rise to three distinct forms (HIN-A, -B and -C) in the placental mammal ancestor. Phylogenetic analyses showed that AIM2 HIN-C and pyrin domains clearly diverge from the rest of the family, and it is the only PYHIN protein with orthology across many species. Interestingly, although AIM2 is important in defence against some bacteria and viruses in mice, AIM2 is a pseudogene in cow, sheep, llama, dolphin, dog and elephant. The other 13 mouse genes have arisen by duplication and rearrangement within the lineage, which has allowed some diversification in expression patterns. CONCLUSIONS: The role of AIM2 in forming the inflammasome is relatively well understood, but molecular interactions of other PYHIN proteins involved in defence against foreign DNA remain to be defined. The non-AIM2 PYHIN protein sequences are very distinct from AIM2, suggesting they vary in effector mechanism in response to foreign DNA, and may bind different DNA structures. The PYHIN family has highly varied gene composition between mammalian species due to lineage-specific duplication and loss, which probably indicates different adaptations for fighting infectious disease. Non-genomic DNA can indicate infection, or a mutagenic threat. We hypothesise that defence of the genome against endogenous retroelements has been an additional evolutionary driver for PYHIN proteins.

Dataset Information

Evolution and expression of the fructokinase gene family in Saccharum.

Publications

Evolution and expression of the fructokinase gene family in Saccharum.

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