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Sucrose metabolism gene families and their biological functions.

Jiang SY, Chi YH, Wang JZ, Zhou JX, Cheng YS, Zhang BL, Ma A, Vanitha J, Ramachandran S - Sci Rep (2015)

Bottom Line: Although studies on general metabolism pathway were well documented, less information is available on the genome-wide identification of these genes, their expansion and evolutionary history as well as their biological functions.They were evolutionarily conserved under purifying selection among species and expression divergence played important roles for gene survival after expansion.Overexpression of 15 sorghum genes in Arabidopsis revealed their roles in biomass accumulation, flowering time control, seed germination and response to high salinity and sugar stresses.

View Article: PubMed Central - PubMed

Affiliation: Genome Structural Biology Group, Temasek Life Sciences Laboratory, National University of Singapore, Singapore 117604.

ABSTRACT
Sucrose, as the main product of photosynthesis, plays crucial roles in plant development. Although studies on general metabolism pathway were well documented, less information is available on the genome-wide identification of these genes, their expansion and evolutionary history as well as their biological functions. We focused on four sucrose metabolism related gene families including sucrose synthase, sucrose phosphate synthase, sucrose phosphate phosphatase and UDP-glucose pyrophosphorylase. These gene families exhibited different expansion and evolutionary history as their host genomes experienced differentiated rates of the whole genome duplication, tandem and segmental duplication, or mobile element mediated gene gain and loss. They were evolutionarily conserved under purifying selection among species and expression divergence played important roles for gene survival after expansion. However, we have detected recent positive selection during intra-species divergence. Overexpression of 15 sorghum genes in Arabidopsis revealed their roles in biomass accumulation, flowering time control, seed germination and response to high salinity and sugar stresses. Our studies uncovered the molecular mechanisms of gene expansion and evolution and also provided new insight into the role of positive selection in intra-species divergence. Overexpression data revealed novel biological functions of these genes in flowering time control and seed germination under normal and stress conditions.

No MeSH data available.


Related in: MedlinePlus

Expression patterns and divergence of both apple SuSy and maize UDPGP gene families among various tissues.(A) The phylogenetic tree of the SuSy family in apple. The apple family was expanded only by tandem duplication. Locus names with black fonts indicate that these genes were not duplicated. A total of 6 tandem clusters were identified and they were labelled with blue, brown, green, white with blue background, red and pink colors. (B) The expression profiling of this gene family among 16 tissues. Expression data were downloaded from the NCBI datasets (Methods) with accession number GSE42873. These issues were listed as below: 1, Flower_M67; 2, Fruit_M74_100 daa; 3, Flower_M74; 4, Fruit_M20_100 daa; 5, Leaf_M14; 6, Fruit_M20_harvest; 7, leaf_M49; 8, Fruit_M74_harvest; 9, Root_GD; 10, Stem_X8877; 11, Root_X8877; 12, Stem_GD; 13, Seedling_GD; 14, Seed_X4442 × X2596; 15, Seedling_X4102; and 16, Seed_X3069 × X922. (C) The phylogenetic tree of the UDPGP family in maize. Locus names with red and green fonts indicate that they were from segmental duplication and TE-mediated expansion, respectively. The locus name with blue fonts indicates that the gene was expanded by TE but was located in a segmentally duplicated block. (D) The expression analysis of two datasets, which were downloaded from the NCBI datasets with accession numbers GSE27004 and SRA012297. These two datasets consisted of 60 and 15 tissues, respectively and their names were listed in their databases. In (A,B) both Ka values and Ka/Ks ratios for these nodes between closely related genes were calculated and were shown in the left and right of semicolon of the node. Normalized expression values were calculated by Agilent GeneSpring GX 11.5 software and were used for heat map analyses as shown in the right panel. Red, black, and green colors indicated the normalized expression values with >0, = 0, and < 0, respectively, in the matrix. The stars “*” indicated the statistical difference in their expression level between these two genes.
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f4: Expression patterns and divergence of both apple SuSy and maize UDPGP gene families among various tissues.(A) The phylogenetic tree of the SuSy family in apple. The apple family was expanded only by tandem duplication. Locus names with black fonts indicate that these genes were not duplicated. A total of 6 tandem clusters were identified and they were labelled with blue, brown, green, white with blue background, red and pink colors. (B) The expression profiling of this gene family among 16 tissues. Expression data were downloaded from the NCBI datasets (Methods) with accession number GSE42873. These issues were listed as below: 1, Flower_M67; 2, Fruit_M74_100 daa; 3, Flower_M74; 4, Fruit_M20_100 daa; 5, Leaf_M14; 6, Fruit_M20_harvest; 7, leaf_M49; 8, Fruit_M74_harvest; 9, Root_GD; 10, Stem_X8877; 11, Root_X8877; 12, Stem_GD; 13, Seedling_GD; 14, Seed_X4442 × X2596; 15, Seedling_X4102; and 16, Seed_X3069 × X922. (C) The phylogenetic tree of the UDPGP family in maize. Locus names with red and green fonts indicate that they were from segmental duplication and TE-mediated expansion, respectively. The locus name with blue fonts indicates that the gene was expanded by TE but was located in a segmentally duplicated block. (D) The expression analysis of two datasets, which were downloaded from the NCBI datasets with accession numbers GSE27004 and SRA012297. These two datasets consisted of 60 and 15 tissues, respectively and their names were listed in their databases. In (A,B) both Ka values and Ka/Ks ratios for these nodes between closely related genes were calculated and were shown in the left and right of semicolon of the node. Normalized expression values were calculated by Agilent GeneSpring GX 11.5 software and were used for heat map analyses as shown in the right panel. Red, black, and green colors indicated the normalized expression values with >0, = 0, and < 0, respectively, in the matrix. The stars “*” indicated the statistical difference in their expression level between these two genes.

Mentions: Our data showed that the SuSy, SPS, SPP and UDPGP families were evolutionarily conserved under purifying selection (Fig. 3). Our data also showed that gene expansion occurred in all the four gene families (Fig. 2). How did these expanded genes survive with limited functional divergence? We further investigated the expression profiling of these genes. We selected two gene families for these analyses. One of them is the SuSy family from the apple genome and another one is the UDPGP family from maize. The SuSy family underwent the rapid expansion during the divergence of M. domestica from F. vesca. In F. vesca, a total of 6 members were identified whereas up to 31 members were annotated in the apple genome (Fig. 2A). Tandem duplication played a key role in the expansion. After duplication, very low divergence was detected. We have selected 10 closely related pairs for Ka/Ks evaluation and the analysis showed that the Ka/Ks ratios were low and some of them had no non- synonymous substitution (Fig. 4A). Expression analysis showed that all of the 31 genes were expressed in at least one of sixteen tissues (Fig. 4B). There were a total of 6 tandem duplicated arrays as shown by different colors in Fig. 4A. Individuals from each array showed expression differentiation in at least one of sixteen detected tissues. We then analyzed the expression divergence between the 10 closely related pairs. The data showed that these pairs also exhibited expression differentiation in at least one out of sixteen tissues by statistical analysis (Fig. 4B).


Sucrose metabolism gene families and their biological functions.

Jiang SY, Chi YH, Wang JZ, Zhou JX, Cheng YS, Zhang BL, Ma A, Vanitha J, Ramachandran S - Sci Rep (2015)

Expression patterns and divergence of both apple SuSy and maize UDPGP gene families among various tissues.(A) The phylogenetic tree of the SuSy family in apple. The apple family was expanded only by tandem duplication. Locus names with black fonts indicate that these genes were not duplicated. A total of 6 tandem clusters were identified and they were labelled with blue, brown, green, white with blue background, red and pink colors. (B) The expression profiling of this gene family among 16 tissues. Expression data were downloaded from the NCBI datasets (Methods) with accession number GSE42873. These issues were listed as below: 1, Flower_M67; 2, Fruit_M74_100 daa; 3, Flower_M74; 4, Fruit_M20_100 daa; 5, Leaf_M14; 6, Fruit_M20_harvest; 7, leaf_M49; 8, Fruit_M74_harvest; 9, Root_GD; 10, Stem_X8877; 11, Root_X8877; 12, Stem_GD; 13, Seedling_GD; 14, Seed_X4442 × X2596; 15, Seedling_X4102; and 16, Seed_X3069 × X922. (C) The phylogenetic tree of the UDPGP family in maize. Locus names with red and green fonts indicate that they were from segmental duplication and TE-mediated expansion, respectively. The locus name with blue fonts indicates that the gene was expanded by TE but was located in a segmentally duplicated block. (D) The expression analysis of two datasets, which were downloaded from the NCBI datasets with accession numbers GSE27004 and SRA012297. These two datasets consisted of 60 and 15 tissues, respectively and their names were listed in their databases. In (A,B) both Ka values and Ka/Ks ratios for these nodes between closely related genes were calculated and were shown in the left and right of semicolon of the node. Normalized expression values were calculated by Agilent GeneSpring GX 11.5 software and were used for heat map analyses as shown in the right panel. Red, black, and green colors indicated the normalized expression values with >0, = 0, and < 0, respectively, in the matrix. The stars “*” indicated the statistical difference in their expression level between these two genes.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4663468&req=5

f4: Expression patterns and divergence of both apple SuSy and maize UDPGP gene families among various tissues.(A) The phylogenetic tree of the SuSy family in apple. The apple family was expanded only by tandem duplication. Locus names with black fonts indicate that these genes were not duplicated. A total of 6 tandem clusters were identified and they were labelled with blue, brown, green, white with blue background, red and pink colors. (B) The expression profiling of this gene family among 16 tissues. Expression data were downloaded from the NCBI datasets (Methods) with accession number GSE42873. These issues were listed as below: 1, Flower_M67; 2, Fruit_M74_100 daa; 3, Flower_M74; 4, Fruit_M20_100 daa; 5, Leaf_M14; 6, Fruit_M20_harvest; 7, leaf_M49; 8, Fruit_M74_harvest; 9, Root_GD; 10, Stem_X8877; 11, Root_X8877; 12, Stem_GD; 13, Seedling_GD; 14, Seed_X4442 × X2596; 15, Seedling_X4102; and 16, Seed_X3069 × X922. (C) The phylogenetic tree of the UDPGP family in maize. Locus names with red and green fonts indicate that they were from segmental duplication and TE-mediated expansion, respectively. The locus name with blue fonts indicates that the gene was expanded by TE but was located in a segmentally duplicated block. (D) The expression analysis of two datasets, which were downloaded from the NCBI datasets with accession numbers GSE27004 and SRA012297. These two datasets consisted of 60 and 15 tissues, respectively and their names were listed in their databases. In (A,B) both Ka values and Ka/Ks ratios for these nodes between closely related genes were calculated and were shown in the left and right of semicolon of the node. Normalized expression values were calculated by Agilent GeneSpring GX 11.5 software and were used for heat map analyses as shown in the right panel. Red, black, and green colors indicated the normalized expression values with >0, = 0, and < 0, respectively, in the matrix. The stars “*” indicated the statistical difference in their expression level between these two genes.
Mentions: Our data showed that the SuSy, SPS, SPP and UDPGP families were evolutionarily conserved under purifying selection (Fig. 3). Our data also showed that gene expansion occurred in all the four gene families (Fig. 2). How did these expanded genes survive with limited functional divergence? We further investigated the expression profiling of these genes. We selected two gene families for these analyses. One of them is the SuSy family from the apple genome and another one is the UDPGP family from maize. The SuSy family underwent the rapid expansion during the divergence of M. domestica from F. vesca. In F. vesca, a total of 6 members were identified whereas up to 31 members were annotated in the apple genome (Fig. 2A). Tandem duplication played a key role in the expansion. After duplication, very low divergence was detected. We have selected 10 closely related pairs for Ka/Ks evaluation and the analysis showed that the Ka/Ks ratios were low and some of them had no non- synonymous substitution (Fig. 4A). Expression analysis showed that all of the 31 genes were expressed in at least one of sixteen tissues (Fig. 4B). There were a total of 6 tandem duplicated arrays as shown by different colors in Fig. 4A. Individuals from each array showed expression differentiation in at least one of sixteen detected tissues. We then analyzed the expression divergence between the 10 closely related pairs. The data showed that these pairs also exhibited expression differentiation in at least one out of sixteen tissues by statistical analysis (Fig. 4B).

Bottom Line: Although studies on general metabolism pathway were well documented, less information is available on the genome-wide identification of these genes, their expansion and evolutionary history as well as their biological functions.They were evolutionarily conserved under purifying selection among species and expression divergence played important roles for gene survival after expansion.Overexpression of 15 sorghum genes in Arabidopsis revealed their roles in biomass accumulation, flowering time control, seed germination and response to high salinity and sugar stresses.

View Article: PubMed Central - PubMed

Affiliation: Genome Structural Biology Group, Temasek Life Sciences Laboratory, National University of Singapore, Singapore 117604.

ABSTRACT
Sucrose, as the main product of photosynthesis, plays crucial roles in plant development. Although studies on general metabolism pathway were well documented, less information is available on the genome-wide identification of these genes, their expansion and evolutionary history as well as their biological functions. We focused on four sucrose metabolism related gene families including sucrose synthase, sucrose phosphate synthase, sucrose phosphate phosphatase and UDP-glucose pyrophosphorylase. These gene families exhibited different expansion and evolutionary history as their host genomes experienced differentiated rates of the whole genome duplication, tandem and segmental duplication, or mobile element mediated gene gain and loss. They were evolutionarily conserved under purifying selection among species and expression divergence played important roles for gene survival after expansion. However, we have detected recent positive selection during intra-species divergence. Overexpression of 15 sorghum genes in Arabidopsis revealed their roles in biomass accumulation, flowering time control, seed germination and response to high salinity and sugar stresses. Our studies uncovered the molecular mechanisms of gene expansion and evolution and also provided new insight into the role of positive selection in intra-species divergence. Overexpression data revealed novel biological functions of these genes in flowering time control and seed germination under normal and stress conditions.

No MeSH data available.


Related in: MedlinePlus