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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

Expansion mechanisms of the SuSy, SPS, SPP and UDPGP families in 15 plants.(A) The phylogenetic tree in left panel was constructed according to the plant genome duplication database (http://chibba.agtec.uga.edu/duplication/) and showed the whole genome duplication history of 15 species. Green and blue stars indicate whole genome duplication and triplication, respectively. Columns in right panel in (A) indicates the contributions of tandem, segmental duplications and mobile elements to the expansion of the SuSy, SPS, SPP and UDPGP families in 15 genomes. The last column showed the summary of all identified family members in 15 species. The star “*” indicates mobile elements including LTR-retrotransposon, retrogene, Pack-Mule, hAT, Helitron and CACTA elements. Figures (B–E) show different types of expansion of family members by transposition. (B) A whole gene fragment was duplicated (type 1). A maize gene GRMZM2G342226 was expanded by a CACTA element in chromosome 4, which was characterized with typical CACTA structures. TSD, target site duplication; TIR, terminal inverted repeat. (C) Only 3′-region of a gene was duplicated (type 2). The 3′-region of a maize gene GRMZM2G139157 was duplicated by the Helitron element on chromosome 10 with typical Helitron features. The Helitron begins with “TC” and ends with CTAG, which were conserved sequence motifs (indicated by bold uppercase letters). These two motifs form parts of 11 bp palindromic sequences (underlined). Helitron sequences are in uppercase letters and the invariant host nucleotides where the Helitrons insert are in lowercase letters. The inverted repeats at the 3′ termini are in blue fonts. The 336 bp fragment is the duplicated gene fragment. (D) The 5′-region of a gene was duplicated (type 3). The strawberry gene gene00357-v1.0-hybrid was duplicated by a LTR-retrotransposon. The figure indicates structural features of this retrotransposon including 5′- and 3′-LTR, both of which start with TG and end with CA. Both PPT (polypurine tract) and PBS (primer binding site) are also indicated. (E) The middle region of a gene was duplicated (type 4). The middle region of a rice gene LOC_Os01g15910 was duplicated by a rice Pack-Mule on chromosome 1. TSD, target site duplication.
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f2: Expansion mechanisms of the SuSy, SPS, SPP and UDPGP families in 15 plants.(A) The phylogenetic tree in left panel was constructed according to the plant genome duplication database (http://chibba.agtec.uga.edu/duplication/) and showed the whole genome duplication history of 15 species. Green and blue stars indicate whole genome duplication and triplication, respectively. Columns in right panel in (A) indicates the contributions of tandem, segmental duplications and mobile elements to the expansion of the SuSy, SPS, SPP and UDPGP families in 15 genomes. The last column showed the summary of all identified family members in 15 species. The star “*” indicates mobile elements including LTR-retrotransposon, retrogene, Pack-Mule, hAT, Helitron and CACTA elements. Figures (B–E) show different types of expansion of family members by transposition. (B) A whole gene fragment was duplicated (type 1). A maize gene GRMZM2G342226 was expanded by a CACTA element in chromosome 4, which was characterized with typical CACTA structures. TSD, target site duplication; TIR, terminal inverted repeat. (C) Only 3′-region of a gene was duplicated (type 2). The 3′-region of a maize gene GRMZM2G139157 was duplicated by the Helitron element on chromosome 10 with typical Helitron features. The Helitron begins with “TC” and ends with CTAG, which were conserved sequence motifs (indicated by bold uppercase letters). These two motifs form parts of 11 bp palindromic sequences (underlined). Helitron sequences are in uppercase letters and the invariant host nucleotides where the Helitrons insert are in lowercase letters. The inverted repeats at the 3′ termini are in blue fonts. The 336 bp fragment is the duplicated gene fragment. (D) The 5′-region of a gene was duplicated (type 3). The strawberry gene gene00357-v1.0-hybrid was duplicated by a LTR-retrotransposon. The figure indicates structural features of this retrotransposon including 5′- and 3′-LTR, both of which start with TG and end with CA. Both PPT (polypurine tract) and PBS (primer binding site) are also indicated. (E) The middle region of a gene was duplicated (type 4). The middle region of a rice gene LOC_Os01g15910 was duplicated by a rice Pack-Mule on chromosome 1. TSD, target site duplication.

Mentions: To evaluate the patterns of expansion and evolutionary history of these four gene families, we broke down the phylogeny tree into ancestral units and estimated the most recent common ancestor (MRCA) among species according to the method described by Shiu et al. (2004)38. Due to possible gene losses and pseudogenes, which were excluded in the phylogenetic trees, the MRCA members may be under-estimated. Only one gene with locus name Cre12.g524000 was identified in the green algae species C. reinhardtii and the MRCA among the 15 species was estimated as 1 (Fig. 1E). Since no member was detected in the algae species for the SPS family, no MRCA exit among analyzed 15 species (Fig. 1E). The MRCA among 14 embryophyte species still had only 1 gene encoding SuSy and SPS, respectively. One more gene was expanded in the MRCA among 13 angiosperm species. During the divergence between monocot and dicot plants, the expansion rate varied. More SuSy and SPS genes were required for monocot plants when compared with dicot plants. The MRCA among 4 monocot plants was estimated at 4 and 5 members for SuSy and SPS, respectively whereas only 3 SuSy and 2 SPS genes were detected in the MRCA among 9 dicot plants (Fig. 1E). We further surveyed the remaining two families including SPP and UDPGP. Both SPP and UDPGP are ancient families with at least 1 and 3 members at the MRCA among 15 organisms (Fig. 1E). Following this era, no expansion occurred until the divergence between dicot and monocot plants. After divergence between dicot and monocot plants, no expansion was detected in dicot plants. However, in monocot plants, additional one for SPP and two for UDPGP members were required, making a total of 2 SPP and 5 UDPGP members in the MRCA among the monocot species. These data demonstrated that both monocot and dicot plants experienced differences in their expansion history for these gene families. Interestingly, the comparison of the general phylogenetic tree of 15 species and their encoded SuSy, SPS, SPP and UDPGP genes also suggested that these species experienced a differentiated family expansion history (Fig. 2A). A relatively large scale of gene expansion should have occurred for some species during species divergence from the MRCA among either monocot or dicot plants. The examples include the expansion of SuSy and UDPGP genes from maize, barrel medic, soybean and apple (Table 1 and Fig. 2A). In apple (M. domestica), a total of 31 SuSy, 7 SPS, 4 SPP and 14 UDPGP genes were detected with at least triple times of expansion from the MRCA among dicot plants. In its closely related species F. vesca (strawberry), only 6 SuSy, 4 SPS, 5 SPP and 5 UDPGP genes were encoded (Fig. 2A). The data suggested that a large scale of expansion occurred after the divergence of apple from strawberry. A similar situation was also observed in the maize species. However, for soybean and barrel medic (M. truncatula), the SuSy gene expansion might occur before the divergence of these two species and the whole-genome duplication might contribute to the expansion (Fig. 2A). On the other hand, our data also showed that most of species required only small families of SuSy, SPS, SPP and UDPGP with less than 10 members each.


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)

Expansion mechanisms of the SuSy, SPS, SPP and UDPGP families in 15 plants.(A) The phylogenetic tree in left panel was constructed according to the plant genome duplication database (http://chibba.agtec.uga.edu/duplication/) and showed the whole genome duplication history of 15 species. Green and blue stars indicate whole genome duplication and triplication, respectively. Columns in right panel in (A) indicates the contributions of tandem, segmental duplications and mobile elements to the expansion of the SuSy, SPS, SPP and UDPGP families in 15 genomes. The last column showed the summary of all identified family members in 15 species. The star “*” indicates mobile elements including LTR-retrotransposon, retrogene, Pack-Mule, hAT, Helitron and CACTA elements. Figures (B–E) show different types of expansion of family members by transposition. (B) A whole gene fragment was duplicated (type 1). A maize gene GRMZM2G342226 was expanded by a CACTA element in chromosome 4, which was characterized with typical CACTA structures. TSD, target site duplication; TIR, terminal inverted repeat. (C) Only 3′-region of a gene was duplicated (type 2). The 3′-region of a maize gene GRMZM2G139157 was duplicated by the Helitron element on chromosome 10 with typical Helitron features. The Helitron begins with “TC” and ends with CTAG, which were conserved sequence motifs (indicated by bold uppercase letters). These two motifs form parts of 11 bp palindromic sequences (underlined). Helitron sequences are in uppercase letters and the invariant host nucleotides where the Helitrons insert are in lowercase letters. The inverted repeats at the 3′ termini are in blue fonts. The 336 bp fragment is the duplicated gene fragment. (D) The 5′-region of a gene was duplicated (type 3). The strawberry gene gene00357-v1.0-hybrid was duplicated by a LTR-retrotransposon. The figure indicates structural features of this retrotransposon including 5′- and 3′-LTR, both of which start with TG and end with CA. Both PPT (polypurine tract) and PBS (primer binding site) are also indicated. (E) The middle region of a gene was duplicated (type 4). The middle region of a rice gene LOC_Os01g15910 was duplicated by a rice Pack-Mule on chromosome 1. TSD, target site duplication.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f2: Expansion mechanisms of the SuSy, SPS, SPP and UDPGP families in 15 plants.(A) The phylogenetic tree in left panel was constructed according to the plant genome duplication database (http://chibba.agtec.uga.edu/duplication/) and showed the whole genome duplication history of 15 species. Green and blue stars indicate whole genome duplication and triplication, respectively. Columns in right panel in (A) indicates the contributions of tandem, segmental duplications and mobile elements to the expansion of the SuSy, SPS, SPP and UDPGP families in 15 genomes. The last column showed the summary of all identified family members in 15 species. The star “*” indicates mobile elements including LTR-retrotransposon, retrogene, Pack-Mule, hAT, Helitron and CACTA elements. Figures (B–E) show different types of expansion of family members by transposition. (B) A whole gene fragment was duplicated (type 1). A maize gene GRMZM2G342226 was expanded by a CACTA element in chromosome 4, which was characterized with typical CACTA structures. TSD, target site duplication; TIR, terminal inverted repeat. (C) Only 3′-region of a gene was duplicated (type 2). The 3′-region of a maize gene GRMZM2G139157 was duplicated by the Helitron element on chromosome 10 with typical Helitron features. The Helitron begins with “TC” and ends with CTAG, which were conserved sequence motifs (indicated by bold uppercase letters). These two motifs form parts of 11 bp palindromic sequences (underlined). Helitron sequences are in uppercase letters and the invariant host nucleotides where the Helitrons insert are in lowercase letters. The inverted repeats at the 3′ termini are in blue fonts. The 336 bp fragment is the duplicated gene fragment. (D) The 5′-region of a gene was duplicated (type 3). The strawberry gene gene00357-v1.0-hybrid was duplicated by a LTR-retrotransposon. The figure indicates structural features of this retrotransposon including 5′- and 3′-LTR, both of which start with TG and end with CA. Both PPT (polypurine tract) and PBS (primer binding site) are also indicated. (E) The middle region of a gene was duplicated (type 4). The middle region of a rice gene LOC_Os01g15910 was duplicated by a rice Pack-Mule on chromosome 1. TSD, target site duplication.
Mentions: To evaluate the patterns of expansion and evolutionary history of these four gene families, we broke down the phylogeny tree into ancestral units and estimated the most recent common ancestor (MRCA) among species according to the method described by Shiu et al. (2004)38. Due to possible gene losses and pseudogenes, which were excluded in the phylogenetic trees, the MRCA members may be under-estimated. Only one gene with locus name Cre12.g524000 was identified in the green algae species C. reinhardtii and the MRCA among the 15 species was estimated as 1 (Fig. 1E). Since no member was detected in the algae species for the SPS family, no MRCA exit among analyzed 15 species (Fig. 1E). The MRCA among 14 embryophyte species still had only 1 gene encoding SuSy and SPS, respectively. One more gene was expanded in the MRCA among 13 angiosperm species. During the divergence between monocot and dicot plants, the expansion rate varied. More SuSy and SPS genes were required for monocot plants when compared with dicot plants. The MRCA among 4 monocot plants was estimated at 4 and 5 members for SuSy and SPS, respectively whereas only 3 SuSy and 2 SPS genes were detected in the MRCA among 9 dicot plants (Fig. 1E). We further surveyed the remaining two families including SPP and UDPGP. Both SPP and UDPGP are ancient families with at least 1 and 3 members at the MRCA among 15 organisms (Fig. 1E). Following this era, no expansion occurred until the divergence between dicot and monocot plants. After divergence between dicot and monocot plants, no expansion was detected in dicot plants. However, in monocot plants, additional one for SPP and two for UDPGP members were required, making a total of 2 SPP and 5 UDPGP members in the MRCA among the monocot species. These data demonstrated that both monocot and dicot plants experienced differences in their expansion history for these gene families. Interestingly, the comparison of the general phylogenetic tree of 15 species and their encoded SuSy, SPS, SPP and UDPGP genes also suggested that these species experienced a differentiated family expansion history (Fig. 2A). A relatively large scale of gene expansion should have occurred for some species during species divergence from the MRCA among either monocot or dicot plants. The examples include the expansion of SuSy and UDPGP genes from maize, barrel medic, soybean and apple (Table 1 and Fig. 2A). In apple (M. domestica), a total of 31 SuSy, 7 SPS, 4 SPP and 14 UDPGP genes were detected with at least triple times of expansion from the MRCA among dicot plants. In its closely related species F. vesca (strawberry), only 6 SuSy, 4 SPS, 5 SPP and 5 UDPGP genes were encoded (Fig. 2A). The data suggested that a large scale of expansion occurred after the divergence of apple from strawberry. A similar situation was also observed in the maize species. However, for soybean and barrel medic (M. truncatula), the SuSy gene expansion might occur before the divergence of these two species and the whole-genome duplication might contribute to the expansion (Fig. 2A). On the other hand, our data also showed that most of species required only small families of SuSy, SPS, SPP and UDPGP with less than 10 members each.

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