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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

Frequency distributions of Ka/Ks ratios between expanded gene pairs and tests of sites with purifying/positive selection in the SuSy, SPS, SPP and UDPGP families.(A,B) Frequency distributions of Ka/Ks ratios were analyzed using expanded pairs from dicot and monocot plants, respectively. (C) The average Ka, Ks and their ratios in monocot and dicot pairs. Asterisks indicate significant differences between monocot and dicot plants at P, 0.05 (*) by t-test. (D–G) Screening for amino acid sites with purifying/positive selection in the four gene families by the SLR program as described in the Methods.
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f3: Frequency distributions of Ka/Ks ratios between expanded gene pairs and tests of sites with purifying/positive selection in the SuSy, SPS, SPP and UDPGP families.(A,B) Frequency distributions of Ka/Ks ratios were analyzed using expanded pairs from dicot and monocot plants, respectively. (C) The average Ka, Ks and their ratios in monocot and dicot pairs. Asterisks indicate significant differences between monocot and dicot plants at P, 0.05 (*) by t-test. (D–G) Screening for amino acid sites with purifying/positive selection in the four gene families by the SLR program as described in the Methods.

Mentions: Since the distinct difference was observed in their expansion history among the four gene families or in the same family between dicot and monocot plants (Figs 1 and 2), we investigated whether they were under different selection forces. We first identified reciprocal best matches for all four gene family members either from dicot or monocot plants by phylogenetic analysis using corresponding domain regions. The domain regions from these identified matches were then used to calculate their Ka (nonsynonymous substitutions per site), Ks (synonymous substitutions per site) and their ratios according to the description in Methods. We first analyzed and compared the Ka/Ks frequency distribution of these four gene families between monocot and dicot plants (Fig. 3A,B). For the SuSy, SPS and UDPGP families, similar frequency distributions of the Ka/Ks ratios were observed between monocot and dicot plants although their distribution patterns showed differences. There was also no significant difference between monocot and dicot plants in the average Ka, Ks and Ka/Ks values for these three gene families (Fig. 3C). For the SuSy family, most of the mass were centered near Ka/Ks > 0.5 whereas most of the mass for both SPS and UDPGP were centered near Ka/Ks = 0.1. Furthermore, the SuSy family also has the higher average Ka/Ks ratios at 0.87 for dicot and 1.04 for monocot plants whereas the average ratios for both SPS and UDPGP families were less than 0.2 for either dicot or monocot plants (Fig. 3C). These data suggested that the SuSy family evolved faster than the SPS and UDPGP families. However, for the SPP family, significant difference was observed between monocot and dicot plants in their Ka/Ks frequency distribution (Fig. 3A,B). In dicot plants, most of the mass was centered near Ka/Ks = 0.2 whereas the peak was near 0.1 for monocot plants. The average Ka/Ks for dicot plants was 0.47, statistically higher than the ratio 0.14, which was calculated for monocot plants (Fig. 3C). To further analyze the reason why both dicot and monocot plants exhibited the difference in their evolutionary rate, we compared their Ka and Ks values separately. We found that the Ka value in monocots is twice the value in dicot plants whereas the Ks value in monocots is more than three times higher than that in dicots (Fig. 3C). As a result, dicots showed significantly higher Ka/Ks ratio than that in monocots. Thus, the SPP family in dicot plants evolved faster than that in monocot plants.


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)

Frequency distributions of Ka/Ks ratios between expanded gene pairs and tests of sites with purifying/positive selection in the SuSy, SPS, SPP and UDPGP families.(A,B) Frequency distributions of Ka/Ks ratios were analyzed using expanded pairs from dicot and monocot plants, respectively. (C) The average Ka, Ks and their ratios in monocot and dicot pairs. Asterisks indicate significant differences between monocot and dicot plants at P, 0.05 (*) by t-test. (D–G) Screening for amino acid sites with purifying/positive selection in the four gene families by the SLR program as described in the Methods.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f3: Frequency distributions of Ka/Ks ratios between expanded gene pairs and tests of sites with purifying/positive selection in the SuSy, SPS, SPP and UDPGP families.(A,B) Frequency distributions of Ka/Ks ratios were analyzed using expanded pairs from dicot and monocot plants, respectively. (C) The average Ka, Ks and their ratios in monocot and dicot pairs. Asterisks indicate significant differences between monocot and dicot plants at P, 0.05 (*) by t-test. (D–G) Screening for amino acid sites with purifying/positive selection in the four gene families by the SLR program as described in the Methods.
Mentions: Since the distinct difference was observed in their expansion history among the four gene families or in the same family between dicot and monocot plants (Figs 1 and 2), we investigated whether they were under different selection forces. We first identified reciprocal best matches for all four gene family members either from dicot or monocot plants by phylogenetic analysis using corresponding domain regions. The domain regions from these identified matches were then used to calculate their Ka (nonsynonymous substitutions per site), Ks (synonymous substitutions per site) and their ratios according to the description in Methods. We first analyzed and compared the Ka/Ks frequency distribution of these four gene families between monocot and dicot plants (Fig. 3A,B). For the SuSy, SPS and UDPGP families, similar frequency distributions of the Ka/Ks ratios were observed between monocot and dicot plants although their distribution patterns showed differences. There was also no significant difference between monocot and dicot plants in the average Ka, Ks and Ka/Ks values for these three gene families (Fig. 3C). For the SuSy family, most of the mass were centered near Ka/Ks > 0.5 whereas most of the mass for both SPS and UDPGP were centered near Ka/Ks = 0.1. Furthermore, the SuSy family also has the higher average Ka/Ks ratios at 0.87 for dicot and 1.04 for monocot plants whereas the average ratios for both SPS and UDPGP families were less than 0.2 for either dicot or monocot plants (Fig. 3C). These data suggested that the SuSy family evolved faster than the SPS and UDPGP families. However, for the SPP family, significant difference was observed between monocot and dicot plants in their Ka/Ks frequency distribution (Fig. 3A,B). In dicot plants, most of the mass was centered near Ka/Ks = 0.2 whereas the peak was near 0.1 for monocot plants. The average Ka/Ks for dicot plants was 0.47, statistically higher than the ratio 0.14, which was calculated for monocot plants (Fig. 3C). To further analyze the reason why both dicot and monocot plants exhibited the difference in their evolutionary rate, we compared their Ka and Ks values separately. We found that the Ka value in monocots is twice the value in dicot plants whereas the Ks value in monocots is more than three times higher than that in dicots (Fig. 3C). As a result, dicots showed significantly higher Ka/Ks ratio than that in monocots. Thus, the SPP family in dicot plants evolved faster than that in monocot plants.

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