Limits...
Differential retention and expansion of the ancestral genes associated with the paleopolyploidies in modern rosid plants, as revealed by analysis of the extensins super-gene family.

Guo L, Chen Y, Ye N, Dai X, Yang W, Yin T - BMC Genomics (2014)

Bottom Line: The majority of extensin genes in each of the modern rosids were found to originate from different ancestral genes.A detailed examination revealed that this group of extensins had proliferated significantly in the genomes of a number of species in the Brassicaceae.These results also provide an example of how it is essential to learn the origination of a gene when analyzing its function across different plant species.

View Article: PubMed Central - PubMed

Affiliation: The Southern Modern Forestry Collaborative Innovation Center, Nanjing Forestry University, 159#, Longpan Road, Nanjing 210037, China. tmyin@njfu.com.cn.

ABSTRACT

Background: All modern rosids originated from a common hexapolyploid ancestor, and the genomes of some rosids have undergone one or more cycles of paleopolyploidy. After the duplication of the ancient genome, wholesale gene loss and gene subfunctionalization has occurred. Using the extensin super-gene family as an example, we tracked the differential retention and expansion of ancestral extensin genes in four modern rosids, Arabidopsis, Populus, Vitis and Carica, using several analytical methods.

Results: The majority of extensin genes in each of the modern rosids were found to originate from different ancestral genes. In Arabidopsis and Populus, almost half of the extensins were paralogous duplicates within the genome of each species. By contrast, no paralogous extensins were detected in Vitis and Carica, which have only undergone the common γ-triplication event. It was noteworthy that a group of extensins containing the IPR006706 domain had actively duplicated in Arabidopsis, giving rise to a neo-extensin around every 3 million years. However, such extensins were absent from, or rare in, the other three rosids. A detailed examination revealed that this group of extensins had proliferated significantly in the genomes of a number of species in the Brassicaceae. We propose that this group of extensins might play important roles in the biology and in the evolution of the Brassicaceae. Our analyses also revealed that nearly all of the paralogous and orthologous extensin-pairs have been under strong purifying selection, leading to the strong conservation of the function of extensins duplicated from the same ancestral gene.

Conclusions: Our analyses show that extensins originating from a common ancestor have been differentially retained and expanded among four modern rosids. Our findings suggest that, if Arabidopsis is used as the model plant, we can only learn a limited amount about the functions of a particular gene family. These results also provide an example of how it is essential to learn the origination of a gene when analyzing its function across different plant species.

Show MeSH
Panoramic picture to visualize the differential retention and expansion of the ancestralextensinsassociated with paleopolyploidy events that have occurred in four modern rosids. Notes: Square represents a SCB duplicated through paleopolyploidy events within and between species. Codes in the square correspond to associated extensin genes. Genes in the same line are thought to have originated from the same ancestral gene. Genes coded with a letter followed by a number (e.g., V1) represent genes retained as extensins; genes coded with an “N” between the letter and the number (e.g., CN1) represent those that have subfunctionalized into non-extensins; “L” represents duplicated extensin that has been lost, but the corresponding SCB has been retained; blank positions correspond to situations where the whole SCBs has been completely lost.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
getmorefigures.php?uid=PMC4117974&req=5

Fig3: Panoramic picture to visualize the differential retention and expansion of the ancestralextensinsassociated with paleopolyploidy events that have occurred in four modern rosids. Notes: Square represents a SCB duplicated through paleopolyploidy events within and between species. Codes in the square correspond to associated extensin genes. Genes in the same line are thought to have originated from the same ancestral gene. Genes coded with a letter followed by a number (e.g., V1) represent genes retained as extensins; genes coded with an “N” between the letter and the number (e.g., CN1) represent those that have subfunctionalized into non-extensins; “L” represents duplicated extensin that has been lost, but the corresponding SCB has been retained; blank positions correspond to situations where the whole SCBs has been completely lost.

Mentions: Based on the gene-collinearity analysis within and between species, we established a panoramic picture of the differential retention and expansion of the ancestral extensins associated with paleopolyploidy in the four modern rosids (Figure 3). The retention and expansion of 24 ancestral extensins in these four modern rosids could be tracked unambiguously through gene collinearity analyses. The duplicates of these ancestral genes through S/WGDs were differentially retained in each species. We detected 19, 23, 6, and 4 extensin genes associated with paleopolyploidy in Arabidopsis, Populus, Carica, and Vitis, respectively (Figure 3). All of the other duplicates of these 24 ancestral genes that arose through S/WGDs were either subfunctionalized into non-extensins or completely lost (Figure 3). For instance, all genes shown in the first line of Figure 3 originated from the same ancestral gene (ancestral extensin-1). The genes that originated from this ancestral gene through ancient S/WGDs, including V1, C6, P5, P7, P6, A35 and A39, were remained as extensins; whereas the duplicates of this ancestral extensin, including VN1, CN1, PN1, AN21, AN22, and AN23 were subfunctionalized into non-extensins. Three duplicates of this ancestral extensin were lost from Arabidopsis, but the corresponding SCBs were retained (represented by an “L” at the corresponding position). Eight whole-SCBs have been completely lost from these four modern rosids (blank at the corresponding positions).Figure 3


Differential retention and expansion of the ancestral genes associated with the paleopolyploidies in modern rosid plants, as revealed by analysis of the extensins super-gene family.

Guo L, Chen Y, Ye N, Dai X, Yang W, Yin T - BMC Genomics (2014)

Panoramic picture to visualize the differential retention and expansion of the ancestralextensinsassociated with paleopolyploidy events that have occurred in four modern rosids. Notes: Square represents a SCB duplicated through paleopolyploidy events within and between species. Codes in the square correspond to associated extensin genes. Genes in the same line are thought to have originated from the same ancestral gene. Genes coded with a letter followed by a number (e.g., V1) represent genes retained as extensins; genes coded with an “N” between the letter and the number (e.g., CN1) represent those that have subfunctionalized into non-extensins; “L” represents duplicated extensin that has been lost, but the corresponding SCB has been retained; blank positions correspond to situations where the whole SCBs has been completely lost.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4117974&req=5

Fig3: Panoramic picture to visualize the differential retention and expansion of the ancestralextensinsassociated with paleopolyploidy events that have occurred in four modern rosids. Notes: Square represents a SCB duplicated through paleopolyploidy events within and between species. Codes in the square correspond to associated extensin genes. Genes in the same line are thought to have originated from the same ancestral gene. Genes coded with a letter followed by a number (e.g., V1) represent genes retained as extensins; genes coded with an “N” between the letter and the number (e.g., CN1) represent those that have subfunctionalized into non-extensins; “L” represents duplicated extensin that has been lost, but the corresponding SCB has been retained; blank positions correspond to situations where the whole SCBs has been completely lost.
Mentions: Based on the gene-collinearity analysis within and between species, we established a panoramic picture of the differential retention and expansion of the ancestral extensins associated with paleopolyploidy in the four modern rosids (Figure 3). The retention and expansion of 24 ancestral extensins in these four modern rosids could be tracked unambiguously through gene collinearity analyses. The duplicates of these ancestral genes through S/WGDs were differentially retained in each species. We detected 19, 23, 6, and 4 extensin genes associated with paleopolyploidy in Arabidopsis, Populus, Carica, and Vitis, respectively (Figure 3). All of the other duplicates of these 24 ancestral genes that arose through S/WGDs were either subfunctionalized into non-extensins or completely lost (Figure 3). For instance, all genes shown in the first line of Figure 3 originated from the same ancestral gene (ancestral extensin-1). The genes that originated from this ancestral gene through ancient S/WGDs, including V1, C6, P5, P7, P6, A35 and A39, were remained as extensins; whereas the duplicates of this ancestral extensin, including VN1, CN1, PN1, AN21, AN22, and AN23 were subfunctionalized into non-extensins. Three duplicates of this ancestral extensin were lost from Arabidopsis, but the corresponding SCBs were retained (represented by an “L” at the corresponding position). Eight whole-SCBs have been completely lost from these four modern rosids (blank at the corresponding positions).Figure 3

Bottom Line: The majority of extensin genes in each of the modern rosids were found to originate from different ancestral genes.A detailed examination revealed that this group of extensins had proliferated significantly in the genomes of a number of species in the Brassicaceae.These results also provide an example of how it is essential to learn the origination of a gene when analyzing its function across different plant species.

View Article: PubMed Central - PubMed

Affiliation: The Southern Modern Forestry Collaborative Innovation Center, Nanjing Forestry University, 159#, Longpan Road, Nanjing 210037, China. tmyin@njfu.com.cn.

ABSTRACT

Background: All modern rosids originated from a common hexapolyploid ancestor, and the genomes of some rosids have undergone one or more cycles of paleopolyploidy. After the duplication of the ancient genome, wholesale gene loss and gene subfunctionalization has occurred. Using the extensin super-gene family as an example, we tracked the differential retention and expansion of ancestral extensin genes in four modern rosids, Arabidopsis, Populus, Vitis and Carica, using several analytical methods.

Results: The majority of extensin genes in each of the modern rosids were found to originate from different ancestral genes. In Arabidopsis and Populus, almost half of the extensins were paralogous duplicates within the genome of each species. By contrast, no paralogous extensins were detected in Vitis and Carica, which have only undergone the common γ-triplication event. It was noteworthy that a group of extensins containing the IPR006706 domain had actively duplicated in Arabidopsis, giving rise to a neo-extensin around every 3 million years. However, such extensins were absent from, or rare in, the other three rosids. A detailed examination revealed that this group of extensins had proliferated significantly in the genomes of a number of species in the Brassicaceae. We propose that this group of extensins might play important roles in the biology and in the evolution of the Brassicaceae. Our analyses also revealed that nearly all of the paralogous and orthologous extensin-pairs have been under strong purifying selection, leading to the strong conservation of the function of extensins duplicated from the same ancestral gene.

Conclusions: Our analyses show that extensins originating from a common ancestor have been differentially retained and expanded among four modern rosids. Our findings suggest that, if Arabidopsis is used as the model plant, we can only learn a limited amount about the functions of a particular gene family. These results also provide an example of how it is essential to learn the origination of a gene when analyzing its function across different plant species.

Show MeSH