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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.

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Phylogenetic tree ofextensinsconstructed by the ME method with MEGA for the four modern rosids.
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Fig1: Phylogenetic tree ofextensinsconstructed by the ME method with MEGA for the four modern rosids.

Mentions: Phylogenetic trees were constructed with MEGA [29] using the ME method (Figure 1) and the NJ method (Additional file 4). The ME and NJ trees showed identical topologies. A total of 106 genes were distributed among 43 branches with bootstrap values ≥60%, and formed three distinct clades (Figure 1). Clade I consisted of 16 extensins from Arabidopsis. This clade consisted of two sub-clades, one containing A20, A22, A18 and A19, and the other containing the large paralogous group of 12 Arabidopsis extensins described above. The fact that all of the extensins in this clade were from Arabidopsis, combined with the results of the paralog analysis (Table 1), indicated that all of the extensins in clade I were intra-specific duplicates in Arabidopsis. Clade II consisted of 12 extensins; two from Arabidopsis, six from Populus, three from Carica, and one from Vitis. Extensins in this clade included two paralogous groups from Populus (P1-P2 and P5-P6-P7) and six orthologous pairs shared by the four modern rosids (C7-P24, P5-A35, P6-A39, C6-P6, V1-P5 and V1-C6). Therefore, most of the extensins in this clade represented the ancestral relics shared between species. The extensins in this clade had expanded most dramatically in Populus. Clade III contained 22 extensins: nine from Arabidopsis, 10 from Populus, two from Carica, and one from Vitis. Paralogous groups in this clade were A24-A28-A49, A26-A27, and A25-A31 from Arabidopsis, and P20-P22-P28, P18-P19, P17-P26, and P10-P12 from Populus. Clade III contained only one orthologous pair, C8-P20. Therefore, most of the extensins in this clade were intra-specific duplicates that have expanded in Arabidopsis and Populus. As well as the three distinct clades described above, there was a small clade containing four paralogous extensins from Populus (P34, P35, P36, and P37). These represented extensins that have specifically expanded within the Populus genome.Figure 1


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)

Phylogenetic tree ofextensinsconstructed by the ME method with MEGA for the four modern rosids.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig1: Phylogenetic tree ofextensinsconstructed by the ME method with MEGA for the four modern rosids.
Mentions: Phylogenetic trees were constructed with MEGA [29] using the ME method (Figure 1) and the NJ method (Additional file 4). The ME and NJ trees showed identical topologies. A total of 106 genes were distributed among 43 branches with bootstrap values ≥60%, and formed three distinct clades (Figure 1). Clade I consisted of 16 extensins from Arabidopsis. This clade consisted of two sub-clades, one containing A20, A22, A18 and A19, and the other containing the large paralogous group of 12 Arabidopsis extensins described above. The fact that all of the extensins in this clade were from Arabidopsis, combined with the results of the paralog analysis (Table 1), indicated that all of the extensins in clade I were intra-specific duplicates in Arabidopsis. Clade II consisted of 12 extensins; two from Arabidopsis, six from Populus, three from Carica, and one from Vitis. Extensins in this clade included two paralogous groups from Populus (P1-P2 and P5-P6-P7) and six orthologous pairs shared by the four modern rosids (C7-P24, P5-A35, P6-A39, C6-P6, V1-P5 and V1-C6). Therefore, most of the extensins in this clade represented the ancestral relics shared between species. The extensins in this clade had expanded most dramatically in Populus. Clade III contained 22 extensins: nine from Arabidopsis, 10 from Populus, two from Carica, and one from Vitis. Paralogous groups in this clade were A24-A28-A49, A26-A27, and A25-A31 from Arabidopsis, and P20-P22-P28, P18-P19, P17-P26, and P10-P12 from Populus. Clade III contained only one orthologous pair, C8-P20. Therefore, most of the extensins in this clade were intra-specific duplicates that have expanded in Arabidopsis and Populus. As well as the three distinct clades described above, there was a small clade containing four paralogous extensins from Populus (P34, P35, P36, and P37). These represented extensins that have specifically expanded within the Populus genome.Figure 1

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