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Comprehensive analysis of CCCH-type zinc finger family genes facilitates functional gene discovery and reflects recent allopolyploidization event in tetraploid switchgrass.

Yuan S, Xu B, Zhang J, Xie Z, Cheng Q, Yang Z, Cai Q, Huang B - BMC Genomics (2015)

Bottom Line: We also found that eight PvC3Hs in Clade-XIV were orthologous to ABA- or stress- responsive CCCH genes in Arabidopsis and rice with functions annotated.Particularly, eight PvC3Hs in Clade-XIV were found involved in stress responses.This information provides a foundation for functional studies of these genes in the future.

View Article: PubMed Central - PubMed

Affiliation: College of Life Science, Nanjing Agricultural University, Nanjing, 210095, PR China. 234435466@qq.com.

ABSTRACT

Background: In recent years, dozens of Arabidopsis and rice CCCH-type zinc finger genes have been functionally studied, many of which confer important traits, such as abiotic and biotic stress tolerance, delayed leaf senescence and improved plant architecture. Switchgrass (Panicum virgatum) is an important bioenergy crop. Identification of agronomically important genes and/or loci is an important step for switchgrass molecular breeding. Annotating switchgrass CCCH genes using translational genomics methods will help further the goal of understanding switchgrass genetics and creating improved varieties.

Results: Taking advantage of the publicly-available switchgrass genomic and transcriptomic databases, we carried out a comprehensive analysis of switchgrass CCCH genes (PvC3Hs). A total of 103 PvC3Hs were identified and divided into 21 clades according to phylogenetic analysis. Genes in the same clade shared similar gene structure and conserved motifs. Chromosomal location analysis showed that most of the duplicated PvC3H gene pairs are in homeologous chromosomes. Evolution analysis of 19 selected PvC3H pairs showed that 42.1% of them were under diversifying selection. Expression atlas of the 103 PvC3Hs in 21 different organs, tissues and developmental stages revealed genes with higher expression levels in lignified cells, vascular cells, or reproductive tissues/organs, suggesting the potential function of these genes in development. We also found that eight PvC3Hs in Clade-XIV were orthologous to ABA- or stress- responsive CCCH genes in Arabidopsis and rice with functions annotated. Promoter and qRT-PCR analyses of Clade-XIV PvC3Hs showed that these eight genes were all responsive to ABA and various stresses.

Conclusions: Genome-wide analysis of PvC3Hs confirmed the recent allopolyploidization event of tetraploid switchgrass from two closely-related diploid progenitors. The short time window after the polyploidization event allowed the existence of a large number of PvC3H genes with a high positive selection pressure onto them. The homeologous pairs of PvC3Hs may contribute to the heterosis of switchgrass and its wide adaptation in different ecological niches. Phylogenetic and gene expression analyses provide informative clues for discovering PvC3H genes in some functional categories. Particularly, eight PvC3Hs in Clade-XIV were found involved in stress responses. This information provides a foundation for functional studies of these genes in the future.

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Evolutionary relationships (A), gene structures (B) and functional motifs (C) of PvC3Hs. The evolutionary history was inferred using the N-J method [26]. The optimal tree with the sum of branch length = 24.37 is shown. Bootstrap values of 1,000 replications were executed [27], and only results with a score above 50 are shown at each node. The evolutionary distances were computed using the p-distance method [28] and are in the units of the number of amino acid differences per site. Evolutionary analyses were conducted in MEGA6 [29].
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Fig2: Evolutionary relationships (A), gene structures (B) and functional motifs (C) of PvC3Hs. The evolutionary history was inferred using the N-J method [26]. The optimal tree with the sum of branch length = 24.37 is shown. Bootstrap values of 1,000 replications were executed [27], and only results with a score above 50 are shown at each node. The evolutionary distances were computed using the p-distance method [28] and are in the units of the number of amino acid differences per site. Evolutionary analyses were conducted in MEGA6 [29].

Mentions: We constructed neighbor-joining (N-J) phylogenetic trees to illustrate the evolutionary relationships between the PvC3Hs (Figure 2a) and between all identified CCCH proteins in switchgrass, maize, rice and Arabidopsis (Additional file 3). We determined the relationships (clades) between proteins and identified a total of 21 clades including 94 PvC3Hs with the rest nine PvC3Hs as singletons based on bootstrap value >50 (Figure 2a). PvC3Hs within the same clade shared similar exon-intron structures of their encoding genes (Figure 2b) and similar numbers and distributions of functional motifs (Figure 2c). Despite the variable lengths and sequences of introns, the number of introns and the lengths of individual exons were highly similar across the PvC3Hs within the same clade. Conserved exon-intron structures and motif distribution orders across the PvC3Hs in each clade strongly supported the reliability of the phylogenetic tree. Taking Clade-XX & -XXI PvC3Hs as examples, proteins in Clade-XX had one RNA-Recognition Motif (RRM) near to the N- terminal and two CCCH motifs after the RRM; while most Clade-XXI proteins had two CCCH motifs and one RRM in-between.Figure 2


Comprehensive analysis of CCCH-type zinc finger family genes facilitates functional gene discovery and reflects recent allopolyploidization event in tetraploid switchgrass.

Yuan S, Xu B, Zhang J, Xie Z, Cheng Q, Yang Z, Cai Q, Huang B - BMC Genomics (2015)

Evolutionary relationships (A), gene structures (B) and functional motifs (C) of PvC3Hs. The evolutionary history was inferred using the N-J method [26]. The optimal tree with the sum of branch length = 24.37 is shown. Bootstrap values of 1,000 replications were executed [27], and only results with a score above 50 are shown at each node. The evolutionary distances were computed using the p-distance method [28] and are in the units of the number of amino acid differences per site. Evolutionary analyses were conducted in MEGA6 [29].
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4352264&req=5

Fig2: Evolutionary relationships (A), gene structures (B) and functional motifs (C) of PvC3Hs. The evolutionary history was inferred using the N-J method [26]. The optimal tree with the sum of branch length = 24.37 is shown. Bootstrap values of 1,000 replications were executed [27], and only results with a score above 50 are shown at each node. The evolutionary distances were computed using the p-distance method [28] and are in the units of the number of amino acid differences per site. Evolutionary analyses were conducted in MEGA6 [29].
Mentions: We constructed neighbor-joining (N-J) phylogenetic trees to illustrate the evolutionary relationships between the PvC3Hs (Figure 2a) and between all identified CCCH proteins in switchgrass, maize, rice and Arabidopsis (Additional file 3). We determined the relationships (clades) between proteins and identified a total of 21 clades including 94 PvC3Hs with the rest nine PvC3Hs as singletons based on bootstrap value >50 (Figure 2a). PvC3Hs within the same clade shared similar exon-intron structures of their encoding genes (Figure 2b) and similar numbers and distributions of functional motifs (Figure 2c). Despite the variable lengths and sequences of introns, the number of introns and the lengths of individual exons were highly similar across the PvC3Hs within the same clade. Conserved exon-intron structures and motif distribution orders across the PvC3Hs in each clade strongly supported the reliability of the phylogenetic tree. Taking Clade-XX & -XXI PvC3Hs as examples, proteins in Clade-XX had one RNA-Recognition Motif (RRM) near to the N- terminal and two CCCH motifs after the RRM; while most Clade-XXI proteins had two CCCH motifs and one RRM in-between.Figure 2

Bottom Line: We also found that eight PvC3Hs in Clade-XIV were orthologous to ABA- or stress- responsive CCCH genes in Arabidopsis and rice with functions annotated.Particularly, eight PvC3Hs in Clade-XIV were found involved in stress responses.This information provides a foundation for functional studies of these genes in the future.

View Article: PubMed Central - PubMed

Affiliation: College of Life Science, Nanjing Agricultural University, Nanjing, 210095, PR China. 234435466@qq.com.

ABSTRACT

Background: In recent years, dozens of Arabidopsis and rice CCCH-type zinc finger genes have been functionally studied, many of which confer important traits, such as abiotic and biotic stress tolerance, delayed leaf senescence and improved plant architecture. Switchgrass (Panicum virgatum) is an important bioenergy crop. Identification of agronomically important genes and/or loci is an important step for switchgrass molecular breeding. Annotating switchgrass CCCH genes using translational genomics methods will help further the goal of understanding switchgrass genetics and creating improved varieties.

Results: Taking advantage of the publicly-available switchgrass genomic and transcriptomic databases, we carried out a comprehensive analysis of switchgrass CCCH genes (PvC3Hs). A total of 103 PvC3Hs were identified and divided into 21 clades according to phylogenetic analysis. Genes in the same clade shared similar gene structure and conserved motifs. Chromosomal location analysis showed that most of the duplicated PvC3H gene pairs are in homeologous chromosomes. Evolution analysis of 19 selected PvC3H pairs showed that 42.1% of them were under diversifying selection. Expression atlas of the 103 PvC3Hs in 21 different organs, tissues and developmental stages revealed genes with higher expression levels in lignified cells, vascular cells, or reproductive tissues/organs, suggesting the potential function of these genes in development. We also found that eight PvC3Hs in Clade-XIV were orthologous to ABA- or stress- responsive CCCH genes in Arabidopsis and rice with functions annotated. Promoter and qRT-PCR analyses of Clade-XIV PvC3Hs showed that these eight genes were all responsive to ABA and various stresses.

Conclusions: Genome-wide analysis of PvC3Hs confirmed the recent allopolyploidization event of tetraploid switchgrass from two closely-related diploid progenitors. The short time window after the polyploidization event allowed the existence of a large number of PvC3H genes with a high positive selection pressure onto them. The homeologous pairs of PvC3Hs may contribute to the heterosis of switchgrass and its wide adaptation in different ecological niches. Phylogenetic and gene expression analyses provide informative clues for discovering PvC3H genes in some functional categories. Particularly, eight PvC3Hs in Clade-XIV were found involved in stress responses. This information provides a foundation for functional studies of these genes in the future.

Show MeSH