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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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Chromosomal locations of 66PvC3Hs. For those with unknown chr locations, we listed them on the right side of the figure. Duplications caused by allotetraploidy were connected by dashed red lines (between genes with known chr. locations) or blue lines. Tandem duplications were marked by red bars.
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Fig4: Chromosomal locations of 66PvC3Hs. For those with unknown chr locations, we listed them on the right side of the figure. Duplications caused by allotetraploidy were connected by dashed red lines (between genes with known chr. locations) or blue lines. Tandem duplications were marked by red bars.

Mentions: According to Okada et al. [34], allotetraploid switchgrass had two subgenomes, designated as A and B. In this study, chromosomal (Chr.) localizations of 66 PvC3Hs were found in the two subgenomes which were unevenly distributed on 18 chromosomes of nine homeologous pairs. According to the phylogenetic tree (Figure 4), we linked the paralogous pairs of PvC3Hs, and found a total of 16 pairs of paralogous PvC3Hs with defined chr. locations (red lined pairs in Figure 4). Most of these 16 pairs were in homeologous chromosomes with only one exception (PvC3H17 & PvC3H50). Tandem gene duplication was defined as paralogous genes physically linked in tandem with less than five gene loci in-between. With that definition, three tandem duplications were found: PvC3H5/6 on Chr1a, PvC3H32/33 on Chr5a, and PvC3H41/42 on Chr5b. Among maize CCCH proteins, two tandem duplications were also found (ZmC3H46/47, ZmC3H13/14) [7]. We checked whether these tandem gene duplications were within large microsyntenous regions between switchgrass and maize. As illustrated in the Additional file 5, PvC3H29/32/33 on switchgrass Chr5a and ZmC3H12/13/14 on maize Chr3, and PvC3H41/42/43 on switchgrass Chr5b and ZmC3H46/47/49 on maize Chr8 were two syntenic gene sets. The conservation and micro-colinearity of CCCH genes suggest a common origin of these genes.Figure 4


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)

Chromosomal locations of 66PvC3Hs. For those with unknown chr locations, we listed them on the right side of the figure. Duplications caused by allotetraploidy were connected by dashed red lines (between genes with known chr. locations) or blue lines. Tandem duplications were marked by red bars.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig4: Chromosomal locations of 66PvC3Hs. For those with unknown chr locations, we listed them on the right side of the figure. Duplications caused by allotetraploidy were connected by dashed red lines (between genes with known chr. locations) or blue lines. Tandem duplications were marked by red bars.
Mentions: According to Okada et al. [34], allotetraploid switchgrass had two subgenomes, designated as A and B. In this study, chromosomal (Chr.) localizations of 66 PvC3Hs were found in the two subgenomes which were unevenly distributed on 18 chromosomes of nine homeologous pairs. According to the phylogenetic tree (Figure 4), we linked the paralogous pairs of PvC3Hs, and found a total of 16 pairs of paralogous PvC3Hs with defined chr. locations (red lined pairs in Figure 4). Most of these 16 pairs were in homeologous chromosomes with only one exception (PvC3H17 & PvC3H50). Tandem gene duplication was defined as paralogous genes physically linked in tandem with less than five gene loci in-between. With that definition, three tandem duplications were found: PvC3H5/6 on Chr1a, PvC3H32/33 on Chr5a, and PvC3H41/42 on Chr5b. Among maize CCCH proteins, two tandem duplications were also found (ZmC3H46/47, ZmC3H13/14) [7]. We checked whether these tandem gene duplications were within large microsyntenous regions between switchgrass and maize. As illustrated in the Additional file 5, PvC3H29/32/33 on switchgrass Chr5a and ZmC3H12/13/14 on maize Chr3, and PvC3H41/42/43 on switchgrass Chr5b and ZmC3H46/47/49 on maize Chr8 were two syntenic gene sets. The conservation and micro-colinearity of CCCH genes suggest a common origin of these genes.Figure 4

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