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Phylogenetic analysis and molecular evolution patterns in the MIR482-MIR1448 polycistron of Populus L.

Zhao JP, Diao S, Zhang BY, Niu BQ, Wang QL, Wan XC, Luo YQ - PLoS ONE (2012)

Bottom Line: Furthermore, by comparing the substitution patterns in the miRNA-target complexes of miR482 and miR1448, we inferred that co-evolution between miRNAs and their targets was the major force that drove the "duplicated MIR482" evolve to MIR1448.We propose a novel miRNA-target pairing pattern called the "frameshift targeted mechanism" to explain the gain of target genes by miR1448.The results also imply that the major role of miR482 was in resistance to disease or other stresses via NBS-LRR proteins, whereas the biological functions of miR1448 are more diverse.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of Tree Genetics and Breeding, Institute of New Forestry Technology, Chinese Academy of Forestry, Beijing, China. zhaojiaping@gmail.com

ABSTRACT
The microRNAs (miRNAs) miR482 and miR1448 are disease resistance-related miRNAs; the former is ubiquitously distributed in seed plants whereas the latter has only been reported in Populus trichocarpa. The precursor and mature sequences of poplar miR1448 are highly homologous to those of poplar miR482, and these two miRNAs are located in one transcript as a polycistron. Therefore, we hypothesized that the MIR1448 gene may have evolved from the MIR482 gene in poplar. However, the molecular evolution patterns of this process remain unclear. In this study, utilizing cloning and Blast analysis in NCBI ESTs and whole-genome shotgun contigs (WGS) dataset, we determined that the MIR482-MIR1448 polycistron is a family-specific clustered miRNA in Salicaceae. Moreover, phylogenetic analysis illustrated that MIR1448 is the product of a tandem duplication event from MIR482. Nucleotide substitution analysis revealed that both MIR482 and MIR1448 have more rapid evolution ratios than ribosomal DNA (rDNA) genes, and that compensatory mutations that occurred in the stem region of the secondary structure were the main mechanisms that drove the evolution of these MIRNA genes. Furthermore, by comparing the substitution patterns in the miRNA-target complexes of miR482 and miR1448, we inferred that co-evolution between miRNAs and their targets was the major force that drove the "duplicated MIR482" evolve to MIR1448. We propose a novel miRNA-target pairing pattern called the "frameshift targeted mechanism" to explain the gain of target genes by miR1448. The results also imply that the major role of miR482 was in resistance to disease or other stresses via NBS-LRR proteins, whereas the biological functions of miR1448 are more diverse.

Show MeSH
Patterns of gain and loss of target genes in miR1448 miRNAs.For the four nucleotide mutations that occurred in the mature sequence of miR1448 when compared to miR482.2, poplar miR1448 lost the control of most of the target genes (miR482.2 targeted 12 NBS-LRR protein-coding genes while miR1448 only targeted 1 NBS-LRR gene). On the other hand, through a frameshift-targeted mechanism, miR1448 captured two ABC transport protein-coding genes as target genes. The underlined nucleotide site in the miRNAs represents the substitution sites when miR1448 is compared to miR482.2.
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pone-0047811-g006: Patterns of gain and loss of target genes in miR1448 miRNAs.For the four nucleotide mutations that occurred in the mature sequence of miR1448 when compared to miR482.2, poplar miR1448 lost the control of most of the target genes (miR482.2 targeted 12 NBS-LRR protein-coding genes while miR1448 only targeted 1 NBS-LRR gene). On the other hand, through a frameshift-targeted mechanism, miR1448 captured two ABC transport protein-coding genes as target genes. The underlined nucleotide site in the miRNAs represents the substitution sites when miR1448 is compared to miR482.2.

Mentions: Mature sequences of miR482.2 and miR1448 both target the sequences encoding the “MGGV(L)GK” peptide in the NB-ARC domain of some NBS-LRR resistance proteins (Figure 6, Table S1). Although the mature sequences of miR1448 were highly homologous to the mature sequences of miR482.2, four transversional substitutions still occurred in mature miR1448 compared to mature miR482.2. In the miRNA-target complex, we found that the wobble positions in the codons of target genes were very complementary to these four mutant nucleotide sites in the miRNAs, while other nucleotide sites that corresponded to the first and second positions in codons remained stable. Although four tranversional substitutions occurred, there were no transitional substitutions in the mature sequences of the MIR1448 gene. However, a two-tailed Fisher's exact test illustrated that the ratio of transversion versus transition did not deviate from the theoretical value of natural mutation. Nucleotide mutations play a major role in the gain or loss of miRNA binding sites during evolution [27]. The results of the present study imply that nucleotide mutations in MIRNA genes might play a vital role in the formation of the MIR1448 gene in poplars. Our results also revealed that the first and second positions in codons of target genes of miR1448 should have a purified selection function in the formation of miR1448. Plant miRNA binding sites exhibit almost the exact Watson–Crick complementarity to the entire mature miRNA. In previous research on rice, some miRNAs gained or lost their target genes in association with mutations that occurred in the mature sequences [27]. In the present study, after mutations occurred at specific sites, some target genes were out of the control of miR1448. For example, there were 10 NBS-LRR target genes targeted by miR482.2 while only 1 NBS-LRR gene, POPTR_0019s00620.1, remained as the solemn target gene of miR1448 in poplars (Table S1). The mutated miR1448 also targeted the mRNA region that encoded the “LWEALE” peptide in two ATP-binding cassette transport proteins (ABC transport proteins, such as POPTR_0249s00200.1) and one unknown protein (POPTR_0005s18270.1) through a mechanism that we describe as “frameshift targeted” (Figure 6, Table S1). This confirms that miR1448 captured a new target gene through mutation. With regard to plant ABC transporter proteins associated with polar auxin transport, lipid catabolism, xenobiotic detoxification, disease resistance, and stomatal function [28], this implies that miR1448 might be more significant than miR482.2 in responses to environmental change. Carrington and his colleagues suggested that MIRNA genes are undergoing relatively frequent birth and death [21]. In the present study, we suggested that the novel regulatory functions that denoted by the newly captured target genes would benefited MIR1448 gene escaped from the doom of many young MIRNA genes might encountered, and was finally stabilized by integration into poplar regulatory networks.


Phylogenetic analysis and molecular evolution patterns in the MIR482-MIR1448 polycistron of Populus L.

Zhao JP, Diao S, Zhang BY, Niu BQ, Wang QL, Wan XC, Luo YQ - PLoS ONE (2012)

Patterns of gain and loss of target genes in miR1448 miRNAs.For the four nucleotide mutations that occurred in the mature sequence of miR1448 when compared to miR482.2, poplar miR1448 lost the control of most of the target genes (miR482.2 targeted 12 NBS-LRR protein-coding genes while miR1448 only targeted 1 NBS-LRR gene). On the other hand, through a frameshift-targeted mechanism, miR1448 captured two ABC transport protein-coding genes as target genes. The underlined nucleotide site in the miRNAs represents the substitution sites when miR1448 is compared to miR482.2.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3475693&req=5

pone-0047811-g006: Patterns of gain and loss of target genes in miR1448 miRNAs.For the four nucleotide mutations that occurred in the mature sequence of miR1448 when compared to miR482.2, poplar miR1448 lost the control of most of the target genes (miR482.2 targeted 12 NBS-LRR protein-coding genes while miR1448 only targeted 1 NBS-LRR gene). On the other hand, through a frameshift-targeted mechanism, miR1448 captured two ABC transport protein-coding genes as target genes. The underlined nucleotide site in the miRNAs represents the substitution sites when miR1448 is compared to miR482.2.
Mentions: Mature sequences of miR482.2 and miR1448 both target the sequences encoding the “MGGV(L)GK” peptide in the NB-ARC domain of some NBS-LRR resistance proteins (Figure 6, Table S1). Although the mature sequences of miR1448 were highly homologous to the mature sequences of miR482.2, four transversional substitutions still occurred in mature miR1448 compared to mature miR482.2. In the miRNA-target complex, we found that the wobble positions in the codons of target genes were very complementary to these four mutant nucleotide sites in the miRNAs, while other nucleotide sites that corresponded to the first and second positions in codons remained stable. Although four tranversional substitutions occurred, there were no transitional substitutions in the mature sequences of the MIR1448 gene. However, a two-tailed Fisher's exact test illustrated that the ratio of transversion versus transition did not deviate from the theoretical value of natural mutation. Nucleotide mutations play a major role in the gain or loss of miRNA binding sites during evolution [27]. The results of the present study imply that nucleotide mutations in MIRNA genes might play a vital role in the formation of the MIR1448 gene in poplars. Our results also revealed that the first and second positions in codons of target genes of miR1448 should have a purified selection function in the formation of miR1448. Plant miRNA binding sites exhibit almost the exact Watson–Crick complementarity to the entire mature miRNA. In previous research on rice, some miRNAs gained or lost their target genes in association with mutations that occurred in the mature sequences [27]. In the present study, after mutations occurred at specific sites, some target genes were out of the control of miR1448. For example, there were 10 NBS-LRR target genes targeted by miR482.2 while only 1 NBS-LRR gene, POPTR_0019s00620.1, remained as the solemn target gene of miR1448 in poplars (Table S1). The mutated miR1448 also targeted the mRNA region that encoded the “LWEALE” peptide in two ATP-binding cassette transport proteins (ABC transport proteins, such as POPTR_0249s00200.1) and one unknown protein (POPTR_0005s18270.1) through a mechanism that we describe as “frameshift targeted” (Figure 6, Table S1). This confirms that miR1448 captured a new target gene through mutation. With regard to plant ABC transporter proteins associated with polar auxin transport, lipid catabolism, xenobiotic detoxification, disease resistance, and stomatal function [28], this implies that miR1448 might be more significant than miR482.2 in responses to environmental change. Carrington and his colleagues suggested that MIRNA genes are undergoing relatively frequent birth and death [21]. In the present study, we suggested that the novel regulatory functions that denoted by the newly captured target genes would benefited MIR1448 gene escaped from the doom of many young MIRNA genes might encountered, and was finally stabilized by integration into poplar regulatory networks.

Bottom Line: Furthermore, by comparing the substitution patterns in the miRNA-target complexes of miR482 and miR1448, we inferred that co-evolution between miRNAs and their targets was the major force that drove the "duplicated MIR482" evolve to MIR1448.We propose a novel miRNA-target pairing pattern called the "frameshift targeted mechanism" to explain the gain of target genes by miR1448.The results also imply that the major role of miR482 was in resistance to disease or other stresses via NBS-LRR proteins, whereas the biological functions of miR1448 are more diverse.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory of Tree Genetics and Breeding, Institute of New Forestry Technology, Chinese Academy of Forestry, Beijing, China. zhaojiaping@gmail.com

ABSTRACT
The microRNAs (miRNAs) miR482 and miR1448 are disease resistance-related miRNAs; the former is ubiquitously distributed in seed plants whereas the latter has only been reported in Populus trichocarpa. The precursor and mature sequences of poplar miR1448 are highly homologous to those of poplar miR482, and these two miRNAs are located in one transcript as a polycistron. Therefore, we hypothesized that the MIR1448 gene may have evolved from the MIR482 gene in poplar. However, the molecular evolution patterns of this process remain unclear. In this study, utilizing cloning and Blast analysis in NCBI ESTs and whole-genome shotgun contigs (WGS) dataset, we determined that the MIR482-MIR1448 polycistron is a family-specific clustered miRNA in Salicaceae. Moreover, phylogenetic analysis illustrated that MIR1448 is the product of a tandem duplication event from MIR482. Nucleotide substitution analysis revealed that both MIR482 and MIR1448 have more rapid evolution ratios than ribosomal DNA (rDNA) genes, and that compensatory mutations that occurred in the stem region of the secondary structure were the main mechanisms that drove the evolution of these MIRNA genes. Furthermore, by comparing the substitution patterns in the miRNA-target complexes of miR482 and miR1448, we inferred that co-evolution between miRNAs and their targets was the major force that drove the "duplicated MIR482" evolve to MIR1448. We propose a novel miRNA-target pairing pattern called the "frameshift targeted mechanism" to explain the gain of target genes by miR1448. The results also imply that the major role of miR482 was in resistance to disease or other stresses via NBS-LRR proteins, whereas the biological functions of miR1448 are more diverse.

Show MeSH