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Diversity, expression and mRNA targeting abilities of Argonaute-targeting miRNAs among selected vascular plants.

Jagtap S, Shivaprasad PV - BMC Genomics (2014)

Bottom Line: Sequences of miR168 and miR403 are not conserved among plant lineages, but surprisingly they differ drastically in their sequence diversity and expression levels even among closely related plants.Variation in miR168 expression among plants correlates well with secondary structures/length of loop sequences of their precursors.We also show that rapid evolution and likely loss of expression of miR168 isoforms in tobacco is related to the insertion of MITE-like transposons between miRNA and miRNA* sequences, a possible mechanism showing how miRNAs are lost in few plant lineages even though other close relatives have abundantly expressing miRNAs.

View Article: PubMed Central - PubMed

Affiliation: National Centre for Biological Sciences, GKVK Campus, Bellary Road, Bangalore 560 065, India. shivaprasad@ncbs.res.in.

ABSTRACT

Background: Micro (mi)RNAs are important regulators of plant development. Across plant lineages, Dicer-like 1 (DCL1) proteins process long ds-like structures to produce micro (mi) RNA duplexes in a stepwise manner. These miRNAs are incorporated into Argonaute (AGO) proteins and influence expression of RNAs that have sequence complementarity with miRNAs. Expression levels of AGOs are greatly regulated by plants in order to minimize unwarranted perturbations using miRNAs to target mRNAs coding for AGOs. AGOs may also have high promoter specificity-sometimes expression of AGO can be limited to just a few cells in a plant. Viral pathogens utilize various means to counter antiviral roles of AGOs including hijacking the host encoded miRNAs to target AGOs. Two host encoded miRNAs namely miR168 and miR403 that target AGOs have been described in the model plant Arabidopsis and such a mechanism is thought to be well conserved across plants because AGO sequences are well conserved.

Results: We show that the interaction between AGO mRNAs and miRNAs is species-specific due to the diversity in sequences of two miRNAs that target AGOs, sequence diversity among corresponding target regions in AGO mRNAs and variable expression levels of these miRNAs among vascular plants. We used miRNA sequences from 68 plant species representing 31 plant families for this analysis. Sequences of miR168 and miR403 are not conserved among plant lineages, but surprisingly they differ drastically in their sequence diversity and expression levels even among closely related plants. Variation in miR168 expression among plants correlates well with secondary structures/length of loop sequences of their precursors.

Conclusions: Our data indicates a complex AGO targeting interaction among plant lineages due to miRNA sequence diversity and sequences of miRNA targeting regions among AGO mRNAs, thus leading to the assumption that the perturbations by viruses that use host miRNAs to target antiviral AGOs can only be species-specific. We also show that rapid evolution and likely loss of expression of miR168 isoforms in tobacco is related to the insertion of MITE-like transposons between miRNA and miRNA* sequences, a possible mechanism showing how miRNAs are lost in few plant lineages even though other close relatives have abundantly expressing miRNAs.

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Related in: MedlinePlus

Alignment of miR168 targeting regions in AGO1 from various plant species. Residues in red are not conserved among others. Start and stop regions in AGO1 mRNAs have been mentioned.
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Fig2: Alignment of miR168 targeting regions in AGO1 from various plant species. Residues in red are not conserved among others. Start and stop regions in AGO1 mRNAs have been mentioned.

Mentions: If the miRNAs and their targets co-evolved with their target genes in different plant lineages as proposed [4, 23, 24], then the target mRNA regions of these miRNAs must have clade-specific changes. However, among the sequences of AGO1 mRNAs from corresponding plant species, there are hardly any clade/family specific changes in the miR168 target regions (FigureĀ 2). The miR168 target region in AGO1 mRNAs does not code for a key RNA motif that will code for a conserved domain, however, there is still high sequence conservation among AGO1 sequences derived from distinct species. This also indicates evolutionarily ancient interaction between miR168 and AGO1. A slightly higher AGO1 sequence divergence in the miRNA target region was observed among phylogenetically unrelated species such as Populus trichocarpa (Salicaceae), Cardamina flexuosa (Brassicaceae), Citrus clementine (Rutaceae), Theobroma cacao (Malvaceae) and Brachypodium distachyon (Poaceae), functional significance of which is unknown.Figure 2


Diversity, expression and mRNA targeting abilities of Argonaute-targeting miRNAs among selected vascular plants.

Jagtap S, Shivaprasad PV - BMC Genomics (2014)

Alignment of miR168 targeting regions in AGO1 from various plant species. Residues in red are not conserved among others. Start and stop regions in AGO1 mRNAs have been mentioned.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4300679&req=5

Fig2: Alignment of miR168 targeting regions in AGO1 from various plant species. Residues in red are not conserved among others. Start and stop regions in AGO1 mRNAs have been mentioned.
Mentions: If the miRNAs and their targets co-evolved with their target genes in different plant lineages as proposed [4, 23, 24], then the target mRNA regions of these miRNAs must have clade-specific changes. However, among the sequences of AGO1 mRNAs from corresponding plant species, there are hardly any clade/family specific changes in the miR168 target regions (FigureĀ 2). The miR168 target region in AGO1 mRNAs does not code for a key RNA motif that will code for a conserved domain, however, there is still high sequence conservation among AGO1 sequences derived from distinct species. This also indicates evolutionarily ancient interaction between miR168 and AGO1. A slightly higher AGO1 sequence divergence in the miRNA target region was observed among phylogenetically unrelated species such as Populus trichocarpa (Salicaceae), Cardamina flexuosa (Brassicaceae), Citrus clementine (Rutaceae), Theobroma cacao (Malvaceae) and Brachypodium distachyon (Poaceae), functional significance of which is unknown.Figure 2

Bottom Line: Sequences of miR168 and miR403 are not conserved among plant lineages, but surprisingly they differ drastically in their sequence diversity and expression levels even among closely related plants.Variation in miR168 expression among plants correlates well with secondary structures/length of loop sequences of their precursors.We also show that rapid evolution and likely loss of expression of miR168 isoforms in tobacco is related to the insertion of MITE-like transposons between miRNA and miRNA* sequences, a possible mechanism showing how miRNAs are lost in few plant lineages even though other close relatives have abundantly expressing miRNAs.

View Article: PubMed Central - PubMed

Affiliation: National Centre for Biological Sciences, GKVK Campus, Bellary Road, Bangalore 560 065, India. shivaprasad@ncbs.res.in.

ABSTRACT

Background: Micro (mi)RNAs are important regulators of plant development. Across plant lineages, Dicer-like 1 (DCL1) proteins process long ds-like structures to produce micro (mi) RNA duplexes in a stepwise manner. These miRNAs are incorporated into Argonaute (AGO) proteins and influence expression of RNAs that have sequence complementarity with miRNAs. Expression levels of AGOs are greatly regulated by plants in order to minimize unwarranted perturbations using miRNAs to target mRNAs coding for AGOs. AGOs may also have high promoter specificity-sometimes expression of AGO can be limited to just a few cells in a plant. Viral pathogens utilize various means to counter antiviral roles of AGOs including hijacking the host encoded miRNAs to target AGOs. Two host encoded miRNAs namely miR168 and miR403 that target AGOs have been described in the model plant Arabidopsis and such a mechanism is thought to be well conserved across plants because AGO sequences are well conserved.

Results: We show that the interaction between AGO mRNAs and miRNAs is species-specific due to the diversity in sequences of two miRNAs that target AGOs, sequence diversity among corresponding target regions in AGO mRNAs and variable expression levels of these miRNAs among vascular plants. We used miRNA sequences from 68 plant species representing 31 plant families for this analysis. Sequences of miR168 and miR403 are not conserved among plant lineages, but surprisingly they differ drastically in their sequence diversity and expression levels even among closely related plants. Variation in miR168 expression among plants correlates well with secondary structures/length of loop sequences of their precursors.

Conclusions: Our data indicates a complex AGO targeting interaction among plant lineages due to miRNA sequence diversity and sequences of miRNA targeting regions among AGO mRNAs, thus leading to the assumption that the perturbations by viruses that use host miRNAs to target antiviral AGOs can only be species-specific. We also show that rapid evolution and likely loss of expression of miR168 isoforms in tobacco is related to the insertion of MITE-like transposons between miRNA and miRNA* sequences, a possible mechanism showing how miRNAs are lost in few plant lineages even though other close relatives have abundantly expressing miRNAs.

Show MeSH
Related in: MedlinePlus