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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

Multiple sequence alignment of miR168 and miR168* sequences from vascular plants. Sequences from miRBase as well those fetched from other sources (in bold, see materials and methods) were aligned using ClustalW. Residues in red are not conserved among others. Expanded names of species that are abbreviated are given in Additional file 1: Table S1.
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Fig1: Multiple sequence alignment of miR168 and miR168* sequences from vascular plants. Sequences from miRBase as well those fetched from other sources (in bold, see materials and methods) were aligned using ClustalW. Residues in red are not conserved among others. Expanded names of species that are abbreviated are given in Additional file 1: Table S1.

Mentions: In order to understand the sequence diversity of miR168, we used sequences from miRBase (version 20) as well as from genome-wide transcriptome data reported from plants that have been studied. A total of 58 sequences were obtained representing 31 families of plants. Among these, 16 were newly designated sequences. All 58 miR168 and miR168* sequences were used for sequence alignment (FigureĀ 1, Additional file 1: Table S1) that shows diversity in mature miRNA sequences. Similar miR168 diversity has been documented by a comprehensive analysis reported recently [12]. The mature miR168 sequences can be classified into 3 groups, a large dicot group representing most of the reported miR168 sequences, a monocot-specific group with sequence variations at positions 14 and 21 and a third group of miRNAs with intermediate sequence variation was observed among Solanaceae members. Solanaceae members exhibited similar sequence in 14th position (G) like other dicots, but had similarity at 21st position (C) identical to monocots. The miR168* sequences, on the other hand, had uniform sequence diversity among monocots. Distinct miR168* sequences for Solanaceae members were not observed. Among Solanaceae members, Nicotiana tabacum showed an unusual sequence diversity with two forms (d, e) showing mature miRNA sequences similar to other dicots while three additional isoforms (a,b,c) having a Solanaceae specific sequence signature. Two sequences from the dicot clade, miR168 from Brassica napus and Medicago truncatula, had variations that could not be compared to three clades and are likely results of rapid independent evolution.Figure 1


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

Jagtap S, Shivaprasad PV - BMC Genomics (2014)

Multiple sequence alignment of miR168 and miR168* sequences from vascular plants. Sequences from miRBase as well those fetched from other sources (in bold, see materials and methods) were aligned using ClustalW. Residues in red are not conserved among others. Expanded names of species that are abbreviated are given in Additional file 1: Table S1.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig1: Multiple sequence alignment of miR168 and miR168* sequences from vascular plants. Sequences from miRBase as well those fetched from other sources (in bold, see materials and methods) were aligned using ClustalW. Residues in red are not conserved among others. Expanded names of species that are abbreviated are given in Additional file 1: Table S1.
Mentions: In order to understand the sequence diversity of miR168, we used sequences from miRBase (version 20) as well as from genome-wide transcriptome data reported from plants that have been studied. A total of 58 sequences were obtained representing 31 families of plants. Among these, 16 were newly designated sequences. All 58 miR168 and miR168* sequences were used for sequence alignment (FigureĀ 1, Additional file 1: Table S1) that shows diversity in mature miRNA sequences. Similar miR168 diversity has been documented by a comprehensive analysis reported recently [12]. The mature miR168 sequences can be classified into 3 groups, a large dicot group representing most of the reported miR168 sequences, a monocot-specific group with sequence variations at positions 14 and 21 and a third group of miRNAs with intermediate sequence variation was observed among Solanaceae members. Solanaceae members exhibited similar sequence in 14th position (G) like other dicots, but had similarity at 21st position (C) identical to monocots. The miR168* sequences, on the other hand, had uniform sequence diversity among monocots. Distinct miR168* sequences for Solanaceae members were not observed. Among Solanaceae members, Nicotiana tabacum showed an unusual sequence diversity with two forms (d, e) showing mature miRNA sequences similar to other dicots while three additional isoforms (a,b,c) having a Solanaceae specific sequence signature. Two sequences from the dicot clade, miR168 from Brassica napus and Medicago truncatula, had variations that could not be compared to three clades and are likely results of rapid independent evolution.Figure 1

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