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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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Structural variations in tobacco miR168 isoforms compared to other representative plants. (A) Variation in average length between miR168 and miR168* sequences among monocots, all dicots except Solanaceae and among Solanaceae. (B) Secondary structures of miR168 members from few plants. Although rice, soybean and Arabidopsis have 2 identical mature miR168 isoforms with almost similar secondary structures, tobacco isoforms have diverse secondary structures. RNA fold (http://rna.tbi.univie.ac.at/cgi-bin/RNAfold.cgi) was used to determine secondary structures. (C) Phylogenetic analysis of miR168 isoforms from tobacco indicating two clusters. Tree was constructed as described in methods section.
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Fig4: Structural variations in tobacco miR168 isoforms compared to other representative plants. (A) Variation in average length between miR168 and miR168* sequences among monocots, all dicots except Solanaceae and among Solanaceae. (B) Secondary structures of miR168 members from few plants. Although rice, soybean and Arabidopsis have 2 identical mature miR168 isoforms with almost similar secondary structures, tobacco isoforms have diverse secondary structures. RNA fold (http://rna.tbi.univie.ac.at/cgi-bin/RNAfold.cgi) was used to determine secondary structures. (C) Phylogenetic analysis of miR168 isoforms from tobacco indicating two clusters. Tree was constructed as described in methods section.

Mentions: The sequence and distance between miRNAs and miRNA* must indicate evolutionary history of miRNAs [29]. However, these sequences that make up the ‘loop’ are critical for host DCL1 to process the long non-coding RNAs into short miRNAs duplexes [30]. The distance between miR and miR* were quite similar among most dicot miR168 precursors, ranging typically between 50 and 80 nts (Additional file 4: Figure S3). Surprisingly, monocots had very short loop sequences in the range of 20–30 (Figure 4A). Among the Solanaceae members there were two distinct groups. One group of precursor sequences that make mature miRNAs common to other dicots, have length of loop sequences between 70–90 typical of other dicots, while some members (nta miR168d and nta miR168e) have unusually long (up to 290 nt) loops.Figure 4


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

Jagtap S, Shivaprasad PV - BMC Genomics (2014)

Structural variations in tobacco miR168 isoforms compared to other representative plants. (A) Variation in average length between miR168 and miR168* sequences among monocots, all dicots except Solanaceae and among Solanaceae. (B) Secondary structures of miR168 members from few plants. Although rice, soybean and Arabidopsis have 2 identical mature miR168 isoforms with almost similar secondary structures, tobacco isoforms have diverse secondary structures. RNA fold (http://rna.tbi.univie.ac.at/cgi-bin/RNAfold.cgi) was used to determine secondary structures. (C) Phylogenetic analysis of miR168 isoforms from tobacco indicating two clusters. Tree was constructed as described in methods section.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig4: Structural variations in tobacco miR168 isoforms compared to other representative plants. (A) Variation in average length between miR168 and miR168* sequences among monocots, all dicots except Solanaceae and among Solanaceae. (B) Secondary structures of miR168 members from few plants. Although rice, soybean and Arabidopsis have 2 identical mature miR168 isoforms with almost similar secondary structures, tobacco isoforms have diverse secondary structures. RNA fold (http://rna.tbi.univie.ac.at/cgi-bin/RNAfold.cgi) was used to determine secondary structures. (C) Phylogenetic analysis of miR168 isoforms from tobacco indicating two clusters. Tree was constructed as described in methods section.
Mentions: The sequence and distance between miRNAs and miRNA* must indicate evolutionary history of miRNAs [29]. However, these sequences that make up the ‘loop’ are critical for host DCL1 to process the long non-coding RNAs into short miRNAs duplexes [30]. The distance between miR and miR* were quite similar among most dicot miR168 precursors, ranging typically between 50 and 80 nts (Additional file 4: Figure S3). Surprisingly, monocots had very short loop sequences in the range of 20–30 (Figure 4A). Among the Solanaceae members there were two distinct groups. One group of precursor sequences that make mature miRNAs common to other dicots, have length of loop sequences between 70–90 typical of other dicots, while some members (nta miR168d and nta miR168e) have unusually long (up to 290 nt) loops.Figure 4

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