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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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Diversity of miR403 sequences. CLUSTAL alignment with sequences from miRBase as well as from other sources (in bold). Residues in red are not conserved among the family members.
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Fig7: Diversity of miR403 sequences. CLUSTAL alignment with sequences from miRBase as well as from other sources (in bold). Residues in red are not conserved among the family members.

Mentions: A similar search for miR403 in miRBase as well as transcript databases recovered 35 sequences (Figure 7). miR403 has been reported to be absent in monocots [4, 39], but a detailed information of plant families where this miRNA is present is not known. Among the plants where miR403 is reported, Glycine max alone has a sequence variation (at position 20) when compared to all other species. This lack of diversity in sequences arises from its recent evolution as this miRNA is present only in few lineages of eudicots. Some plant species have many copies of miR403, for example Vitis has 5 copies, all with the same mature sequence but with diverse miR* sequences. The most common and abundant form of the miR403 is 5’-UUAGAUUCACGCACAAACUCG-3’. Few interesting deviations from this sequence were observed in Solanaceae members (S. pennellii and S. tubersum) and some Malvids (Carica papaya) sharing 5’-CUAGAUUCACGCACAAACUCG-3’ as the major miR403 isoform. This isoform is extremely interesting in that it has an unusual 5’ terminal nucleotide as C. One more abundant form specific to Gossypium arboreum is 5’-UUAGAUUCACGCACAAACUCA-3’, thus, Malvids seem to have the most diversity in miR403 sequences.Figure 7


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

Jagtap S, Shivaprasad PV - BMC Genomics (2014)

Diversity of miR403 sequences. CLUSTAL alignment with sequences from miRBase as well as from other sources (in bold). Residues in red are not conserved among the family members.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig7: Diversity of miR403 sequences. CLUSTAL alignment with sequences from miRBase as well as from other sources (in bold). Residues in red are not conserved among the family members.
Mentions: A similar search for miR403 in miRBase as well as transcript databases recovered 35 sequences (Figure 7). miR403 has been reported to be absent in monocots [4, 39], but a detailed information of plant families where this miRNA is present is not known. Among the plants where miR403 is reported, Glycine max alone has a sequence variation (at position 20) when compared to all other species. This lack of diversity in sequences arises from its recent evolution as this miRNA is present only in few lineages of eudicots. Some plant species have many copies of miR403, for example Vitis has 5 copies, all with the same mature sequence but with diverse miR* sequences. The most common and abundant form of the miR403 is 5’-UUAGAUUCACGCACAAACUCG-3’. Few interesting deviations from this sequence were observed in Solanaceae members (S. pennellii and S. tubersum) and some Malvids (Carica papaya) sharing 5’-CUAGAUUCACGCACAAACUCG-3’ as the major miR403 isoform. This isoform is extremely interesting in that it has an unusual 5’ terminal nucleotide as C. One more abundant form specific to Gossypium arboreum is 5’-UUAGAUUCACGCACAAACUCA-3’, thus, Malvids seem to have the most diversity in miR403 sequences.Figure 7

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