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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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Abundance and sequence diversity of miR168 members across plant families. (A) Highest abundance of miR168 among monocots. Color bars represent most abundant forms of miR168 in leaf tissues. Blue, red and green bars represent monocot, dicot and Solanaceae-specific forms as shown in Figure 1. Abundance was measured as discussed in methods section. (B) Percentage abundance of miR168 across plant families. Phylogenetic relationships among plant species have been indicated.
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Fig6: Abundance and sequence diversity of miR168 members across plant families. (A) Highest abundance of miR168 among monocots. Color bars represent most abundant forms of miR168 in leaf tissues. Blue, red and green bars represent monocot, dicot and Solanaceae-specific forms as shown in Figure 1. Abundance was measured as discussed in methods section. (B) Percentage abundance of miR168 across plant families. Phylogenetic relationships among plant species have been indicated.

Mentions: We used small RNA datasets derived from 42 plant species representing 25 plant families to compare expression and diversity of miR168 sequences. Next generation small RNA sequence datasets from the corresponding species were taken from GEO and other published sources (See materials and methods). The abundance of miR168 and those reads that match to miR168 with 1 or 2 mismatches were taken into consideration (‘miRProf’ tool, [32]) as genomes of many of these plants and information about their miRNAs are not readily available. The data presented in Figure 6A indicates that there is very high expression of miR168 sequences among most monocot families when compared to dicots. The most abundant form of miR168 among Poaceae was the monocot-specific form of miR168 (Figure 1, Figure 6B). Similar observations were made in a recent study that compared miRNA diversity across vascular plants [12]. The other major monocot order Zingiberales (Musa acuminata) on the other hand, seem to have the common dicot specific form as the most abundant. Musa not only has a dicot specific form as most abundant form, but also has accumulation of miR168 levels matching those of dicots in that it has low accumulation. The monocot specific form surprisingly is found also among Cycads (Cycas rumphii), Gingkophyta (Gingko biloba) and Pinophyta (Picea abies). These species represent forms that are ancient to monocot/dicot divergence and it is easy to speculate that these two forms are ancient. Magnoliids (Aristolochia and Persea) show abundance of either mature miR168 form depending on the species. Depending on the plant lineage some miR168 forms could have evolved and expressed better than the other forms. Vitis vinifera (Vitales), a eudicot, has higher expression of monocot specific form unlike other eudicots for those a sequence information is available, is an example wherein both forms co-exist.Figure 6


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

Jagtap S, Shivaprasad PV - BMC Genomics (2014)

Abundance and sequence diversity of miR168 members across plant families. (A) Highest abundance of miR168 among monocots. Color bars represent most abundant forms of miR168 in leaf tissues. Blue, red and green bars represent monocot, dicot and Solanaceae-specific forms as shown in Figure 1. Abundance was measured as discussed in methods section. (B) Percentage abundance of miR168 across plant families. Phylogenetic relationships among plant species have been indicated.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig6: Abundance and sequence diversity of miR168 members across plant families. (A) Highest abundance of miR168 among monocots. Color bars represent most abundant forms of miR168 in leaf tissues. Blue, red and green bars represent monocot, dicot and Solanaceae-specific forms as shown in Figure 1. Abundance was measured as discussed in methods section. (B) Percentage abundance of miR168 across plant families. Phylogenetic relationships among plant species have been indicated.
Mentions: We used small RNA datasets derived from 42 plant species representing 25 plant families to compare expression and diversity of miR168 sequences. Next generation small RNA sequence datasets from the corresponding species were taken from GEO and other published sources (See materials and methods). The abundance of miR168 and those reads that match to miR168 with 1 or 2 mismatches were taken into consideration (‘miRProf’ tool, [32]) as genomes of many of these plants and information about their miRNAs are not readily available. The data presented in Figure 6A indicates that there is very high expression of miR168 sequences among most monocot families when compared to dicots. The most abundant form of miR168 among Poaceae was the monocot-specific form of miR168 (Figure 1, Figure 6B). Similar observations were made in a recent study that compared miRNA diversity across vascular plants [12]. The other major monocot order Zingiberales (Musa acuminata) on the other hand, seem to have the common dicot specific form as the most abundant. Musa not only has a dicot specific form as most abundant form, but also has accumulation of miR168 levels matching those of dicots in that it has low accumulation. The monocot specific form surprisingly is found also among Cycads (Cycas rumphii), Gingkophyta (Gingko biloba) and Pinophyta (Picea abies). These species represent forms that are ancient to monocot/dicot divergence and it is easy to speculate that these two forms are ancient. Magnoliids (Aristolochia and Persea) show abundance of either mature miR168 form depending on the species. Depending on the plant lineage some miR168 forms could have evolved and expressed better than the other forms. Vitis vinifera (Vitales), a eudicot, has higher expression of monocot specific form unlike other eudicots for those a sequence information is available, is an example wherein both forms co-exist.Figure 6

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