Abstract
MicroRNA160 is a class of nitrogen-starvation responsive genes which governs establishment of root system architecture by down-regulating AUXIN RESPONSE FACTOR genes (ARF10, ARF16 and ARF17) in plants. The high copy number of MIR160 variants discovered by us from land plants, especially polyploid crop Brassicas, posed questions regarding genesis, duplication, evolution and function. Absence of studies on impact of whole genome and segmental duplication on retention and evolution of MIR160 homologs in descendent plant lineages prompted us to undertake the current study. Herein, we describe ancestry and fate of MIR160 homologs in Brassicaceae in context of polyploidy driven genome re-organization, copy number and differentiation. Paralogy amongst Brassicaceae MIR160a, MIR160b and MIR160c was inferred using phylogenetic analysis of 468 MIR160 homologs from land plants. The evolutionarily distinct MIR160a was found to represent ancestral form and progenitor of MIR160b and MIR160c. Chronology of evolutionary events resulting in origin and diversification of genomic loci containing MIR160 homologs was delineated using derivatives of comparative synteny. A prescient model for causality of segmental duplications in establishment of paralogy in Brassicaceae MIR160, with whole genome duplication accentuating the copy number increase, is being posited in which post-segmental duplication events viz. differential gene fractionation, gene duplications and inversions are shown to drive divergence of chromosome segments. While mutations caused the diversification of MIR160a, MIR160b and MIR160c, duplicated segments containing these diversified genes suffered gene rearrangements via gene loss, duplications and inversions. Yet the topology of phylogenetic and phenetic trees were found congruent suggesting similar evolutionary trajectory. Over 80% of Brassicaceae genomes and subgenomes showed a preferential retention of single copy each of MIR160a, MIR160b and MIR160c suggesting functional relevance. Thus, our study provides a blue-print for reconstructing ancestry and phylogeny of MIRNA gene families at genomics level and analyzing the impact of polyploidy on organismal complexity. Such studies are critical for understanding the molecular basis of agronomic traits and deploying appropriate candidates for crop improvement.
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Acknowledgements
This work was supported by grants from Department of Biotechnology, Govt. of India (BT/PR10071/AGR/36/31/2007) and SERB-Department of Science and Technology, Govt. of India (EMR/2016/007813) received by AS. Fellowship to SS from Department of Science and Technology, Govt. of India, is gratefully acknowledged. Infrastructural support from TERI and TERI School of Advanced Studies is duly acknowledged.
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438_2021_1797_MOESM1_ESM.tif
Supplementary file1 (TIF 29298 KB) Identification of 468 homologs of MIR160 from 31 families of plant kingdom. The numerical values signify number of MIR160 sequences identified within each family.
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Supplementary file2 (TIF 34183 KB) Phylogenetic reconstruction of MIR160 homologs from Brassicaceae, Bryophytes and Gymnosperms. Relative to clades corresponding to MIR160b (green) and MIR160c (yellow), the clade specific to MIR160a (red) is evolutionarily closer to Bryophytes and Gymnosperms.
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Supplementary file3 (TIF 28914 KB) Phylogenetic reconstruction depicting evolutionary relationships between Brassicaceae MIR160 homologs. Clade specific to MIR160a (red) is distinct from clade containing MIR160b (green) & MIR160c (yellow). Within each clade, homologs of Brassica species derived from progenitor genomes AA, BB and CC group together in accordance with their sub-genome of origin (LF, MF1 and MF2).
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Supplementary file4 (TIF 99707 KB) Synteny analysis of 15 chromosomal segments (100 kb) containing MIR160a across 4 Brassica species including with A. thaliana as reference genome reveals gene preservation, duplication, and rearrangements. Synteny was established by mapping gene homologs of A. thaliana onto orthologous segments of Brassicaceae species. Position of MIR160a is depicted as a red triangle. Dashed connectors represent gene duplications within a genome/subgenome. Black rectangular boxes represent tandem duplicated blocks within each genome/subgenome.
438_2021_1797_MOESM5_ESM.tif
Supplementary file5 (TIF 70788 KB) Synteny analysis of 10 chromosomal segments containing MIR160b across 8 non-Brassica species with A. thaliana as reference reveals gene preservation, duplication, and rearrangements. Synteny was established by mapping gene homologs of A. thaliana onto orthologous segments (100 kb) of Brassicaceae species. Position of MIR160b is depicted as a red triangle. Dashed connectors represent gene duplications within a genome/subgenome. Black rectangular boxes represent tandem duplicated blocks within each genome/subgenome.
438_2021_1797_MOESM6_ESM.tif
Supplementary file6 (TIF 106077 KB) Synteny analysis of 16 chromosomal segments (100 kb) containing MIR160b across 4 Brassica species with A. thaliana as reference reveals gene preservation, duplication, and rearrangements. Position of MIR160b is depicted as a red triangle. Dashed connectors represent gene duplications within a genome / subgenome. Black rectangular boxes represent tandem duplicated blocks within each genome/subgenome.
438_2021_1797_MOESM7_ESM.tif
Supplementary file7 (TIF 77521 KB) Synteny analysis of 11chromosomal segments (100 kb) containing MIR160c across 8 non-Brassica species of Brassicaceae with A. thaliana as reference reveals gene preservation, duplication, and rearrangements. Position of MIR160c is depicted as a red triangle. Dashed connectors represent gene duplications within a genome/subgenome. Black rectangular boxes represent tandem duplicated blocks within each genome/subgenome.
438_2021_1797_MOESM8_ESM.tif
Supplementary file8 (TIF 99590 KB) Synteny analysis of 13 chromosomal segments (100 kb) containing MIR160c across 4 Brassica species of Brassicaceae with A. thaliana as reference reveals gene preservation, duplication, and rearrangements. Position of MIR160c is depicted as a red triangle. Dashed connectors represent gene duplications within a genome/subgenome. Black rectangular boxes represent tandem duplicated blocks within each genome/subgenome.
438_2021_1797_MOESM9_ESM.tif
Supplementary file9 (TIF 286293 KB) Comparative genome fractionation analysis across chromosomal segments (100 kb) harboring MIR160a, MIR160b and MIR160c derived from three subgenomes (LF, MF1 and MF2) of B. rapa. Comparative gene retention across subgenome specific chromosomal segments is interpreted using a hypothetical composite gene list as a reference. The reference is a non-redundant gene list comprising of both co-retained and unique genes present across the chromosomal segments derived from three subgenomes of B. rapa. The data is illustrated separately for chromosomal segments containing MIR160a (panel a), MIR160b (panel c) and MIR160c (panel e), respectively. The chromosomal segments are represented as rows of cells with cells depicting gene homologs. The extent of co-retention is depicted using mustard cells (gene retention across all the 3 subgenome), blue cells (gene retention across two subgenomes), black cells (gene homologs that are unique to a subgenome), and red cells (MIR160 homologs). Subgenome specific copy number of genes present across the three subgenomes of B. rapa is represented for each of the MIR160a (panel b), MIR160b (panel d), and MIR160c (panel f), respectively. The vertically arranged list of genes is organized based on copy number. Solid connectors join these to respective subgenome of origin shown in the right. The thickness of the connector depicts the copy number in a specific subgenome. The key for colored cells adjoining each of the listed gene correlates with the key proposed for panel a, c and e.
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Supplementary file10 (TIF 101383 KB) Multiple sequence alignment across the complete length of precursor sequences of 52 MIR160 homologs of Brassica species. The mature and star region mapping to locations of the least polymorphism in the precursor is indicated by miRNA and miRNA* respectively. SNP within miRNA and miRNA* is marked with the red arrow.
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Supplementary file11 (TIF 103378 KB) Diversity in predicted fold back structures of MIR160b precursor sequences from Brassica species (mFOLD server: RNA folding Form V2.3). The structures have been categorized into six groups based upon structural similarity.
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Supplementary file12 (TIF 96112 KB) Diversity in predicted fold back structures of MIR160c precursor sequences from Brassica species (mFOLD server: RNA folding Form V2.3). The structures have been categorized into four groups based upon structural similarity.
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Singh, S., Singh, A. A prescient evolutionary model for genesis, duplication and differentiation of MIR160 homologs in Brassicaceae. Mol Genet Genomics 296, 985–1003 (2021). https://doi.org/10.1007/s00438-021-01797-8
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DOI: https://doi.org/10.1007/s00438-021-01797-8