A prescient evolutionary model for genesis, duplication and differentiation of MIR160 homologs in Brassicaceae

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.