Microsynteny and phylogenetic analysis of tandemly organised miRNA families across five members of Brassicaceae reveals complex retention and loss history

• Published in: Plant science (Limerick) Vol. 247; pp. 35 - 48
• Main Authors: Rathore, Priyanka, Geeta, R., Das, Sandip
• Format: Journal Article
• Language: English
• Published: Ireland Elsevier Ireland Ltd 01.06.2016
• Subjects: Arabidopsis; Arabidopsis - genetics; Arabidopsis thaliana; Brassica rapa; Brassicaceae; Brassicaceae - genetics; Capsella; Capsella rubella; Evolution; Evolution, Molecular; Genome, Plant - genetics; Halophila; MicroRNAs - genetics; miRNA; Phylogeny; RNA, Plant - genetics; Synteny - genetics; Tandem organisation; Thellungiella; RISC; mya; Tandem organisation; miRNA; Evolution; my; Brassicaceae
• ISSN: 0168-9452; 1873-2259
• DOI: 10.1016/j.plantsci.2016.03.002

•Synteny at tandemly organised miRNA families is conserved in the Arabidopsis-Capsella lineage, compared to in Brassica Thellungiella lineage.•Synteny and phylogenetic analysis of miR169 reveal a unique evolutionary history of expansion.•miRNA family miR845 has a complex history of birth retention and loss as homologs of miR845 were detected only in Arabidopsis and Thellungiella.•Mir447A-B and miR5020 family were specific to Arabidopsis indicating these to be of recent origin. Plant genomes are characterized by the presence of large miRNA gene families which are few in number. The expansion of miRNA families is thought to be driven by gene and genome duplication. Some members of these miRNA gene families are tandemly arranged and their analysis is of interest because such organisation may indicate origin through tandem duplication and also to investigate whether some such tandem clusters have similar expression patterns, and whether these are regulated through a common set of cis-regulatory elements (eg. promoters and enhancers). As a first step, we undertake a comprehensive study using micro-synteny analyses of tandemly organised miRNA families across the Brassicaceae spanning an evolutionary time scale of ca. 45 million years, among Arabidopsis, Capsella, Brassica and Thellungiella species, to address the following questions: Are most miRNA gene families present as tandem clusters? To what extent are these tandem patterns retained? To what extent can family sizes be ascribed to genome duplication? Our analysis of thirteen tandemly organised miRNA families revealed that synteny is largely conserved among Arabidopsis thaliana, A. lyrata and Capsella rubella, which form a clade spanning approximately between 6.2–9.8 my (Acarkan et al., 2000) [1]. On the other hand, comparison of sequences from these species with Brassica rapa, B. oleracea and Thellungiella halophila, which form a separate clade spanning 31 my (Franzke et al., 2011) [2] reveals many differences. The latter clade reveals several paralogous duplications that probably resulted from whole genome duplication, as well as disrupted synteny. Phylogenetic analyses of precursor sequences generally support the history inferred from synteny analysis. Synteny and phylogenetic analysis of six members of the tandemly organised miR169 family suggest that the Brassicaceae ancestral state consisted of a “dimer as a unit” which may have undergone direct local duplication to retain the transcriptional orientation followed by lineage specific changes. MiR169, to the best of our knowledge, is one of the largest tandemly organised miRNA gene family across plant kingdom and further analysis should reveal the generality of this pattern of evolution. The conserved organisation of miR395A-B-C and miR395 D-E-F as two clusters on same chromosome/scaffold across A. thaliana, B. rapa and salsuginea demonstrates retention of the large chromosomal segment across the two lineages. MiRNA family miR845 was detected only in Arabidopsis species and Thellungiella indicating a complex loss and retention history. MiR447A-B family was only found in A. thaliana indicating that it is a species-specific gene family of recent origin.