Origin and evolution of MIR1444 genes in Salicaceae

Abstract

miR1444s are functionally significant miRNAs targeting polyphenol oxidase (PPO) genes for cleavage. MIR1444 genes were reported only in Populus trichocarpa. Through the computational analysis of 215 RNA-seq data, four whole genome sequences of Salicaceae species and deep sequencing of six P. trichocarpa small RNA libraries, we investigated the origin and evolution history of MIR1444s. A total of 23 MIR1444s were identified. Populus and Idesia species contain two MIR1444 genes, while Salix includes only one. Populus and Idesia MIR1444b genes and Salix MIR1444s were phylogenetically separated from Populus and Idesia MIR1444a genes. Ptr-miR1444a and ptr-miR1444b showed sequence divergence. Compared with ptr-miR1444b, ptr-miR1444a started 2 nt upstream of precursor, resulting in differential regulation of PPO targets. Sequence alignments showed that MIR1444 genes exhibited extensive similarity to their PPO targets, the characteristics of MIRs originated from targets through an inverted gene duplication event. Genome sequence comparison showed that MIR1444 genes in Populus and Idesia were expanded through the Salicoid genome duplication event. A copy of MIR1444 gene was lost in Salix through DNA segment deletion during chromosome rearrangements. The results provide significant information for the origin of plant miRNAs and the mechanism of Salicaceae gene evolution and divergence.

De novo origination of MIRNAs through generation of short inverted repeats in target genes

“…Recently, three polyphenol oxidase (PPO) gene-targeting and lineage-specific young MIR families, termed MIR1444, MIR058 and MIR12112, have been reported in Populus, Vitis and Salvia, respectively [9][10][11][12][13][14]. MIR1444 is a Salicaceaespecific MIR widely existing in Salicaceae, including Populus, Salix and Idesia [9][10][11][12][13][14]. Mature miR1444 targets a subset of PPOs in a region encoding the conserved CuB domain [12].…”

“…MIR1444 is a Salicaceaespecific MIR widely existing in Salicaceae, including Populus, Salix and Idesia [9][10][11][12][13][14]. Mature miR1444 targets a subset of PPOs in a region encoding the conserved CuB domain [12]. Precursor sequence of MIR1444 exhibits extensive sequence The inverted gene duplication model [2].…”

“…Green arrows indicate transcription direction. similarity to the PPO targets and was proposed to originate from an ancient PPO gene before the Salicoid whole-genome duplication event, which happened 60 million years ago (Ma) before the divergence of Populus, Salix and Idesia [12,15]. No sequence similarity was observed for the other parts of MIR1444 and PPO genes.…”

“…CuRE contains a core sequence of GTAC and was firstly identified in the promoters of cytochrome C6 (CYC6) and coprogen oxidase (CPX1) genes in the green alga Chlamydomonas reinhardtii [22,23]. Nowadays, people have learned that CuRE is a significant cis-element widely existing in promoters of Cu-responsive protein genes and plant MIRs, such as MIR397, MIR398, MIR408, and MIR1444 [11][12][13][14][15][16][17][18][19][20][21][22][23][24]. All of these MIRs regulate the expression of genes encoding Cu-binding proteins, such as laccases (LACs), Cu-Zn superoxide dismutases (CSDs), plastocyaninlike proteins (PCLs), and PPOs.…”

“…With long-term interests in plant miRNAs [9][10][11][12]14,[31][32][33], particularly those targeting Cu-binding protein genes, I performed a systematic analysis of PPO-targeting and lineage-specific young MIRs to address various fundamental questions of their origination and evolution, such as how did the hairpin sequence originate, how did the promoter activity gain, what was the sequence of pre-MIR origination and promoter activity gain, and what could be the role of Cu in the origination and evolution of PPO-targeting MIRs?…”