title: Function and evolution of a MicroRNA that regulates a Ca2+-ATPase and triggers the formation of phased small interfering RNAs in tomato reproductive growth.
abstract: MicroRNAs (miRNAs) regulate a wide variety of biological processes in most eukaryotes. We investigated the function and evolution of miR4376 in the family Solanaceae. We report that the 22-nucleotide miR4376 regulates the expression of an autoinhibited Ca(2+)-ATPase, tomato (Solanum lycopersicum) ACA10, which plays a critical role in tomato reproductive growth. Deep phylogenetic mapping suggested (1) an evolution course of MIR4376 loci and posttranscriptional processing of pre-miR4376 as a likely limiting step for the evolution of miR4376, (2) an independent phylogenetic origin of the miR4376 target site in ACA10 homologs, and (3) alternative splicing as a possible mechanism of eliminating such a target in some ACA10 homologs. Furthermore, miR4376 triggers the formation of phased small interfering RNAs (siRNAs) from Sl ACA10 and its Solanum tuberosum homolog. Together, our data provide experimental evidence of miRNA-regulated expression of universally important Ca(2+)-ATPases. The miR4376-regulated expression of ACA10 itself, and possibly also the associated formation of phased siRNAs, may function as a novel layer of molecular mechanisms underlying tomato reproductive growth. Finally, our data suggest that the stochastic emergence of a miRNA-target gene combination involves multiple molecular events at the genomic, transcriptional, and posttranscriptional levels that may vary drastically in even closely related species.
authors.affiliation: Department of Molecular Genetics, Ohio State University, Columbus, Ohio 43210, USA.
authors.forename: Ying
authors.initials: Y
authors.lastname: Wang
authors.forename: Asuka
authors.initials: A
authors.lastname: Itaya
authors.forename: Xuehua
authors.initials: X
authors.lastname: Zhong
authors.forename: Yang
authors.initials: Y
authors.lastname: Wu
authors.forename: Jianfeng
authors.initials: J
authors.lastname: Zhang
authors.forename: Esther
authors.initials: E
authors.lastname: van der Knaap
authors.forename: Richard
authors.initials: R
authors.lastname: Olmstead
authors.forename: Yijun
authors.initials: Y
authors.lastname: Qi
authors.forename: Biao
authors.initials: B
authors.lastname: Ding
mesh_terms: D001483:Base Sequence; D020013:Calcium Signaling; D000252:Calcium-Transporting ATPases / Q000235:genetics*; D002874:Chromosome Mapping; D003001:Cloning, Molecular; D019143:Evolution, Molecular; D035264:Flowers / Q000235:genetics / Q000254:growth & development; D005638:Fruit / Q000235:genetics / Q000254:growth & development; D018506:Gene Expression Regulation, Plant; D018551:Solanum lycopersicum / Q000201:enzymology / Q000235:genetics*; D035683:MicroRNAs / Q000235:genetics*; D008969:Molecular Sequence Data; D010802:Phylogeny; D030821:Plants, Genetically Modified / Q000201:enzymology / Q000235:genetics; D018749:RNA, Plant / Q000235:genetics*
chemical_list: D035683:MicroRNAs; D018749:RNA, Plant; D000252:Calcium-Transporting ATPases