Rapid sequence and functional diversification of a miRNA superfamily targeting calcium signaling components in seed plants
Sharrock, Robert A.
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MicroRNA (miRNA)-directed posttranscriptional gene silencing (miR-PTGS) is an integral component of gene regulatory networks governing plant development and responses to the environment. The sequence homology between Sly-miR4376, a miRNA common to Solanaceae and reported to target autoinhibited Ca2+-ATPase 10 (ACA10) messenger RNA (mRNA) in tomato, and Arabidopsis miR391 (Ath-miR391), previously annotated as a nonconserved member of the deeply conserved miR390 family, has prompted us to revisit the function of Ath-miR391, as well as its regulatory conservation. A combination of genetic, molecular, and bioinformatic analyses revealed a hidden conservation for miR-PTGS of ACA10 homologs in spermatophytes. We found that the Arabidopsis ACA10 mRNA undergoes miR391-directed cleavage in vivo. Furthermore, transgenic overexpression of miR391 recapitulated the compact inflorescence (cif) phenotypes characteristic of ACA10 loss-of function mutants, due to miR391-directed PTGS of ACA10. Significantly, comprehensive data mining revealed robust evidence for widespread PTGS of ACA10 homologs directed by a superfamily of related miRNAs sharing a conserved sequence core. Intriguingly, the ACA-targeting miRNAs in Poaceae also direct PTGS for calmodulin-like proteins which are putative Ca2+ sensors. The PTGS of ACA10 homologs is therefore directed by a miRNA superfamily that is of ancient origin and has undergone rapid sequence diversification associated with functional innovation.
This is the peer reviewed version of the following article: [Rapid sequence and functional diversification of a miRNA superfamily targeting calcium signaling components in seed plants. New Phytologist 235, 3 p1082-1095 (2022)], which has been published in final form at https://doi.org/10.1111/nph.18185. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Use of Self-Archived Versions: https://authorservices.wiley.com/author-resources/Journal-Authors/licensing/self-archiving.html#3.
Attri, K., Zhang, Z., Singh, A., Sharrock, R. A., & Xie, Z. (2022). Rapid sequence and functional diversification of a miRNA superfamily targeting calcium signaling components in seed plants. New Phytologist.