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MicroRNA in ovule morphogenesis

The ovule of flowering plants consists of a central embryo sac and peripheral integuments. The embryo sac is derived from one of the four daughter cells produced via meiosis and contains an egg and a central cell, which after fertilization give rise to the embryo and endosperm, respectively. On the other hand, the integuments become the seed coat at maturation. Morphogenesis of such a elaborate ovule stucture is essential not only for germ cell formation, but also for successful fertilization, embryogenesis and seed formation. Then, what makes it possible to form the ovules with such a complex structure? 
In Arabidopsis, integument formation requires functions of HD-ZIP III transcription factors, as simultaneous loss of multiple HD-ZIP III genes results in ovules lacking outer integuments. Interestingly, gain-of-function mutations to disrupt the microRNA165/166 (miR165/6)-target site of an HD-ZIP III gene PHABULOSA (PHB) also results in ovules with arrested integuments, indicating that miR165/6-dependent control of HD-ZIP III expression patterns is essential for ovule morphogenesis. However, when and where miR165/6 are produced in ovule development, and how miR165/6 affect expression patterns of HD-ZIP III genes were largely unknown.


We analyzed the expression patterns of all nine MIR165/6 genes that potentially produce functional miR165/6 molecules in the course of ovule development in Arabidopsis. Our results indicated that MIR166D and MIR166G, previously uncharacterized members of the MIR165/6 gene family, are transcribed in the basal part of developing ovules and restrict PHB expression to the inner side of the inner integuments, allowing the formation of ovules with correctly organized integuments.


Our previous studies indicated that one of the nine MIR165/6 genes, MIR165A, alone is sufficient to regulate PHB expression patterns in roots, leaves and embryos, leaving in question the significance of having multiple MIR165/6 genes to produce functionally equivalent miR165/6 molecules. Our data uncover a previously undetected functional diversification of MIR165/6 genes and significance of having multiple MIR genes for a single or functionally equivalent miRNA species in plant development.

Hashimoto, K., Miyashima, S., Sato-Nara, K., Yamada, T. and Nakajima, K. Functionally diversified members of the MIR165/6 gene family regulate ovule morphogenesis in Arabidopsis thaliana. Plant Cell Physiol. 59, 1017-1026 (2018). PubMed Publisher (Open Access)