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The stamen produces pollen grains for pollination in higher plants. Coordinated development of four microsporangia in the stamen is essential for normal fertility. The roles of miR165/166-directed pathways in the establishment of adaxial-abaxial polarity have been well defined in leaves. However, the molecular mechanism underlying the adaxial-abaxial polarity of the stamen is elusive. Here it is reported that HYPONASTIC LEAVES1 (HYL1), a general regulator of microRNA (miRNA) biogenesis, plays an essential role in establishing the stamen architecture of the four microsporangia in Arabidopsis thaliana. In stamens, HYL1 and miR165/6 expression are progressively restricted to the lateral region, microsporangia, microspore mother cells, and microspores, whereas HD-ZIP III genes are preferentially expressed in the middle region, vascular bundle, and stomium. Loss of HYL1 leads to the formation of two rather than four microsporangia in each stamen. In the stamen of the hyl1 mutant, miR165/6 accumulation is reduced, whereas miR165/6-targeted HD-ZIP III genes are up-regulated and FILAMENTOUS FLOWER (FIL) is down-regulated; and, specifically, REVOLUTA (REV) is overexpressed in the adaxial region and FIL is underexpressed in the abaxial regions, concomitant with the aberrance of the two inner microsporangia and partial adaxialization of the connectives. Genetic analysis reveals that FIL works downstream of HYL1, and the defects in hyl1 stamens are partially rescued by rev-9 or phv-5 phb-6 alleles. These results suggest that HYL1 modulates inner microsporangia and stamen architecture by repression of HD-ZIP III genes and promotion of the FIL gene through miR165/6. Thus, the role of HYL1 in establishment of stamen architecture provides insight into the molecular mechanism of male fertility.

HYL1 is required for establishment of stamen architecture with four microsporangia in Arabidopsis