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microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity

Abstract

In both animals and plants, many developmentally important regulatory genes have complementary microRNAs (miRNAs), which suggests that these miRNAs constitute a class of developmental signalling molecules1. Leaves of higher plants exhibit a varying degree of asymmetry along the adaxial/abaxial (upper/lower) axis. This asymmetry is specified through the polarized expression of class III homeodomain/leucine zipper (HD-ZIPIII) genes2,3,4. In Arabidopsis, three such genes, PHABULOSA (PHB), PHAVOLUTA (PHV) and REVOLUTA (REV), are expressed throughout the incipient leaf, but become adaxially localized after primordium emergence. Downregulation of the HD-ZIPIII genes allows expression of the KANADI and YABBY genes, which specify abaxial fate5,6,7,8. PHB, PHV and REV transcripts contain a complementary site for miRNA165 and miRNA166, which can direct their cleavage in vitro9,10,11. Here we show that miRNA166 constitutes a highly conserved polarizing signal whose expression pattern spatially defines the expression domain of the maize hd-zipIII family member rolled leaf1 (rld1). Moreover, the progressively expanding expression pattern of miRNA166 during leaf development and its accumulation in phloem suggests that miRNA166 may form a movable signal that emanates from a signalling centre below the incipient leaf.

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Acknowledgements

We thank T. Phelps-Durr, C. Kidner, T. Volpe and G. Hannon for discussions and comments on the manuscript. We also thank T. Mulligan for plant care. This work was supported by grants from the USDA. and the NSF (to M.C.P.T.). M.T.J. is funded in part by a W. Burghardt Turner Fellowship, and J.S.K. is an Alfred Hershey Fellow of the Watson School of Biological Sciences and is supported by a grant from the National Institute of General Medical Sciences, NIH.

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Correspondence to Marja C. P. Timmermans.

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The authors declare that they have no competing financial interests.

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Further reading

Figure 1: Effects of Rld1-O on leaf polarity.
Figure 2: Dominant Rld1 mutations affect the miRNA166 complementary site.
Figure 3: rld1 and phb expression in the wild type and Rld1-O.
Figure 4: Complementary hd-zipIII and miRNA166 expression.

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