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 molecules. 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) genes. 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 fate. PHB, PHV and REV transcripts contain a complementary site for miRNA165 and miRNA166, which can direct their cleavage in vitro. 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.

Recent developments in understanding the mechanism and functions of microRNAs

“…miR-165/166 regulates the expression of prohibitin (PHB) in Arabidopsis and RLD1 in maize. Mutations in the miR-165/166 complementary site in RLD1 causes an accumulation of RLD1-mRNA, suggesting the role of miRNAs in the regulation of genes involved in the development of maize [42]. In Arabidopsis, APETALA2 (AP2) regulates the developmental timing of flowers.…”

Fine tuning of auxin signaling by miRNAs

“…They are involved in regulating the various aspects of shoot morphogenesis from meristem establishment and maintenance (Juarez et al, 2004, McHale and Koning, 2004, Mallory et al, 2004aJuarez et al, 2004;Zhong and Ye, 2004;Bowman, 2004;Bao et al, 2004;Kim et al, 2005) to leaf development including abaxial-adaxial polarity (Palatnik et al, 2003), organ boundaries (Laufs et al, 2004), shape and complexity (Ori et al, 2007).…”

“…Leaf development is regulated by modulating the expression of class-III homeodomain leucine zipper (HD-ZIP) transcription factor genes, which control leaf patterning along adaxial/abaxial axis (Juarez et al, 2004). PHABULOSA (PHB), PHAVOLUTA (PHV), and REVOLUTA (REV) are three closely related Arabidopsis HD-ZIP transcription factors that are the targets of miR165 and miR166 (Emery et al, 2003;Bao et al, 2004;Bowman, 2004;Juarez et al, 2004;Mallory et al, 2004b;Zhong and Ye, 2004;Kim et al, 2005;Williams et al, 2005b;Ko et al, 2006).…”

“…PHABULOSA (PHB), PHAVOLUTA (PHV), and REVOLUTA (REV) are three closely related Arabidopsis HD-ZIP transcription factors that are the targets of miR165 and miR166 (Emery et al, 2003;Bao et al, 2004;Bowman, 2004;Juarez et al, 2004;Mallory et al, 2004b;Zhong and Ye, 2004;Kim et al, 2005;Williams et al, 2005b;Ko et al, 2006). Altered expression of miR165 and miR166 resulted in leaf developmental abnormalities in Arabidopsis and corn (Juarez et al, 2004). It was recently observed that overexpression of miR165 affects apical meristem formation, organ polarity establishment and vascular development in Arabidopsis (Zhou et al, 2007).…”

Genetic modification of plant architecture and variety improvement in rice

“…Analysis of the rolled-leaf mutants in maize shows that the role of HD-ZIPIIIs in adaxial specification is conserved between monocots and eudicots. Juarez et al (2004a) have demonstrated that the maize ortholog of the revoluta gene, Rld1, was misexpression in the semidominant mutant Rld1-Original (Rld1-O), which results from a single nucleotide substitution in the miRNA166 complementary site.…”