The ASYMMETRIC LEAVES Complex Employs Multiple Modes of Regulation to Affect Adaxial-Abaxial Patterning and Leaf Complexity.

Aman Y Husbands,Mukesh Lodha,Anna H Benkovics,Fabio T.S Nogueira,Marja C.P Timmermans

doi:10.1105/tpc.15.00454

Aman Y Husbands, Mukesh Lodha + Show 3 more

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https://doi.org/10.1105/tpc.15.00454

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Abstract

Flattened leaf architecture is not a default state but depends on positional information to precisely coordinate patterns of cell division in the growing primordium. This information is provided, in part, by the boundary between the adaxial (top) and abaxial (bottom) domains of the leaf, which are specified via an intricate gene regulatory network whose precise circuitry remains poorly defined. Here, we examined the contribution of the ASYMMETRIC LEAVES (AS) pathway to adaxial-abaxial patterning in Arabidopsis thaliana and demonstrate that AS1-AS2 affects this process via multiple, distinct regulatory mechanisms. AS1-AS2 uses Polycomb-dependent and -independent mechanisms to directly repress the abaxial determinants MIR166A, YABBY5, and AUXIN RESPONSE FACTOR3 (ARF3), as well as a nonrepressive mechanism in the regulation of the adaxial determinant TAS3A. These regulatory interactions, together with data from prior studies, lead to a model in which the sequential polarization of determinants, including AS1-AS2, explains the establishment and maintenance of adaxial-abaxial leaf polarity. Moreover, our analyses show that the shared repression of ARF3 by the AS and trans-acting small interfering RNA (ta-siRNA) pathways intersects with additional AS1-AS2 targets to affect multiple nodes in leaf development, impacting polarity as well as leaf complexity. These data illustrate the surprisingly multifaceted contribution of AS1-AS2 to leaf development showing that, in conjunction with the ta-siRNA pathway, AS1-AS2 keeps the Arabidopsis leaf both flat and simple.

Highlights

The formation of a stable, precisely defined boundary between two distinct cell fates is a fundamental feature of plant and animal development
To better understand the molecular basis for the mutual exclusivity of adaxial and abaxial cell fates, we set out to define the role ASYMMETRIC LEAVES1 (AS1) and AS2 play in regulating adaxial-abaxial polarity
Putative AS1-AS2 targets were selected based on adherence to the following criteria: First, putative targets must include both Motifs I and II, but as the consensus sequences for these AS1-AS2 binding elements are based on data from just two targets, specifications for these motifs were relaxed to be as inclusive as possible of putative targets

Summary

Introduction

The formation of a stable, precisely defined boundary between two distinct cell fates is a fundamental feature of plant and animal development. Adaxial-abaxial leaf polarity, which directs the acquisition of distinct cell fates within the leaf’s adaxial/ top and abaxial/bottom domains, must be carefully controlled. The boundary between these domains drives the flattened outgrowth of the leaf (Waites and Hudson, 1995), and slight perturbations in either adaxial or abaxial identity cause progressive leaf curling with severe consequences for physiological function (Lang et al, 2004; Zhang et al, 2009; Nakata et al, 2012). Adaxial-abaxial leaf polarity in particular poses an unusual and mechanistically challenging problem, namely, how to create a stable boundary

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