Abstract

Leaves are flat determinate organs derived from indeterminate shoot apical meristems. The presence of a specific leaf meristem is debated, as anatomical features typical of meristems are not present in leaves. Here we demonstrate that multiple NGATHA (NGA) and CINCINNATA-class-TCP (CIN-TCP) transcription factors act redundantly, shortly after leaf initiation, to gradually restrict the activity of a leaf meristem in Arabidopsis thaliana to marginal and basal domains, and that their absence confers persistent marginal growth to leaves, cotyledons and floral organs. Following primordia initiation, the restriction of the broadly acting leaf meristem to the margins is mediated by the juxtaposition of adaxial and abaxial domains and maintained by WOX homeobox transcription factors, whereas other marginal elaboration genes are dispensable for its maintenance. This genetic framework parallels the morphogenetic program of shoot apical meristems and may represent a relic of an ancestral shoot system from which seed plant leaves evolved.

Highlights

  • Plant organs are divided into organs with indeterminate growth such as shoots, roots and vascular cambia, whose growth is maintained by meristems, groups of pluripotent cells, and organs with determinate growth such as leaves or floral organs

  • In Arabidopsis, leaf morphogenesis is initiated at the flanks of the shoot apical meristem (SAM) where leaf primordia develop as flattened lamina with defined abaxial, adaxial and marginal cell types (Tsukaya, 2013)

  • Expression of adaxial/abaxial polarity and central WUSCHEL RELATED HOMEOBOX (WOX) genes is maintained at the leaf margins when CIN-TCP and NGATHA gene activities are reduced

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Summary

Introduction

Plant organs are divided into organs with indeterminate growth such as shoots, roots and vascular cambia, whose growth is maintained by meristems, groups of pluripotent cells, and organs with determinate growth such as leaves or floral organs. In one of the first detailed examinations of development at the plant shoot apex Caspar Wolff described the leaf lamina arising from the margins of Brassica ’capitata’ (cabbage) leaves (Wolff, 1759). It had already been noted that later protracted growth in leaves occurs in tissues that are not marginal, but rather within the developing lamina in a region described as a ’plate meristem’ (Schuepp, 1918, 1926). An early ephemeral phase of cell divisions without cell expansion produces the characteristic 6–10 cell layers of the leaf thickness via submarginal periclinal cell divisions and epidermal anticlinal divisions. This is followed by a later prolonged growth phase where the bulk of two-dimensional lamina

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