Dynamic growth program regulated by LANCEOLATE enables flexible leaf patterning

Abstract

SUMMARYDuring their development, leaves progress through a highly controlled yet flexible developmental program. Transcription factors from the CIN-TCP family affect leaf shape by regulating the timing of leaf maturation. Characterization of mutants in the tomato (Solanum lycopersicum) CIN-TCP gene LANCEOLATE (LA) led us to hypothesize that a threshold LA-like activity promotes leaf differentiation. Here, we examined the relationship between LA activity, leaf maturation, and final leaf size and shape. Leaves of diverse shapes from various Solanaceae species or from different positions on the tomato plant differed in the timing of growth and maturation, and these were often associated with altered LA expression dynamics. Accordingly, genetic manipulations of LA activity in tomato altered leaf growth and maturation, leading to changes in leaf size and shape. LA expression sustained until late stages of tomato leaf development, and stage-specific overexpression of miR319, a negative regulator of CIN-TCP genes, confirmed that LA-like proteins affect leaf development through these late stages. Together, our results imply that dynamic spatial and temporal leaf maturation, coordinated by LA-like genes, enables the formation of variable leaf forms.

Leaf development and morphogenesis

“…A subset of CIN-TCPs, including LANCEOLATE (LA) from tomato, is negatively regulated by the microRNA miR319. In the tomato semi-dominant gain-of-function mutant La, a mutation in the miR319-binding site leads to precocious LA expression, resulting in precocious differentiation and small, simplified leaves (Dengler, 1984;Mathan and Jenkins, 1962;Ori et al, 2007;Shleizer-Burko et al, 2011;Stettler, 1964). Concurrently, premature expression of the miR319-insensitive TCP4 in Arabidopsis plants causes early onset of maturation, resulting in a range of leaf patterning defects (Efroni et al, 2008;Palatnik et al, 2003).…”

“…Concurrently, premature expression of the miR319-insensitive TCP4 in Arabidopsis plants causes early onset of maturation, resulting in a range of leaf patterning defects (Efroni et al, 2008;Palatnik et al, 2003). By contrast, downregulation of CIN-TCP genes by overexpression of miR319 results in a substantial delay in leaf maturation and prolonged indeterminate growth in the leaf margin (Efroni et al, 2008;Koyama et al, 2007;Ori et al, 2007;Shleizer-Burko et al, 2011). It would thus seem that maintenance of the morphogenic window is dependent on low TCP activity during the early stages of leaf development.…”

“…Recent studies have shown that leaf size and the rate of leaf maturation are regulated by partially overlapping pathways, including those involving CIN-TCPs, ARP/AS2 and hormone dynamics. However, leaf size is not always correlated with leaf complexity or with the number of cells, pointing to partially independent regulation of these three processes Kaplan, 1992;Shleizer-Burko et al, 2011). The issue of leaf size has been the recent focus of several reviews to which we refer the reader (Hepworth and Lenhard, 2014;Powell and Lenhard, 2012).…”

Heterochrony underpins natural variation inCardamine hirsutaleaf form

“…This process involves the leaf-specific homeobox gene REDUCED COMPLEXITY (RCO) (7). Furthermore, in dissected leafed species, leaf complexity is regulated by the activity of TEOSINTE BRANCHED1/CYCLOIDEA/PROLIFERATING CELL FACTOR (TCP) genes, which modulate the competence of the leaf margin to respond to organogenic signals (8,9).…”

Enhancing crop yield by optimizing plant developmental features

“…For example, wavy auricle in blade1 (wab1), which encodes a maize TCP transcription factor, regulates leaf width, proximal-distal patterning and lateral vein number in a cell-autonomous manner (Foster et al, 2004). TCPs also regulate the differentiation, patterning and maturation of leaves by maintaining GA/cytokinin homeostasis in Arabidopsis and tomato, and thus could be used to control the timing of photosynthetic capacity in leaves (Shleizer-Burko et al, 2011).…”