Mechanisms of leaf tooth formation in Arabidopsis

Abstract

SUMMARYSerration found along leaf margins shows species-specific characters. Whereas compound leaf development is well studied, the process of serration formation is largely unknown. To understand mechanisms of serration development, we investigated distinctive features of cells that could give rise to tooth protrusion in the simpleleaf plant Arabidopsis. After the emergence of a tooth, marginal cells, except for cells at the sinuses and tips, started to elongate rapidly. Localized cell division seemed to keep cells at the sinus smaller, rather than halt cell elongation. As leaves matured, the marginal cell number between teeth became similar in any given tooth. These results suggest that teeth are formed by repetition of an unknown mechanism that spatially monitors cell number and regulates cell division. We then examined the role of CUP-SHAPED COTYLEDON 2 (CUC2) in serration development. cuc2-3 forms fewer hydathodes and auxin maxima, visualized by DR5rev::GFP, at the leaf margin, suggesting that CUC2 patterns serration through the regulation of auxin. In contrast to a previous interpretation, comparison of leaf outlines revealed that CUC2 promotes outgrowth of teeth rather than suppression of growth at the sinuses. We found that mutants with increased CUC2 expression form ectopic tissues and mis-express SHOOT MERISTEMLESS (STM) at the sinus between the enhanced teeth. Similar but infrequent STM expression was found in the wild type, indicating STM involvement in the serration of simple leaves. Our study provides insights into the morphological and molecular mechanisms for leaf development and tooth formation, and highlights similarities between serration and compound leaf development.

Multiscale quantification of morphodynamics: MorphoLeaf, software for 2-D shape analysis

“…CUC2 has been suggested to lead to Arabidopsis leaf serration by two mechanisms: repression of growth to form the sinuses and/or growth promotion to lead to tooth outgrowth (Nikovics et al, 2006;Kawamura et al, 2010;Bilsborough et al, 2011). Our precise comparison of the early shapes of wild type versus cuc2 mutants indeed showed that the two mechanisms occur but at different stages.…”

“…Role of CUC2 during leaf serration CUC2 is an important regulator of leaf margin serration and has been proposed to either locally repress growth to form the tooth sinuses (Nikovics et al, 2006) to promote tooth outgrowth (Kawamura et al, 2010) or a combination of both (Bilsborough et al, 2011). We used MorphoLeaf to finely compare early stages of leaf development between the wild type and the cuc2-1 mutant (Fig.…”

“…Numerous factors, including transcription factors, miRNAs and hormones control leaf development (Bar and Ori, 2014;Rodriguez et al, 2014;Sluis and Hake, 2015). Transcription factors of the CUP-SHAPED COTYLEDON2 (CUC2) family, for example, have a central role in the dissection of the leaf margin into teeth or leaflets (Nikovics et al, 2006;Blein et al, 2008;Berger et al, 2009;Kawamura et al, 2010;Bilsborough et al, 2011;Hasson et al, 2011;Cheng et al, 2012). Other factors have also been shown to affect the patterns of cell division, growth or differentiation and have been associated with changes in leaf shape and/or size (Vlad et al, 2014;Das Gupta and Nath, 2015;Gonzalez et al, 2015).…”

Morphological changes of Rosa×hybrida by a chimeric repressor of Arabidopsis TCP3

“…Comparisons between the mild and severe phenotypes of the TCP3SRDX rose plants suggested that CIN-type TCPs may control the molecular mechanisms for the both leaf-tooth and leaf/leaflet formation. The formation process of leaf teeth is similar to that of simple leaves and leaflets (Kawamura et al 2010); the CUC genes are involved in the development of both leaf teeth (Nikovics et al 2006) and leaves and leaflets (Aida et al 1997;Blein et al 2008). These results imply that rose KNOX1 and CUC2 homologues may be involved in excessive compound-leaf formations and the deep serrations observed in TCP3SRDX rose plants.…”

Trifoliate encodes an MYB transcription factor that modulates leaf and shoot architecture in tomato

“…In the leaf, CUC genes repress growth at blade indentations and between leaflets (14-16) and promote the outgrowth of teeth (17). CUC genes are also important regulators of axillary meristem formation in Arabidopsis and tomato (18)(19)(20).…”