Model for the regulation of Arabidopsis thaliana leaf margin development

Abstract

Biological shapes are often produced by the iterative generation of repeated units. The mechanistic basis of such iteration is an area of intense investigation. Leaf development in the model plant Arabidopsis is one such example where the repeated generation of leaf margin protrusions, termed serrations, is a key feature of final shape. However, the regulatory logic underlying this process is unclear. Here, we use a combination of developmental genetics and computational modeling to show that serration development is the morphological read-out of a spatially distributed regulatory mechanism, which creates interspersed activity peaks of the growth-promoting hormone auxin and the CUP-SHAPED COTYLEDON2 (CUC2) transcription factor. This mechanism operates at the growing leaf margin via a regulatory module consisting of two feedback loops working in concert. The first loop relates the transport of auxin to its own distribution, via polar membrane localization of the PIN-FORMED1 (PIN1) efflux transporter. This loop captures the potential of auxin to generate self-organizing patterns in diverse developmental contexts. In the second loop, CUC2 promotes the generation of PIN1-dependent auxin activity maxima while auxin represses CUC2 expression. This CUC2-dependent loop regulates activity of the conserved auxin efflux module in leaf margins to generate stable serration patterns. Conceptualizing leaf margin development via this mechanism also helps to explain how other developmental regulators influence leaf shape.L eaf margin morphology is commonly used to distinguish different plant species and often evolves in close correspondence with the environment. For example, the degree of leaf serration is a good predictor of mean annual temperature of landmasses over geological timescales (1). Variations in margin morphology were first documented in antiquity (2) and were among the first heritable traits studied in plants (3). Nonetheless, a predictive model of leaf margin shape acquisition is lacking. Recent genetic analyses have revealed two key processes required for serration formation: regulated auxin transport by the efflux carrier PINFORMED1 (PIN1) (4) and activity of the growth repressor CUP-SHAPED COTYLEDON2 (CUC2), which is negatively regulated by miR164 (5). PIN1 has a polar subcellular localization and forms convergence points at the margins of leaves, creating localized auxin activity maxima that are required for the outgrowth of serrations (4, 6). Leaves of both pin1 and cuc2 mutants fail to initiate serrations and have smooth margins, highlighting the importance of these gene products for leaf morphogenesis (4, 5). Here, we show how CUC2 activity and auxin transport and signaling are regulated and integrated to sculpt leaf margin serrations.

PLETHORA Genes Control Regeneration by a Two-Step Mechanism

“…How does CUC2 complete the shoot formation program from shoot progenitor cells? A possible mode of action is to promote PIN polarity at the periphery of shoot progenitors and thereby lateral organ outgrowth [21,30].…”

“…CUC1 and CUC2 redundantly control various developmental processes [3,24,29,30]. Among these two, we chose CUC2 as its role is more elaborately analysed in leaf development [30]. We therefore overexpressed CUC2 in plt3; plt5-2; plt7 mutants (plt3; plt5-2; plt7; pPLT7::cPLT1:vYFP; 35S::CUC2) and shoot regeneration was evaluated on SIM.…”

Transcriptomic Analyses Indicate That Maize Ligule Development Recapitulates Gene Expression Patterns That Occur during Lateral Organ Initiation

“…The role of KNOX proteins in establishing the blade-sheath boundary may be analogous to the formation of dissected or compound leaves, where reactivation of knox gene expression juxtaposed to PIN-induced auxin maxima creates new boundaries that lead to leaflet formation Barkoulas et al, 2008;Shani et al, 2009). Interactions between CUC2, whose expression is antagonized by auxin (Bilsborough et al, 2011), and its posttranscriptional regulator miR164 are important in the control of leaf serration and lobing (Nikovics et al, 2006). Given that KNOX-BEL-auxin modules act in multiple contexts during plant development, it is possible that different SBP family members are expressed depending on context, thus contributing to the elaboration of different developmental boundaries.…”

“…Bars = 100 mm. expression is negatively regulated by auxin (Furutani et al, 2004;Bilsborough et al, 2011;Q. Wang et al, 2014;Y.…”

Size and shape—integration of morphometrics, mathematical modelling, developmental and evolutionary biology

“…Similar to modern weather forecasts, this allows for describing regulatory networks and interactions of systems that would otherwise be too complex to handle. Recent cornerstones of a successful integration of mathematical models into evolutionary and developmental studies about shape variation are the prediction of a link between dorsal-ventral patterning mechanisms and tissue polarity organizers for proper flower shape formation, for example (Green et al 2010;Sauret-Güeto et al 2013), or insights into how leaf shape is established (Bilsborough et al 2011;Kuchen et al 2012). Population level variation in teeth morphology and tooth type differences in seals have been translated into mathematical models to disentangle the stages of development and the respective signaling changes responsible for the observed shape changes (Salazar-Ciudad and Jernvall 2010).…”