Dissecting the pathways coordinating patterning and growth by plant boundary domains

Aude Maugarny-Calès, Millán Cortizo, Bernard Adroher, Nero Borrega, Beatriz Gonçalves, Geraldine Brunoud, Teva Vernoux, Nicolas Arnaud, Patrick Laufs*

*Corresponding author for this work

Research output: Contribution to journalArticle (Academic Journal)peer-review

21 Citations (Scopus)

Abstract

Boundary domains play important roles during morphogenesis in plants and animals, but how they contribute to patterning and growth coordination in plants is not understood. The CUC genes determine the boundary domains in the aerial part of the plants and, in particular, they have a conserved role in regulating leaf complexity across Angiosperms. Here, we used tooth formation at the Arabidopsis leaf margin controlled by the CUC2 transcription factor to untangle intertwined events during boundary-controlled morphogenesis in plants. Combining conditional restoration of CUC2 function with morphometrics as well as quantification of gene expression and hormone signaling, we first established that tooth morphogenesis involves a patterning phase and a growth phase. These phases can be separated, as patterning requires CUC2 while growth can occur independently of CUC2. Next, we show that CUC2 acts as a trigger to promote growth through the activation of three functional relays. In particular, we show that KLUH acts downstream of CUC2 to modulate auxin response and that expressing KLUH can compensate for deficient CUC2 expression during tooth growth. Together, we reveal a genetic and molecular network that allows coordination of patterning and growth by CUC2-defined boundaries during morphogenesis at the leaf margin.

Original languageEnglish
Article numbere1007913
JournalPLoS Genetics
Volume15
Issue number1
DOIs
Publication statusPublished - 2019

Bibliographical note

Funding Information:
This work was supported by the Agence National de la Recherche grants MorphoLeaf (project reference ANR-10-BLAN-1614) and LeafNet (project reference ANR-12-PDOC-0003). MC was partly supported by the Fundacion Alfonso Martin Escudero. The IJPB benefits from the support of the Labex Saclay Plant Sciences-SPS (ANR-10-LABX-0040-SPS). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We thank Y. Bellaiche, O. Hamant, A. de Saint Germain, J. Traas and members of the FTA group for helpful discussion and comments on the manuscript. The greenhouse staff of the IJPB is acknowledged for excellent plant care and we thank M. Goussot for technical assistance. This paper is dedicated to the memory of the late Olivier Grandjean who was a great help with confocal microscopy.

Publisher Copyright:
© 2019 Maugarny-Calès et al.

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