A change in the cell wall status initiates the elimination of the nucellus in <i>Arabidopsis</i>
Abstract
The evolution of the seed habit can be traced back to a change in the cell fate of the nucellus, the sporophytic tissue responsible for female meiosis. Seeds arose when the nucellus retained the female spores instead of releasing them into the environment. As a consequence, the nucellus was partially eliminated to accommodate the growth of the female gametophyte inside the sporophyte. With the evolution of angiosperm seeds, the process of nucellus elimination was requisitioned to allow the growth of the endosperm, the fertilization product devoted to storing nutrients that are at the foundation of the human diet. Cell elimination differs from most known cell death programs as it leads to the apparent dismantling of the cell wall. Here, we show that nucellus elimination in Arabidopsis is initiated by demethylesterification and subsequent lysis of the pectic polysaccharides in the cell wall. This process exposes other cell wall components to possible further degradation and precedes a cell death program that leads to nuclear DNA fragmentation. Both pathways are regulated by TRANSPARENT TESTA 16, a MADS-domain transcription factor that evolved with seed plants. Our results highlight a convergence in the structure and function of extracellular polysaccharides in animals and plants and emphasize their crucial contribution to the development of multicellular organisms.
Article Details
Journal Info
Proceedings of the National Academy of Sciences
National Academy of Sciences
Authors (12)
Miryam Iannaccone
Institut Jean-Pierre Bourgin, Institut National de Rrecherche pour l’Agriculture, l’Alimentation et l’Environnement, AgroParisTech, CNRS, University of Paris-Saclay
Wenjia Xu
Institut Jean-Pierre Bourgin, Institut National de Rrecherche pour l’Agriculture, l’Alimentation et l’Environnement, AgroParisTech, CNRS, University of Paris-Saclay
Dennys-Marcela Gomez-Paez
Institut Jean-Pierre Bourgin, Institut National de Rrecherche pour l’Agriculture, l’Alimentation et l’Environnement, AgroParisTech, CNRS, University of Paris-Saclay
Sandrine Choinard
Institut Jean-Pierre Bourgin, Institut National de Rrecherche pour l’Agriculture, l’Alimentation et l’Environnement, AgroParisTech, CNRS, University of Paris-Saclay
Elisa Maricchiolo
Section of Biological and Biotechnological Sciences, Department of Biomolecular Sciences, University of Urbino Carlo Bo
Alexis Peaucelle
Institut Jean-Pierre Bourgin, Institut National de Rrecherche pour l’Agriculture, l’Alimentation et l’Environnement, AgroParisTech, CNRS, University of Paris-Saclay
Aline Voxeur
Institut Jean-Pierre Bourgin, Institut National de Rrecherche pour l’Agriculture, l’Alimentation et l’Environnement, AgroParisTech, CNRS, University of Paris-Saclay
Kalina Tamara Haas
Institut Jean-Pierre Bourgin, Institut National de Rrecherche pour l’Agriculture, l’Alimentation et l’Environnement, AgroParisTech, CNRS, University of Paris-Saclay
Catherine Lapierre
Institut Jean-Pierre Bourgin, Institut National de Rrecherche pour l’Agriculture, l’Alimentation et l’Environnement, AgroParisTech, CNRS, University of Paris-Saclay
Jose M. Jiménez-Gómez
Centro de Biotecnología y Genómica de Plantas
Andrea Pompa
Section of Biological and Biotechnological Sciences, Department of Biomolecular Sciences, University of Urbino Carlo Bo
Enrico Magnani
Institut Jean-Pierre Bourgin, Institut National de Rrecherche pour l’Agriculture, l’Alimentation et l’Environnement, AgroParisTech, CNRS, University of Paris-Saclay