Development of schizogenous intercellular spaces in plants

Abstract

Gas exchange is essential for multicellular organisms. In contrast to the circulatory systems of animals, land plants have tissues with intercellular spaces (ICSs), called aerenchyma, that are critical for efficient gas exchange. Plants form ICSs by two different mechanisms: schizogeny, where localized cell separation creates spaces; and lysogeny, where cells die to create ICSs. In schizogenous ICS formation, specific molecular mechanisms regulate the sites of cell separation and coordinate extensive reorganization of cell walls. Emerging evidence suggests the involvement of extracellular signaling, mediated by peptide ligands and leucine-rich repeat receptor-like kinases, in the regulation of cell wall remodeling during cell separation. Recent work on the liverwort Marchantia polymorpha has demonstrated a critical role for a plasma membrane-associated plant U-box E3 ubiquitin ligase in ICS formation. In this review, I discuss the mechanism of schizogenous ICS formation, focusing on the potential role of extracellular signaling in the regulation of cell separation.

Keywords: Marchantia polymorpha; aerenchyma; cell separation; cell wall remodeling; extracellular signaling; intercellular space formation.

FIGURE 1

Schizogenous intercellular space (ICS) formation in Marchantia polymorpha. (A) Schematic representation of ICS formation during air chamber development. After a periclinal cell division to generate the protodermal and sub-protodermal cell layers, ICSs first appear as an initial aperture, between the anticlinal walls of protodermal cells. The base of the initial aperture broadens. The primary air chamber is formed via anticlinal cell divisions and protodermal and subprotodermal cell growth surrounding the ICS. (B) Hypothetical model of NOP1-mediated signaling involved in schizogenous ICS formation. Extracellular signals such as peptide ligands that are perceived by a receptor, Y, promote ICS formation via modulation of regulatory factor X that otherwise suppresses activation of cell-wall-remodeling enzymes. In the modulation of regulatory factor X, receptor Y signaling activates the E3 ligase NOP1 via phosphorylation of the ARM-repeat domain. NOP1 catalyzes the ubiquitination and subsequent degradation of regulatory factor X, which promotes cell separation through transcriptional activation of cell-wall-remodeling genes. In nop1, cell separation is constitutively suppressed by the action of regulatory factor X.