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.

Immunoprofiling of Cell Wall Carbohydrate Modifications During Flooding-Induced Aerenchyma Formation in Fabaceae Roots

“…Research into genes involved in alternative processes, such as lateral root emergence, may identify similar functions during aerenchyma formation due to both events requiring cell wall remodeling to accommodate new structures within root tissues (Péret et al, 2009;Ishizaki, 2015;Porco et al, 2016;Leite et al, 2017). Specifically, genes involved in the auxin signaling pathway and cell wall remodeling genes such as those for auxin response factors in A. thaliana (Sénéchal et al, 2014) and polygalacturonases (PGLR, PGAZAT) in O. sativa (Kumpf et al, 2013) may have orthologs in legumes that also regulate pectin modification during aerenchyma formation.…”

“…Aerenchyma is often classified as either primary aerenchyma, forming within cortical tissues, or secondary aerenchyma, forming from cell divisions of meristematic phellogen layers (Shimamura et al, 2010). Primary aerenchyma can be either schizogenous, forming through separation of middle lamella between cells, or lysigenous, utilizing programmed cell death (PCD) of specific cells and tissues to form new cavities (Gunawardena et al, 2001a;Evans, 2004;Ishizaki, 2015). Lysigenous aerenchyma may also be formed in non-cortical tissues, such as the stele of legume roots such as Pisum sativum (pea) (Rost et al, 1991;Gladish and Niki, 2000;Sarkar and Gladish, 2012;Pegg et al, 2018) and Phaseolus coccineus (scarlet runner bean) roots under conditions of flooding stress (Takahashi et al, 2016).…”

The evolution of the stomatal apparatus: intercellular spaces and sporophyte water relations in bryophytes—two ignored dimensions

“…Although schizolytic processes are involved in setting the initial framework in marchantialean air chambers [22,87], these almost exclusively involve surface cells. The cavernous lumina subsequently produced are almost exclusively the result of cell overgrowth and not cell separation: from the outset the chambers are open to the exterior of the thalli and are gas-filled throughout.…”

“…While recent structural, developmental, physiological and molecular data have raised lively polarized debates and vexed questions about the evolution and functioning of stomata [1][2][3][4][5][6][7][8][9][10][11][12], not to mention the unresolved issue of unitary versus multiple origins [13][14][15][16][17][18][19][20][21], these have focused almost exclusively on the guard cells and a veritable army of genes that might affect aperture changes in the same. A growing multitude of genes are thought to be allied to stomatal biology, particularly in the context of the roles of abscisic acid (ABA); many of these are also found in bryophytes, including the liverworts-the only extant land plant clade that completely lacks stomata [22,23]. However, hard experimental data on putatively active aperture movements viz.…”

“…Like those in hornworts, the ICSs in moss sporophytes are said to resemble those in vascular plants. A subsequent review [42] makes but a brief mention of bryophytes while Ishizaki's [22] account of extracellular signalling in the regulation of cell separation focuses almost entirely on the air chambers in Marchantia. Most recent papers address cell separation either in the context of abscission or enzymatic activities associated with wall breakdown (e.g.…”