Unique Characteristics of Cell Division in Vascular Plants

Abstract

In eukaryotes, both microtubules ( MTs ) and microfilaments ( MFs ) are cytoskeletal polymers involved in meristematic cell proliferation. While animal cells build their MT arrays from structured organelles, such as centrosomes, and while they depolymerise their MFs and become round during mitosis, vascular plant cells lack centrosomes, maintain a filamentous actin cage around the spindle and are surrounded by a cell wall, preventing cellular mobility. During the cell cycle, plants activate specific dispersed MT nucleating sites, revealing successive plant‐specific cytoskeletal arrays. The MF meshwork surrounding the spindle eventually drives the centrifugal growth of MTs , which leads Golgi‐derived vesicles to fuse and separate each daughter cell during cytokinesis. The main orientation of actin fibres is parallel to that of spindle MTs , while a perpendicular constriction ring ensures animal daughter cell separation. However, despite the differences in their cytoskeleton behaviour and dynamics, both cell types succeed in controlled chromosome segregation. Key Concepts Mitosis is a short cell cycle period during which the cytoskeleton ensures balanced segregation of duplicated sister chromatids into two daughter cells. Plant cells have to deal with their pecto‐cellulosic cell wall, constraining the orientation of the division axis in order to control morphogenesis. In plants, primary stem cells are located in shoot and root apical meristems (SAM and RAM) and secondary growth is ensured by cambium activation. Besides the conservation of microtubules (MTs) and actin filaments (MFs), required for successful karyokinesis and cytokinesis, respectively, in all eukaryotes, plant mitotic cells present an original cytoskeleton organisation. All the somatic cells of vascular plants lack centrosomes, and microtubule organising centres are spread all over the nuclear envelope, at the cell cortex and along pre‐existing microtubules. Preceding the mitotic step per se , maintenance of centromere/kinetochore cohesion and integrity is required for the building of a bipolar spindle and accurate chromosome segregation. During mitosis, the activity of MT nucleating complexes (TuRCs) and MT‐associated proteins (MAPs) leads to a succession of MT arrays that reorganise in the cytoplasm: cortical MTs/perinuclear MTs/pre‐prophase band MTs/spindle MTs/phragmoplast MTs. The spindle apparatus, consisting of kinetochore fibres and interpolar MTs, is barrel‐shaped and lacks polar asters. Some of the MAPs also connect MFs. Gamma‐tubulin containing complexes and augmin complexes participate in the nucleation of new highly dynamic MTs that ensure spindle robustness. Actin filaments intermingle with MTs and do not depolymerise during mitosis, except in the PPB, which becomes an actin‐deplete zone (ADZ). The cell plate expands centrifugally to the cell edges thanks to actin filaments, preceding MTs on which Golgi‐derived vesicles move towards the equator and fuse together.

OPENER Is a Nuclear Envelope and Mitochondria Localized Protein Required for Cell Cycle Progression in Arabidopsis

“…Individual cell cycle phases were associated with specific changes in the localization of SUN2 (Oda and Fukuda, 2011) and microtubules (Chabouté and Schmit, 2001). The OPNR-YFP signals were present both in the nuclear envelope and mitochondria from interphase to early mitotic prophase (Supplemental Figure 5), but from prometaphase to anaphase, it was primarily found only in the mitochondria (Supplemental Figure 5).…”

Random chromosome distribution in the first meiosis of F1 disomic substitution line 2R(2D) x rye hybrids (ABDR, 4× = 28) occurs without bipolar spindle assembly

“…Most of our knowledge about MTs and chromosome dynamics in higher plants was obtained while studying mitosis. MT nucleation sites are the inner surface of the plasma membrane, chromosomes and nuclear envelope ( Baskin and Cande 1990 , Canaday et al 2004 , Masoud et al 2013 , de Keijzer et al 2014 , Chabout and Schmit 2016 , Lee and Liu 2019 ). The main structures formed by MTs in dividing cells during mitosis are interphase cortical or radial networks, preprophase band ( PPB ), prophase spindle and phragmoplast ( De Mey et al 1982 , Baskin and Cande 1990 , Hepler et al 1993 , Smirnova and Bajer 1992 , 1994 , 1998 ).…”

“…The pro-spindle is formed with MTs that nucleate from ɣTuRCs sites and/or H1 histone complexes on the nucleus surface ( Lee and Liu 2019 ). Motor and non-motor proteins ( MAP ) associated with microtubules, re-organise microtubules through sliding, cross-linking and severing into MT arrays, specific to the cell cycle phases ( Chabout and Schmit 2016 ).…”