Midbodies and phragmoplasts: analogous structures involved in cytokinesis

Abstract

Cytokinesis is an event common to all organisms that involves the precise coordination of independent pathways involved in cell-cycle regulation and microtubule, membrane, actin and organelle dynamics. In animal cells, the spindle midzone/midbody with associated endo-membrane system are required for late cytokinesis events, including furrow ingression and scission. In plants, cytokinesis is mediated by the phragmoplast, an array of microtubules, actin filaments and associated molecules that act as a framework for the future cell wall. In this article (which is part of the Cytokinesis series), we discuss recent studies that highlight the increasing number of similarities in the components and function of the spindle midzone/midbody in animals and the phragmoplast in plants, suggesting that they might be analogous structures.

Figure 1

Overview of animal and plant cytokinesis. (a) Cytokinesis in animal cells. The spindle midzone/midbody forms when microtubules (MTs) from opposite poles overlap. It consists of the overlapping microtubules as well as associated proteins that bundle these MTs and other proteins that together form a dense protein matrix. This matrix excludes antibodies against MTs, giving a stereotypical region devoid of staining. As the furrow ingresses, the midzone is swept into one larger structure called the midbody. The Golgi and endoplasmic reticulum (ER) membranes are also found in the midbody during telophase to cytokinesis. It is proposed that vesicles (V) traffic along the midbody microtubules toward the ingressing furrow. (b) Cytokinesis in somatic plant cells. The forming cell plate is assisted by the phragmoplast at the future site of the new cell wall. Two topographic regions can be distinguished in the phragmoplast: the phragmoplast midline (Ph M), where the opposing set of microtubules interdigitate, and the distal phragmoplast (distal Ph), at both sides of the phragmoplast midline. A filamentous cell-plate assembly matrix (CPAM) accumulates at the phragmoplast midline. Key: MT, microtubule (green); N, nucleus (tan); V, vesicle (yellow); Golgi (pale blue); midbody matrix (gray box); CPAM (gray circles).

Figure 2

Models for assembly of the midbody and phragmoplast. (a) Model depicting midbody organization. Overlapping microtubule plus-ends are embedded within the midbody matrix. The midbody microtubules are stabilized and crosslinked by several kinesins, microtubule-associated proteins (MAPs), kinases and other proteins, such as MKLP1/ZEN-4/PAV, MgcRACGAP/CYK-4, PRC1/SPD-1/FEO/Ase1p, chTOG/ZYG-9/Msps, TACC/TAC-1, CLIP-170, EB1, KLP61F/BimC, and the chromosomal passengers Aurora B/AIR-2, Survivin/BIR-1, INCENP/ICP-1, -2 and Borealin/CSC-1. PRC1 is possibly transported by KIF4 along the midzone microtubules (MTs). It is possible that KIF4 also transports Golgi-derived vesicles along midbody MTs where they fuse with the ingressing furrow. ZEN-4 and PRC1 are phosphorylated by Cdk1. Golgi assembly occurs when Cdk1 activity is low in telophase. Golgi stack assembly is also promoted by the degradation of Polo kinase and MEK1 in telophase (U: ubiquitin moiety). NIR2, a Golgi-associated protein, is found more prominently on the cleavage furrow as well as the spindle midzone in telophase to cytokinesis in a complex with Polo kinase. Membrane fusion occurs at the tips and along the ingressing furrow and involves a variety of proteins such as the exocyst complex, SNAREs, dynamin/DYN-1 and their interactors. Note: to simplify the figure, we have omitted several homologs/orthologs of several proteins. (b) Model depicting phragmoplast organization in plant cells. Microtubule plus-ends enclosed inside the cell-plate assembly matrix (CPAM) are stabilized and crosslinked by several MAPs, such as MAP55-1, MAP65-3, MOR1/GEM1, and by kinesin motor proteins. Golgi-derived vesicles are transported to the division plane along MTs by a kinesin motor protein, where they fuse with others while enclosed by the CPAM. Membrane fusion at the cell plate involves a variety of proteins such as tethering factors, SNAREs and their interactors. Formation of tubular domains in the developing cell plate appears to be mediated by DRP1A.