Plant Actin Biology

Abstract

Actin is a major component of the plant cytoskeleton. Filamentous actin (F‐actin) contributes to the maintenance of the internal architecture of the cell, drives cytoplasmic streaming (the movement of components around the cytosol) and contributes to the process of cell division. The biochemistry of plant actin has many similarities to that of yeast and animals, but has developed its own strategies and molecular machinery to organise actin filaments. F‐actin provides tracks for myosin molecular motors to transport organelles at high velocities, and actin is required for specific stages of vesicle trafficking that underpin cell growth and development. The means by which plant cells control the nucleation of new actin filaments from G‐actin have diverged considerably from yeast and metazoans. The unique aspects of the plant actin cytoskeleton are likely to have arisen from a combination of the environmental challenges to a sessile multicellular existence and an ancient diversification from the ancestors of the Opisthokonta and Amoebozoa model organisms from which the majority of eukaryote cytoskeletal paradigms have been established.

Key Concepts

  • The basic principles of actin biochemistry applicable to animals, fungi and protists are conserved in plants but there are a number of specific modifications as plants do not possess the full complement of animal actin‐binding proteins.
  • Actin filaments in plants have to fulfil unique functions. Actin focuses on the expansion of tip growing cells, maintains cytoarchitecture and responds to the environment (e.g. polarising in response to pathogen stimulation). During cell division actin filaments participate in all major plant‐specific arrays.
  • A stationary cell is NOT a physically inactive cell. Actin cables are exploited for organelle transport. Actin‐based transport tends to dominate over microtubule‐based movement. Plants utilise the fastest known type V myosin (known in plants as type XI) within the eukaryote kingdom. Polymerisation dynamics are thought to add to trafficking capabilities as low levels of antiactin drugs disrupt vesicle delivery and fusion during cell growth yet preserve myosin‐mediated transport.
  • Plant‐specific proteins and novel domain combinations have become established in plants to regulate the actin cytoskeleton in accordance with the demands of sessile multicellular photosynthetic autotrophy. These cytoskeletal adaptations to sedentary life within a cell wall are distinct from fungi, possibly reflecting the ancient diversification between the opisthokonts and plants.

Keywords: actin; myosin; plant; microtubules; trafficking

Figure 1. The current molecular model for the dynamic instability of plant actin. The majority of monomeric globular actin (G‐actin; grey rectangles) in the plant cytoplasm is complexed with profilin. In pollen, profilin concentration is equimolar to actin. When ATP‐actin is bound to profilin the spontaneous nucleation of new filaments is prohibited, but sequestered actin can be added to uncapped barbed ends and nucleation factors such as formins can access the profilin–actin complexes to initiate new filaments. Actin filaments (F‐actin; in grey) are then organised into higher‐order structures by a variety of bundling, cross linking and severing proteins. After ATP hydrolysis and phosphate release actin depolymerising factor (ADF; coloured red) binds to F‐actin and accelerates subunit release from the pointed end. Actin monomers exchange ADP for ATP; actin purified from pollen has 20 times the nucleotide exchange activity of skeletal muscle actin. This process is augmented by the action of cyclase‐associated protein (CAP). Barbed ends are marked ‘+’ and pointed ends are marked ‘−’.
Figure 2. Filamentous actin in a plant cell. (a) Full projection of an image stack captured using a confocal laser‐scanning microscope. A Nicotiana tabacum BY2 tissue culture cell is shown expressing GFP fused to the second actin‐binding domain of fimbrin. The fimbrin domain associates with F‐actin, localising GFP fluorescence to the actin filaments within the cytoplasm. (b) Partial projection of the same image stack showing the volume occupied by the central vacuole. A cytoplasmic strand supported by a thick actin cable is visible (marked by asterisk). (c) Blue/red stereo image and full projection of the same cell. Scale bar is 20 µm.
Figure 3. Simple schematic of F‐actin distribution within typical plant cells. Concentrations of actin filaments are represented by blue lines. At interphase actin filaments can be observed throughout the cytoplasm. Prominent actin cables support cytoplasmic strands and encapsulate the nucleus (labelled ‘N’). Chloroplasts (labelled ‘C’) are anchored by the actin–myosin system and may have the capability to remodel the local network (see main text). The round inset illustrates the association of small organelles such as mitochondria, peroxisomes and Golgi stacks (labelled ‘G’) with actin via active myosin motors. In lower plants the cytoplasmic stream can reach speeds of 100 µm s−1. The endoplasmic reticulum (labelled ‘ER’) is also associated with the actin cytoskeleton. The rectangular insert illustrates the requirement for actin for some routes of post‐Golgi transport to the plasma membrane. The recycling of proteins from the plasma membrane through early endosomes (labelled ‘E’) also requires an intact actin cytoskeleton (see main text for details). During pre‐prophase the actin cytoskeleton coaligns with microtubules (represented by red lines) in a circular cortical array known as the preprophase band (PPB). The PPB is disassembled immediately prior to the formation of the spindle, and an actin depleted zone (ADZ) appears in the same region at the cell cortex. Subpopulations of F‐actin have been observed associated with the microtubule spindle (Traas et al., ; Yasuda et al., ) and are represented by dashed blue lines. At telophase the growing cell plate is sandwiched between an array of actin filaments and microtubules called the phragmoplast. This array can form in the absence of F‐actin but the rate of cell plate growth and the final disassembly of the microtubule component of the phragmoplast are enhanced by the actin cytoskeleton. The new cell plate finally fuses with the ADZ.
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Deeks, Michael J, and Hussey, Patrick J(Jul 2016) Plant Actin Biology. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0021255.pub2]