Regulation of organ straightening and plant posture by an actin–myosin XI cytoskeleton

Abstract

Plants are able to bend nearly every organ in response to environmental stimuli such as gravity and light(1,2). After this first phase, the responses to stimuli are restrained by an independent mechanism, or even reversed, so that the organ will stop bending and attain its desired posture. This phenomenon of organ straightening has been called autotropism(3) and autostraightening(4) and modelled as proprioception(5). However, the machinery that drives organ straightening and where it occurs are mostly unknown. Here, we show that the straightening of inflorescence stems is regulated by an actin-myosin XI cytoskeleton in specialized immature fibre cells that are parallel to the stem and encircle it in a thin band. Arabidopsis mutants defective in myosin XI (specifically XIf and XIk) or ACTIN8 exhibit hyperbending of stems in response to gravity, an effect independent of the physical properties of the shoots. The actin-myosin XI cytoskeleton enables organs to attain their new position more rapidly than would an oscillating series of diminishing overshoots in environmental stimuli. We propose that the long actin filaments in elongating fibre cells act as a bending tensile sensor to perceive the organ's posture and trigger the straightening system.

Update on Myosin Motors: Molecular Mechanisms and Physiological Functions

“…These fiber cells contain long actin filament bundles and also show rapid movement of plastids. While the plastid movements are much slower in the myosin mutant (Okamoto et al, 2015), we do not know whether the organization of actin filaments also is affected. This latter point is of particular importance, since we know that myosins can affect actin organization (Peremyslov et al, 2010;Ueda et al, 2010;Madison et al, 2015) and since fiz1 mutants that are defective in ACTIN8 also show similar defects in straightening behavior (Okamoto et al, 2015).…”

“…While the plastid movements are much slower in the myosin mutant (Okamoto et al, 2015), we do not know whether the organization of actin filaments also is affected. This latter point is of particular importance, since we know that myosins can affect actin organization (Peremyslov et al, 2010;Ueda et al, 2010;Madison et al, 2015) and since fiz1 mutants that are defective in ACTIN8 also show similar defects in straightening behavior (Okamoto et al, 2015). More fundamentally, it is not clear at this time whether these two myosins function in sensing the growth curvature, possibly via the actin cytoskeleton, or whether the mutant phenotype results from a defect in the response pathway after detection of the growth curvature.…”

“…In this case, a myo11e myo11h (xik xif) mutant of Arabidopsis was found to show initially normal gravitropic bending but then overshot beyond a vertical orientation (Okamoto et al, 2015). Experiments with plants on klinostats demonstrated that the mutant defect only concerns the straightening reaction, suggesting that these two myosins are crucial in reestablishing symmetrical growth once the stem reaches an orientation close to vertical.…”

“…Experiments with plants on klinostats demonstrated that the mutant defect only concerns the straightening reaction, suggesting that these two myosins are crucial in reestablishing symmetrical growth once the stem reaches an orientation close to vertical. Interestingly, Myo11H is expressed almost exclusively in a thin layer of fiber cell surrounding the xylem cells (Okamoto et al, 2015), indicating that this cell layer is particularly important in establishing straight growth. These fiber cells contain long actin filament bundles and also show rapid movement of plastids.…”

Myosin-driven transport network in plants is functionally robust and distinctive

“…In this model, the myosin XI-MyoB compartments represent a specialized transport system that drives streaming, rather than directly engaging individual organelles and secretory vesicles, which in turn delivers organelles and other types of vesicles to their destinations throughout the cell (14). Furthermore, existing genetic evidence indicates that cytoplasmic streaming is required for both polarized and diffuse cell growth because: (i) inactivation of myosins alone results in reduced cell elongation and expansion and affects plant growth and morphogenesis (15)(16)(17)(18)(19)(20); (ii) simultaneous inactivation of myosins and MyoBs results in synergistic phenotypes (13,14); and (iii) reduction in streaming velocity reduces plant growth, whereas increased velocity boosts that growth (21).…”