Tensile Tissue Stress Affects the Orientation of Cortical Microtubules in the Epidermis of Sunflower Hypocotyl

Abstract

In turgid multicellular organs, it is convenient to differentiate between the two kinds of tensile forces acting in cell walls as a result of turgor pressure. The primary forces occur both in situ and in cells isolated from the organ, whereas the secondary forces occur only in situ. The latter are an unavoidable physical consequence of the variation in mechanical parameters of tissues forming layers or strands. The most rigid tissue is under maximal tensile force, whereas the least rigid is under maximal compressive force. These forces cause tissue stresses (that is, certain tissues are under tensile stress, whereas others are under compressive stress in the organ). The primary and secondary forces result in primary and secondary stress in cell walls, respectively. The anisotropy of the primary stress is a function of cell shape. For instance, in cylindric cells the anisotropy expressed as the ratio of longitudinal to transverse stresses is 0.5. The anisotropy of the secondary stress is a function of the compound structure of the organ. For example, in the epidermis of sunflower hypocotyl, the longitudinal secondary stress is much higher than the transverse stress. The primary and secondary stresses are superimposed, and, as a consequence, the stress anisotropy in the outer thick walls of epidermal cells is greater than 1. These outer epidermal walls transmit most of the tissue stress. When the epidermis is peeled but remains turgid, only primary stress remains, but loading of the peel can reestablish the original stress anisotropy. We studied the effect of stress anisotropy changes on the orientation of cortical microtubules (CMTs) in the sunflower hypocotyl epidermis. We showed that changes in stress anisotropy cause the CMT orientation to change in the direction of maximal wall stress. In situ, the relatively high tensile tissue stress in the epidermis causes maximal stress in the longitudinal direction and relatively steep CMT orientation. When the tissue stress is removed from the epidermis by peeling, the CMTs tend to reorient toward the transverse direction, which is the direction of maximal stress in the primary component. On application of external longitudinal stress, to substitute for tissue stress, CMTs tend to reorient in the longitudinal direction. However, a relatively high rate of plastic strain is caused by the stress applied to the peel in an acid medium. This produces a less steep orientation of CMTs. It appears that the change in stress anisotropy orients the CMT in the direction in which the stress is maximal after the change, but there is also some effect of the growth rate on the orientation.

Circumnutation as a visible plant action and reaction

“…Moreover, in sunflower, the epidermis is vital in the hypocotyl growth control. 46 In Phaseolus vulgaris, it is epidermal cells that display partially reversible changes in the length of the bending, mobile part of the shoot. 44 The endodermal cells (statocytes with amyloplasts functioning as statoliths) also play an important role in circumnutations, as revealed by scr mutants of Arabidopsis and Pharbitis nil.…”

“…53,54 Epidermal cells as well as parenchymal-subepidermal cells are involved in generation of circumnutations. 22,46 Therefore, epidermal and parenchymal cells might function as motor cells. Figure 5 presents a scheme of a hypothetical cell, i.e., a part of the stem motor tissue, with marked elements constituting the oscillator and elements involved in circumnutations.…”

Chiral changes of cortical microtubule orientations in epidermls of sunflower hypocotyls. The effect of blue and red light

“…Many external factors, like plant growth regulators (see review by Shibaoka, 1994), electric field (Hush and Overall 1991;Blackman and Overall 1995), mechanical stresses Schopfer 1997, 1998;Hejnowicz et al 2000), and developmental factors (Liang et al 1996;Granger and Cyr 2001) affect the cMT orientation with respect to cell axis. The same is true also for light (Laskowski 1990;Nick et al 1990;Zandomeni and Schopfer 1993;Ueda and Matsuyama 2000).…”

In Memoriam: Zygmunt Hejnowicz (1929–2016)

“…The last significant scientific contribution pointed out by Zygmunt himself were his works with the late Andreas Sievers, devoted to tissue stresses. [16][17][18] They explained the existence of structural tissue stresses that are the indirect result of the turgor pressure. These stresses exist in "green" plant organs composed of turgid tissues that differ in cell size and thickness, and mechanical properties of the cell walls.…”

“…Together with Lewis J. Feldman, Zygmunt showed the role that mechanical forces generated by microtubules at kinetochores play in chromosome segregation during Oenothera meiosis. 33 In other papers, Zygmunt with colleagues from his Department at the University of Silesia, showed that, in sunflower hypocotyl epidermis, cortical microtubules orientation is related to mechanical stress (it is noteworthy that one of these papers 18 appeared in the volume of Journal of Plant Growth Regulation devoted to memory of Zygmunt's friend -Paul B. Green).…”