Plant ‘muscles’: fibers with a tertiary cell wall

Abstract

Plants, although sessile organisms, are nonetheless able to move their body parts; for example, during root contraction of geophytes or in the gravitropic reaction by woody stems. One of the major mechanisms enabling these movements is the development of specialized structures that possess contractile properties. Quite unlike animal muscles, for which the action is driven by protein-protein interactions in the protoplasma, the action of plant 'muscles' is polysaccharide-based and located in the uniquely designed, highly cellulosic cell wall that is deposited specifically in fibers. This review describes the development of such cell walls as a widespread phenomenon in the plant kingdom, gives reasons why it should be considered as a tertiary cell wall, and discusses the mechanism of action of the 'muscles'. The origin of the contractile properties lies in the tension of the axially oriented cellulose microfibrils due to entrapment of rhamnogalacturonan-I aggregates that limits the lateral interaction of microfibrils. Long side chains of the nascent rhamnogalacturonan-I are trimmed off during cell wall maturation leading to tension development. Similarities in the tertiary cell wall design in fibers of different plant origin indicate that the basic principles of tension creation may be universal in various ecophysiological situations.

Evidence and quantitative evaluation of tensile maturation strain in flax phloem through longitudinal splitting

“…5B; Table 2), meaning another parameter (or parameters) determine the magnitude of maturation strain. One of these parameters may be the surface area of the G-layers, which are considered as the primary source of maturation strain (Gorshkova et al 2018). Their surface area is not the same as that of phloem and may not even be proportional to it in different plants.…”

“…Flax fibers belong to the so-called "gelatinous fibers" that are widespread in plants of many taxa, can be present in various plant parts, and are described as "plant muscles" (Gorshkova et al 2018). They have special composition and architecture of the cell wall, which is named either the G-layer of secondary cell wall (Clair et al 2019), or tertiary cell wall (Gorshkova et al 2018).…”

“…Flax fibers belong to the so-called "gelatinous fibers" that are widespread in plants of many taxa, can be present in various plant parts, and are described as "plant muscles" (Gorshkova et al 2018). They have special composition and architecture of the cell wall, which is named either the G-layer of secondary cell wall (Clair et al 2019), or tertiary cell wall (Gorshkova et al 2018). The effects provided by such fibers include visible organ contraction, as observed in roots and hypocotyls of geophytes (Fisher 2008;Schreiber et al 2010), or in aerial roots (Fisher 1982;Abasolo et al 2009), as well as the formation of stem curvature in the course of negative gravitropic reaction, like in tension wood of most angiosperm tree species (Dadswell and Wardrop 1955;.…”

Three-dimensional printing, muscles, and skeleton: mechanical functions of living wood

“…fibres, performs very similar functions to those of xylem. The muscle function of phloem seems to be of utmost importance for stems with very small diameters (Gorshkova et al, 2018).…”

Flax rhamnogalacturonan lyases: phylogeny, differential expression and modeling of protein structure

“…RG-I is a crucial component of the primary (Carpita Abbreviations -CAZy, database of carbohydrate-active enzymes; FIB, isolated fibers with tertiary cell wall; GDP, guanosine diphosphate; iFIB, intrusively elongating fibers with primary cell wall; MID, segment of the whole flax stem taken below snap point; NADP(H), nicotinamide adenine dinucleotide phosphate (reduced); PL, polysaccharide lyase; PL4, pectin lyase family 4; qRT-PCR, quantitative real-time polymerase chain reaction; RG-I, rhamnogalacturonan I; RGL, rhamnogalacturonan lyase; SYBR Green, N',N'-dimethyl-N-[4-[(E)-(3-methyl-1,3-benzothiazol-2-ylidene)methyl]-1-phenylquinolin-1-ium-2-yl]-N-propylpropane-1,3-diamine; TCW, tertiary cell wall; TOP, segment of the whole flax stem taken above snap point. and Gibeaut 1993, Ridley et al 2001) and tertiary cell walls (TCWs; Gorshkova et al 2018a). The side chains of such polysaccharides, after their incorporation into the cell walls, may be subjected to postsynthetic modifications, including degradation; for example, expression of -galactosidases and -arabinofuranosidases that trim off RG-I side chains is reported (Arsovski et al 2009, Roach et al 2011.…”