Regulation of Growth Anisotropy in Well-Watered and Water-Stressed Maize Roots. II. Role of Cortical Microtubules and Cellulose Microfibrils1

Abstract

We tested the hypothesis that the degree of anisotropic expansion of plant tissues is controlled by the degree of alignment of cortical microtubules or cellulose microfibrils. Previously, for the primary root of maize (Zea mays L.), we quantified spatial profiles of expansion rate in length, radius, and circumference and the degree of growth anisotropy separately for the stele and cortex, as roots became thinner with time from germination or in response to low water potential (B.M. Liang, A.M. Dennings, R.E. Sharp, T.I. Baskin [1997] Plant Physiol 115:101-111). Here, for the same material, we quantified microtubule alignment with indirect immunofluorescence microscopy and microfibril alignment throughout the cell wall with polarized-light microscopy and from the innermost cell wall layer with electron microscopy. Throughout much of the growth zone, mean orientations of microtubules and microfibrils were transverse, consistent with their parallel alignment specifying the direction of maximal expansion rate (i.e. elongation). However, where microtubule alignment became helical, microfibrils often made helices of opposite handedness, showing that parallelism between these elements was not required for helical orientations. Finally, contrary to the hypothesis, the degree of growth anisotropy was not correlated with the degree of alignment of either microtubules or microfibrils. The mechanisms plants use to specify radial and tangential expansion rates remain uncharacterized.

Axis elongation can occur with net longitudinal orientation of wall microfibrils

“…A similar emphasis on the matrix was observed in coenocytic algae where cell expansion was not regulated by wall microfibril orientation (Kimura & Mizuta, 1995). Also, although in the cells of higher plants the direction of maximum cell expansion may be specified by the orientation of wall microfibrils, the degree of growth anisotrophy at the cellular level is not (Baskin et al, 1999). The authors further suggest that there may be an independent yield point for walls in the longitudinal versus transverse direction, and that in higher plant cells all layers of the wall, and not just the inner 25 % as in giant algal cells, may participate in the load-bearing capabilities of the wall.…”

Disorganization of Cortical Microtubules Stimulates Tangential Expansion and Reduces the Uniformity of Cellulose Microfibril Alignment among Cells in the Root of Arabidopsis

“…The degree of anisotropy was hypothesized by Green (1964) to be proportional to the degree of alignment among microfibrils; that is, the more parallel cellulose microfibrils are laid down, the greater the difference between maximal and minimal expansion rates. This hypothesis was tested for the maize root, which grows more anisotropically under water deficit (Liang et al, 1997) and falsified; despite there being a more than 10-fold difference in the degree of anisotropy, there was no difference in microfibril alignment (Baskin et al, 1999). Likewise, decreased anisotropy occurs in several Arabidopsis mutants without detectable disorganization among microfibrils (Wiedemeier et al, 2002;Sugimoto et al, 2003).…”

“…Furthermore, microfibril alignment by microtubules is at odds with some recent results. For example, most cells in the maturation zone of the water-stressed maize (Zea mays) root have microtubule arrays in right-handed helices but microfibrils in left-handed helices (Baskin et al, 1999). Similarly, the Arabidopsis (Arabidopsis thaliana) mutant, microtubule organization 1 (mor1), has aberrant microtubule arrays but apparently unaltered microfibril alignment Sugimoto et al, 2003).…”

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

“…Developmental changes of cMT orientations from transverse to oblique and longitudinal have been observed in many cell types and organs like primary root, stems, or cotton fibers (Seagull 1985;Laskowski 1990;Liang et al 1996;Baskin et al 1999). Furthermore, it has been shown that in primary roots of maize and Arabidopsis cMT orientations have the same handedness (chirality) at a given position, and the form of cMT chirality changes along the organ (Liang et al 1996;Baskin et al 1999).…”

“…The cMT bundles are more or less parallel to one another, and are aligned at a particular angle with respect to cell axis. In rapidly elongating cells cMTs are transverse but they shift to oblique and then longitudinal orientation as elongation rate declines (Baskin et al 1999;Granger and Cyr 2001).…”