Mechanistic Insights into Plant Chiral Growth

Abstract

The latent left–right asymmetry (chirality) of vascular plants is best witnessed as a helical elongation of cylindrical organs in climbing plants. Interestingly, helical handedness is usually fixed in given species, suggesting genetic control of chirality. Arabidopsis thaliana, a small mustard plant, normally does not twist but can be mutated to exhibit helical growth in elongating organs. Genetic, molecular and cell biological analyses of these twisting mutants are providing mechanistic insights into the left–right handedness as well as how potential organ skewing is suppressed in most plants. Growth direction of elongating plant cells is determined by alignment of cellulose microfibrils in cell walls, which is guided by cortical microtubules localized just beneath the plasma membrane. Mutations in tubulins and regulators of microtubule assembly or organization give rise to helical arrangements of cortical microtubule arrays in Arabidopsis cells and cause helical growth of fixed handedness in axial organs such as roots and stems. Whether tubulins are assembled into a microtubule composed of straight or tilted protofilaments might determine straight or twisting growth. Mechanistic understanding of helical plant growth will provide a paradigm for connecting protein filament structure to cellular organization.

Three-dimensional quantification of twisting in the Arabidopsis petiole

“…What is the difference between the basal region and non-basal regions that contributed to the observed differences in distribution of bending and twisting? Molecular factors such as auxin distribution and cortical microtubule arrangement, which are suggested to be involved in bending and twisting (Buschmann and Borchers, 2020 ; Ishida et al 2007 ; Nakamura and Hashimoto 2020 ; Smyth 2016 ; Snow 1962 ) might be different between the basal region and other parts of the petiole. To check this hypothesis, our method based on data from laser microscopy will enable the monitoring of the distribution of molecules with florescent reporters for comparison with the degrees of deformation, providing insight into the mechanisms underlying petiole movement.…”

“…Thus, our method is not limited to petioles but instead, is applicable to other rod-shaped plant organs that exhibit twisting in various species (e.g. leaf petiole, pulvinus, flower stalk, pedicel, stem, and root) (Buschmann and Borchers 2020 ; Nakamura and Hashimoto 2020 ; Smyth 2016 ). The underlying molecular mechanism might be different as suggested by different trend in chirality (Buschmann and Borchers 2020 ; Nakamura and Hashimoto 2020 ; Smyth 2016 ) and by difference in cell deformation mechanisms (Abraham and Elbaum 2013 ; Borchers et al 2018 ).…”

“…leaf petiole, pulvinus, flower stalk, pedicel, stem, and root) (Buschmann and Borchers 2020 ; Nakamura and Hashimoto 2020 ; Smyth 2016 ). The underlying molecular mechanism might be different as suggested by different trend in chirality (Buschmann and Borchers 2020 ; Nakamura and Hashimoto 2020 ; Smyth 2016 ) and by difference in cell deformation mechanisms (Abraham and Elbaum 2013 ; Borchers et al 2018 ). Applying our method to them, the diversity of flexible plant organ movements will be elucidated.…”

“…In addition to the twisting in photoresponse, there are variety of twisting in plants also in radially symmetric organs (Fig. 1 d, f) (reviewed in Buschmann and Borchers 2020 ; Nakamura and Hashimoto 2020 ; Smyth 2016 ). Those twisted growths sometimes are associated with the spiral growth of organ (e.g.…”

“…In the case of twisting of microtubule-related mutants, cellular and molecular basis is progressively being revealed (Buschmann et al 2009 ; Nakamura and Hashimoto 2020 ; Thitamadee et al 2002 ), but detailed analysis on spatial distribution of the twisting is lacking. Similarly, also in other mutants (Geisler et al 2003 ; Saffer et al 2017 ) and other naturally occurring twisting (Abraham and Elbaum 2013 ; Darwin and Darwin 1880 ; Smyth 2016 ), quantification of twisting distribution would help further understanding of varieties of underlying mechanisms.…”