Yin Chang, Rox Middleton, Yu Ogawa, Tom Gregory, Lisa M. Steiner, Alexander Kovalev, Rebecca H. N. Karanja, Paula J. Rudall, Beverley J. Glover, Stanislav N. Gorb, and Silvia Vignolini

PNAS December 21, 2021 118 (51) e2111723118

Significance

Helicoidal architectures are widespread in nature; several species adopt this structure to produce brilliant colorations. Such chiral architectures are usually left-handed in plants, with the only exception found in the cell walls of epicarp cells of Pollia condensata, where both handednesses are observed. Here, we aim to understand the origin of handednesses by analyzing optical and mechanical responses of single cells. Surprisingly, we discover that left-handed and right-handed cells show different distributions of spectra and elasticity. We verified by using finite element analysis simulation that the elasticity of helicoids is sensitive to the ratio of cellulose/cell wall matrix. Our findings reveal that cell wall composition affects the helicoidal architectures, suggesting that chemical composition plays a role in morphogenesis of the chirality reversal.

Abstract

Chiral asymmetry is important in a wide variety of disciplines and occurs across length scales. While several natural chiral biomolecules exist only with single handedness, they can produce complex hierarchical structures with opposite chiralities. Understanding how the handedness is transferred from molecular to the macroscopic scales is far from trivial. An intriguing example is the transfer of the handedness of helicoidal organizations of cellulose microfibrils in plant cell walls. These cellulose helicoids produce structural colors if their dimension is comparable to the wavelength of visible light. All previously reported examples of a helicoidal structure in plants are left-handed except, remarkably, in the Pollia condensata fruit; both left- and right-handed helicoidal cell walls are found in neighboring cells of the same tissue. By simultaneously studying optical and mechanical responses of cells with different handednesses, we propose that the chirality of helicoids results from differences in cell wall composition. In detail, here we showed statistical substantiation of three different observations: 1) light reflected from right-handed cells is red shifted compared to light reflected from left-handed cells, 2) right-handed cells occur more rarely than left-handed ones, and 3) right-handed cells are located mainly in regions corresponding to interlocular divisions. Finally, 4) right-handed cells have an average lower elastic modulus compared to left-handed cells of the same color. Our findings, combined with mechanical simulation, suggest that the different chiralities of helicoids in the cell wall may result from different chemical composition, which strengthens previous hypotheses that hemicellulose might mediate the rotations of cellulose microfibrils.

See https://www.pnas.org/content/118/51/e2111723118

Fig. 1.

Polarized coloration and distribution of differently colored left- and right-handed cells on the epicarp of P. condensata fruits. (A) P. condensata: slightly ovoid shaped fruit of about 4 to 5 mm in diameter exhibiting striped coloration including the following: a white interseptum stripe (1), the blue nonstripe regions (2), and a red septum stripe (3). (B) Polarization-resolved optical micrograph of epicarp measured using left- (black arrow) and right-handed (white arrow) polarized light, respectively. In the images, structurally colored cells are recognizable (cell contour outlined with white dashed lines). The color of the cell is seen as a line along the Top Center due to the curvature of the cell and the numerical aperture of the objective. (C) Statistical analysis of colors and chirality of cells across four fruits revealing that right-handed cells (green plot) generate more red-shifted colors than left-handed cells (blue plot). (D) The cell ratio of left-handed and right-handed cells with specific reflected wavelength at the three differently colored regions marked in (A) are calculated and normalized to the total numbers of cells. A higher proportion of right-handed cells with longer reflected wavelengths in the stripe regions (1) and (3) contribute to the white or red macroscopic coloration.