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Cell wall composition determines handedness reversal in helicoidal cellulose architectures of Pollia condensata fruits

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 fro...

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Autores principales: Chang, Yin, Middleton, Rox, Ogawa, Yu, Gregory, Tom, Steiner, Lisa M., Kovalev, Alexander, Karanja, Rebecca H. N., Rudall, Paula J., Glover, Beverley J., Gorb, Stanislav N., Vignolini, Silvia
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8713805/
https://www.ncbi.nlm.nih.gov/pubmed/34911759
http://dx.doi.org/10.1073/pnas.2111723118
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author Chang, Yin
Middleton, Rox
Ogawa, Yu
Gregory, Tom
Steiner, Lisa M.
Kovalev, Alexander
Karanja, Rebecca H. N.
Rudall, Paula J.
Glover, Beverley J.
Gorb, Stanislav N.
Vignolini, Silvia
author_facet Chang, Yin
Middleton, Rox
Ogawa, Yu
Gregory, Tom
Steiner, Lisa M.
Kovalev, Alexander
Karanja, Rebecca H. N.
Rudall, Paula J.
Glover, Beverley J.
Gorb, Stanislav N.
Vignolini, Silvia
author_sort Chang, Yin
collection PubMed
description 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.
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spelling pubmed-87138052022-01-21 Cell wall composition determines handedness reversal in helicoidal cellulose architectures of Pollia condensata fruits Chang, Yin Middleton, Rox Ogawa, Yu Gregory, Tom Steiner, Lisa M. Kovalev, Alexander Karanja, Rebecca H. N. Rudall, Paula J. Glover, Beverley J. Gorb, Stanislav N. Vignolini, Silvia Proc Natl Acad Sci U S A Biological Sciences 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. National Academy of Sciences 2021-12-15 2021-12-21 /pmc/articles/PMC8713805/ /pubmed/34911759 http://dx.doi.org/10.1073/pnas.2111723118 Text en Copyright © 2021 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Chang, Yin
Middleton, Rox
Ogawa, Yu
Gregory, Tom
Steiner, Lisa M.
Kovalev, Alexander
Karanja, Rebecca H. N.
Rudall, Paula J.
Glover, Beverley J.
Gorb, Stanislav N.
Vignolini, Silvia
Cell wall composition determines handedness reversal in helicoidal cellulose architectures of Pollia condensata fruits
title Cell wall composition determines handedness reversal in helicoidal cellulose architectures of Pollia condensata fruits
title_full Cell wall composition determines handedness reversal in helicoidal cellulose architectures of Pollia condensata fruits
title_fullStr Cell wall composition determines handedness reversal in helicoidal cellulose architectures of Pollia condensata fruits
title_full_unstemmed Cell wall composition determines handedness reversal in helicoidal cellulose architectures of Pollia condensata fruits
title_short Cell wall composition determines handedness reversal in helicoidal cellulose architectures of Pollia condensata fruits
title_sort cell wall composition determines handedness reversal in helicoidal cellulose architectures of pollia condensata fruits
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8713805/
https://www.ncbi.nlm.nih.gov/pubmed/34911759
http://dx.doi.org/10.1073/pnas.2111723118
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