Cellulose-rich secondary walls in wave-swept red macroalgae fortify flexible tissues

Kyra Janot, Patrick T. Martone, Miki Fujita, Geoffrey Wasteneys, Katia Ruel, Jean Paul Joseleau, José M. Estevez

Resultado de la investigación: Article

Resumen

Main conclusion: Cellulosic secondary walls evolved convergently in coralline red macroalgae, reinforcing tissues against wave-induced breakage, despite differences in cellulose abundance, microfibril orientation, and wall structure. Abstract: Cellulose-enriched secondary cell walls are the hallmark of woody vascular plants, which develop thickened walls to support upright growth and resist toppling in terrestrial environments. Here we investigate the striking presence and convergent evolution of cellulosic secondary walls in coralline red algae, which reinforce thalli against forces applied by crashing waves. Despite ostensible similarities to secondary wall synthesis in land plants, we note several structural and mechanical differences. In coralline red algae, secondary walls contain three-times more cellulose (~ 22% w/w) than primary walls (~ 8% w/w), and their presence nearly doubles the total thickness of cell walls (~ 1.2 µm thick). Field emission scanning electron microscopy revealed that cellulose bundles are cylindrical and lack any predominant orientation in both primary and secondary walls. His-tagged recombinant carbohydrate-binding module differentiated crystalline and amorphous cellulose in planta, noting elevated levels of crystalline cellulose in secondary walls. With the addition of secondary cell walls, Calliarthron genicular tissues become significantly stronger and tougher, yet remain remarkably extensible, more than doubling in length before breaking under tension. Thus, the development of secondary walls contributes to the strong-yet-flexible genicular tissues that enable coralline red algae to survive along wave-battered coastlines throughout the NE Pacific. This study provides an important evolutionary perspective on the development and biomechanical significance of secondary cell walls in a non-model, non-vascular plant.

Idioma originalEnglish
Páginas (desde-hasta)1867-1879
Número de páginas13
PublicaciónPlanta
Volumen250
N.º6
DOI
EstadoPublished - 1 dic 2019

Huella dactilar

Seaweed
Cellulose
macroalgae
cellulose
Rhodophyta
Cell Wall
cell walls
knees
Calliarthron
Knee
non-vascular plants
Embryophyta
Microfibrils
carbohydrate binding
convergent evolution
embryophytes
Plantae
thallus
woody plants
vascular plants

ASJC Scopus subject areas

  • Genetics
  • Plant Science

Citar esto

Janot, K., Martone, P. T., Fujita, M., Wasteneys, G., Ruel, K., Joseleau, J. P., & Estevez, J. M. (2019). Cellulose-rich secondary walls in wave-swept red macroalgae fortify flexible tissues. Planta, 250(6), 1867-1879. https://doi.org/10.1007/s00425-019-03269-1
Janot, Kyra ; Martone, Patrick T. ; Fujita, Miki ; Wasteneys, Geoffrey ; Ruel, Katia ; Joseleau, Jean Paul ; Estevez, José M. / Cellulose-rich secondary walls in wave-swept red macroalgae fortify flexible tissues. En: Planta. 2019 ; Vol. 250, N.º 6. pp. 1867-1879.
@article{fa35aeeba69e44819242fd5505c0ed7c,
title = "Cellulose-rich secondary walls in wave-swept red macroalgae fortify flexible tissues",
abstract = "Main conclusion: Cellulosic secondary walls evolved convergently in coralline red macroalgae, reinforcing tissues against wave-induced breakage, despite differences in cellulose abundance, microfibril orientation, and wall structure. Abstract: Cellulose-enriched secondary cell walls are the hallmark of woody vascular plants, which develop thickened walls to support upright growth and resist toppling in terrestrial environments. Here we investigate the striking presence and convergent evolution of cellulosic secondary walls in coralline red algae, which reinforce thalli against forces applied by crashing waves. Despite ostensible similarities to secondary wall synthesis in land plants, we note several structural and mechanical differences. In coralline red algae, secondary walls contain three-times more cellulose (~ 22{\%} w/w) than primary walls (~ 8{\%} w/w), and their presence nearly doubles the total thickness of cell walls (~ 1.2 µm thick). Field emission scanning electron microscopy revealed that cellulose bundles are cylindrical and lack any predominant orientation in both primary and secondary walls. His-tagged recombinant carbohydrate-binding module differentiated crystalline and amorphous cellulose in planta, noting elevated levels of crystalline cellulose in secondary walls. With the addition of secondary cell walls, Calliarthron genicular tissues become significantly stronger and tougher, yet remain remarkably extensible, more than doubling in length before breaking under tension. Thus, the development of secondary walls contributes to the strong-yet-flexible genicular tissues that enable coralline red algae to survive along wave-battered coastlines throughout the NE Pacific. This study provides an important evolutionary perspective on the development and biomechanical significance of secondary cell walls in a non-model, non-vascular plant.",
keywords = "Biomechanics, Calliarthron, Carbohydrate-binding module, Convergent evolution, Coralline, Genicula, Intertidal, Macroalgae, Rhodophyta, Seaweed",
author = "Kyra Janot and Martone, {Patrick T.} and Miki Fujita and Geoffrey Wasteneys and Katia Ruel and Joseleau, {Jean Paul} and Estevez, {Jos{\'e} M.}",
year = "2019",
month = "12",
day = "1",
doi = "10.1007/s00425-019-03269-1",
language = "English",
volume = "250",
pages = "1867--1879",
journal = "Planta",
issn = "0032-0935",
publisher = "Springer Verlag",
number = "6",

}

Janot, K, Martone, PT, Fujita, M, Wasteneys, G, Ruel, K, Joseleau, JP & Estevez, JM 2019, 'Cellulose-rich secondary walls in wave-swept red macroalgae fortify flexible tissues', Planta, vol. 250, n.º 6, pp. 1867-1879. https://doi.org/10.1007/s00425-019-03269-1

Cellulose-rich secondary walls in wave-swept red macroalgae fortify flexible tissues. / Janot, Kyra; Martone, Patrick T.; Fujita, Miki; Wasteneys, Geoffrey; Ruel, Katia; Joseleau, Jean Paul; Estevez, José M.

En: Planta, Vol. 250, N.º 6, 01.12.2019, p. 1867-1879.

Resultado de la investigación: Article

TY - JOUR

T1 - Cellulose-rich secondary walls in wave-swept red macroalgae fortify flexible tissues

AU - Janot, Kyra

AU - Martone, Patrick T.

AU - Fujita, Miki

AU - Wasteneys, Geoffrey

AU - Ruel, Katia

AU - Joseleau, Jean Paul

AU - Estevez, José M.

PY - 2019/12/1

Y1 - 2019/12/1

N2 - Main conclusion: Cellulosic secondary walls evolved convergently in coralline red macroalgae, reinforcing tissues against wave-induced breakage, despite differences in cellulose abundance, microfibril orientation, and wall structure. Abstract: Cellulose-enriched secondary cell walls are the hallmark of woody vascular plants, which develop thickened walls to support upright growth and resist toppling in terrestrial environments. Here we investigate the striking presence and convergent evolution of cellulosic secondary walls in coralline red algae, which reinforce thalli against forces applied by crashing waves. Despite ostensible similarities to secondary wall synthesis in land plants, we note several structural and mechanical differences. In coralline red algae, secondary walls contain three-times more cellulose (~ 22% w/w) than primary walls (~ 8% w/w), and their presence nearly doubles the total thickness of cell walls (~ 1.2 µm thick). Field emission scanning electron microscopy revealed that cellulose bundles are cylindrical and lack any predominant orientation in both primary and secondary walls. His-tagged recombinant carbohydrate-binding module differentiated crystalline and amorphous cellulose in planta, noting elevated levels of crystalline cellulose in secondary walls. With the addition of secondary cell walls, Calliarthron genicular tissues become significantly stronger and tougher, yet remain remarkably extensible, more than doubling in length before breaking under tension. Thus, the development of secondary walls contributes to the strong-yet-flexible genicular tissues that enable coralline red algae to survive along wave-battered coastlines throughout the NE Pacific. This study provides an important evolutionary perspective on the development and biomechanical significance of secondary cell walls in a non-model, non-vascular plant.

AB - Main conclusion: Cellulosic secondary walls evolved convergently in coralline red macroalgae, reinforcing tissues against wave-induced breakage, despite differences in cellulose abundance, microfibril orientation, and wall structure. Abstract: Cellulose-enriched secondary cell walls are the hallmark of woody vascular plants, which develop thickened walls to support upright growth and resist toppling in terrestrial environments. Here we investigate the striking presence and convergent evolution of cellulosic secondary walls in coralline red algae, which reinforce thalli against forces applied by crashing waves. Despite ostensible similarities to secondary wall synthesis in land plants, we note several structural and mechanical differences. In coralline red algae, secondary walls contain three-times more cellulose (~ 22% w/w) than primary walls (~ 8% w/w), and their presence nearly doubles the total thickness of cell walls (~ 1.2 µm thick). Field emission scanning electron microscopy revealed that cellulose bundles are cylindrical and lack any predominant orientation in both primary and secondary walls. His-tagged recombinant carbohydrate-binding module differentiated crystalline and amorphous cellulose in planta, noting elevated levels of crystalline cellulose in secondary walls. With the addition of secondary cell walls, Calliarthron genicular tissues become significantly stronger and tougher, yet remain remarkably extensible, more than doubling in length before breaking under tension. Thus, the development of secondary walls contributes to the strong-yet-flexible genicular tissues that enable coralline red algae to survive along wave-battered coastlines throughout the NE Pacific. This study provides an important evolutionary perspective on the development and biomechanical significance of secondary cell walls in a non-model, non-vascular plant.

KW - Biomechanics

KW - Calliarthron

KW - Carbohydrate-binding module

KW - Convergent evolution

KW - Coralline

KW - Genicula

KW - Intertidal

KW - Macroalgae

KW - Rhodophyta

KW - Seaweed

UR - http://www.scopus.com/inward/record.url?scp=85072119530&partnerID=8YFLogxK

U2 - 10.1007/s00425-019-03269-1

DO - 10.1007/s00425-019-03269-1

M3 - Article

AN - SCOPUS:85072119530

VL - 250

SP - 1867

EP - 1879

JO - Planta

JF - Planta

SN - 0032-0935

IS - 6

ER -

Janot K, Martone PT, Fujita M, Wasteneys G, Ruel K, Joseleau JP y otros. Cellulose-rich secondary walls in wave-swept red macroalgae fortify flexible tissues. Planta. 2019 dic 1;250(6):1867-1879. https://doi.org/10.1007/s00425-019-03269-1