Cellulose-rich secondary walls in wave-swept red macroalgae fortify flexible tissues
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.
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.
KeywordsBiomechanics Carbohydrate-binding module Calliarthron Convergent evolution Coralline Genicula Intertidal Macroalgae Rhodophyta Seaweed
Field emission scanning electron microscopy
We would like to thank Chris Somerville and Mark Denny for all of their support and insight during the early development of this project. We thank the UBC BioImaging Facility for state-of-the-art infrastructure and technical assistance. We thank Paul Knox (Leeds, UK) and H. Gilbert (Newcastle) for providing CBM3a and CBM28 to K. R. and J-P. J. This manuscript benefitted from helpful discussions with Mark Denny, Shawn Mansfield, and Sam Starko. P. T. M. acknowledges support from a Natural Sciences and Engineering Research Council (NSERC) Discovery Grant, and J. M. E to ANPCyT (PICT2016-0132 and PICT2017-0066) and ICGEB (CRP/ARG16-03).
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