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1.
Integr Comp Biol ; 2022 Apr 28.
Article in English | MEDLINE | ID: mdl-35482591

ABSTRACT

Seaweeds inhabiting wave-battered coastlines are generally flexible, bending with the waves to adopt more streamlined shapes and reduce drag. Coralline algae, however, are firmly calcified, existing largely as crusts that avoid drag altogether or as upright branched forms with uncalcified joints (genicula) that confer flexibility to otherwise rigid thalli. Upright corallines have evolved from crustose ancestors independently multiple times, and the repeated evolution of genicula has contributed to the ecological success of articulated corallines worldwide. Structure and development of genicula are significantly different across evolutionary lineages, and yet biomechanical performance is broadly similar. Because chemical composition plays a central role in both calcification and biomechanics, we explored evolutionary trends in cell wall chemistry across crustose and articulated taxa. We compared the carbohydrate content of genicula across convergently-evolved articulated species, as well as the carbohydrate content of calcified tissues from articulated and crustose species, to search for phylogenetic trends in cell wall chemistry during the repeated evolution of articulated taxa. We also analysed the carbohydrate content of one crustose coralline species that evolved from articulated ancestors, allowing us to examine trends in chemistry during this evolutionary reversal and loss of genicula. We found several key differences in carbohydrate content between calcified and uncalcified coralline tissues, though the significance of these differences in relation to the calcification process requires more investigation. Comparisons across a range of articulated and crustose species indicated that carbohydrate chemistry of calcified tissues was generally similar, regardless of morphology or phylogeny; conversely, chemical composition of genicular tissues was different across articulated lineages, suggesting that significantly different biochemical trajectories have led to remarkably similar biomechanical innovations.

3.
Planta ; 250(6): 1867-1879, 2019 Dec.
Article in English | MEDLINE | ID: mdl-31482328

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. 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.


Subject(s)
Cell Wall/metabolism , Cellulose/metabolism , Seaweed/metabolism , Biomechanical Phenomena , Cell Wall/ultrastructure , Microfibrils/metabolism , Microscopy, Electron, Scanning , Seaweed/ultrastructure
4.
J Phycol ; 54(3): 305-316, 2018 06.
Article in English | MEDLINE | ID: mdl-29505102

ABSTRACT

The evolution of uncalcified genicula in upright calcified corallines has occurred at least three times independently, resulting in articulated corallines within Corallinoideae, Lithophylloideae, and Metagoniolithoideae. Genicula confer flexibility to otherwise rigid thalli, and the localization of bending at discrete intervals amplifies bending stress in genicular tissue. Genicular morphology must, therefore, be balanced between maintaining flexibility while mitigating or resisting stress. Genicula in the three articulated lineages differ in both cellular construction and development, which may result in different constraints on morphology. By studying the interaction between flexibility and morphological variation in multiple species, we investigate whether representatives of convergently evolving clades follow similar strategies to generate mechanically successful articulated fronds. By using computational models to explore different bending strategies, we show that there are multiple ways to generate flexibility in upright corallines but not all morphological strategies are mechanically equivalent. Corallinoids have many joints, lithophylloids have pliant joints, and metagoniolithoids have longer joints-while these strategies can lead to comparable thallus flexibility, they also lead to different levels of stress amplification in bending. Moreover, genicula at greatest risk of stress amplification are typically the strongest, universally mitigating the trade-off between flexibility and stress reduction.


Subject(s)
Biological Evolution , Rhodophyta/anatomy & histology , Rhodophyta/physiology , Biomechanical Phenomena , Rhodophyta/cytology , Seaweed/cytology , Seaweed/physiology
5.
J Exp Biol ; 219(Pt 3): 383-91, 2016 Feb.
Article in English | MEDLINE | ID: mdl-26596529

ABSTRACT

Flexible joints are a key innovation in the evolution of upright coralline algae. These structures have evolved in parallel at least three separate times, allowing the otherwise rigid, calcified thalli of upright corallines to achieve flexibility when subjected to hydrodynamic stress. As all bending occurs at the joints, stress is amplified, which necessitates that joints be made of material that is both extensible and strong. Data presented here indicate that coralline joints are in fact often stronger and more extensible, as well as tougher, than fleshy seaweed tissues. Corallinoids are particularly strong and tough, which is largely due to the presence of secondary cell walls that strengthen the joint tissue without adding bulk to the joint itself. Cell wall thickness is shown to be a large contributing factor to strength across all groups, with the exception of the corallinoid Cheilosporum sagittatum, which likely possesses distinct chemical composition in its walls to increase strength beyond that of all other species tested.


Subject(s)
Biological Evolution , Rhodophyta/anatomy & histology , Seaweed , Biomechanical Phenomena , Rhodophyta/classification , Seaweed/classification , Water Movements
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