Wood and plant fibres are formidable biological materials with outstanding properties. In some cases they should be strong enough to maintain trees standing tall for tens of meters and in other cases they must be flexible enough to bend without breaking when withstanding strong winds. These range of properties are confered just by three main molecular components – cellulose, hemicelluloses and lignin – that are arranged by an exquisite hierarchical organization in the plant cell walls from the nanoscale to the macroscopic scale.
Cellulose constitutes the main structural component of plant fibres and are formed by long linear polymeric chains of glucose units linked by β-(1→4) glycosidic linkages. This linear conformation of the cellulose chains enables their arrangement in semicrystalline microfibrils during biosynthesis, which is responsible for their excellent mechanical properties. Lignin, on the other hand, is a polyphenolic polymer confering hydrophobicity to plant cell walls, so that they can perform their vascular function.
Hemicelluloses comprise one third of the total mass in wood, but they are traditionally overlooked compared to cellulose fibres and lignins. Hemicelluloses are similar in some ways to cellulose, sharing a similar backbone of sugar units (not only glucose, but also xylose and mannose) linked by β-(1→4) glycosidic linkages; however, they are decorated by a wide range of neutral sugar and uronic acid substitutions, and chemically-modified by acetylation and methylation (Figure 1). There are two main types of hemicelluloses in wood and similar plant tissues, namely xylans and mannans, each with different abundance and molecular structure in different plants. For example, evergreens (e.g. spruce) have mannan as the main hemicellulose, whereas flowering plants (e.g. birch) have xylan as the main hemicellulose.
In the scope of the Wallenberg Wood Science Centre (WWSC) we are investigating the structure – property relations of wood hemicelluloses. In the recent years, the combination of plant molecular biology, advanced characterization by mass spectrometry (MS)-based glycomics and solid-state nuclear magnetic resonance (ssNMR), and computational chemistry, has revealed a detailed level of molecular control and organization of the hemicelluloses in plant fibres. Recent advances by ourselves and other colleagues in the field have revealed the occurrence of regular molecular motifs in wood hemicelluloses that modulate their interactions with cellulose microfibrils and lignin. Therefore, we can envisage the dual role of hemicelluloses in plant fibres as the ‘molecular glue’ interacting at the same time with cellulose fibrils and lignins, thus contributing to wood integrity. However, up till now the influence of the individual wood hemicelluloses on the mechanical properties of plant fibres has not been elucidated yet. This is due to the molecular heterogeneity existing in plant fibres, and due to the fact that no wood exists without both hemicellulose components.
In order to tackle this challenge, a collaboration between researchers at the WWSC in KTH Royal Institute of Technology (Sweden) and at the Centre for Nutrition and Food Sciences (CNAFS), part of the Queensland Alliance for Agricultural and Food Innovation (QAAFI) at The University of Queensland (Australia) was proposed. Francisco Vilaplana, Associate Professor at KTH and one of the corresponding authors of the article, is an Honorary QAAFI Research Fellow at The University of Queensland, where he performed his postdoctoral research and started his research on plant cell walls. This long-standing collaboration enabled Jennie Berglund, back then PhD student at the WWSC researching the structure and function of wood hemicelluloses, to perform a research secondment in Brisbane (Australia) under the supervision of Dr. Deirdre Mikkelsen, Dr. Gleb Yakubov (now at The University of Nottingham, UK) and Prof. Mike Gidley.
Prof. Mike Gidley and his team have pioneered and developed the use of bacterial cellulose as a model system to study the molecular interactions and mechanical properties in plant fibres. This bacterial model is very valuable, as the bacteria we used (Komagataeibacter xylinus) synthesizes and secretes pure cellulose into the media, without the presence of other plant cell wall components. The KTH team extracted and carefully purified mannans and xylans from Scandinavian forests (spruce and birch) with distinct molecular structures. Back in Australia, these hemicelluloses were dispersed in the media where Komagataeibacter xylinus secretes extracellularly pure cellulose, and they were integrated in the fibrillar netwok mimicking the way plant cell walls are assembled (Figure 2). This procedure allowed to study for the first time the distinct biomechanical contributions of specific wood hemicellulose populations to cellulose fibrillar networks. While mannans improve the compression properties, xylans on the other hand drastically improve the extensibility.
These research results have important implications, not only to understand the biological function of hemicelluloses in plant fibres, but also for their use in materials and food applications. One could think using specifically mannans to improve the properties of cellulose based foams, where compressive strength is required, or using xylans to specifically improve the stretchability of cellulose films to be used in food packaging applications replacing fossil-based plastics. On the other hand, this fundamental advance on the structure of plant fibres could lead to the design of functional plant-based food products based with tailored textures, that could be selectively fermented in the gut contributed to an improved nutrition and human health.
Further reading
A. Martínez-Abad, A. Jiménez-Quero, J. Wohlert and F. Vilaplana, Green Chemistry, 2020, 22, 3956-3970.
O. M. Terrett, J. J. Lyczakowski, L. Yu, D. Iuga, W. T. Franks, S. P. Brown, R. Dupree and P. Dupree, Nature Communications, 2019, 10, 4978.
T. J. Simmons, J. C. Mortimer, O. D. Bernardinelli, A.-C. Pöppler, S. P. Brown, E. R. deAzevedo, R. Dupree and P. Dupree, Nature Communications, 2016, 7, 13902.
M. Busse-Wicher, A. Li, R. L. Silveira, C. S. Pereira, T. Tryfona, T. C. F. Gomes, M. S. Skaf and P. Dupree, Plant Physiology, 2016, 171, 2418-2431.
M. Busse-Wicher, T. C. F. Gomes, T. Tryfona, N. Nikolovski, K. Stott, N. J. Grantham, D. N. Bolam, M. S. Skaf and P. Dupree, The Plant Journal, 2014, 79, 492-506.
J. Berglund, S. Kishani, D. Morais de Carvalho, M. Lawoko, J. Wohlert, G. Henriksson, M. E. Lindström, L. Wågberg and F. Vilaplana, ACS Sustainable Chemistry & Engineering, 2020, 8, 10027-10040.
J. Berglund, T. Angles d'Ortoli, F. Vilaplana, G. Widmalm, M. Bergenstråhle-Wohlert, M. Lawoko, G. Henriksson, M. Lindström and J. Wohlert, The Plant Journal, 2016, 88, 56-70.
S.-L. Chong, L. Virkki, H. Maaheimo, M. Juvonen, M. Derba-Maceluch, S. Koutaniemi, M. Roach, B. Sundberg, P. Tuomainen, E. J. Mellerowicz and M. Tenkanen, Glycobiology, 2014, 24, 494-506.
N. J. Grantham, J. Wurman-Rodrich, O. M. Terrett, J. J. Lyczakowski, K. Stott, D. Iuga, T. J. Simmons, M. Durand-Tardif, S. P. Brown, R. Dupree, M. Busse-Wicher and P. Dupree, Nature Plants, 2017, 3, 859-865.
J. R. Bromley, M. Busse-Wicher, T. Tryfona, J. C. Mortimer, Z. Zhang, D. M. Brown and P. Dupree, The Plant Journal, 2013, 74, 423-434.
A. Martínez-Abad, N. Giummarella, M. Lawoko and F. Vilaplana, Green Chemistry, 2018, 20, 2534-2546.
A. Martínez-Abad, J. Berglund, G. Toriz, P. Gatenholm, G. Henriksson, M. Lindström, J. Wohlert and F. Vilaplana, Plant Physiology, 2017, 175, 1579-1592.
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