Architecture-Based Multiscale Computational Modeling of Plant Cell Wall Mechanics to Examine the Hydrogen-Bonding Hypothesis of the Cell Wall Network Structure Model

Abstract

A primary plant cell wall network was computationally modeled using the finite element approach to study the hypothesis of hemicellulose (HC) tethering with the cellulose microfibrils (CMFs) as one of the major load-bearing mechanisms of the growing cell wall. A computational primary cell wall network fragment (10 3 10 mm) comprising typical compositions and properties of CMFs and HC was modeled with well-aligned CMFs. The tethering of HC to CMFs is modeled in accordance with the strength of the hydrogen bonding by implementing a specific load-bearing connection (i.e. the joint element). The introduction of the CMF-HC interaction to the computational cell wall network model is a key to the quantitative examination of the mechanical consequences of cell wall structure models, including the tethering HC model. When the cell wall network models with and without joint elements were compared, the hydrogen bond exhibited a significant contribution to the overall stiffness of the cell wall network fragment. When the cell wall network model was stretched 1% in the transverse direction, the tethering of CMF-HC via hydrogen bonds was not strong enough to maintain its integrity. When the cell wall network model was stretched 1% in the longitudinal direction, the tethering provided comparable strength to maintain its integrity. This substantial anisotropy suggests that the HC tethering with hydrogen bonds alone does not manifest sufficient energy to maintain the integrity of the cell wall during its growth (i.e. other mechanisms are present to ensure the cell wall shape).The mechanics of plant cell wall growth is one of the challenging problems in plant biology. This fundamental research question is about what and how constituents of the plant cell wall contribute to strength while maintaining the flexibility required for growth. The cell wall's delicate balance of competing requirements of strength and flexibility is a manifestation of the underlying molecular structure and biochemical interactions. This aspect has led plant biologists to postulate cell wall structure models based on observations from biochemical experiments. However, the mechanistic consequences of such models are not directly verifiable because of the lack of an adequate quantitative tool (Ha et al., 1997).The characterization of cell wall structure models has followed two complementary pathways. One pathway is concerned with the architectural structure, such as the multinet model (Roelofsen, 1951;Preston, 1974Preston, , 1982) and the helicoidal model (Neville, 1985;Abeysekera and Willison, 1987). The other pathway emphasizes the biochemical structure of plant cell walls (Keegstra et al., 1973;Fry, 1989;Hayashi, 1989;Talbott and Ray, 1992;Ha et al., 1997;Cosgrove, 2000Cosgrove, , 2001Park and Cosgrove, 2012). At present, a universal (i.e. generalized) structure model that fully and satisfactorily explains the mechanical behavior of the cell wall remains to be developed and validated (Niklas, 1992;Albersheim et al., 2010). Therefore, it is not surprising ...

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