Quo vadis plant biomechanics: Old wine in new bottles or an up‐and‐coming field of modern plant science?

Abstract

In this essay, we present a personal view of plant biomechanics today and of the directions in which plant biomechanics will or should move during the next few decades. Biomechanics deals with mechanical investigations on plants, animals, fungi, and bacteria, covering all orders of magnitude—from the molecule to the entire organism—applying methods also used in physics, engineering, and materials sciences. In our opinion, the field of plant biomechanics cannot be considered without mechanically testing, analyzing, and characterizing the underlying structural setup of the hierarchical organization of plant cells, tissues, organs, and organisms. As a consequence, only a thorough analysis of the materials systems of a plant will enable reliable quantitative mechanical investigations. In turn, a quantitative analysis of the form–structure–function relations in plants is only possible if the functional morphology is studied in conjunction with a biomechanical investigation. The mechanical properties of plants and plant structures have been of interest and importance to humans since the very beginnings of humankind. On the one hand, plants always were important parts of the human diet, and the mechanics of plant products influences aspects such as chewability, palatability, and digestibility. On the other hand, the use of plant fibers, wood, and bark for various purposes, e.g., clothing, fishing, hunting, and housing, represents one of the first and most important achievements during the early cultural evolution. In this phase, humans had considerable pre-scientific knowledge concerning the mechanical properties of plants and plant organs, a prerequisite for the meaningful use of plant materials for various purposes. Even during the early phases of modern natural sciences in the 15th to 17th centuries, an interest in the mechanical and structural properties of plants was apparent. Leonardo da Vinci (1452–1519) was fascinated by various aspects of plant biomechanics and in the information that can be gained from plants for technical applications, a field of science that we now term biomimetics. Most notable were his ideas for parachutes inspired by the pappus of anemochorus dandelion fruits (implemented for the first time in a working model by Sir George Cayley [1773–1857]) and for autogyroscopic propellers inspired by spinning samara fruits. Galileo Galilei (1564–1642) found inspiration when considering the physics of tubes in his studies of the bending and buckling behavior of hollow grass culms (Geitmann et al., 2019). At the same time, the scientific exchange between the botanist Nehemiah Grew (1641–1712) and the physicist Robert Hooke (1635–1703) reveals that plant biologists used physical and engineering approaches from the very beginning to better understand certain aspects of plant life, in this case, the hydrostatic (turgor) stabilization of parenchyma cells. By the end of the 19th century, with the publication of Simon Schwendener's book Das mechanische Princip im anatomischen Bau der Monocotylen mit vergleichenden Ausblicken auf die übrigen Pflanzenklassen (The Mechanical Principles of the Anatomy of Monocotyledons with an Overview of the Other Plant Classes) (Schwendener, 1874), plant biomechanics had become a well-defined field of science integrating aspects of biology, physics, and engineering (Geitmann et al., 2019). These short historical considerations alone indicate that the topic of plant biomechanics was from its very beginning, and still is, an intrinsically interdisciplinary field of science. Today, in addition to the use of a multitude of methodologies typical for biology, plant biomechanics also borrows methods from physics, chemistry, engineering, and materials sciences. This combination is necessary for the study of mechanical properties on and over all relevant length scales and for the analysis of underlying structures at various length scales. However, plant biomechanics is not only interdisciplinary in t