Three-dimensional functional gradients direct stem curling in the resurrection plant Selaginella lepidophylla.

Véronique Brulé,Damiano Pasini,Tamara L Western,Meisam Asgari,Ahmad Rafsanjani

doi:10.1098/rsif.2019.0454

Abstract

Upon hydration and dehydration, the vegetative tissue of Selaginella lepidophylla can reversibly swell and shrink to generate complex morphological transformations. Here, we investigate how structural and compositional properties at tissue and cell wall levels in S. lepidophylla lead to different stem curling profiles between inner and outer stems. Our results show that directional bending in both stem types is associated with cross-sectional gradients of tissue density, cell orientation and secondary cell wall composition between adaxial and abaxial stem sides. In inner stems, longitudinal gradients of cell wall thickness and composition affect tip-to-base tissue swelling and shrinking, allowing for more complex curling as compared to outer stems. Together, these features yield three-dimensional functional gradients that allow the plant to reproducibly deform in predetermined patterns that vary depending on the stem type. This study is the first to demonstrate functional gradients at different hierarchical levels combining to operate in a three-dimensional context.

Highlights

Functional gradients are the foundation of many biological processes, ranging from the migration of unicellular organisms through to influencing mechanical responses in complex, multicellular organisms [1,2]
We aim to address two related questions: (1) what properties lead to directional stem deformation and (2) how do these properties contribute to the different degrees of curling observed in inner and outer S. lepidophylla stem types? We take advantage of an array of techniques to explore how morphology (micro-computed X-ray tomography and transmission electron microscopy (TEM)), composition and mechanical properties at the tissue and cell wall levels lead to deformation in S. lepidophylla
We show that a combination of morphological and compositional properties gives rise to three-dimensional functional gradients that drive water-responsive shape transformation in S. lepidophylla, and that the variation in curling of inner and outer stem types results from specific combinations of functional gradients

Summary

Introduction

Functional gradients are the foundation of many biological processes, ranging from the migration of unicellular organisms through to influencing mechanical responses in complex, multicellular organisms [1,2]. One of the most fascinating examples of FGM-based function in plants is actuation: the process of autonomous deformation that is triggered by an external stimulus [6,8] Biological actuators, such as the pinecone, the seeds of the ice plant and the wheat awn undergo a set of well-defined and reproducible shape transformations as part of their physiological response to changes in hydration status [6,8,9,10,11,12]. Deformation in these species arises from differential swelling/shrinking of juxtaposed tissues with distinctive material properties [12,13,14,15].

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