Cell differentiation and tissue formation in the unique fruits of devil's claws (Martyniaceae)

Abstract

• Premise of the study: Martyniaceae are characterized by capsules with two upwardly curved, horn-shaped extensions representing morphologically specialized epizoochorous fruits. Because the capsules are assumed to cling to hooves and ankles of large mammals, fiber arrangement and tissue combinations within the endocarp ensuring proper attachment to the vector's feet during transport are of particular interest. In this first detailed anatomical investigation, the functional adaptation of the fruits and their implications for the specific dispersal mode are provided. The peculiar fiber arrangement may also be of interest for future biomimetic composite materials.• Methods: Endocarp anatomy and details of tissue differentiation were examined in fruits of Ibicella lutea and Proboscidea louisianica subsp. fragrans combining light microscopy, SEM, and x-ray microtomography analysis.• Key results: While tips of the extensions are predominantly reinforced by longitudinally oriented fibers, in the middle segment these fibers are densely packed in individual bundles entwined and separated by transversely elongated cells. Within the capsule wall, the fiber bundles are embedded in a dense mesh of transversely oriented fibers that circularly reinforce and protect the loculus. This fibrous pericarp tissue develops within few days by localized cell divisions and intrusive growth of primarily isodiametric parenchyma cells in the pistil.• Conclusions: The study allows insight into a unique and complex example of functionally driven cell growth and tissue formation. Long-horned fruits of Martyniaceae obviously are highly specialized to epizoochorous dispersal, pointing to primary vector-related seed dispersal. The highly ordered arrangement of fibers results in a great mechanical firmness.

A materials perspective of Martyniaceae fruits: Exploring structural and micromechanical properties

“…The fruit endocarp and especially the hook-shaped extensions of several species of Martyniaceae are formed by an intriguing system of well-ordered fibres [15]. Since it is presumed that trample burrs interlock with hooves of large mammals, it can be expected that an evolutionary optimisation of the anatomical structure happened with respect to this specific mode of epizoochory.…”

“…Mature fruits from plants of P. louisianica subsp. fragrans (further P. louisianica) and I. lutea, grown in the Botanical Garden of the Technical University of Dresden, Germany were collected about 50 days after pollination (see [15] for details). Wood of scots pine (P. sylvestris) was purchased from commerce.…”

“…However, reliable data on dispersal are scarce. Our previous, anatomical study revealed a complex arrangement of fibrous tissues within the endocarp having a specific ontogeny, which is exceptional and intriguing among plants [15]. The fruit extensions are reinforced by axially running fibres, densely packed in individual bundles (hereinafter called longitudinal sclerenchyma), entwined and separated by transversely elongated fibres (hereinafter called transverse sclerenchyma) (Fig.…”

“…Both annual herbs develop capsules composed of a thick and soft outer layer (exo-and mesocarp), which is shed after desiccation exposing a woody endocarp upon ripening, characterised by about 8-11 cm long, upwardly curved extensions (Fig. 1A,A1) [14,15]. At fruit maturity, the extension tip splits longitudinally into two parts resulting in a shape, which led to the origin of the common plant names: desert unicorn plants or devil's claws (Fig.…”

“…1E). This peculiar fibre arrangement has been interpreted as an anatomical adaptation of the fruits to secure the proper attachment and withstand multiple mechanical loads during the transport by animals [15].…”