Ingenious floral structure drives explosive pollination in Hydrilla verticillata (Hydrocharitaceae)

Abstract

In explosive pollination, many structures and mechanisms have evolved to achieve high-speed stamen movement. The male flower of the submerged plant Hydrilla verticillata is reported to be able to release pollen explosively some time after leaving the mother plant time, but the mechanism of stamen movement and the related functional structure in this species are unclear.• In this study, we observed the male flower structure and pollen dispersal process of H. verticillata. We analysed the stamen movements during the pollen dispersal process and conducted several controlled experiments to study the process of storage and release of elastic potential energy in explosive pollination.• When the male flower of H. verticillata is bound to the united bracts, the sepals accumulate elastic potential energy through the expansion of basal extensor cells. After the male flower is liberated from the mother plant, the stamens unfold rapidly with the sepals under adhesion and transfer the elastic potential energy to the filament in seconds. Once stamens unfold to a critical angle, at which the elasticity of the filament just exceeds the adhesion between sepals and anthers, the stamens automatically rebound and release pollen in milliseconds.• These results reveal that Catapult-like stamens, spoon-shaped sepals and enclosed united bracts in the spathe together constitute the functional structure in rapid stamen movement of H. verticillata. They ensure that the pollen can be released on the water surface, and thus adapt successfully to the pollen-epihydrophilous pollination.

Mutualisms and (A)symmetry in Plant–Pollinator Interactions

“…Plants evolved a range of specialised biomechanical adaptations to regulate access to rewards and optimise pollen transfer (Figure 2), including keel flowers 35 , lever-mechanism flowers 36,37 , trigger flowers 38,39 , explosive pollen release 40,41 , heteranthery 42 , and buzz-pollinated flowers 43 . For example, keel flowers present in many Fabaceae and Polygalaceae require floral visitors to exert a significant amount of force to access nectar and pollen rewards 37,44 .…”

High‐speed video and plant ultrastructure define mechanisms of gametophyte dispersal

“…Magnifications of up to 100× are crucial for observing relatively small structures such as anthers involved in pollen dispersal, and specimens can be observed at varying stages of dehiscence (pre‐ versus post‐dispersal). Images captured using dissecting microscopes have been used to observe the mechanics of explosive pollination in flowering plants, including the positioning and shape of floral organs that allow for the “catapult”‐like dehiscence of stamens documented by high‐speed video (Taylor et al, 2006 ; Edwards et al, 2019 ; Zhang et al, 2020 ; Table 2 ). For instance, in the aquatic flowering plant Hydrilla verticillata (L. f.) Royle (Hydrocharitaceae), dissecting microscope images of male flowers before, during, and after anther movement displayed the positioning and importance of the sepals and the overall catapult‐like structure involved in pollen dispersal (Zhang et al, 2020 ).…”

“…Images captured using dissecting microscopes have been used to observe the mechanics of explosive pollination in flowering plants, including the positioning and shape of floral organs that allow for the “catapult”‐like dehiscence of stamens documented by high‐speed video (Taylor et al, 2006 ; Edwards et al, 2019 ; Zhang et al, 2020 ; Table 2 ). For instance, in the aquatic flowering plant Hydrilla verticillata (L. f.) Royle (Hydrocharitaceae), dissecting microscope images of male flowers before, during, and after anther movement displayed the positioning and importance of the sepals and the overall catapult‐like structure involved in pollen dispersal (Zhang et al, 2020 ). Dissecting microscopes have a limited field of range, but specialized hardware and software, such as the focus stacking system of Macroscopic Solutions (Macroscopic Solutions LLC, Tolland, Connecticut, USA) or Helicon Focus (Helicon Soft Ltd., Kharkiv, Ukraine) can take multiple images of samples on multiple focal planes and stack them into clear and accurate images for samples >10 µm (Brecko et al, 2014 ; Cameron and Zaspel, 2019 ).…”

“…Fixation of materials, sectioning, and staining for light microscopy allow for the observation of organs and cells layer by layer throughout the three‐dimensional structure of the organ(s) of interest at up to 1000× magnification. Viewing longitudinal sections of organs in enclosed buds and floral structures helps to understand the development of these organs and how their positioning affects explosive pollination, beyond what is observable on the surface through high‐speed video or when viewed using a dissecting microscope (Taylor et al, 2006 ; Whitaker et al, 2007 ; Zhang et al, 2020 ). Furthermore, staining of these organs can also lead to insights into chemical composition.…”

“…For instance, in the explosive flowers of Cornus canadensis (described above), staining of organs with ruthenium red and hydroxylamine hydrochloride–ferric chloride revealed that cell walls in the “hinge” section of stamens are high in acidic pectin and low in esterified pectin, resulting in tissue softening (Edwards et al, 2019 ). Light microscope images are also used in the identification of the shapes and water‐absorbing abilities of some cells involved in these rapid movements (Taylor et al, 2006 ; Zhang et al, 2020 ). In non‐flowering plants, light microscopy has allowed for more detailed observation of the dehiscence of moss and liverwort sporophyte capsules (Gallenmüller et al, 2018 ; Duckett and Pressel, 2019 ) and has elucidated the importance of gas bubbles and cavitation in the dispersal of fern spores (Hovenkamp et al, 2009 ; Poppinga et al, 2015 ).…”