Fissures and pores in the capsule walls and hydrophobic elaters in Haplomitrium: a transmission and cryo-scanning electron microscope study

ABSTRACT

Introduction. Whereas the capsule wall in liverworts is usually described as smooth, our discovery of deep schizogenous fissures in the unistratose walls in Haplomitrium appears unique to this earliest diverging liverwort genus and may have important implications for understanding the evolution of the stomatal toolkit in land plants.

Methods. Sporophytes of Haplomitrium gibbsiae and H. mnioides were examined by light, transmission and cryo-scanning electron microscopy.

Key results. In striking contrast to cell breakage along the dehiscence grooves in the capsule walls, development of the schizogenous fissures is predetermined by a middle lamellar region of the radial walls comprising globular and fibrillar elements. The capsule wall cells remain alive, even after dehiscence, and have many cytological features in common with food-conducting cells in bryophytes including highly differentiated plasmodesmata. Whereas the highly ornamented spore exine retains water, the elaters are hydrophobic due to a coating of lipid droplets secreted by these cells.

Conclusions. The development of regular thickened bands together with the schizogenous splitting of the capsule walls suggests that Haplomitrium may contain a possible primeval structural toolkit facilitating capsule desiccation and spore discharge. Thus we may be seeing, in this earliest extant liverwort lineage, the basic features needed for the assembly of stomata. There is no cytological evidence for a possible nutritive tapetal function for the capsule walls in Haplomitrium and the hydrophobic envelopes of the elaters probably enhance their effectiveness in spore dispersal.

KEYWORDS:

• Cryo-scanning electron microscopy
• liverworts
• schizogeny
• plasmodesmata
• spore dispersal
• stomatal toolkit

Acknowledgements

Zophia Ludlinska (Nanovision Centre, Queen Mary University of London), Alex Ball (Imaging and Analysis Centre, Natural History Museum, London) for skilled technical assistance using the cryo-SEM and TEM. Travel funds to SP from the Natural History Museum and FCO funded cooperation with Fairylake Botanical Garden, Shenzhen and Chinese Academy of Sciences, and a Leverhulme Emeritus Fellowship to JGD enabled the collection of the materials used in this study.

Notes on contributors

Jeff Duckett is a Research Associate, working with Silvia Pressel at the Natural History Museum, London, on diverse aspects of bryophyte biology and evolution. Ongoing projects include the evolution and function of the stomatal apparatus, fungal symbioses in early land plant lineages and London's changing bryophyte flora.

Silvia Pressel is a Researcher and Head of the Algae, Fungi and Plants Division in the Life Sciences Department at the Natural History Museum, London. Current research foci in her laboratory include bryophyte diversity and biogeography on South Atlantic Oceanic Islands; bryophyte ex-situ conservation; the evolution and diversity of mycorrhizal associations in land plants; stomata development and function in bryophytes.

ORCID

Jeffrey G. Duckett http://orcid.org/0000-0001-7101-6673

Silvia Pressel http://orcid.org/0000-0001-9652-6338