Life history biology of early land plants: Deciphering the gametophyte phase

Abstract

The ca. 400-million-year-old Rhynie chert biota represents a benchmark for studies of early terrestrial ecosystems. The exquisite preservation of the organisms documents an ancient biodiversity that also includes various levels of biological interaction. Absent from the picture until recently has been detailed information about the development of the gametophyte phase and the alternation of generations of the macroplants in this ecosystem. Here, we trace the development of the gametophyte phase of Aglaophyton, an early land plant with an unusual complement of structural and morphological characters. Mature gametophytes consist of a fleshy protocorm attached to the substrate by basal rhizoids; arising from the upper surface are one to several upright gametangiophores bearing multiple gametangia. Stomata are present on the upper surface of the protocorm and gametangiophore, and endomycorrhizal fungi extend throughout the gametophyte. Gametophytes are unisexual, producing either antheridiophores or archegoniophores. There is no evidence that gametophytes later become hermaphroditic. The sexual dimorphism of the Rhynie chert gametophytes is inconsistent with theoretical ideas about the haploid phase of early land plants. The gametophyte phase of early land plants can now be considered within an ecological and evolutionary framework that, in turn, can be used to develop hypotheses about some aspects of the population dynamics and growth of these early land plants.Early Devonian ͉ fossil gametophytes ͉ Rhynie chert ͉ spore development ͉ alteration of generations

Acaulosporoid glomeromycotan spores with a germination shield from the 400-million-year-old Rhynie chert

“…Nevertheless, the fact that the life history of some of these early land plants included two distinct generations, both associated with AMF (see Taylor et al 2005), implies that this mutualism was both widespread and a significant factor in driving the evolution of early terrestrial ecosystems. The Rhynie chert fossils now push back the evolutionary origin of all main spore types in the Glomeromycota to a time before the evolution of true roots, and thus suggest their symbiotic nature predates root formation and the evolution of the mycorrhiza (= fungus-root).…”

“…Within the 400-million-year-old Rhynie chert are arbuscular mycorrhizae that were produced by glomeromycotan fungi (Remy et al 1994;Taylor et al 1995Taylor et al , 2005Helgason and Fitter 2005). An exact systematic placement of the fungal partners, however, has not been possible to date; the only glomeromycotan fungus from the Rhynie chert that has tentatively been related to a modern genus and family based on spore morphology is Scutellosporites devonicus (Dotzler et al 2006).…”

“…Such apparent symbioses are known to have existed for at least 400 million years based on exquisitely preserved fossils from the Early Devonian Rhynie chert (e.g. Remy et al 1994;Taylor et al 1995Taylor et al , 2004Taylor et al , 2005Krings et al 2007). Although the Rhynie chert AM have been studied intensively, the reproductive biology of their fungal partners (AMF) remains largely unknown.…”

Homologous Versus Antithetic Alternation of Generations and the Origin of Sporophytes

“…Second, these gametophytes produced archegoniophores that elevated archegonia above the substrate. Third, no gametophytes have been found with attached sporophytes (Remy, 1980;Remy et al, 1993;Taylor et al, 2005).…”

Phylogenetisches Symposium Göttingen

“…Thus, the fossil record suggest a sequence in which polysporangiate sporophytes were established first and differentiation of vascular tissue evolved later. The fossil record does not allow us to interpret the evolution of the establishment of the second character -dominance of the diploid generation -because only exceptionally preserved fossil beds provide sufficient information to reconstruct the life cycle of Siluarian or Devonian land plants (Taylor et al 2005). A second example for the importance of fossils in studies focusing on the evolution of complex traits is given within the ancestors of the seed plants (Fig.…”