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  1. ABSTRACT

    Periderm is a well‐known structural feature with vital roles in protection of inner plant tissues and wound healing. Despite its importance to plant survival, knowledge of periderm occurrences outside the seed plants is limited and the evolutionary origins of periderm remain poorly explored. Here, we review the current knowledge of the taxonomic distribution of periderm in its two main forms – canonical periderm (periderm formed as a typical ontogenetic stage) and wound periderm (periderm produced as a self‐repair mechanism) – with a focus on major plant lineages, living and extinct. We supplement the published occurrences with data based on our own observations and experiments. This updated body of data reveals that the distribution of wound periderm is more widespread taxonomically than previously recognized and some living and extinct groups are capable of producing wound periderm, despite canonical periderm being absent from their normal developmental program. A critical review of canonical and wound periderms in extant and fossil lineages indicates that not all periderms are created equal. Their organisation is widely variable and the differences can be characterised in terms of variations in three structural features: (i) the consistency in orientation of periclinal walls within individual files of periderm cells; (ii) the lateral coordination of periclinal walls between adjacent cell files; and (iii) whether a cambial layer and conspicuous layering of inward and outward derivatives can be distinguished. Using a new system of scoring periderm structure based on these criteria, we characterise the level of organisation of canonical and wound periderms in different lineages. Looking at periderms through the lens provided by their level of organisation reveals that the traditional image of periderm as a single generalised feature, is best viewed as a continuum of structural configurations that are all predicated by the same basic process (periclinal divisions), but can fall anywhere between very loosely organized (diffuse periclinal growth) to very tightly coordinated (organized periclinal growth). Overall, wound periderms in both seed plants and seed‐free plants have lower degrees of organisation than canonical periderms, which may be due to their initiation in response to inherently disruptive traumatic events. Wound and canonical periderms of seed plants have higher degrees of organisation than those of seed‐free plants, possibly due to co‐option of the programs responsible for organizing their vascular cambial growth. Given the importance of wound periderm to plant survival, its widespread taxonomic distribution, and its early occurrence in the fossil record, we hypothesise that wound periderm may have had a single origin in euphyllophytes and canonical periderm may have originated separately in different lineages by co‐option of the basic regulatory toolkit of wound periderm formation. In one evolutionary scenario, wound periderm regulators activated initially by tissue tearing due to tensional stresses elicited by woody growth underwent heterochronic change that switched their activation trigger from tissue tearing to the tensional stresses that precede it, with corresponding changes in the signalling that triggered the regulatory cascade of periderm development from tearing‐induced signals to signalling induced by tension in cells.

     
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  2. Summary

    We analyze the oldest fossil occurrences of wound‐response periderm to characterize the development of wound responses in early tracheophytes. The origin of periderm production by a cambium (phellogen), an innovation with key roles in protection of inner plant tissues, is poorly explored; understanding periderm development in early tracheophytes can illuminate key aspects of this process.

    Anatomy of wound‐response tissues is characterized in serial sections in a new Early Devonian (Emsian;c. 400 Ma) euphyllophyte from Quebec (Canada) –Nebuloxyla mikmaqianasp. nov. – and compared to previously described euphyllophyte periderm from the same fossil locality to reconstruct periderm development.

    Characterizing development in these oldest periderm occurrences allows us to propose a model for the development of wound‐response periderm in early tracheophytes: by phellogen activity that is poorly coordinated laterally but bifacial, producing secondary tissues initially outwardly and subsequently inwardly.

    The earliest occurrences of wound periderm pre‐date the oldest known periderm produced systemically as a regular ontogenetic stage (canonical periderm), suggesting that periderm evolved initially as a wound‐response mechanism. We hypothesize that canonical periderm evolved by exaptation of this wound sealing mechanism, whose deployment was triggered by tangential tensional stresses induced in the superficial tissues by vascular cambial growth from within.

     
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  3. Abstract

    The Beartooth Butte Formation hosts the most extensive Early Devonian macroflora of western North America. The age of the flora at Cottonwood Canyon (Wyoming) has been constrained to the Lochkovian–Pragian interval, based on fish biostratigraphy and unpublished palynological data. We present a detailed palynological analysis of the plant‐bearing layers at Cottonwood Canyon. The palynomorphs consist of 32 spore, five cryptospore, two prasinophycean algae and an acritarch species. The stratigraphic ranges of these palynomorphs indicate a late Lochkovian or Pragian age, confirming previous age assignments. Analysis of samples from three different depositional environments of the plant‐bearing sequence (layers within situlycophyte populations, flood layers that buried those populations and an organic matter accumulation zone within a flood layer) demonstrate distinct palynofacies. Comparisons between palynomorph and plant macrofossil diversity reveal some discrepancies. Whereas zosterophylls and lycophytes, most diverse and abundant among the macrofossils, have only one known corresponding spore type (assignable to zosterophylls) in the palynomorph assemblage, the trimerophytes, rare in the macrofossil assemblage, are represented by three spore types. Some of these discrepancies reflect taphonomic differences between the macrofossils and palynomorphs, while others could be due to the fact that the parent plants of most palynomorph types in the Cottonwood Canyon assemblage are unknown. These observations emphasize the need for concerted efforts to bring together the knowledge of macro‐ and microfloras within Early Devonian localities. Nevertheless, given the palaeophytogeographic significance of the Beartooth Butte Formation flora, its palynofossil and macrofossil assemblages, taken together, provide new data relevant to future discussions of Early Devonian biogeography.

     
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  4. Background

    In extant ecosystems, complex networks of ecological interactions between organisms can be readily studied. In contrast, understanding of such interactions in ecosystems of the geologic past is incomplete. Specifically, in past terrestrial ecosystems we know comparatively little about plant biotic interactions besides saprotrophy, herbivory, mycorrhizal associations, and oviposition. Due to taphonomic biases, epiphyte communities are particularly rare in the plant-fossil record, despite their prominence in modern ecosystems. Accordingly, little is known about how terrestrial epiphyte communities have changed across geologic time. Here, we describe a tinyin situfossil epiphyte community that sheds light on plant-animal and plant-plant interactions more than 50 million years ago.

    Methods

    A single silicifiedTodea(Osmundaceae) rhizome from a new locality of the early Eocene (ca. 52 Ma) Tufolitas Laguna del Hunco (Patagonia, Argentina) was studied in serial thin sections using light microscopy. The community of organisms colonizing the tissues of the rhizome was characterized by identifying the organisms and mapping and quantifying their distribution. A 200 × 200 µm grid was superimposed onto the rhizome cross section, and the colonizers present at each node of the grid were tallied.

    Results

    Preservedin situ, this community offers a rare window onto aspects of ancient ecosystems usually lost to time and taphonomic processes. The community is surprisingly diverse and includes the first fossilized leafy liverworts in South America, also marking the only fossil record of leafy bryophyte epiphytes outside of amber deposits; as well as several types of fungal hyphae and spores; microsclerotia with possible affinities in several ascomycete families; and evidence for oribatid mites.

    Discussion

    The community associated with the Patagonian rhizome enriches our understanding of terrestrial epiphyte communities in the distant past and adds to a growing body of literature on osmundaceous rhizomes as important hosts for component communities in ancient ecosystems, just as they are today. Because osmundaceous rhizomes represent an ecological niche that has remained virtually unchanged over time and space and are abundant in the fossil record, they provide a paleoecological model system that could be used to explore epiphyte community structure through time.

     
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