Jonathan P. Wilson

Four hundred million years of silica biomineralization in land plants.

Significance Amorphous silica (SiO2) phases produced by plants are principal mass fluxes in the global silica cycle. The study of silica biomineralization in plants has largely focused on angiosperms, leaving open questions about its early evolution. To address the effect of early plants on the silica cycle, we measured the silica contents of extant members of plant groups known from fossils to have been major components of the terrestrial landscape in the past, as grasses are today. Most of these early-diverging plant lineages accumulate substantial amounts of silica. We compared these observations with the distribution and evolution of plant silica transport proteins, suggesting convergent evolution of silica use. Results presented here outline an extensive evolutionary history of silica biomineralization in plants. Biomineralization plays a fundamental role in the global silicon cycle. Grasses are known to mobilize significant quantities of Si in the form of silica biominerals and dominate the terrestrial realm today, but they have relatively recent origins and only rose to taxonomic and ecological prominence within the Cenozoic Era. This raises questions regarding when and how the biological silica cycle evolved. To address these questions, we examined silica abundances of extant members of early-diverging land plant clades, which show that silica biomineralization is widespread across terrestrial plant linages. Particularly high silica abundances are observed in lycophytes and early-diverging ferns. However, silica biomineralization is rare within later-evolving gymnosperms, implying a complex evolutionary history within the seed plants. Electron microscopy and X-ray spectroscopy show that the most common silica-mineralized tissues include the vascular system, epidermal cells, and stomata, which is consistent with the hypothesis that biomineralization in plants is frequently coupled to transpiration. Furthermore, sequence, phylogenetic, and structural analysis of nodulin 26-like intrinsic proteins from diverse plant genomes points to a plastic and ancient capacity for silica accumulation within terrestrial plants. The integration of these two comparative biology approaches demonstrates that silica biomineralization has been an important process for land plants over the course of their >400 My evolutionary history.

EVOLUTIONARY VOYAGE OF ANGIOSPERM VESSEL STRUCTURE-FUNCTION AND ITS SIGNIFICANCE FOR EARLY ANGIOSPERM SUCCESS

A hypothesized advantage of the building block of the angiosperm vascular network, the vessel, is often cited as a critical innovation that elevated the competitive abilities of early angiosperms above nonangiosperms during the Cretaceous. Here we synthesize recent discoveries on the hydraulic functions of living basal angiosperm lineages with evidence from the fossil record to trace the early evolutionary significance of vessels in the early ecophysiological radiation of angiosperms. Evidence from extant comparative biology and the Early Cretaceous fossil record of leaves and wood do not support the hypotheses that vessels improved drought tolerance of angiosperms, increased angiosperm’s photosynthetic abilities, or provided an immediate leap in hydraulic capacity. Instead, later tuning of vessel structure for increased flow efficiency—in particular, by the evolution of simple perforation plates—enabled major increases in xylem hydraulic efficiency.

DEEP-WATER INCISED VALLEY DEPOSITS AT THE EDIACARAN-CAMBRIAN BOUNDARY IN SOUTHERN NAMIBIA CONTAIN ABUNDANT TREPTICHNUS PEDUM

Abstract Valley-filling deposits of the Nama Group, southern Namibia, record two episodes of erosional downcutting and backfill, developed close together in time near the Ediacaran-Cambrian boundary. Geochronological constraints indicate that the older valley fill began 539.4 ± 1 Ma or later; the younger of these deposits contains unusually well-preserved populations of the basal Cambrian trace fossil Treptichnus pedum. Facies analysis shows that T. pedum is closely linked to a nearshore sandstone deposit, indicating a close environmental or taphonomic connection to very shallow, mud-draped sandy seafloor swept by tidal currents. Facies restriction may limit the biostratigraphic potential of T. pedum in Namibia and elsewhere, but it also illuminates functional and ecological interpretation. The T. pedum tracemaker was a motile bilaterian animal that lived below the sediment-water interface—propelling itself forward in upward-curving projections that breached the sediment surface. The T. pedum animal, therefore, lived infaunally, perhaps to avoid predation, surfacing regularly to feed and take in oxygen. Alternatively, the T. pedum animal may have been a deposit feeder that surfaced largely for purposes of gas exchange, an interpretation that has some support in the observed association of T. pedum with mud drapes. Treptichnus pedum provides our oldest record of animals that combined anatomical and behavioral complexity. Insights from comparative biology suggest that basal Cambrian T. pedum animals already possessed the anatomical, neurological, and genetic complexity needed to enable the body plan and behavioral diversification recorded by younger Cambrian fossils.

Geochemical support for a climbing habit within the Paleozoic seed fern genus Medullosa

A long-standing problem in paleobotany is the accurate identification of the growth habits and statures of fossil plants. Tissue-specific analysis of stable carbon isotope ratios in plant fossils can provide an independent perspective on this issue. Lignin, a fundamental biopolymer providing structural support in plant tissues and the second most abundant organic material in plants, is 13C depleted by several parts per thousand, averaging 4.1‰, relative to other plant constructional materials (e.g. cellulose). With this isotopic difference, the biochemical structural composition of ancient plants (and inferred stature) can be interrogated using microscale in situ isotope analysis between different tissues in fossils. We applied this technique to a well-preserved specimen of the Late Paleozoic seed plant Medullosa, an extinct genus with a variety of growth habits that includes several enigmatic yet abundant small-stemmed species widely found in calcium carbonate concretions (“coal balls”) in the Pennsylvanian coal beds of Iowa, USA. It remains unclear which of the medullosans were freestanding, and recent analysis of the medullosan vascular system has shown that this system provided little structural support to the whole plant. The leading hypothesis for small-stemmed medullosan specimens predicts that cortical tissues could have provided additional structural support, but only if they were lignified. The expected isotopic difference between lignified tissue and unlignified tissue is smaller than that expected from pure extracts, for the simple reason that even woody tissues maximally contain 40% lignin (by mass). This reduces the expected maximum difference between weakly and heavily lignified tissues by 60%, down to ∼0.5‰–2‰. Analysis of the medullosan stem reveals a consistent difference in isotope ratios of 0.7‰–1.0‰ between lignified xylem and cortical tissues. This implies low abundances of lignin (between 0% and 11%) within the cortex. This inferred structural biochemistry supports hypotheses that the peripheral portions of these medullosan stems were not biomechanically reinforced to permit the plants to grow as freestanding, arborescent trees. A number of climbing or scandent medullosans have been identified in the fossil record, and this mode of growth has been suggested to be common within the group on the basis of observations from comparative biomechanics, hydraulics, and development. Finally, this mode of growth is common in several clades of stem group seed plants, including Lyginopteris and Callistophyton, along with Medullosa. This study provides further support for ideas that place a great portion of early seed plant diversity under the canopy, rather than forming it.

Hydraulics of Asteroxylon mackei, an early Devonian vascular plant, and the early evolution of water transport tissue in terrestrial plants

The core of plant physiology is a set of functional solutions to a tradeoff between CO(2) acquisition and water loss. To provide an important evolutionary perspective on how the earliest land plants met this tradeoff, we constructed a mathematical model (constrained geometrically with measurements of fossils) of the hydraulic resistance of Asteroxylon, an Early Devonian plant. The model results illuminate the water transport physiology of one of the earliest vascular plants. Results show that Asteroxylons vascular system contains cells with low hydraulic resistances; these resistances are low because cells were covered by scalariform pits, elliptical structures that permit individual cells to have large areas for water to pass from one cell to another. Asteroxylon could move a large amount of water quickly given its large pit areas; however, this would have left these plants particularly vulnerable to damage from excessive evapotranspiration. These results highlight a repeated pattern in plant evolution, wherein the evolution of highly conductive vascular tissue precedes the appearance of adaptations to increase water transport safety. Quantitative insight into the vascular transport of Asteroxylon also allows us to reflect on the quality of CO(2) proxy estimates based on early land plant fossils. Because Asteroxylons vascular tissue lacked any safety features to prevent permanent damage, it probably used stomatal abundance and behavior to prevent desiccation. If correct, low stomatal frequencies in Asteroxylon reflect the need to limit evapotranspiration, rather than adaptation to high CO(2) concentrations in the atmosphere. More broadly, methods to reveal and understand water transport in extinct plants have a clear use in testing and bolstering fossil plant-based paleoclimate proxies.