C. Kevin Boyce

Angiosperm leaf vein evolution was physiologically and environmentally transformative

The veins that irrigate leaves during photosynthesis are demonstrated to be strikingly more abundant in flowering plants than in any other vascular plant lineage. Angiosperm vein densities average 8 mm of vein per mm2 of leaf area and can reach 25 mm mm−2, whereas such high densities are absent from all other plants, living or extinct. Leaves of non-angiosperms have consistently averaged close to 2 mm mm−2 throughout 380 million years of evolution despite a complex history that has involved four or more independent origins of laminate leaves with many veins and dramatic changes in climate and atmospheric composition. We further demonstrate that the high leaf vein densities unique to the angiosperms enable unparalleled transpiration rates, extending previous work indicating a strong correlation between vein density and assimilation rates. Because vein density is directly measurable in fossils, these correlations provide new access to the physiology of extinct plants and how they may have impacted their environments. First, the high assimilation rates currently confined to the angiosperms among living plants are likely to have been unique throughout evolutionary history. Second, the transpiration-driven recycling of water that is important for bolstering precipitation in modern tropical rainforests might have been significantly less in a world before the angiosperms.

The evolution and functional significance of leaf shape in the angiosperms

Angiosperm leaves manifest a remarkable diversity of shapes that range from developmental sequences within a shoot and within crown response to microenvironment to variation among species within and between communities and among orders or families. It is generally assumed that because photosynthetic leaves are critical to plant growth and survival, variation in their shape reflects natural selection operating on function. Several non-mutually exclusive theories have been proposed to explain leaf shape diversity. These include: thermoregulation of leaves especially in arid and hot environments, hydraulic constraints, patterns of leaf expansion in deciduous species, biomechanical constraints, adaptations to avoid herbivory, adaptations to optimise light interception and even that leaf shape variation is a response to selection on flower form. However, the relative importance, or likelihood, of each of these factors is unclear. Here we review the evolutionary context of leaf shape diversification, discuss the proximal mechanisms that generate the diversity in extant systems, and consider the evidence for each the above hypotheses in the context of the functional significance of leaf shape. The synthesis of these broad ranging areas helps to identify points of conceptual convergence for ongoing discussion and integrated directions for future research.

Forest productivity and water stress in Amazonia: observations from GOSAT chlorophyll fluorescence

It is unclear to what extent seasonal water stress impacts on plant productivity over Amazonia. Using new Greenhouse gases Observing SATellite (GOSAT) satellite measurements of sun-induced chlorophyll fluorescence, we show that midday fluorescence varies with water availability, both of which decrease in the dry season over Amazonian regions with substantial dry season length, suggesting a parallel decrease in gross primary production (GPP). Using additional SeaWinds Scatterometer onboard QuikSCAT satellite measurements of canopy water content, we found a concomitant decrease in daily storage of canopy water content within branches and leaves during the dry season, supporting our conclusion. A large part (r2 = 0.75) of the variance in observed monthly midday fluorescence from GOSAT is explained by water stress over moderately stressed evergreen forests over Amazonia, which is reproduced by model simulations that include a full physiological representation of photosynthesis and fluorescence. The strong relationship between GOSAT and model fluorescence (r2 = 0.79) was obtained using a fixed leaf area index, indicating that GPP changes are more related to environmental conditions than chlorophyll contents. When the dry season extended to drought in 2010 over Amazonia, midday basin-wide GPP was reduced by 15 per cent compared with 2009.

Evolution of developmental potential and the multiple independent origins of leaves in Paleozoic vascular plants

Abstract Four vascular plant lineages, the ferns, sphenopsids, progymnosperms, and seed plants, evolved laminated leaves in the Paleozoic. A principal coordinate analysis of 641 leaf species from North American and European floras ranging in age from Middle Devonian through the end of the Permian shows that the clades followed parallel trajectories of evolution: each clade exhibits rapid radiation of leaf morphologies from simple (and similar) forms in the Late Devonian/Early Carboniferous to diverse, differentiated leaf forms, with strong constraint on further diversification beginning in the mid Carboniferous. Similar morphospace trajectories have been documented in studies of morphological evolution in animals; however, plant fossils present unique opportunities for understanding the developmental processes that underlie such patterns. Detailed comparison of venation in Paleozoic leaves with that of modern leaves for which developmental mechanisms are known suggests developmental interpretations for the origination and early evolution of leaves. The parallel evolution of a marginal meristem by the modification of developmental mechanisms available in the common ancestor of all groups resulted in the pattern of leaf evolution repeated by each clade. Early steps of leaf evolution were followed by constraint on further diversification as the possible elaborations of marginal growth were exhausted. Hypotheses of development in Paleozoic leaves can be tested by the study of living plants with analogous leaf morphologies.

An exceptional role for flowering plant physiology in the expansion of tropical rainforests and biodiversity

Movement of water from soil to atmosphere by plant transpiration can feed precipitation, but is limited by the hydraulic capacities of plants, which have not been uniform through time. The flowering plants that dominate modern vegetation possess transpiration capacities that are dramatically higher than any other plants, living or extinct. Transpiration operates at the level of the leaf, however, and how the impact of this physiological revolution scales up to the landscape and larger environment remains unclear. Here, climate modelling demonstrates that angiosperms help ensure aseasonally high levels of precipitation in the modern tropics. Most strikingly, replacement of angiosperm with non-angiosperm vegetation would result in a hotter, drier and more seasonal Amazon basin, decreasing the overall area of ever-wet rainforest by 80 per cent. Thus, flowering plant ecological dominance has strongly altered climate and the global hydrological cycle. Because tropical biodiversity is closely tied to precipitation and rainforest area, angiosperm climate modification may have promoted diversification of the angiosperms themselves, as well as radiations of diverse vertebrate and invertebrate animal lineages and of epiphytic plants. Their exceptional potential for environmental modification may have contributed to divergent responses to similar climates and global perturbations, like mass extinctions, before and after angiosperm evolution.

Organic Chemical Differentiation Within Fossil Plant Cell Walls Detected with X-ray Spectromicroscopy

Organic matter preserved in cell walls of permineralized plant fossils was analyzed by using scanning transmission X-ray microscopy and spectroscopy at energies near the 1s absorption edge of carbon. Microchemical analyses were performed directly on cellulose acetate peels of the fossils, preserving information on the anatomical distribution of organic materials. Individual tracheid walls in both Eocene and Early Devonian fossils exhibit spatially distinct chemical zoning inherited from original wall biopolymers and cell-wall microstructure. Molecular analysis of submicrometer domains using carbon X-ray absorption near-edge spectroscopy documents the differential distribution of hydroxylated aromatic and alcohol (and/or ether) carbon in the inner and outer regions of tracheid walls. This zonation reflects the deposition of lignin and structural polysaccharides in Devonian plants, indicating biochemical and developmental pathways similar to those of living tracheophytes.

CHEMICAL EVIDENCE FOR CELL WALL LIGNIFICATION AND THE EVOLUTION OF TRACHEIDS IN EARLY DEVONIAN PLANTS

Anatomically preserved land plant fossils from the Lower Devonian Rhynie Chert contain conducting tissues with cells that range from dark‐colored, elongated cells without secondary wall thickenings to tracheids similar to those of extant tracheophytes. A suite of tissue‐specific microanalytical techniques was used to assess lignification in fossils of Aglaophyton, Rhynia, and Asteroxylon. Isotope ratio mass spectrometry provides millimeter‐scale resolution of carbon isotopic abundances, whereas soft X‐ray carbon (1s) spectromicroscopy provides micrometer‐scale resolution of the preservation of organic molecular functionality. The isotopic and organic chemistry of Rhynie Chert plants indicates that the earliest vascular thickenings were probably unlignified and that cell wall lignification may have first appeared in the outer cortex. Only in more derived plants, it seems, was lignin deposited in conducting cells to produce the true tracheids seen today in vascular plants.

Patterns of segregation and convergence in the evolution of fern and seed plant leaf morphologies

Abstract Global information on Paleozoic, Mesozoic, and extant non-angiosperm leaf morphologies has been gathered to investigate morphological diversity in leaves consistent with marginal growth and to identify likely departures from such development. Two patterns emerge from the principal coordinates analysis of this data set: (1) the loss of morphological diversity associated with marginal leaf growth among seed plants after sharing the complete Paleozoic range of such morphologies with ferns and (2) the repeated evolution of more complex, angiosperm-like leaf traits among both ferns and seed plants. With regard to the first pattern, morphological divergence of fern and seed plant leaf morphologies, indirectly recognized as part of the Paleophytic-Mesophytic transition, likely reflects reproductive and ecological divergence. The leaf-borne reproductive structures that are common to the ferns and Paleozoic seed plants may promote leaf morphological diversity, whereas the separation of vegetative and reproductive roles into distinct organs in later seed plant groups may have allowed greater functional specialization—and thereby morphological simplification—as the seed plants came to be dominated by groups originating in more arid environments. With regard to the second pattern, the environmental and ecological distribution of angiosperm-like leaf traits among fossil and extant plants suggests that these traits preferentially evolve in herbaceous to understory plants of warm, humid environments, thus supporting inferences concerning angiosperm origins based upon the ecophysiology of basal extant taxa.

Devonian Landscape Heterogeneity Recorded by a Giant Fungus

The enigmatic Paleozoic fossil Prototaxites [Dawson 1859][1] consists of tree-like trunks as long as 8 m constructed of interwoven tubes <50 mm in diameter. Prototaxites specimens from five localities differ from contemporaneous vascular plants by exhibiting a carbon isotopic range, within and between localities, of as much as 13‰ δ13C. Pyrolysis–gas chromatography–mass spectrometry highlights compositional differences between Prototaxites and co-occurring plant fossils and supports interpretation of isotopic distinctions as biological rather than diagenetic in origin. Such a large isotopic range is difficult to reconcile with an autotrophic metabolism, suggesting instead that, consistent with anatomy-based interpretation as a fungus, Prototaxites was a heterotroph that lived on isotopically heterogeneous substrates. Light isotopic values of Prototaxites approximate those of vascular plants from the same localities; in contrast, heavy extremes seen in the Lower Devonian appear to reflect consumption of primary producers with carbon-concentrating mechanisms, such as cryptobiotic soil crusts, or possibly bryophytes. Prototaxites biogeochemistry thus suggests that a biologically heterogeneous mosaic of primary producers characterized land surfaces well into the vascular plant era. [1]: #ref-10

How green was Cooksonia? The importance of size in understanding the early evolution of physiology in the vascular plant lineage

Abstract Because of the fragmentary preservation of the earliest Cooksonia-like terrestrial plant macrofossils, younger Devonian fossils with complete anatomical preservation and documented gametophytes often have received greater attention concerning the early evolution of vascular plants and the alternation of generations. Despite preservational deficits, however, possible physiologies of Cooksonia-like fossils can be constrained by considering the overall axis size in conjunction with the potential range of cell types and sizes, because their lack of organ differentiation requires that all plant functions be performed by the same axis. Once desiccation resistance, support, and transport functions are taken into account, smaller fossils do not have volume enough left over for an extensive aerated photosynthetic tissue, thus arguing for physiological dependence on an unpreserved gametophyte. As in many mosses, axial anatomy is more likely to have ensured continued spore dispersal despite desiccation of the sporophyte than to have provided photosynthetic independence. Suppositions concerning size constraints on physiology are supported by size comparisons with fossils of demonstrable physiological independence, by preserved anatomical detail, and by size correlations between axis, sporangia, and sporangial stalk in Silurian and Early Devonian taxa. Several Cooksonia-like taxa lump fossils with axial widths spanning over an order of magnitude—from necessary physiological dependence to potential photosynthetic competence—informing understanding of the evolution of an independent sporophyte and the phylogenetic relationships of early vascular plants.