Early angiosperm evolution, beginning approximately 140 million years ago, saw many innovations that enabled flowering plants to alter ecosystems globally. These included the development of novel, ...flower-based pollinator attraction mechanisms and the development of increased water transport capacity in stems and leaves. Vein length per area (VLA) of leaves increased nearly threefold in the first 30–40 million years of angiosperm evolution, increasing the capacity for transpiration and photosynthesis. In contrast to leaves, high water transport capacities in flowers may not be an advantage because flowers do not typically contribute to plant carbon gain. Although flowers of extant basal angiosperms are hydrated by the xylem, flowers of more recently derived lineages may be hydrated predominantly by the phloem. In the present study, we measured leaf and flower VLA for a phylogenetically diverse sample of 132 species from 52 angiosperm families to ask (i) whether flowers have lower VLA than leaves, (ii) whether flowers of basal angiosperm lineages have higher VLA than more recently derived lineages because of differences between xylem and phloem hydration, and (iii) whether flower and leaf VLA evolved independently. It was found that floral structures had lower VLA than leaves, but basal angiosperm flowers did not have higher VLA than more derived lineages. Furthermore, the independent evolution of leaf and petal VLA suggested that these organs may be developmentally modular. Unlike leaves, which have experienced strong selection for increased water transport capacity, flowers may have been shielded from such selective pressures by different developmental processes controlling VLA throughout the plant bauplan.
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.
Why the leaves of cold temperate deciduous and moisture-loving angiosperms are so often toothed has long puzzled biologists because the functional consequences of teeth remain poorly understood. Here ...we provide functional and structural evidence that marginal leaf teeth of Chloranthus japonicus, an understory herb, enable the release of guttation sap during root pressure. When guttation from teeth hydathodes was experimentally blocked, we found that the leaf intercellular airspaces became flooded. Measurements of chlorophyll a fluorescence revealed that internal flooding resulted in an inhibition of photosynthesis, most likely through the formation of a film of water within the leaf that reduced CO2 diffusion. Comparing a developmental series of leaves with and without teeth experimentally covered with wax, we found that teeth did not affect overall leaf stomatal conductance and CO2 uptake. However, maximal and effective light-saturation PSII quantum yields of teeth were found to be lower or equal to the surrounding lamina throughout leaf ontogeny. Collectively, our results suggest hydathodes and their development on teeth apices enable the avoidance of mesophyll flooding by root pressure. We discuss how these new findings bear on the potential physiological interpretations of models that apply leaf marginal traits to infer ancient climates.
Gnetum (Gnetales) species are suggested to be unique extant gymnosperms that have acquired high photosynthetic and transpiration capacities as well as greater xylem hydraulic capacity and efficiency ...compared with all other extant gymnosperms. This is because Gnetum is the only extant gymnosperm lineage that combines vessels, broad pinnate-veined leaves and an ecological distribution in wet, productive lowland tropical rainforest habitats. Yet, field-based observations on the group's ecophysiological performance are lacking. To test a hypothesis that Gnetum species are ecophysiologically analogous to light-demanding woody tropical angiosperms, stem xylem hydraulic performance, photosynthesis and stomatal conductance were investigated in Gnetum as compared with a diverse group of co-occurring woody plants in a lowland tropical rainforest. It was found that Gnetum species combined low photosynthetic capacity and low stomatal conductances with a low stem water transport ability. The physiological observations are consistent with the general occurrence of Gnetum species in shady, primary forest habitats. These results on Gnetum ecophysiology indicate that the coupling of vessels, broad pinnate-veined leaves and the liana habit do not signal the evolution of a highly opportunistic, light-demanding life history in gymnosperms.
The effect of freezing on stem xylem hydraulic conductivity and leaf chlorophyll a fluorescence was measured in 12 tree and shrub species from a treeline heath in Tasmania, Australia. Reduction in ...stem hydraulic conductivity after a single freeze-thaw cycle was minimal in conifers and the vessel-less angiosperm species Tasmannia lanceolata (Winteraceae), whereas mean loss of conductivity in vessel-forming angiosperms fell in the range 17-83%. A positive linear relationship was observed between percentage loss of hydraulic conductivity by freeze-thaw and the average conduit diameter across all 12 species. This supports the hypothesis that large-diameter vascular conduits have a greater likelihood of freeze-thaw cavitation because larger bubbles are produced, which are more likely to expand under tension. Leaf frost tolerances, as measured by a 50% loss of maximum PSII quantum yield, varied from -6 to -13°C, indicating that these species were more frost-sensitive than plants from northern hemisphere temperate forest and treeline communities. There was no evidence of a relationship between frost tolerance of leaves and the resilience of stem water transport to freezing, suggesting that low temperature survival and the resistance of stem water transport to freezing are independently evolving traits. The results of this study bear on the ecological importance of stem freezing in the southern hemisphere treeline zones.
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•Canellaceae phylogeny with broad sampling.•Phylogenetics provide basis for amended systematics of Canellaceae genera.•Spatio-temporal origin of Canellaceae post-dates Gondwana ...breakup.•Long-distance dispersal events are recovered from the New to the Old World.•Nuclear gene provides information toward resolving low sequence divergence.
Canellales, a clade consisting of Winteraceae and Canellaceae, represent the smallest order of magnoliid angiosperms. The clade shows a broad distribution throughout the Southern Hemisphere, across a diverse range of dry to wet tropical forests. In contrast to their sister-group, Winteraceae, the phylogenetic relations and biogeography within Canellaceae remain poorly studied. Here we present the phylogenetic relationships of all currently recognized genera of Canellales with a special focus on the Old World Canellaceae using a combined dataset consisting of the chloroplast trnK-matK-trnK-psbA and the nuclear single copy gene mag1 (Maigo 1). Within Canellaceae we found high statistical support for the monophyly of Warburgia and Cinnamosma. However, we also found relationships that differ from previous studies. Cinnamodendron splitted into two clades, a South American clade and a second clade confined to the Antilles and adjacent areas. Cinnamodendron from the Antilles, as well as Capsicodendron, South American Cinnamodendron and Pleodendron were not monophyletic. Consequently, Capsicodendron should be included in the South American Cinnamodendron clade and the genus Pleodendron merged with the Cinnamodendron clade from the Antilles. We also found that Warburgia (restricted to mainland eastern Africa) together with the South American Cinnamodendron and Capsicodendron are sister to the Malagasy genus Cinnamosma. In addition to the unexpected geographical relationships, both biogeographic and molecular clock analyses suggest vicariance, extinction, and at least one intercontinental long-distance-dispersal event. Our dating result contrasts previous work on Winteraceae. Diversification of Winteraceae took place in the Paleocene, predating the Canellaceae diversification by 13 MA in the Eocene. The phylogenetic relationships for Canellaceae supported here offer a solid framework for a future taxonomic revision of the Canellaceae.
Gaps between molecular ages and fossils undermine the validity of time-calibrated molecular phylogenies. An example of the time gap surrounds the age of angiosperms' origin. We calculate molecular ...ages of the earliest flowering plant lineages using 22 fossil calibrations (101 genera, 40 families). Our results reveal the origin of angiosperms at the late Permian, ∼275 million years ago. Different prior probability curves of molecular age calculations on dense calibration point distributions had little effect on overall age estimates compared to the effects of altered calibration points. The same is true for reasonable root age constraints. We conclude that our age estimates based on multiple datasets, priors, and calibration points are robust and the true ages are likely between our extremes. Our results, when integrated with the ecophysiological evolution of early angiosperms, imply that the ecology of the earliest angiosperms is critical to understand the pre-Cretaceous evolution of flowering plants.
The flowering plants - angiosperms - appeared during the Early Cretaceous period and within 10-30 Myr dominated the species composition of many floras worldwide. Emerging insights into the ...phylogenetics of development and discoveries of early angiosperm fossils are shedding increased light on the patterns and processes of early angiosperm evolution. However, we also need to integrate ecology, in particular how early angiosperms established a roothold in pre-existing Mesozoic plant communities. These events were critical in guiding subsequent waves of angiosperm diversification during the Aptian-Albian. Previous pictures of the early flowering plant ecology have been diverse, ranging from large tropical rainforest trees, weedy drought-adapted and colonizing shrubs, disturbance- and sun-loving rhizomatous herbs, and, more recently, aquatic herbs; however, none of these images were tethered to a robust hypothesis of angiosperm phylogeny. Here, we synthesize our current understanding of early angiosperm ecology, focusing on patterns of functional ecology, by merging recent molecular phylogenetic studies and functional studies on extant 'basal angiosperms' with the picture of early angiosperm evolution drawn by the fossil record.
We investigated phloem-xylem interactions in Acer rubrum L. and Acer saccharum Marsh. Our experimental method allowed us to determine xylem conductance of an intact branch by measuring the flow rate ...of water supplied at two delivery pressures to the cut end of a small side branch. We found that removal of bark tissue (phloem girdling) upstream of the point at which deionized water was delivered to the branch resulted in a decrease (24% for A. rubrum and 15% for A. saccharum) in branch xylem hydraulic conductance. Declines in hydraulic conductance with girdling were accompanied by a decrease in the osmotic concentration of xylem sap. The decrease in xylem sap concentration following phloem girdling suggests that ion redistribution from the phloem was responsible for the observed decline in hydraulic conductance. When the same measurements were made on branches perfused with KCl solution (~140 mOsm kg-1), phloem girdling had no effect on xylem hydraulic conductance. These results suggest a functional link between phloem and xylem hydraulic systems that is mediated by changes in the ionic content of the cell sap.
Flowering depends upon long-distance transport to supply water for reproductive mechanisms to function. Previous physiological studies suggested that flowers operated uncoupled from stem xylem ...transport and received water primarily from the phloem. We demonstrate that the water balance of Southern magnolia (Magnolia grandiflora) flowers is regulated in a manner opposite from that of previously examined flowers. We show that flowers of Southern magnolia rely upon relatively efficient xylem hydraulic transport to support high water demand during anthesis. We measured rapid rates of perianth transpiration ranging from twice to 100 times greater than previous studies. We found that relatively efficient xylem pathways existed between the xylem and flower. Perianth hydraulic conductance and the amount of xylem to transpirational surface area ratios of flowers were both approximately one-third those measured for leafy shoots. Furthermore, we observed that perianth tissues underwent significant diurnal depressions in water status during transpiring conditions. Decreases in water potential observed between flowers and vegetative tissues were consistent with water moving from the stem xylem into the flower during anthesis. Xylem hydraulic coupling of flowers to the stem was supported by experiments showing that transpiring flowers were unaffected by bark girdling. With Southern magnolia being a member of a nearly basal evolutionary lineage, our results suggest that flower water balance represents an important functional dimension that influenced early flower evolution.
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