The flowering plants that dominate modern vegetation possess leaf gas exchange potentials that far exceed those of all other living or extinct plants. The great divide in maximal ability to exchange CO 2 for water between leaves of nonangiosperms and angiosperms forms the mechanistic foundation for speculation about how angiosperms drove sweeping ecological and biogeochemical change during the Cretaceous. However, there is no empirical evidence that angiosperms evolved highly photosynthetically active leaves during the Cretaceous. Using vein density (D V ) measurements of fossil angiosperm leaves, we show that the leaf hydraulic capacities of angiosperms escalated severalfold during the Cretaceous. During the first 30 million years of angiosperm leaf evolution, angiosperm leaves exhibited uniformly low vein D V that overlapped the D V range of dominant Early Cretaceous ferns and gymnosperms. Fossil angiosperm vein densities reveal a subsequent biphasic increase in D V . During the first mid-Cretaceous surge, angiosperm D V first surpassed the upper bound of D V limits for nonangiosperms. However, the upper limits of D V typical of modern megathermal rainforest trees first appear during a second wave of increased D V during the Cretaceous-Tertiary transition. Thus, our findings provide fossil evidence for the hypothesis that significant ecosystem change brought about by angiosperms lagged behind the Early Cretaceous taxonomic diversification of angiosperms.angiosperm evolution | plant evolution | transpiration | tropical rainforest | venation P hotosynthesis and transpiration by leaves fundamentally influence the cycling of carbon and water in the terrestrial realm. Consequently, evolutionary changes in the rates at which leaves exchange water for carbon bear on the origin and maintenance of biodiversity by varying the size and resource stoichiometry of the primary productivity base. How leaves exchange gases also shape climate and atmospheric gas composition by changing the amounts of water vapor and carbon in the atmosphere (1-3). Recent evidence has suggested that the evolution of flowering plants involved a sharp rise in the capacity of leaves to transport water and extract CO 2 from the atmosphere (4, 5).The evolution of unrivaled CO 2 uptake and transpirational output by angiosperm leaves form the mechanistic cornerstone for a multitude of hypotheses citing angiosperms as agents of expansive ecosystem change during the Cretaceous (6-8). These hypotheses include (i) intensified mineral weathering by angiosperms that decreased global atmospheric CO 2 concentration; (ii) heightened transpirational input to the atmosphere that increased regional rainfall and favored the spread and diversity of tropical rainforest vegetation; (iii) the nearly complete competitive exclusion by angiosperms of diverse gymnosperms and ferns from high-productivity sites worldwide; and (iv) the spread of novel fire regimes that entrained a positive feedback on angiosperm takeover (3,4,6,(9)(10)(11)(12)(13)(14)(15).
C 4 photosynthesis is a series of anatomical and biochemical modifications to the typical C 3 pathway that increases the productivity of plants in warm, sunny, and dry conditions. Despite its complexity, it evolved more than 62 times independently in flowering plants. However, C 4 origins are absent from most plant lineages and clustered in others, suggesting that some characteristics increase C 4 evolvability in certain phylogenetic groups. The C 4 trait has evolved 22-24 times in grasses, and all origins occurred within the PACMAD clade, whereas the similarly sized BEP clade contains only C 3 taxa. Here, multiple foliar anatomy traits of 157 species from both BEP and PACMAD clades are quantified and analyzed in a phylogenetic framework. Statistical modeling indicates that C 4 evolvability strongly increases when the proportion of vascular bundle sheath (BS) tissue is higher than 15%, which results from a combination of short distance between BS and large BS cells. A reduction in the distance between BS occurred before the split of the BEP and PACMAD clades, but a decrease in BS cell size later occurred in BEP taxa. Therefore, when environmental changes promoted C 4 evolution, suitable anatomy was present only in members of the PACMAD clade, explaining the clustering of C 4 origins in this lineage. These results show that key alterations of foliar anatomy occurring in a C 3 context and preceding the emergence of the C 4 syndrome by millions of years facilitated the repeated evolution of one of the most successful physiological innovations in angiosperm history.precursor | preadaptation | phylogeny | Poaceae
Clarifying the evolution and mechanisms for photosynthetic productivity is a key to both improving crops and understanding plant evolution and habitat distributions. Current theory recognizes a role for the hydraulics of water transport as a potential determinant of photosynthetic productivity based on comparative data across disparate species. However, there has never been rigorous support for the maintenance of this relationship during an evolutionary radiation. We tested this theory for 30 species of Viburnum, diverse in leaf shape and photosynthetic anatomy, grown in a common garden. We found strong support for a fundamental requirement for leaf hydraulic capacity (Kleaf) in determining photosynthetic capacity (Amax), as these traits diversified across this lineage in tight coordination, with their proportionality modulated by the climate experienced in the species' range. Variation in Kleaf arose from differences in venation architecture that influenced xylem and especially outside-xylem flow pathways. These findings substantiate an evolutionary basis for the coordination of hydraulic and photosynthetic physiology across species, and their co-dependence on climate, establishing a fundamental role for water transport in the evolution of the photosynthetic rate.
Today, angiosperms are fundamental players in the diversity and biogeochemical functioning of the planet. Yet despite the omnipresence of angiosperms in today's ecosystems, the basic evolutionary understanding of how the earliest angiosperms functioned remains unknown. Here we synthesize ecophysiological, paleobotanical, paleoecological, and phylogenetic lines of evidence about early angiosperms and their environments. In doing so, we arrive at a hypothesis that early angiosperms evolved in evermoist tropical terrestrial habitats, where three of their emblematic innovations - including net-veined leaves, xylem vessels, and flowers - found ecophysiological advantages. However, the adaptation of early angiosperm ecophysiology to wet habitats did not initially promote massive diversification and ecological dominance. Instead, wet habitats were permissive for the ecological roothold of the clade, a critical phase of early diversification that entailed experimentation with a range of functional innovations in the leaves, wood, and flowers. Later, our results suggest that some of these innovations were co-opted gradually for new roles in the evolution of greater productivity and drought tolerance, which are characteristics seen across the vast majority of derived and ecologically dominant angiosperms today.
Adaptation to changing environments often requires novel traits, but how such traits directly affect the ecological niche remains poorly understood. Multiple plant lineages have evolved C4 photosynthesis, a combination of anatomical and biochemical novelties predicted to increase productivity in warm and arid conditions. Here, we infer the dispersal history across geographical and environmental space in the only known species with both C4 and non-C4 genotypes, the grass Alloteropsis semialata. While non-C4 individuals remained confined to a limited geographic area and restricted ecological conditions, C4 individuals dispersed across three continents and into an expanded range of environments, encompassing the ancestral one. This first intraspecific investigation of C4 evolutionary ecology shows that, in otherwise similar plants, C4 photosynthesis does not shift the ecological niche, but broadens it, allowing dispersal into diverse conditions and over long distances. Over macroevolutionary timescales, this immediate effect can be blurred by subsequent specialisation towards more extreme niches.
Strong latitudinal patterns in leaf form are well documented in floristic comparisons and palaeobotanical studies. However, there is little agreement about their functional significance; in fact, it is still unknown to what degree these patterns were generated by repeated evolutionary adaptation. We analysed leaf form in the woody angiosperm clade Viburnum (Adoxaceae) and document evolutionarily correlated shifts in leafing habit, leaf margin morphology, leaf shape and climate. Multiple independent shifts between tropical and temperate forest habitats have repeatedly been accompanied by a change between evergreen, elliptical leaves with entire margins and deciduous, more rounded leaves with toothed or lobed margins. These consistent shifts in Viburnum support repeated evolutionary adaptation as a major determinant of the global correlation between leaf form and mean annual temperature. Our results provide a new theoretical grounding for the inference of past climates using fossil leaf assemblages.
Summary1. The leaf economics spectrum (LES) has been an organizing framework of plant functional ecology for the past decade. The LES describes a set of trade-offs among traits related to plant carbon balance. Species with a long leaf life span (LLS) invest additional material for leaf protection and structural support and consequently tend to have a lower leaf photosynthetic rate per unit mass than species with a shorter LLS. 2. While the LES is most apparent in comparing species with extreme differences in their traits, it has nonetheless been adopted as a general explanation of leaf trait variation at all scales and in all plants. It highlights the 'trait-based' approach to plant ecology, which has generally used a small set of traits to predict whole organism and even whole ecosystem attributes. Few studies have investigated the relationships between LES traits and organismal attributes not directly related to carbon economy. 3. We explored the LES in 32 deciduous woody species of Viburnum (Adoxaceae). We found no evidence for any mass-based LES trade-offs. Rather, on an area basis, photosynthetic rates were positively correlated with leaf mass per area (LMA); higher LMA was associated with greater investment in photosynthetic tissue, with most of the variation due to changes in the thickness of photosynthetic mesophyll. 4. Species' mean LLS varied between 19 and 26 weeks and was not correlated with other LES traits. Instead, LLS was strongly associated with the diverse set of whole-plant branching patterns in Viburnum. In the most common growth pattern, LLS was significantly correlated with flowering time, because branches end in terminal inflorescences, and all leaves and inflorescences are preformed in overwintering buds. 5. Synthesis. Plants may recover the cost of their leaves early in the growing season, allowing LLS to vary independently of the plant carbon budget. In deciduous species, LLS may be strongly influenced by whole plant architecture, which, in Viburnum, is evolutionarily conserved. In general, positive area-based LES trait relationships will limit the relevance of LLS to this spectrum and allow LLS to vary for reasons that are not directly related to carbon economy.
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.Sexual reproduction is the primary function of the flower. Most investigations of how flowers orchestrate reproductive processes have focused on developmental biology and biochemical mechanisms operating inside flowers (Franklin-Tong and Franklin, 2003;Glover, 2007). Although such approaches have been successful in understanding the inner workings of flowers, the function of flowers is linked to processes operating in the rest of the plant (Galen, 2005;Lambrecht and Dawson, 2007). As such, the physiological mechanisms that make reproduction possible in the face of environmental stresses are best understood through studies that integrate reproductive and vegetative physiology.
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