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The fact that angiosperms are so species-rich and ecologically diverse – Darwin’s second abominable mystery – could be explained by their ability to ‘reinvent’ themselves by evolving functional traits repeatedly over time, space and taxonomic clades. These trait innovations may facilitate adaptation and increase diversification rates. In this article, I quantify this ‘trait flexibility’ by reviewing the literature on trait transition rates and trait-dependent diversification rates in angiosperms and their extant sister clade, acrogymnosperms. I show that angiosperms indeed evolved elevated trait transition and trait-dependent diversification rates compared to gymnosperms, and rates are highest within species-rich angiosperm orders (e.g. Fabales, Lamiales). The (genetic) ability of certain angiospermlineages to repeatedly evolve adaptive traits may have facilitated sustained high net diversification resulting from numerous episodic radiations.

Climate change-driven increases in drought frequency and severity could compromise forest ecosystems and the terrestrial carbon sink1–3. While the impacts of single droughts on forests have been widely studied4–6, understanding whether forests acclimate to or become more vulnerable to sequential droughts remains largely unknown and is crucial for predicting future forest health. We combine cross-biome datasets of tree growth, tree mortality and ecosystem water content to quantify the effects of multiple droughts at a range of scales from individual trees to the globe from 1900 to 2018. We find that subsequent droughts generally have a more deleterious impact than initial droughts, but this effect differs enormously by clade and ecosystem, with gymnosperms and conifer-dominated ecosystems more often exhibiting increased vulnerability to multiple droughts. The differential impacts of multiple droughts across clades and biomes indicate that drought frequency changes may have fundamentally different ecological and carbon-cycle consequences across ecosystems.Drought frequency will probably increase under climate change, posing a potential risk to forests. Forest response is variable, but subsequent droughts generally have a negative impact at the tree and ecosystem scales, with systems dominated by conifers particularly vulnerable.

Severe droughts have the potential to reduce forest productivity and trigger tree mortality. Most trees face several drought events during their life and therefore resilience to dry conditions may be crucial to long-term survival. We assessed how growth resilience to severe droughts, including its components resistance and recovery, is related to the ability to survive future droughts by using a tree-ring database of surviving and now-dead trees from 118 sites (22 species, >3,500 trees). We found that, across the variety of regions and species sampled, trees that died during water shortages were less resilient to previous non-lethal droughts, relative to coexisting surviving trees of the same species. In angiosperms, drought-related mortality risk is associated with lower resistance (low capacity to reduce impact of the initial drought), while it is related to reduced recovery (low capacity to attain pre-drought growth rates) in gymnosperms. The different resilience strategies in these two taxonomic groups open new avenues to improve our understanding and prediction of drought-induced mortality.

Sucrose is the end product of photosynthesis and the primary sugar transported in the phloem of most plants. Sucrose synthase (SuSy) is a glycosyl transferase enzyme that plays a key role in sugar metabolism, primarily in sink tissues. SuSy catalyzes the reversible cleavage of sucrose into fructose and either uridine diphosphate glucose (UDP-G) or adenosine diphosphate glucose (ADP-G). The products of sucrose cleavage by SuSy are available for many metabolic pathways, such as energy production, primary-metabolite production, and the synthesis of complex carbohydrates. SuSy proteins are usually homotetramers with an average monomeric molecular weight of about 90 kD (about 800 amino acids long). Plant SuSy isozymes are mainly located in the cytosol or adjacent to plasma membrane, but some SuSy proteins are found in the cell wall, vacuoles, and mitochondria. Plant gene families are usually small, containing between four to seven genes, with distinct exon-intron structures. Plant genes are divided into three separate clades, which are present in both monocots and dicots. A comprehensive phylogenetic analysis indicates that a first duplication event may have occurred before the divergence of the gymnosperms and angiosperms and a second duplication event probably occurred in a common angiosperm ancestor, leading to the existence of all three clades in both monocots and dicots. Plants with reduced SuSy activity have been shown to have reduced growth, reduced starch, cellulose or callose synthesis, reduced tolerance to anaerobic-stress conditions and altered shoot apical meristem function and leaf morphology. Plants overexpressing have shown increased growth, increased xylem area and xylem cell-wall width, and increased cellulose and starch contents, making high-potential candidate genes for the improvement of agricultural traits in crop plants. This review summarizes the current knowledge regarding plant SuSy, including newly discovered possible developmental roles for SuSy in meristem functioning that involve sugar and hormonal signaling.

Biomass allocation in plants is fundamental for understanding and predicting terrestrial carbon storage. Yet, our knowledge regarding warming effects on root: shoot ratio (R/S) remains limited. Here, we present a meta-analysis encompassing more than 300 studies and including angiosperms and gymnosperms as well as different biomes (cropland, desert, forest, grassland, tundra, and wetland). The meta-analysis shows that average warming of 2.50 °C (median = 2 °C) significantly increases biomass allocation to roots with a mean increase of 8.1% in R/S. Two factors associate significantly with this response to warming: mean annual precipitation and the type of mycorrhizal fungi associated with plants. Warming-induced allocation to roots is greater in drier habitats when compared to shoots (+15.1% in R/S), while lower in wetter habitats (+4.9% in R/S). This R/S pattern is more frequent in plants associated with arbuscular mycorrhizal fungi, compared to ectomycorrhizal fungi. These results show that precipitation variability and mycorrhizal association can affect terrestrial carbon dynamics by influencing biomass allocation strategies in a warmer world, suggesting that climate change could influence belowground C sequestration. Biomass allocation in plants is fundamental for understanding and predicting terrestrial carbon storage. Here, the authors conduct a meta-analysis showing that warming effect on plant root:shoot is influenced by precipitation and the type of mycorrhizal fungi associated.

Global vegetation models use conceived relationships between functional traits to simulate ecosystem responses to environmental change. In this context, the concept of the leaf economics spectrum (LES) suggests coordinated leaf trait variation, and separates species which invest resources into short-lived leaves with a high expected energy return rate from species with longer-lived leaves and slower energy return. While it has been assumed that being fast (acquisitive) or slow (conservative) is a general feature for all organ systems, the translation of the LES into a root economics spectrum (RES) for tree species has been hitherto inconclusive. This may be partly due to the assumption that the bulk of tree fine roots have similar uptake functions as leaves, despite the heterogeneity of their environments and resources. In this study we investigated well-established functional leaf and stature traits as well as a high number of fine root traits (14 traits split by different root orders) of 13 dominant or subdominant temperate tree species of Central Europe, representing two phylogenetic groups (gymnosperms and angiosperms) and two mycorrhizal associations (arbuscular and ectomycorrhizal). We found reflected variation in leaf and lower-order root traits in some (surface areas and C:N) but not all (N content and longevity) traits central to the LES. Accordingly, the LES was not mirrored belowground. We identified significant phylogenetic signal in morphological lower-order root traits, i.e., in root tissue density, root diameter, and specific root length. By contrast, root architecture (root branching) was influenced by the mycorrhizal association type which developed independent from phylogeny of the host tree. In structural equation models we show that root branching significantly influences both belowground (direct influence on root C:N) and aboveground (indirect influences on specific leaf area and leaf longevity) traits which relate to resource investment and lifespan. We conclude that branching of lower order roots can be considered a leading root trait of the plant economics spectrum of temperate trees, since it relates to the mycorrhizal association type and belowground resource exploitation; while the dominance of the phylogenetic signal over environmental filtering makes morphological root traits less central for tree economics spectra across different environments.

Studies have demonstrated that pervasive gene tree conflict underlies several important phylogenetic relationships where different species tree methods produce conflicting results. Here, we present a means of dissecting the phylogenetic signal for alternative resolutions within a data set in order to resolve recalcitrant relationships and, importantly, identify what the data set is unable to resolve. These procedures extend upon methods for isolating conflict and concordance involving specific candidate relationships and can be used to identify systematic error and disambiguate sources of conflict among species tree inference methods.We demonstrate these on a large phylogenomic plant data set. Our results support the placement of Amborella as sister to the remaining extant angiosperms, Gnetales as sister to pines, and themonophyly of extant gymnosperms. Several other contentious relationships, including the resolution of relationships within the bryophytes and the eudicots, remain uncertain given the lownumber of supporting gene trees. To address whether concatenation of filtered genes amplified phylogenetic signal for relationships, we implemented a combinatorial heuristic to test combinability of genes. We found that nested conflicts limited the ability of data filtering methods to fully ameliorate conflicting signal amongst gene trees. These analyses confirmed that the underlying conflicting signal does not support broad concatenation of genes. Our approach provides a means of dissecting a specific data set to address deep phylogenetic relationships while also identifying the inferential boundaries of the data set.

Species assemble into communities through ecological and evolutionary processes. Phylogenetic niche conservatism—the tendency of species to retain ancestral ecological distributions—is thought to influence which species from a regional species pool can persist in a particular environment. We analyzed data for seed plants in China to test hypotheses about the distribution of species within regional floras. Of 16 environmental variables, actual evapotranspiration, minimum temperature of the coldest month, and annual precipitation most strongly influenced regional species richness, phylogenetic dispersion, and phylogenetic diversity for both gymnosperms (cone-bearing plants) and angiosperms (flowering plants). For most evolutionary clades at, and above, the family level, the relationships between metrics of phylogenetic dispersion (i.e., average phylogenetic distance among species), or phylogenetic diversity, and the 3 environmental variables were consistent with the tropical niche conservatism hypothesis, which predicts closer phylogenetic relatedness and reduced phylogenetic diversity with increasing environmental stress. The slopes of the relationships between phylogenetic relatedness and the 3 environmental drivers identified in this analysis were steeper for primarily tropical clades, implying greater niche conservatism, than for primarily temperate clades. These observations suggest that the distributions of seed plants across large-scale environmental gradients in China are constrained by conserved adaptations to the physical environment, i.e., phylogenetic niche conservatism.

After decades of molecular phylogenetic studies, the deep phylogeny of gymnosperms has not been resolved, and the phylogenetic placement of Gnetales remains one of the most controversial issues in seed plant evolution. To resolve the deep phylogeny of seed plants and to address the sources of phylogenetic conflict, we conducted a phylotranscriptomic study with a sampling of all 13 families of gymnosperms and main lineages of angiosperms. Multiple datasets containing up to 1 296 042 sites across 1308 loci were analysed, using concatenation and coalescence approaches. Our study generated a consistent and well-resolved phylogeny of seed plants, which places Gnetales as sister to Pinaceae and thus supports the Gnepine hypothesis. Cycads plus Ginkgo is sister to the remaining gymnosperms. We also found that Gnetales and angiosperms have similar molecular evolutionary rates, which are much higher than those of other gymnosperms. This implies that Gnetales and angiosperms might have experienced similar selective pressures in evolutionary histories. Convergent molecular evolution or homoplasy is partially responsible for the phylogenetic conflicts in seed plants. Our study provides a robustly reconstructed backbone phylogeny that is important for future molecular and morphological studies of seed plants, in particular gymnosperms, in the light of evolution.

Competition among species and entire clades can impact species diversification and extinction, which can shape macroevolutionary patterns. The fossil record shows successive biotic turnovers such that a dominant group is replaced by another. One striking example involves the decline of gymnosperms and the rapid diversification and ecological dominance of angiosperms in the Cretaceous. It is generally believed that angiosperms outcompeted gymnosperms, but the macroevolutionary processes and alternative drivers explaining this pattern remain elusive. Using extant time trees and vetted fossil occurrences for conifers, we tested the hypotheses that clade competition or climate change led to the decline of conifers at the expense of angiosperms. Here, we find that both fossil and molecular data show high congruence in revealing 1) low diversification rates, punctuated by speciation pulses, during warming events throughout the Phanerozoic and 2) that conifer extinction increased significantly in the Mid- Cretaceous (100 to 110 Ma) and remained high ever since. Their extinction rates are best explained by the rise of angiosperms, rejecting alternative models based on either climate change or time alone. Our results support the hypothesis of an active clade replacement, implying that direct competition with angiosperms increased the extinction of conifers by pushing their remaining species diversity and dominance out of the warm tropics. This study illustrates how entire branches on the Tree of Life may actively compete for ecological dominance under changing climates.