Genetic factors explaining anthocyanin pigmentation differences.

BACKGROUND: Anthocyanins are important contributors to coloration across a wide phylogenetic range of plants. Biological functions of anthocyanins span from reproduction to protection against biotic and abiotic stressors. Owing to a clearly visible phenotype of mutants, the anthocyanin biosynthesis and its sophisticated regulation have been studied in numerous plant species. Genes encoding the anthocyanin biosynthesis enzymes are regulated by a transcription factor complex comprising MYB, bHLH and WD40 proteins. RESULTS: A systematic comparison of anthocyanin-pigmented vs. non-pigmented varieties was performed within numerous plant species covering the taxonomic diversity of flowering plants. The literature was screened for cases in which genetic factors causing anthocyanin loss were reported. Additionally, transcriptomic data sets from four previous studies were reanalyzed to determine the genes possibly responsible for color variation based on their expression pattern. The contribution of different structural and regulatory genes to the intraspecific pigmentation differences was quantified. Differences concerning transcription factors are by far the most frequent explanation for pigmentation differences observed between two varieties of the same species. Among the transcription factors in the analyzed cases, MYB genes are significantly more prone to account for pigmentation differences compared to bHLH or WD40 genes. Among the structural genes, DFR genes are most often associated with anthocyanin loss. CONCLUSIONS: These findings support previous assumptions about the susceptibility of transcriptional regulation to evolutionary changes and its importance for the evolution of novel coloration phenotypes. Our findings underline the particular significance of MYBs and their apparent prevalent role in the specificity of the MBW complex.

Integration of large and diverse angiosperm DNA fragments into Asian Gnetum mitogenomes.

BACKGROUND: Horizontal gene transfer (HGT) events have rarely been reported in gymnosperms. Gnetum is a gymnosperm genus comprising 25‒35 species sympatric with angiosperms in West African, South American, and Southeast Asian rainforests. Only a single acquisition of an angiosperm mitochondrial intron has been documented to date in Asian Gnetum mitogenomes. We wanted to develop a more comprehensive understanding of frequency and fragment length distribution of such events as well as their evolutionary history in this genus. RESULTS: We sequenced and assembled mitogenomes from five Asian Gnetum species. These genomes vary remarkably in size and foreign DNA content. We identified 15 mitochondrion-derived and five plastid-derived (MTPT) foreign genes. Our phylogenetic analyses strongly indicate that these foreign genes were transferred from diverse eudicots-mostly from the Rubiaceae genus Coptosapelta and ten genera of Malpighiales. This indicates that Asian Gnetum has experienced multiple independent HGT events. Patterns of sequence evolution strongly suggest DNA-mediated transfer between mitochondria as the primary mechanism giving rise to these HGT events. Most Asian Gnetum species are lianas and often entwined with sympatric angiosperms. We therefore propose that close apposition of Gnetum and angiosperm stems presents opportunities for interspecific cell-to-cell contact through friction and wounding, leading to HGT. CONCLUSIONS: Our study reveals that multiple HGT events have resulted in massive amounts of angiosperm mitochondrial DNA integrated into Asian Gnetum mitogenomes. Gnetum and its neighboring angiosperms are often entwined with each other, possibly accounting for frequent HGT between these two phylogenetically remote lineages.

Exploring the interplay between angiosperm chlorophyll metabolism and environmental factors.

MAIN CONCLUSION: In this review, we summarize how chlorophyll metabolism in angiosperm is affected by the environmental factors: light, temperature, metal ions, water, oxygen, and altitude. The significance of chlorophyll (Chl) in plant leaf morphogenesis and photosynthesis cannot be overstated. Over time, researchers have made significant advancements in comprehending the biosynthetic pathway of Chl in angiosperms, along with the pivotal enzymes and genes involved in this process, particularly those related to heme synthesis and light-responsive mechanisms. Various environmental factors influence the stability of Chl content in angiosperms by modulating Chl metabolic pathways. Understanding the interplay between plants Chl metabolism and environmental factors has been a prominent research topic. This review mainly focuses on angiosperms, provides an overview of the regulatory mechanisms governing Chl metabolism, and the impact of environmental factors such as light, temperature, metal ions (iron and magnesium), water, oxygen, and altitude on Chl metabolism. Understanding these effects is crucial for comprehending and preserving the homeostasis of Chl metabolism.

Zygomorphic flowers last longer: the evolution of floral symmetry and floral longevity.

Floral longevity, the length of time a flower remains open and functional, is a phylogenetically conserved trait that balances floral costs against the rate at which flowers are pollinated. Floral symmetry has long been considered a key trait in floral evolution. Although zygomorphic (bilaterally symmetric) flowers typically receive fewer floral visitors than actinomorphic (radially symmetric) flowers, it is yet to be determined whether this could be associated with longer floral longevity. Using newly collected field data combined with data from the literature on 1452 species in 168 families, we assess whether floral longevity covaries with floral symmetry in a phylogenetic framework. We find that zygomorphic flowers last on average 1.1 days longer than actinomorphic flowers, a 26.5% increase in longevity, with considerable variation across both groups. Our results provide a basis to discuss the ecological and evolutionary costs of zygomorphy for plants. Despite these costs, zygomorphy has evolved numerous times throughout angiosperm history, and we discuss which rewards may outweigh the costs of slower pollination in zygomorphic flowers.

Elevated atmospheric CO2 has small, species-specific effects on pollen chemistry and plant growth across flowering plant species.

Elevated atmospheric carbon dioxide (eCO2) can affect plant growth and physiology, which can, in turn, impact herbivorous insects, including by altering pollen or plant tissue nutrition. Previous research suggests that eCO2 can reduce pollen nutrition in some species, but it is unknown whether this effect is consistent across flowering plant species. We experimentally quantified the effects of eCO2 across multiple flowering plant species on plant growth in 9 species and pollen chemistry (%N an estimate for protein content and nutrition in 12 species; secondary chemistry in 5 species) in greenhouses. For pollen nutrition, only buckwheat significantly responded to eCO2, with %N increasing in eCO2; CO2 treatment did not affect pollen amino acid composition but altered secondary metabolites in buckwheat and sunflower. Plant growth under eCO2 exhibited two trends across species: plant height was taller in 44% of species and flower number was affected for 63% of species (3 species with fewer and 2 species with more flowers). The remaining growth metrics (leaf number, above-ground biomass, flower size, and flowering initiation) showed divergent, species-specific responses, if any. Our results indicate that future eCO2 is unlikely to uniformly change pollen chemistry or plant growth across flowering species but may have the potential to alter ecological interactions, or have particularly important effects on specialized pollinators.

Eco-evolutionary processes shaping floral nectar sugar composition.

Floral nectar sugar composition is assumed to reflect the nutritional demands and foraging behaviour of pollinators, but the relative contributions of evolutionary and abiotic factors to nectar sugar composition remain largely unknown across the angiosperms. We compiled a comprehensive dataset on nectar sugar composition for 414 insect-pollinated plant species across central Europe, along with phylogeny, paleoclimate, flower morphology, and pollinator dietary demands, to disentangle their relative effects. We found that phylogeny was strongly related with nectar sucrose content, which increased with the phylogenetic age of plant families, but even more strongly with historic global surface temperature. Nectar sugar composition was also defined by floral morphology, though it was not related to our functional measure of pollinator dietary demands. However, specialist pollinators of current plant-pollinator networks predominantly visited plant species with sucrose-rich nectar. Our results suggest that both physiological mechanisms related to plant water balance and evolutionary effects related to paleoclimatic changes have shaped floral nectar sugar composition during the radiation and specialisation of plants and pollinators. As a consequence, the high velocity of current climate change may affect plant-pollinator interaction networks due to a conflicting combination of immediate physiological responses and phylogenetic conservatism.

A trait-based root acquisition-defence-decomposition framework in angiosperm tree species.

To adapt to the complex belowground environment, plants make trade-offs between root resource acquisition and defence ability. This includes forming partnerships with different types of root associating microorganisms, such as arbuscular mycorrhizal and ectomycorrhizal fungi. These trade-offs, by mediating root chemistry, exert legacy effects on nutrient release during decomposition, which may, in turn, affect the ability of new roots to re-acquire resources, thereby generating a feedback loop. However, the linkages at the basis of this potential feedback loop remain largely unquantified. Here, we propose a trait-based root 'acquisition-defence-decomposition' conceptual framework and test the strength of relevant linkages across 90 angiosperm tree species. We show that, at the plant species level, the root-fungal symbiosis gradient within the root economics space, root chemical defence (condensed tannins), and root decomposition rate are closely linked, providing support to this framework. Beyond the dichotomy between arbuscular mycorrhizal-dominated versus ectomycorrhizal-dominated systems, we suggest a continuous shift in feedback loops, from 'high arbuscular mycorrhizal symbiosis-low defence-fast decomposition-inorganic nutrition' by evolutionarily ancient taxa to 'high ectomycorrhizal symbiosis-high defence-slow decomposition-organic nutrition' by more modern taxa. This 'acquisition-defence-decomposition' framework provides a foundation for testable hypotheses on multidimensional linkages between species' belowground strategies and ecosystem nutrient cycling in an evolutionary context.

Landform and lithospheric development contribute to the assembly of mountain floras in China.

Although it is well documented that mountains tend to exhibit high biodiversity, how geological processes affect the assemblage of montane floras is a matter of ongoing research. Here, we explore landform-specific differences among montane floras based on a dataset comprising 17,576 angiosperm species representing 140 Chinese mountain floras, which we define as the collection of all angiosperm species growing on a specific mountain. Our results show that igneous bedrock (granitic and karst-granitic landforms) is correlated with higher species richness and phylogenetic overdispersion, while the opposite is true for sedimentary bedrock (karst, Danxia, and desert landforms), which is correlated with phylogenetic clustering. Furthermore, we show that landform type was the primary determinant of the assembly of evolutionarily older species within floras, while climate was a greater determinant for younger species. Our study indicates that landform type not only affects montane species richness, but also contributes to the composition of montane floras. To explain the assembly and differentiation of mountain floras, we propose the 'floristic geo-lithology hypothesis', which highlights the role of bedrock and landform processes in montane floristic assembly and provides insights for future research on speciation, migration, and biodiversity in montane regions.

Comparative venation costs of monocotyledon and dicotyledon species in the eastern Colorado steppe.

MAIN CONCLUSION: Leaf vein network cost (total vein surface area per leaf volume) for major veins and vascular bundles did not differ between monocot and dicot species in 21 species from the eastern Colorado steppe. Dicots possessed significantly larger minor vein networks than monocots. Across the tree of life, there is evidence that dendritic vascular transport networks are optimized, balancing maximum speed and integrity of resource delivery with minimal resource investment in transport and infrastructure. Monocot venation, however, is not dendritic, and remains parallel down to the smallest vein orders with no space-filling capillary networks. Given this departure from the "optimized" dendritic network, one would assume that monocots are operating at a significant energetic disadvantage. In this study, we investigate whether monocot venation networks bear significantly greater carbon/construction costs per leaf volume than co-occurring dicots in the same ecosystem, and if so, what physiological or ecological advantage the monocot life form possesses to compensate for this deficit. Given that venation networks could also be optimized for leaf mechanical support or provide herbivory defense, we measured the vascular system of both monocot and dicots at three scales to distinguish between leaf investment in mechanical support (macroscopic vein), total transport and capacitance (vascular bundle), or exclusively water transport (xylem) for both parallel and dendritic venation networks. We observed that vein network cost (total vein surface area per leaf volume) for major veins and vascular bundles was not significantly different between monocot species and dicot species. Dicots, however, possess significantly larger minor vein networks than monocots. The 19 species subjected to gas-exchange measurement in the field displayed a broad range of Amax and but demonstrated no significant relationships with any metric of vascular network size in major or minor vein classes. Given that monocots do not seem to display any leaf hydraulic disadvantage relative to dicots, it remains an important research question why parallel venation (truly parallel, down to the smallest vessels) has not arisen more than once in the history of plant evolution.

Interspecific variation in Rubisco CO2/O2 specificity along the leaf economic spectrum across 23 woody angiosperm plants in the Pacific islands.

The coordinated interspecific variation in leaf traits and leaf lifespan is known as the leaf economic spectrum (LES). The limitation of CO2 diffusion to chloroplasts within the lamina is significant in C3 photosynthesis, resulting in a shortage of CO2 for Rubisco. Although Rubisco CO2/O2 specificity (SC/O) should be adaptively adjusted in response to the interspecific variation in CO2 concentrations [CO2] associated with Rubisco, SC/O variations across species along the LES remain unknown. We investigated the coordination among leaf traits, including SC/O, CO2 conductance, leaf protein content, and leaf mass area, across 23 woody C3 species coexisting on an oceanic island through phylogenetic correlation analyses. A high SC/O indicates a high CO2 specificity of Rubisco. SC/O was negatively correlated with [CO2] at Rubisco and total CO2 conductance within lamina, while it was positively correlated with leaf protein across species, regardless of phylogenetic constraint. A simulation analysis shows that the optimal SC/O for maximizing photosynthesis depends on both [CO2] at Rubisco sites and leaf protein per unit leaf area. SC/O is a key parameter along the LES axis and is crucial for maximizing photosynthesis across species and the adaptation of woody plants.

Shifts in evolutionary lability underlie independent gains and losses of root-nodule symbiosis in a single clade of plants.

Root nodule symbiosis (RNS) is a complex trait that enables plants to access atmospheric nitrogen converted into usable forms through a mutualistic relationship with soil bacteria. Pinpointing the evolutionary origins of RNS is critical for understanding its genetic basis, but building this evolutionary context is complicated by data limitations and the intermittent presence of RNS in a single clade of ca. 30,000 species of flowering plants, i.e., the nitrogen-fixing clade (NFC). We developed the most extensive de novo phylogeny for the NFC and an RNS trait database to reconstruct the evolution of RNS. Our analysis identifies evolutionary rate heterogeneity associated with a two-step process: An ancestral precursor state transitioned to a more labile state from which RNS was rapidly gained at multiple points in the NFC. We illustrate how a two-step process could explain multiple independent gains and losses of RNS, contrary to recent hypotheses suggesting one gain and numerous losses, and suggest a broader phylogenetic and genetic scope may be required for genome-phenome mapping.

Diversifying floral organ identity.

A fascinating component of floral morphological diversity is the evolution of novel floral organ identities. Perhaps the best-understood example of this is the evolutionary sterilization of stamens to yield staminodes, which have evolved independently numerous times across angiosperms and display a considerable range of morphologies. We are only beginning to understand how modifications of the ancestral stamen developmental program have produced staminodes, but investigating this phenomenon has the potential to help us understand both the origin of floral novelty and the evolution of genetic networks more broadly.

Characterization of Optical, Thermal, and Viscoelastic Properties of Pollenkitt in Angiosperm Pollen Using In-Line Digital Holographic Microscopy.

Pollen grains are remarkable material composites, with various organelles in their fragile interior protected by a strong shell made of sporopollenin. The outermost layer of angiosperm pollen grains contains a lipid-rich substance called pollenkitt, which is a natural bioadhesive that helps preserve structural integrity when the pollen grain is exposed to external environmental stresses. In addition, its viscous nature enables it to adhere to various floral and insect surfaces, facilitating the pollination process. To examine the physicochemical properties of aqueous pollenkitt droplets, we used in-line digital holographic microscopy to capture light scattering from individual pollenkitt particles. Comparison of pollenkitt holograms to those modeled using the Lorenz-Mie theory enables investigations into the minute variations in the refractive index and size resulting from changes in local temperature and pollen aging.

Twenty years of big plant genera.

In 2004, David Frodin published a landmark review of the history and concepts of big plant genera. Two decades of taxonomic activity have taken place since, coinciding with a revolution in phylogenetics and taxonomic bioinformatics. Here we use data from the World Flora Online (WFO) to provide an updated list of big (more than 500 species) and megadiverse (more than 1000 species) flowering plant genera and highlight changes since 2004. The number of big genera has increased from 57 to 86; today one of every four plant species is classified as a member of a big genus, with 14% in just 28 megadiverse genera. Most (71%) of the growth in big genera since 2000 is the result of new species description, not generic re-circumscription. More than 15% of all currently accepted flowering plant species described in the last two decades are in big genera, suggesting that groups previously considered intractable are now being actively studied taxonomically. Despite this rapid growth in big genera, they remain a significant yet understudied proportion of plant diversity. They represent a significant proportion of global plant diversity and should remain a priority not only for taxonomy but for understanding global diversity patterns and plant evolution in general.

A molecular atlas of plastid and mitochondrial proteins reveals organellar remodeling during plant evolutionary transitions from algae to angiosperms.

Algae and plants carry 2 organelles of endosymbiotic origin that have been co-evolving in their host cells for more than a billion years. The biology of plastids and mitochondria can differ significantly across major lineages and organelle changes likely accompanied the adaptation to new ecological niches such as the terrestrial habitat. Based on organelle proteome data and the genomes of 168 phototrophic (Archaeplastida) versus a broad range of 518 non-phototrophic eukaryotes, we screened for changes in plastid and mitochondrial biology across 1 billion years of evolution. Taking into account 331,571 protein families (or orthogroups), we identify 31,625 protein families that are unique to primary plastid-bearing eukaryotes. The 1,906 and 825 protein families are predicted to operate in plastids and mitochondria, respectively. Tracing the evolutionary history of these protein families through evolutionary time uncovers the significant remodeling the organelles experienced from algae to land plants. The analyses of gained orthogroups identifies molecular changes of organelle biology that connect to the diversification of major lineages and facilitated major transitions from chlorophytes en route to the global greening and origin of angiosperms.

Convergent evolution of fern nectaries facilitated independent recruitment of ant-bodyguards from flowering plants.

Plant-herbivore interactions reciprocally influence species' evolutionary trajectories. These interactions have led to many physical and chemical defenses across the plant kingdom. Some plants have even evolved indirect defense strategies to outsource their protection to ant bodyguards by bribing them with a sugary reward (nectar). Identifying the evolutionary processes underpinning these indirect defenses provide insight into the evolution of plant-animal interactions. Using a cross-kingdom, phylogenetic approach, we examined the convergent evolution of ant-guarding nectaries across ferns and flowering plants. Here, we discover that nectaries originated in ferns and flowering plants concurrently during the Cretaceous, coinciding with the rise of plant associations in ants. While nectaries in flowering plants evolved steadily through time, ferns showed a pronounced lag of nearly 100 My between their origin and subsequent diversification in the Cenozoic. Importantly, we find that as ferns transitioned from the forest floor into the canopy, they secondarily recruited ant bodyguards from existing ant-angiosperm relationships.

Why are graminoid species more dominant? Trait-mediated plant-soil feedbacks shape community composition.

Species traits may determine plant interactions along with soil microbiome, further shaping plant-soil feedbacks (PSFs). However, how plant traits modulate PSFs and, consequently, the dominance of plant functional groups remains unclear. We used a combination of field surveys and a two-phase PSF experiment to investigate whether forbs and graminoids differed in PSFs and in their trait-PSF associations. When grown in forb-conditioned soils, forbs experienced stronger negative feedbacks, while graminoids experienced positive feedbacks. Graminoid-conditioned soil resulted in neutral PSFs for both functional types. Forbs with thin roots and small seeds showed more-negative PSFs than those with thick roots and large seeds. Conversely, graminoids with acquisitive root and leaf traits (i.e., thin roots and thin leaves) demonstrated greater positive PSFs than graminoids with thick roots and tough leaves. By distinguishing overall and soil biota-mediated PSFs, we found that the associations between plant traits and PSFs within both functional groups were mainly mediated by soil biota. A simulation model demonstrated that such differences in PSFs could lead to a dominance of graminoids over forbs in natural plant communities, which might explain why graminoids dominate in grasslands. Our study provides new insights into the differentiation and adaptation of plant life-history strategies under selection pressures imposed by soil biota.

Chemical diversity in angiosperms - monoterpene synthases control complex reactions that provide the precursors for ecologically and commercially important monoterpenoids.

Monoterpene synthases (MTSs) catalyze the first committed step in the biosynthesis of monoterpenoids, a class of specialized metabolites with particularly high chemical diversity in angiosperms. In addition to accomplishing a rate enhancement, these enzymes manage the formation and turnover of highly reactive carbocation intermediates formed from a prenyl diphosphate substrate. At each step along the reaction path, a cationic intermediate can be subject to cyclization, migration of a proton, hydride, or alkyl group, or quenching to terminate the sequence. However, enzymatic control of ligand folding, stabilization of specific intermediates, and defined quenching chemistry can maintain the specificity for forming a signature product. This review article will discuss our current understanding of how angiosperm MTSs control the reaction environment. Such knowledge allows inferences about the origin and regulation of chemical diversity, which is pertinent for appreciating the role of monoterpenoids in plant ecology but also for aiding commercial efforts that harness the accumulation of these specialized metabolites for the food, cosmetic, and pharmaceutical industries.

Cytochrome b5 diversity in green lineages preceded the evolution of syringyl lignin biosynthesis.

Lignin production marked a milestone in vascular plant evolution, and the emergence of syringyl (S) lignin is lineage specific. S-lignin biosynthesis in angiosperms, mediated by ferulate 5-hydroxylase (F5H, CYP84A1), has been considered a recent evolutionary event. F5H uniquely requires the cytochrome b5 protein CB5D as an obligatory redox partner for catalysis. However, it remains unclear how CB5D functionality originated and whether it coevolved with F5H. We reveal here the ancient evolution of CB5D-type function supporting F5H-catalyzed S-lignin biosynthesis. CB5D emerged in charophyte algae, the closest relatives of land plants, and is conserved and proliferated in embryophytes, especially in angiosperms, suggesting functional diversification of the CB5 family before terrestrialization. A sequence motif containing acidic amino residues in Helix 5 of the CB5 heme-binding domain contributes to the retention of CB5D function in land plants but not in algae. Notably, CB5s in the S-lignin-producing lycophyte Selaginella lack these residues, resulting in no CB5D-type function. An independently evolved S-lignin biosynthetic F5H (CYP788A1) in Selaginella relies on NADPH-dependent cytochrome P450 reductase as sole redox partner, distinct from angiosperms. These results suggest that angiosperm F5Hs coopted the ancient CB5D, forming a modern cytochrome P450 monooxygenase system for aromatic ring meta-hydroxylation, enabling the reemergence of S-lignin biosynthesis in angiosperms.