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1.
BMC Genomics ; 22(1): 750, 2021 Oct 18.
Artigo em Inglês | MEDLINE | ID: mdl-34663228

RESUMO

BACKGROUND: Chloroplast transfer RNAs (tRNAs) can participate in various vital processes. Gymnosperms have important ecological and economic value, and they are the dominant species in forest ecosystems in the Northern Hemisphere. However, the evolution and structural changes in chloroplast tRNAs in gymnosperms remain largely unclear. RESULTS: In this study, we determined the nucleotide evolution, phylogenetic relationships, and structural variations in 1779 chloroplast tRNAs in gymnosperms. The numbers and types of tRNA genes present in the chloroplast genomes of different gymnosperms did not differ greatly, where the average number of tRNAs was 33 and the frequencies of occurrence for various types of tRNAs were generally consistent. Nearly half of the anticodons were absent. Molecular sequence variation analysis identified the conserved secondary structures of tRNAs. About a quarter of the tRNA genes were found to contain precoded 3' CCA tails. A few tRNAs have undergone novel structural changes that are closely related to their minimum free energy, and these structural changes affect the stability of the tRNAs. Phylogenetic analysis showed that tRNAs have evolved from multiple common ancestors. The transition rate was higher than the transversion rate in gymnosperm chloroplast tRNAs. More loss events than duplication events have occurred in gymnosperm chloroplast tRNAs during their evolutionary process. CONCLUSIONS: These findings provide novel insights into the molecular evolution and biological characteristics of chloroplast tRNAs in gymnosperms.


Assuntos
Cycadopsida , Ecossistema , Cloroplastos/genética , Cycadopsida/genética , Filogenia , RNA de Transferência/genética
2.
Am J Bot ; 108(10): 2055-2065, 2021 10.
Artigo em Inglês | MEDLINE | ID: mdl-34647319

RESUMO

PREMISE: The Crato Konservat-Lagerstätte in Brazil preserves an exceptionally rich assemblage of plant macrofossils from the Early Cretaceous (late Aptian), including rare early angiosperm fossils related to Nymphaeales, monocots, and magnoliids, and a variety of angiosperms of uncertain affinities. Macrofossils of eudicot angiosperms have not been described previously, despite the presence of tricolpate pollen. We describe a fossil leaf with morphology characteristic of eudicot angiosperms. METHODS: The fossil was collected from a quarry in the Lower Cretaceous (late Aptian) Crato Formation of northeastern Brazil in the state of Ceará. We compared the leaf architecture with that of ferns, gymnosperms, and similar living and fossil angiosperms. RESULTS: The leaf of Baderadea pinnatissecta gen. et sp. nov. is simple and petiolate, with leaf architecture similar to that of some herbaceous Ranunculales. The blade is 5 cm long and the margin is untoothed and twice pinnately lobed with narrow lobes (pinnatisect). The primary vein framework is pinnate and there are multiple orders of reticulate venation. CONCLUSIONS: The combination of characters preserved in the fossil supports the interpretation that B. pinnatissecta was an herbaceous eudicot similar to some members of Ranunculales and distinguished from other lobate Aptian angiosperms by leaf shape, presence of multiple orders of reticulate venation, and the absence of glandular teeth. The presence of eudicots in the flora of the Crato was already supported by pollen; the discovery of macrofossils like these provides additional information about their morphology and ecological role in low-latitude Early Cretaceous plant communities.


Assuntos
Fósseis , Magnoliopsida , Cycadopsida , Filogenia , Folhas de Planta
4.
Int J Mol Sci ; 22(12)2021 Jun 21.
Artigo em Inglês | MEDLINE | ID: mdl-34205739

RESUMO

The incidence of various types of cancer is increasing globally. To reduce the critical side effects of cancer chemotherapy, naturally derived compounds have been considered for cancer treatment. Gymnosperms are a group of plants found worldwide that have traditionally been used for therapeutic applications. Paclitaxel is a commercially available anticancer drug derived from gymnosperms. Other natural compounds with anticancer activities, such as pinostrobin and pinocembrin, are extracted from pine heartwood, and pycnogenol and enzogenol from pine bark. Gymnosperms have great potential for further study for the discovery of new anticancer compounds. This review aims to provide a rational understanding and the latest developments in potential anticancer compounds derived from gymnosperms.


Assuntos
Antineoplásicos Fitogênicos , Cycadopsida/química , Neoplasias/tratamento farmacológico , Humanos
5.
Ann Bot ; 128(5): 577-588, 2021 09 07.
Artigo em Inglês | MEDLINE | ID: mdl-34265043

RESUMO

BACKGROUND AND AIMS: The gymnosperm order Cycadales is pivotal to our understanding of seed-plant phylogeny because of its phylogenetic placement close to the root node of extant spermatophytes and its combination of both derived and plesiomorphic character states. Although widely considered a 'living fossil' group, extant cycads display a high degree of morphological and anatomical variation. We investigate stomatal development in Zamiaceae to evaluate variation within the order and homologies between cycads and other seed plants. METHODS: Leaflets of seven species across five genera representing all major clades of Zamiaceae were examined at various stages of development using light microscopy and confocal microscopy. KEY RESULTS: All genera examined have lateral subsidiary cells of perigenous origin that differ from other pavement cells in mature leaflets and could have a role in stomatal physiology. Early epidermal patterning in a 'quartet' arrangement occurs in Ceratozamia, Zamia and Stangeria. Distal encircling cells, which are sclerified at maturity, are present in all genera except Bowenia, which shows relatively rapid elongation and differentiation of the pavement cells during leaflet development. CONCLUSIONS: Stomatal structure and development in Zamiaceae highlights some traits that are plesiomorphic in seed plants, including the presence of perigenous encircling subsidiary cells, and reveals a clear difference between the developmental trajectories of cycads and Bennettitales. Our study also shows an unexpected degree of variation among subclades in the family, potentially linked to differences in leaflet development and suggesting convergent evolution in cycads.


Assuntos
Zamiaceae , Cycadopsida , Fósseis , Filogenia , Sementes
6.
Nat Commun ; 12(1): 4247, 2021 07 12.
Artigo em Inglês | MEDLINE | ID: mdl-34253727

RESUMO

The gymnosperm Welwitschia mirabilis belongs to the ancient, enigmatic gnetophyte lineage. It is a unique desert plant with extreme longevity and two ever-elongating leaves. We present a chromosome-level assembly of its genome (6.8 Gb/1 C) together with methylome and transcriptome data to explore its astonishing biology. We also present a refined, high-quality assembly of Gnetum montanum to enhance our understanding of gnetophyte genome evolution. The Welwitschia genome has been shaped by a lineage-specific ancient, whole genome duplication (~86 million years ago) and more recently (1-2 million years) by bursts of retrotransposon activity. High levels of cytosine methylation (particularly at CHH motifs) are associated with retrotransposons, whilst long-term deamination has resulted in an exceptionally GC-poor genome. Changes in copy number and/or expression of gene families and transcription factors (e.g. R2R3MYB, SAUR) controlling cell growth, differentiation and metabolism underpin the plant's longevity and tolerance to temperature, nutrient and water stress.


Assuntos
Cycadopsida/genética , Clima Desértico , Genoma de Planta , África , Metilação de DNA/genética , Evolução Molecular , Geografia , Meristema/genética , Anotação de Sequência Molecular , Folhas de Planta/genética , Chuva , Análise de Sequência de DNA , Especificidade da Espécie , Transcriptoma/genética
7.
Nat Plants ; 7(8): 1015-1025, 2021 08.
Artigo em Inglês | MEDLINE | ID: mdl-34282286

RESUMO

Inferring the intrinsic and extrinsic drivers of species diversification and phenotypic disparity across the tree of life is a major challenge in evolutionary biology. In green plants, polyploidy (or whole-genome duplication, WGD) is known to play a major role in microevolution and speciation, but the extent to which WGD has shaped macroevolutionary patterns of diversification and phenotypic innovation across plant phylogeny remains an open question. Here, we examine the relationship of various facets of genomic evolution-including gene and genome duplication, genome size, and chromosome number-with macroevolutionary patterns of phenotypic innovation, species diversification, and climatic occupancy in gymnosperms. We show that genomic changes, such as WGD and genome-size shifts, underlie the origins of most major extant gymnosperm clades, and notably, our results support an ancestral WGD in the gymnosperm lineage. Spikes of gene duplication typically coincide with major spikes of phenotypic innovation, while increased rates of phenotypic evolution are typically found at nodes with high gene-tree conflict, representing historic population-level dynamics during speciation. Most shifts in gymnosperm diversification since the rise of angiosperms are decoupled from putative WGDs and instead are associated with increased rates of climatic occupancy evolution, particularly in cooler and/or more arid climatic conditions, suggesting that ecological opportunity, especially in the later Cenozoic, and environmental heterogeneity have driven a resurgence of gymnosperm diversification. Our study provides critical insight on the processes underlying diversification and phenotypic evolution in gymnosperms, with important broader implications for the major drivers of both micro- and macroevolution in plants.


Assuntos
Cycadopsida/genética , Evolução Molecular , Variação Genética , Genoma de Planta , Filogenia , Poliploidia , Fenótipo
8.
Nat Plants ; 7(6): 748-756, 2021 06.
Artigo em Inglês | MEDLINE | ID: mdl-34135482

RESUMO

Gymnosperms are a unique lineage of plants that currently lack a high-quality reference genome due to their large genome size and high repetitive sequence content. Here, we report a nearly complete genome assembly for Ginkgo biloba with a genome size of 9.87 Gb, an N50 contig size of 1.58 Mb and an N50 scaffold size of 775 Mb. We were able to accurately annotate 27,832 protein-coding genes in total, superseding the inaccurate annotation of 41,840 genes in a previous draft genome assembly. We found that expansion of the G. biloba genome, accompanied by the notable extension of introns, was mainly caused by the insertion of long terminal repeats rather than the recent occurrence of whole-genome duplication events, in contrast to the findings of a previous report. We also identified candidate genes in the central pair, intraflagellar transport and dynein protein families that are associated with the formation of the spermatophore flagellum, which has been lost in all seed plants except ginkgo and cycads. The newly obtained Ginkgo genome provides new insights into the evolution of the gymnosperm genome.


Assuntos
Evolução Biológica , Genoma de Planta , Ginkgo biloba/genética , Proteínas de Plantas/genética , Cycadopsida/genética , Cycadopsida/fisiologia , Elementos de DNA Transponíveis , Flores/genética , Íntrons , Filogenia , Folhas de Planta/genética , Sequências Repetidas Terminais
11.
Am J Bot ; 108(4): 559-570, 2021 04.
Artigo em Inglês | MEDLINE | ID: mdl-33861866

RESUMO

Gymnosperm taxa are incredibly diverse in many traits, including taxa with evergreen or deciduous leaves; broad, compound, needle-like or scale-like leaves; trees, shrubs, and lianas; and taxa with seed cones that range from fleshy to woody. Although less appreciated, xylem conduits are also diverse in structure among extant gymnosperm taxa. Within the xylem of gymnosperms, axial transport occurs predominantly via tracheids, although 10-40% of gymnosperm taxa, particularly within the Gnetophyta and Cycadophyta, also contain vessels. Gymnosperm taxa vary greatly in their inter-conduit pit structure, with different types of pit membranes and pitting arrangements. While some taxa display torus-margo bordered pits (60%), many others do not contain tori (40%), and at least some taxa without tori occur within each of the four extant phyla (Coniferophyta, Cycadophyta, Ginkgophyta, and Gnetophyta). Pit membrane types vary within families but appear relatively conserved within genera. Woody species with torus-bearing pit membranes occur in colder environments (lower mean annual temperature) compared to those without tori; but occurrence does not differ with mean annual precipitation. Detailed descriptions of pit membrane types are lacking for many species and genera, indicating a need for increased anatomical study. Increased knowledge of these traits could provide a unique experimental context in which to study the evolution of conduit networks, the hydraulic implications of conduit and pit structure, and the diverse structural and functional strategies utilized by gymnosperms. There are myriad potential study questions and research opportunities within this unique and diverse group of plants.


Assuntos
Cycadopsida , Traqueófitas , Cycadopsida/genética , Árvores , Água , Xilema
12.
Carbohydr Polym ; 261: 117831, 2021 Jun 01.
Artigo em Inglês | MEDLINE | ID: mdl-33766335

RESUMO

Arabinogalactan-proteins (AGPs), important signalling molecules of the plant cell wall, are structurally extensively investigated in angiosperms, but information on AGPs in gymnosperms is still limited. We characterized AGPs from the gymnosperms Ginkgo biloba, Ephedra distachya, Encephalartos longifolius and Cycas revoluta. The protein contents are comparable to that of angiosperm AGPs. Hydroxyproline is the site of linking the carbohydrate part and was detected in all AGPs with highest concentration in Cycas AGP (1.1 % of the AGP). Interestingly, with the exception of Cycas, all AGPs contained the monosaccharide 3-O-methylrhamnose not present in angiosperm polysaccharides. The carbohydrate moieties of Cycas and Ephredra showed the main components 1,3,6-linked galactose and terminal arabinose typical of angiosperm AGPs, whereas that of Ginkgo AGP was unique with 1,4-linked galactose as dominant structural element. Bioinformatic search for glycosyltransferases in Ginkgo genome also revealed a lower number of galactosyltransferases responsible for biosynthesis of the 1,3-Gal/1,6-Gal AGP backbone.


Assuntos
Parede Celular/química , Cycadopsida/química , Mucoproteínas/química , Evolução Biológica , Sequência de Carboidratos , Parede Celular/metabolismo , Biologia Computacional , Cycadopsida/classificação , Cycadopsida/metabolismo , Cycas/química , Cycas/metabolismo , Ephedra/química , Ephedra/metabolismo , Galactanos/química , Ginkgo biloba/química , Ginkgo biloba/metabolismo , Estrutura Molecular , Mucoproteínas/isolamento & purificação , Mucoproteínas/metabolismo , Proteínas de Plantas/química , Proteínas de Plantas/isolamento & purificação , Proteínas de Plantas/metabolismo , Conformação Proteica , Zamiaceae/química , Zamiaceae/metabolismo
13.
Am J Bot ; 108(1): 129-144, 2021 01.
Artigo em Inglês | MEDLINE | ID: mdl-33528044

RESUMO

PREMISE: Fossils can reveal long-vanished characters that inform inferences about the timing and patterns of diversification of living fungi. Through analyzing well-preserved fossil scutella, shield-like covers of fungal sporocarps, we describe a new taxon of early Dothideomycetes with a combination of characters unknown among extant taxa. METHODS: Macerated clays from the Potomac Group, lower Zone 1, from the Lower Cretaceous (Aptian, 125-113 Ma) of Virginia USA yielded one gymnospermous leaf cuticle colonized by 21 sporocarps of a single fungal morphotype. We inferred a tree from nuclear ribosomal DNA of extant species, and coded morphological characters to evaluate alternative, equally parsimonious placements of the fossil in a molecular constraint tree of extant species. RESULTS: Bleximothyrium ostiolatum gen. et sp. nov. has an ostiolate scutellum of radiate, dichotomizing hyphae. Unlike otherwise similar extant and fossil taxa, B. ostiolatum has tangled hyphae at its scutellum margin. Scutella of B. ostiolatum are connected to superficial mycelium, to intercalary and lateral appressoria, and to extensive subcuticular "mycélium en palmettes". The gymnospermous host has characters consistent with identity as a non-papillate ginkgophyte or cycad. CONCLUSIONS: Bleximothyrium ostiolatum is the oldest known fossil fly-speck fungus that occurs on plant cuticles and has the radiate, ostiolate scutellum known only from Dothideomycetes. Its combination of characters, its scutellum margin, and mycélium en palmettes are unknown in other extant and fossil species, and Bleximothyrium ostiolatum likely represents a new group of fly-speck fungi that may now be extinct.


Assuntos
Cycadopsida , Fósseis , Filogenia , Folhas de Planta , Virginia
14.
New Phytol ; 230(6): 2186-2199, 2021 06.
Artigo em Inglês | MEDLINE | ID: mdl-33570753

RESUMO

The woody stems of coniferous gymnosperms produce specialised compression wood to adjust the stem growth orientation in response to gravitropic stimulation. During this process, tracheids develop a compression-wood-specific S2 L cell wall layer with lignins highly enriched with p-hydroxyphenyl (H)-type units derived from H-type monolignol, whereas lignins produced in the cell walls of normal wood tracheids are exclusively composed of guaiacyl (G)-type units from G-type monolignol with a trace amount of H-type units. We show that laccases, a class of lignin polymerisation enzymes, play a crucial role in the spatially organised polymerisation of H-type and G-type monolignols during compression wood formation in Japanese cypress (Chamaecyparis obtusa). We performed a series of chemical-probe-aided imaging analysis on C. obtusa compression wood cell walls, together with gene expression, protein localisation and enzymatic assays of C. obtusa laccases. Our data indicated that CoLac1 and CoLac3 with differential oxidation activities towards H-type and G-type monolignols were precisely localised to distinct cell wall layers in which H-type and G-type lignin units were preferentially produced during the development of compression wood tracheids. We propose that, not only the spatial localisation of laccases, but also their biochemical characteristics dictate the spatial patterning of lignin polymerisation in gymnosperm compression wood.


Assuntos
Lignina , Madeira , Cycadopsida , Lacase , Polímeros
15.
Mol Phylogenet Evol ; 159: 107107, 2021 06.
Artigo em Inglês | MEDLINE | ID: mdl-33609714

RESUMO

The influence of plants in the diversification of herbivorous insects, specifically those that utilize moribund and dead hosts, is little explored. Host shifts are expected because the effectiveness of toxic secondary chemicals is lessened by decay of dead plants. Feeding on dead plants also releases herbivorous insect lineages from diversifying within a particular plant lineage. Thus, phylogenetic constraints on the herbivorous insect lineage imposed by the host plants are diminished and repeated patterns of species diversification in an association with unrelated host trees is hypothesized (i.e., taxon cycle). Scolytini, a diverse weevil tribe, specialize on many different dead and moribund plant taxa as a source of food. These species and their hosts offer an opportunity to examine the association between dead host plants and the extent of phylogenetic constraints. A phylogeny of the Scolytini was reconstructed with likelihood and Bayesian analyses of DNA sequence data from nuclear (28S, CAD, ArgK) and mitochondrial (COI) genes. Ancestral host usage and geography was reconstructed using likelihood criteria and conservation of host use was tested. Results supported a monophyletic Scolytini, Ceratolepis, Loganius, and a paraphyletic Scolytus, Camptocerus and Cnemonyx. Diversification of the Scolytini generally occurred well after their host taxa diversified and suggests a sequential evolution of host use. In this scenario the beetle imposes little selection pressure on the tree but the tree provides a platform for beetle evolution. Major changes in host tree use occurred during periods of global cooling associated with changes in beetle biogeography. Diversification of beetles occurred on common and widespread hosts and there was likely a single origination of conifer-feeding from angiosperm-feeding species during the early Pliocene and a radiation of beetle species from the Palearctic to the Nearctic. Overall, the observed patterns of Scolytini host use are conserved and are similar to those expected in a taxon pulse diversification. That is, after a host switch to an unrelated tree, the beetles diversify within the host plant lineage. The need to locate an ephemeral food resource, i.e., a dying tree, likely maintains host specificity once a host shift occurs. These findings suggest that characteristics of dead and moribund host plants (e.g. secondary chemicals) influence the diversification of these saproxlic weevils despite the reduction of selection pressures.


Assuntos
Herbivoria , Especificidade de Hospedeiro , Filogenia , Gorgulhos , Animais , Sequência de Bases , Teorema de Bayes , Cycadopsida , Comportamento Alimentar , Geografia , Funções Verossimilhança , Magnoliopsida , Modelos Genéticos , Árvores , Gorgulhos/classificação
16.
Proc Natl Acad Sci U S A ; 118(7)2021 02 16.
Artigo em Inglês | MEDLINE | ID: mdl-33568532

RESUMO

We assembled a complete reference genome of Eumaeus atala, an aposematic cycad-eating hairstreak butterfly that suffered near extinction in the United States in the last century. Based on an analysis of genomic sequences of Eumaeus and 19 representative genera, the closest relatives of Eumaeus are Theorema and Mithras We report natural history information for Eumaeus, Theorema, and Mithras Using genomic sequences for each species of Eumaeus, Theorema, and Mithras (and three outgroups), we trace the evolution of cycad feeding, coloration, gregarious behavior, and other traits. The switch to feeding on cycads and to conspicuous coloration was accompanied by little genomic change. Soon after its origin, Eumaeus split into two fast evolving lineages, instead of forming a clump of close relatives in the phylogenetic tree. Significant overlap of the fast evolving proteins in both clades indicates parallel evolution. The functions of the fast evolving proteins suggest that the caterpillars developed tolerance to cycad toxins with a range of mechanisms including autophagy of damaged cells, removal of cell debris by macrophages, and more active cell proliferation.


Assuntos
Borboletas/genética , Cycadopsida/toxicidade , Evolução Molecular , Comportamento Alimentar , Animais , Borboletas/classificação , Borboletas/fisiologia , Especiação Genética , Genoma de Inseto , Filogenia
17.
New Phytol ; 229(3): 1431-1439, 2021 02.
Artigo em Inglês | MEDLINE | ID: mdl-32981122

RESUMO

Bordered pits of many conifers include a torus-margo structure acting as a valve that prevents air from spreading between tracheids, although the extent of torus deflection as a function of applied pressure is not well known. Models were developed from images of pits in roots and stems of Picea mariana (Mill.) BSP. A computational solid mechanics approach was utilised to determine the extent of torus deflection from pressure applied to the torus and margo. Torus deflection increased in nonlinear fashion with applied pressure. The average pressure required for sealing the pit was 0.894 MPa for stems and 0.644 MPa for roots, although considerable variation was apparent between individual pits. The pits of roots were wider and deeper than those of stems. For stems, the pit depth did not increase with pit width; thus the torus displacement needed to seal the pit was less than for pits from roots. The pressure required to seal the pit depends upon anatomical characteristics such as pit width and pit depth. Although the torus displacement for sealing was greater for roots because of their greater depth, the pressures leading to sealing were not significantly different between roots and stems.


Assuntos
Picea , Traqueófitas , Cycadopsida , Raízes de Plantas
18.
Int J Mol Sci ; 21(24)2020 Dec 13.
Artigo em Inglês | MEDLINE | ID: mdl-33322128

RESUMO

Pollen grain is a unique haploid organism characterized by two key physiological processes: activation of metabolism upon exiting dormancy and polar tube growth. In gymnosperms and flowering plants, these processes occur in different time frames and exhibit important features; identification of similarities and differences is still in the active phase. In angiosperms, the growth of male gametophyte is directed and controlled by its microenvironment, while in gymnosperms it is relatively autonomous. Recent reviews have detailed aspects of interaction between angiosperm female tissues and pollen such as interactions between peptides and their receptors; however, accumulated evidence suggests low-molecular communication, in particular, through ion exchange and ROS production, equally important for polar growth as well as for pollen germination. Recently, it became clear that ROS and ionic currents form a single regulatory module, since ROS production and the activity of ion transport systems are closely interrelated and form a feedback loop.


Assuntos
Íons/metabolismo , Plantas/embriologia , Pólen/crescimento & desenvolvimento , Pólen/metabolismo , Espécies Reativas de Oxigênio/metabolismo , Cycadopsida/metabolismo , Germinação , Homeostase , Plantas/metabolismo , Reprodução/genética , Reprodução/fisiologia , Transdução de Sinais/genética , Transdução de Sinais/fisiologia
20.
Proc Natl Acad Sci U S A ; 117(46): 28867-28875, 2020 11 17.
Artigo em Inglês | MEDLINE | ID: mdl-33139543

RESUMO

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.


Assuntos
Magnoliopsida/metabolismo , Seleção Genética/fisiologia , Traqueófitas/metabolismo , Biodiversidade , Evolução Biológica , Mudança Climática , Cycadopsida , Evolução Molecular , Fósseis , Filogenia
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