Rosid radiation and the rapid rise of angiosperm-dominated forests

Wang, Hengchang; Moore, Michael J.; Soltis, Pamela S.; Bell, Charles D.; Brockington, Samuel F.; Alexandre, Roolse; Davis, Charles C.; Latvis, Maribeth; Manchester, Steven R.; Soltis, Douglas E.

doi:10.1073/pnas.0813376106

Cited by 389 publications

(434 citation statements)

References 48 publications

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“…Within Rosidae, relationships among major clades were almost entirely congruent with those obtained from a recent analysis of 12 targeted genes and the chloroplast inverted repeat for 104 species of rosids by Wang et al (23). The only difference was the position of Celastrales vs. Oxalidales and Malpighiales, but the relationships among these clades have long been difficult to reconstruct (reviewed in ref.…”

Section: Discussionsupporting

confidence: 68%

Phylogenetic analysis of 83 plastid genes further resolves the early diversification of eudicots

Moore

Soltis

Bell

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

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622

625

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Although Pentapetalae (comprising all core eudicots except Gunnerales) include ≈70% of all angiosperms, the origin of and relationships among the major lineages of this clade have remained largely unresolved. Phylogenetic analyses of 83 protein-coding and rRNA genes from the plastid genome for 86 species of seed plants, including new sequences from 25 eudicots, indicate that soon after its origin, Pentapetalae diverged into three clades: (i) a "superrosid" clade consisting of Rosidae, Vitaceae, and Saxifragales; (ii) a "superasterid" clade consisting of Berberidopsidales, Santalales, Caryophyllales, and Asteridae; and (iii) Dilleniaceae. Maximum-likelihood analyses support the position of Dilleniaceae as sister to superrosids, but topology tests did not reject alternative positions of Dilleniaceae as sister to Asteridae or all remaining Pentapetalae. Molecular dating analyses suggest that the major lineages within both superrosids and superasterids arose in as little as 5 million years. This phylogenetic hypothesis provides a crucial historical framework for future studies aimed at elucidating the underlying causes of the morphological and species diversity in Pentapetalae.Angiosperm Tree of Life | Pentapetalae | plastid genome T he Eudicotyledoneae (sensu) (1), or eudicots, comprise ≈75% of all angiosperm species (2) and encompass enormous morphological, biochemical, and ecological diversity. More than 90% of eudicot species diversity is found within the clade Pentapetalae (1), which includes major clades such as Rosidae, Caryophyllales, Saxifragales, Asteridae, and Santalales, as well as smaller lineages such as Berberidopsidales and Dilleniaceae (3-8). Previous analyses of multigene data sets have failed to resolve relationships among the major clades of Pentapetalae (6, 9). The inability to resolve these relationships suggests that the major lineages of Pentapetalae diverged rapidly, a hypothesis supported by the fossil record (10, 11). However, our understanding of the origins and evolution of Pentapetalae diversity, and consequently much of angiosperm diversity, is hindered by the lack of a well-supported phylogenetic hypothesis.Phylogenetic analyses based on complete plastid genome sequences have resolved several enigmatic relationships within angiosperms (12, 13). However, these analyses have not included data for many crucial eudicot clades. To resolve relationships among the major clades of Eudicotyledoneae (with a focus on Pentapetalae), we performed phylogenetic analyses using a data set composed of 83 genes derived from 86 complete plastid genome sequences, 25 of which were eudicot sequences generated for this study. To date, this is the largest plastid genome data set used for phylogenetic inference and includes representatives of nearly all (37 of 42) orders of eudicots sensu Angiosperm Phylogeny Group (APG) III (14). The resulting phylogenetic hypothesis helps to clarify the diversification of Pentapetalae and provides an improved framework for investigating evolutionary processes that accompanie...

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Section: Discussionsupporting

confidence: 68%

Phylogenetic analysis of 83 plastid genes further resolves the early diversification of eudicots

Moore

Soltis

Bell

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

622

625

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“…Since plant epiphytes require frequent and aseasonal rainfall, they would have benefited more directly from the increased precipitation that angiosperms initiated (Boyce 2008), and epiphytic angiosperms, ferns, lycopods and bryophytes all radiated only after angiosperms came to dominate tropical ecosystems (Boyce et al Indeed, numerous lineages of vertebrate and invertebrate animals are also now thought to have radiated shortly after angiosperm diversification (Wang et al 2009), and the propagation of high rainfall conditions by angiosperms provides a potential causal mechanism explaining this phenomenon. Because angiosperms can so strongly modify their climates, any environmental perturbation severe enough to degrade that vegetation would be exacerbated by its loss.…”

Section: Discussionmentioning

confidence: 99%

An exceptional role for flowering plant physiology in the expansion of tropical rainforests and biodiversity

Boyce

Lee

2010

Proc. R. Soc. B.

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Movement of water from soil to atmosphere by plant transpiration can feed precipitation, but is limited by the hydraulic capacities of plants, which have not been uniform through time. The flowering plants that dominate modern vegetation possess transpiration capacities that are dramatically higher than any other plants, living or extinct. Transpiration operates at the level of the leaf, however, and how the impact of this physiological revolution scales up to the landscape and larger environment remains unclear. Here, climate modelling demonstrates that angiosperms help ensure aseasonally high levels of precipitation in the modern tropics. Most strikingly, replacement of angiosperm with non-angiosperm vegetation would result in a hotter, drier and more seasonal Amazon basin, decreasing the overall area of ever-wet rainforest by 80 per cent. Thus, flowering plant ecological dominance has strongly altered climate and the global hydrological cycle. Because tropical biodiversity is closely tied to precipitation and rainforest area, angiosperm climate modification may have promoted diversification of the angiosperms themselves, as well as radiations of diverse vertebrate and invertebrate animal lineages and of epiphytic plants. Their exceptional potential for environmental modification may have contributed to divergent responses to similar climates and global perturbations, like mass extinctions, before and after angiosperm evolution.

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“…Studies employing broad taxon sampling but a modest number of genes 8 have consistently recovered two very well-supported clades of eurosids-the fabids and malvids-and grouped Eucalyptus and other Myrtales with the malvids. Our analysis alternatively places Eucalyptus as a sister taxon to the eurosids (Extended Data Fig.…”

Section: Genome Evolution and Phylogenymentioning

confidence: 99%

The genome of Eucalyptus grandis

Myburg¹,

Grattapaglia²,

Tuskan³

et al. 2014

Nature

706

705

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Eucalypts are the world's most widely planted hardwood trees. Their outstanding diversity, adaptability and growth have made them a global renewable resource of fibre and energy. We sequenced and assembled .94% of the 640-megabase genome of Eucalyptus grandis. Of 36,376 predicted protein-coding genes, 34% occur in tandem duplications, the largest proportion thus far in plant genomes. Eucalyptus also shows the highest diversity of genes for specialized metabolites such as terpenes that act as chemical defence and provide unique pharmaceutical oils. Genome sequencing of the E. grandis sister species E. globulus and a set of inbred E. grandis tree genomes reveals dynamic genome evolution and hotspots of inbreeding depression. The E. grandis genome is the first reference for the eudicot order Myrtales and is placed here sister to the eurosids. This resource expands our understanding of the unique biology of large woody perennials and provides a powerful tool to accelerate comparative biology, breeding and biotechnology.A major opportunity for a sustainable energy and biomaterials economy in many parts of the world lies in a better understanding of the molecular basis of superior growth and adaptation in woody plants. Part of this opportunity involves species of Eucalyptus L'Hér, a genus of woody perennials native to Australia 1 . The remarkable adaptability of eucalypts coupled with their fast growth and superior wood properties has driven their rapid adoption for plantation forestry in more than 100 countries across six continents (.20 million ha) 2 , making eucalypts the most widely planted hardwood forest trees in the world. The subtropical E. grandis and the temperate E. globulus stand out as targets of breeding programmes worldwide. Planted eucalypts provide key renewable resources for the production of pulp, paper, biomaterials and bioenergy, while mitigating human pressures on native forests 3 . Eucalypts also have a large diversity and high concentration of essential oils (mixtures of mono-and sesquiterpenes), many of which have ecological functions as well as medicinal and industrial uses. Predominantly outcrossers 1 with hermaphroditic animal-pollinated flowers, eucalypts are highly heterozygous and display pre-and postzygotic barriers to selfing to reduce inbreeding depression for fitness and survival 4 .To mitigate the challenge of assembling a highly heterozygous genome, we sequenced the genome of 'BRASUZ1', a 17-year-old E. grandis genotype derived from one generation of selfing. The availability of annotated forest tree genomes from two separately evolving rosid lineages, Eucalyptus (order Myrtales) and Populus (order Malpighiales 5 ), in combination with genomes from domesticated woody plants (for example, Vitis, Prunus, Citrus), provides a comparative foundation for addressing

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Rosid radiation and the rapid rise of angiosperm-dominated forests

Cited by 389 publications

References 48 publications

Phylogenetic analysis of 83 plastid genes further resolves the early diversification of eudicots

Phylogenetic analysis of 83 plastid genes further resolves the early diversification of eudicots

An exceptional role for flowering plant physiology in the expansion of tropical rainforests and biodiversity

The genome of Eucalyptus grandis

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