Key questions and challenges in angiosperm macroevolution

Sauquet, Hervé; Magallón, Susana

doi:10.1111/nph.15104

Cited by 108 publications

(113 citation statements)

References 210 publications

(303 reference statements)

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“…Our study allowed to clarify a long-standing question 2 , but such reconstruction necessarily comes with limitations. Nevertheless, this is a major step forward in understanding the ancestral chromosome number for angiosperms, and we believe that this issue should be added to the angiosperm macroevolutionary agenda 34 . Progress in reconstructing the ancestral chromosome number may require the development of models that include heterogeneity in the patterns of chromosome evolution across a phylogenetic tree 23 , along with a deeper insight into genome and karyotype evolution.…”

Section: Resultsmentioning

confidence: 99%

A deep dive into the ancestral chromosome number and genome size of flowering plants

Carta

Bedini

Peruzzi

2020

Preprint

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7Chromosome rearrangements are a well-known evolutionary feature in eukaryotic organisms 1 , 8 especially plants. The remarkable diversity of flowering plants (angiosperms) has been 9 attributed, in part, to the tremendous variation in their chromosome number 2 . This variation has 10 stimulated a blossoming number of speculations about the ancestral chromosome number of 11 angiosperms 2-7 , but estimates so far remain equivocal and relied on algebraic approaches lacking 12 an explicit phylogenetic framework. Here we used a probabilistic approach to model haploid 13 chromosome number (n) changes 8 along a phylogeny embracing more than 10 thousands taxa, 14 to reconstruct the ancestral chromosome number of the common ancestor of extant angiosperms 15 and the most recent common ancestor for single angiosperm families. 16Bayesian inference revealed an ancestral haploid chromosome number for angiosperms n = 7, 17 reinforcing previous hypotheses 2-7 that suggested a low ancestral basic number. Inferred n for 18 single families, more than half of which are provided here for the first time, are mostly 19 congruent with previous evaluations. Chromosome fusion (loss) and duplication (polyploidy) 20 are the predominant transition types inferred along the phylogenetic tree, emphasising the 21 importance of both dysploidy 6,9,10 and genome duplication 2,7,11-13 in chromosome number 22 evolution. Significantly, while dysploidy is equally distributed early and late across the whole 23 phylogeny, polyploidy is detected mainly towards the tips of the tree. Therefore, little evidence 24 exists for a link between ancestral chromosome numbers and putative ancient polyploidization 25 events 14 , suggesting that further insights are needed to elucidate the organization of genome 26 packaging into chromosomes. 27 28 Each eukaryotic organism has a characteristic chromosome complement, its karyotype, which 29 represents the highest level of structural and functional organization of the nuclear genome 15 . 30 Karyotype constancy ensures the transfer of the same genetic material to the next generation, 31 while karyotype variation provides genetic support to ecological differentiation and 32 adaptation 2,15 . Cytogenetic studies have shown that the tremendous inter-and intra-taxonomic 33 variation of chromosome number documented in flowering plants 2,5,16 is mostly driven by two 34 major mechanisms: a) increases through polyploidy (which may entail a Whole Genome 35 Duplication [WGD] or an increase by half of the genome, demi-duplication 8 ); b) decreases or 36 increases through structural chromosomal rearrangements like chromosome fusion, i.e. 37descending dysploidy, and chromosome fission, i.e. ascending dysploidy. 38Polyploidy is a common and ongoing phenomenon, especially in plants 13 , that has played an 39 important role in many lineages, with evidence of several rounds of both ancient and recent 40 polyploidization 11,17,18 , albeit its distribution in time remains contested 14 . Indeed, although the 41 crucial role of polyploidy i...

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Section: Resultsmentioning

confidence: 99%

A deep dive into the ancestral chromosome number and genome size of flowering plants

Carta

Bedini

Peruzzi

2020

Preprint

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“…The apparent stability of the Annona genome over time is notable given that gene family expansion (such as in (Chaw et al 2019 increase of transposable elements (Belyayev 2014;Joly-Lopez and Bureau 2018) and WGD events (Hoffman et al 2012) are potential triggers of morphological or adaptive key innovations and rapid diversification (Tank et al 2015;Soltis and Soltis 2016). These aspects raise further questions regarding the origin and evolutionary mechanisms giving rise to the diversity of magnoliids (Sauquet and Magallón 2018). The slow but regular reduction in population size of Annona muricata is compatible with the Quaternary contraction of tropical regions in several parts of the world, and suggests that the soursop could be severely affected by climate changes, as may other tropical taxa.…”

Section: Discussionmentioning

confidence: 99%

“…The emergence of flowering plants (angiosperms) was a geologically sudden and ecologically transformative event in the history of life. Recent analyses have suggested that the major angiosperm clades diverged in quick succession within the Cretaceous, with monocots, magnoliids and eudicots starting to diversify within ca 5 Ma (Sauquet and Magallón 2018).…”

Section: Introductionmentioning

confidence: 99%

The soursop genome and comparative genomics of basal angiosperms provide new insights on evolutionary incongruence

Strijk¹,

Hinsinger²,

Mm³

et al. 2019

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Deep relationships and the sequence of divergence among major lineages of angiosperms (magnoliids, monocots and eudicots) remain ambiguous and differ depending on analytical approaches and datasets used.Complete genomes potentially provide opportunities to resolve these uncertainties, but two recently published magnoliid genomes instead deliver further conflicting signals. To disentangle key angiosperm relationships, we report a high-quality draft genome for the soursop (Annona muricata, Annonaceae). We reconstructed phylogenomic trees and show that the soursop represents a genomic mosaic supporting different histories, with scaffolds almost exclusively supporting single topologies. However, coalescent methods and a majority of genes support magnoliids as sister to monocots and eudicots, where previous whole genome-based studies remained inconclusive. This result is clear and consistent with recent studies using plastomes. The soursop genome highlights the need for more early diverging angiosperm genomes and critical assessment of the suitability of such genomes for inferring evolutionary history. 36 37 38 39 40 41 42 43 44 45 46 47 2 successive reductions in the number of whorls of both the perianth and the androecium. In both cases, disparate reductions may have paved the way for the evolution of clade specific features of genomes and flower morphology in contemporary clades. Since the publication of the first plant genome, that of Arabidopsis thaliana (Initiative 2000), there has been a steady increase in the number of sequenced eudicot and monocot genomes. However, with the exception of the iconic Amborella trichopoda, basal angiosperm diversity represented by the ancient lineages of Nymphaeales, Austrobaileyales, Chloranthales, and magnoliids has largely been overlooked. After eudicots and monocots, Magnoliidae are the most diverse clade of angiosperms (Massoni et al. 2014) with 9,000-10,000 species in four orders (Canellales, Piperales, Laurales and Magnoliales). However, despite this diversity and economic value (e.g. avocado, black pepper, cinnamon, soursop), only two genomes have been

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“…Analyses of diversification rates have shed light on potential drivers of diversity gradients across wide phylogenetic and geographic scales (Jetz et al, 2012; Rabosky et al, 2018; Landis et al, 2018). However, inferring diversification processes based solely on extant species phylogenies is very challenging (Etienne et al, 2011; Didier et al, 2017; Sauquet and Magallón, 2018; Mitchell et al, 2019), and the accuracy of these methods is an area of intensive research and heated controversy (O’Meara and Beaulieu, 2016; Moore et al, 2016; Rabosky et al, 2017; Meyer et al, 2018; Rabosky, 2018). Many contemporary analytical workflows for studying diversification have seen little vetting to date with empirical datasets (but see Title and Rabosky, 2017), and much remains to be explored about the response of diversification methods to missing and biased species sampling (Sauquet and Magallón, 2018).…”

Section: Introductionmentioning

confidence: 99%

Estimating rates and patterns of diversification with incomplete sampling: A case study in the rosids

Sun

Folk

Gitzendanner

et al. 2019

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42 Premise of the Study 43 Recent advances in generating large-scale phylogenies enable broad-scale estimation of 44 species diversification rates. These now-common approaches typically (1) are characterized 45 by incomplete coverage without explicit sampling methodologies, and/or (2) sparse backbone 46 representation, and usually rely on presumed phylogenetic placements to account for species 47 without molecular data. Here we use an empirical example to examine effects of incomplete 48 sampling on diversification estimation and provide constructive suggestions to ecologists and 49 evolutionists based on those results. 50Methods 51 We used a supermatrix for rosids, a large clade of angiosperms, and its well-sampled 52 subclade Cucurbitaceae, as empirical case studies. We compared results using this large 53 phylogeny with those based on a previously inferred, smaller supermatrix and on a synthetic 54 tree resource with complete taxonomic coverage. Finally, we simulated random and 55 representative taxon sampling and explored the impact of sampling on three commonly used 56 methods, both parametric (RPANDA, BAMM) and semiparametric (DR). 57 Key Results 58We find the impact of sampling on diversification estimates is idiosyncratic and often strong. 59As compared to full empirical sampling, representative and random sampling schemes either 60 depress or exaggerate speciation rates depending on methods and sampling schemes. No 61 method was entirely robust to poor sampling, but BAMM was least sensitive to moderate 62 levels of missing taxa. 63 Conclusions 64We (1) urge caution in use of summary backbone trees containing only higher-level taxa, (2) 65 caution against uncritical modeling of missing taxa using taxonomic data for poorly sampled 66 4 trees, and (3) stress the importance of explicit sampling methodologies in macroevolutionary 67 studies. 68

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Key questions and challenges in angiosperm macroevolution

Cited by 108 publications

References 210 publications

A deep dive into the ancestral chromosome number and genome size of flowering plants

A deep dive into the ancestral chromosome number and genome size of flowering plants

The soursop genome and comparative genomics of basal angiosperms provide new insights on evolutionary incongruence

Estimating rates and patterns of diversification with incomplete sampling: A case study in the rosids

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