Genome size evolution of the extant lycophytes and ferns

Wang, Faguo; Wang, Aihua; Bai, Chen; Jin, Dongmei; Nie, Li-Yun; Harris, AJ; Che, Le; Wang, Sheng; Li, Shiyu; Xu, Lixin; Shen, Hui; Gu, Yu‐Cheng; Shang, Hui; Duan, Lei; Zhang, Xian‐Chun; Chen, Hongfeng; Yan, Yue‐Hong

doi:10.1016/j.pld.2021.11.007

Cited by 14 publications

(9 citation statements)

References 71 publications

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“…Previous studies recognized a significant positive relationship between genome size and chromosome number in lycophytes and ferns, but not in the other vascular plants, suggesting that the chromosome architecture of seed-free vascular plants is more static than that in seed-bearing plants (Barker & Wolf 2010; Nakazato et al, 2008; Sessa & Der, 2016; Szövényi et al, 2021). These observations lend support to the longstanding hypothesis that the evolution of genome size in seed-free vascular plants is mainly shaped by the variation of chromosome number mainly resulting from whole genome duplications (WGDs) (Klekowski & Baker, 1966; Haufler, 1987; Huang et al, 2020; Wagner et al, 1979; Wang et al, 2022). However, the genome silencing and rearrangement after recurrent WGDs are contradictory to the relative stasis of chromosomes in seed-free vascular plants, suggesting other processes involved in the evolution of genome size.…”

Section: Introductionsupporting

confidence: 76%

The first homosporous lycophyte genome revealed the association between the dynamic accumulation of LTR-RTs and genome size variation

Tang

Wei

et al. 2022

Preprint

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Lycophytes and euphyllophytes (ferns and seed plants) are the two surviving lineages of vascular plants. The modern lycophytes (clubmosses) are herbaceous found either heterosporous (Isoetales and Selaginellales) or homosporous (Lycopodiales). The contrasting genome size between homosporous and heterosporous plants has long been an attractive topic. Most clubmosses are the resource plants of Huperzine A (HupA) which is invaluable for treating Alzheimer's disease, but the evolutionary trajectory of which in land plants is unexplored. To better understand these fundamental questions, the genome data of a homosporous lycophyte is urgently required. We generated the Lycopodium clavatum L. genome by applying a reformed pipeline for filtering out non-plant sequences. The obtained genome size is 2.30 Gb, distinguished in more than 85% repetitive elements of which 62% is LTR. Two whole genome duplications (WGDs) are rigorously detected. The content of LTR-RTs was more than ten times higher in homosporous lycophytes than heterosporous ones, although most appeared within one Mya. Then, we find that the LTR-RTs' birth-death mode (a much greater birth and extremely slower death) contributes the accumulation of LTR-RTs resulting homosporous lycophyte genome expansion, while in heterosporous lycophytes, the mode is exactly the opposite. Furthermore, the five necessary enzymes of the HupA biosynthetic pathway were identified in the L. clavatum genome, but absent in the other land plants. This decoded genome data will be a key cornerstone to elucidating the fundamental aspects of lycophyte biology and land plant evolution.

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Section: Introductionsupporting

confidence: 76%

The first homosporous lycophyte genome revealed the association between the dynamic accumulation of LTR-RTs and genome size variation

Tang

Wei

et al. 2022

Preprint

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“…More strikingly, Ophioglossum reticulatum is a fern species with the highest chromosome number known amongst eukaryotes, with 2n = 1,440 chromosomes (Khandelwal 1990). The huge diversity as well as the high numbers of chromosomes of ferns are compelling mysteries that have fascinated evolutionary biologists for decades (Haufler and Soltis 1986, Barker 2009, Clark et al 2016, Wang et al 2022). Given that polyploidizations can increase both genome size and numbers of chromosomes directly, multiple rounds of polyploidizations, along with potential changes of chromosome compositions and/or processes of genome downsizing, have been hypothesized to explain the evolution of (numbers of) chromosomes and genome sizes in ferns (Clark et al 2016, Wang et al 2022).…”

Section: Introductionmentioning

confidence: 99%

“…Indeed, within the past two decades strong evidence accumulated for recurrent WGDs in seed plants (Van de Peer et al 2017) and their roles in the evolution of innovative traits and in facilitating the diversification of species (Soltis and Soltis 2016, Van de Peer et al 2017, Landis et al 2018). Different from the lineage of seed plants, seed-free vascular plants or pteridophytes form a paraphyletic group, including Lycopodiopsida (lycophytes) and Polypodiopsida (ferns), and for a long time, WGDs in seed-free vascular plants were indefinite, although cytological evidence suggested that polyploidization may not be uncommon in ferns (Wood et al 2009, Clark et al 2016, Wang et al 2022).…”

Section: Introductionmentioning

confidence: 99%

Revisiting Ancient Polyploidy in Leptosporangiate Ferns

Chen

Fang

Zwaenepoel

et al. 2022

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Ferns, and particularly homosporous ferns, have long been assumed to have experienced recurrent whole-genome duplication (WGD) events because of their substantially large genome sizes, surprisingly high chromosome numbers, and high degrees of polyploidy among many extant members. Although, consequently, the number of sequenced fern genomes is very limited, recent studies using transcriptome data to find evidence for WGDs in ferns reached conflicting results concerning the occurrence of ancient polyploidy, for instance, in the lineage of leptosporangiate ferns. Because identifying WGDs in a phylogenetic context is the foremost step in studying the contribution of ancient polyploidy to evolution, we revisited earlier identified WGDs in leptosporangiate ferns, mainly the core leptosporangiate ferns, by building age distributions and applying substitution rate corrections and by conducting statistical gene tree - species tree reconciliation analyses. Our integrative analyses confidently identified four ancient WGDs in the sampled core leptosporangiates and suggest both false positives and false negatives for the WGDs that recent studies have reported earlier. In conclusion, we underscore the significance of substitution rate corrections and uncertainties in gene tree - species tree reconciliations in calling WGD events, and that failing to do so likely leads to incorrect conclusions.

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“…Within the past two decades, strong evidence has accumulated for recurrent paleo-polyploidizations, or ancient whole-genome duplications (WGDs) in seed plants ( Cui et al ., 2006 ; Vekemans et al ., 2012 ; Vanneste et al ., 2014 ; Ming et al ., 2015 ; Van de Peer et al ., 2017 ; Stull et al ., 2021 ) and their importance for the evolution of innovative traits and in facilitating the diversification of seed plant species are undisputed ( Soltis & Soltis, 2016 ; Van de Peer et al ., 2017 ; Landis et al ., 2018 ; Fox et al ., 2020 ; Van de Peer et al ., 2021). Different from the lineage of seed plants, strong evidence for WGDs in lycophytes and ferns was lacking, although cytological evidence suggested that polyploidization may not be uncommon in ferns ( Wood et al ., 2009 ; Clark et al ., 2016 ; Wang et al ., 2022 ).…”

Section: Introductionmentioning

confidence: 99%

“…More strikingly, Ophioglossum reticulatum is a fern species with the highest chromosome number known amongst eukaryotes, with 2n = 1,440 chromosomes ( Khandelwal, 1990 ). The huge diversity as well as the high numbers of chromosomes of ferns are compelling mysteries that have fascinated evolutionary biologists for decades ( Haufler & Soltis, 1986 ; Barker, 2009 ; Clark et al ., 2016 ; Wang et al ., 2022 ). Given that polyploidizations can increase both genome sizes and chromosome numbers directly, multiple rounds of polyploidizations, along with potential changes in chromosome compositions and/or processes of genome downsizing, have been hypothesized to explain the evolution of chromosomes and genomes ( Clark et al ., 2016 ; Wang et al ., 2022 ) and further the species diversity in ferns ( Fujiwara et al ., 2021 ).…”

Section: Introductionmentioning

confidence: 99%

Revisiting ancient polyploidy in leptosporangiate ferns

et al. 2022

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 Ferns, and particularly homosporous ferns, have long been assumed to have experienced recurrent whole-genome duplication (WGD) events because of their substantially large genome sizes, surprisingly high chromosome numbers, and high degrees of polyploidy among many extant members. As the number of sequenced fern genomes is limited, recent studies have employed transcriptome data to find evidence for WGDs in ferns. However, they have reached conflicting results concerning the occurrence of ancient polyploidy, for instance, in the lineage of leptosporangiate ferns. Because identifying WGDs in a phylogenetic context is the foremost step in studying the contribution of ancient polyploidy to evolution, we here revisited earlier identified WGDs in leptosporangiate ferns, mainly the core leptosporangiate ferns, by building KS-age distributions and applying substitution rate corrections, and by conducting statistical gene tree -species tree reconciliation analyses. Our integrative analyses confidently identified four ancient WGDs in the sampled core leptosporangiate ferns but also identified false positives and false negatives for WGDs that recent studies have reported earlier. In conclusion, we underscore the significance of substitution rate corrections and uncertainties in gene tree -species tree reconciliations in calling WGD events and advance an exemplar workflow to overcome such often-overlooked issues.

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Genome size evolution of the extant lycophytes and ferns

Cited by 14 publications

References 71 publications

The first homosporous lycophyte genome revealed the association between the dynamic accumulation of LTR-RTs and genome size variation

The first homosporous lycophyte genome revealed the association between the dynamic accumulation of LTR-RTs and genome size variation

Revisiting Ancient Polyploidy in Leptosporangiate Ferns

Revisiting ancient polyploidy in leptosporangiate ferns

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