The mechanisms underpinning lateral gene transfer between grasses

Pereira, Lara; Christin, Pascal‐Antoine; Dunning, Luke T.

doi:10.1002/ppp3.10347

Cited by 6 publications

(6 citation statements)

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“…HGTs lead to increased genetic and functional diversity in many eukaryotic genomes ( Husnik and McCutcheon 2017 ; Van Etten and Bhattacharya 2020 ; Pereira et al 2022 ). We analyzed rhythmic genes in G .…”

Section: Resultsmentioning

confidence: 99%

Diurnal Rhythms in the Red Seaweed Gracilariopsis chorda are Characterized by Unique Regulatory Networks of Carbon Metabolism

Lee,

Yang,

Weber

et al. 2024

Molecular Biology and Evolution

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Cellular and physiological cycles are driven by endogenous pacemakers, the diurnal and circadian rhythms. Key functions such as cell cycle progression and cellular metabolism are under rhythmic regulation, thereby maintaining physiological homeostasis. The photoreceptors phytochrome and cryptochrome, in response to light cues, are central input pathways for physiological cycles in most photosynthetic organisms. However, among Archaeplastida, red algae are the only taxa that lack phytochromes. Current knowledge about oscillatory rhythms is primarily derived from model species such as Arabidopsis thaliana and Chlamydomonas reinhardtii in the Viridiplantae, whereas little is known about these processes in other clades of the Archaeplastida, such as the red algae (Rhodophyta). We used genome-wide expression profiling of the red seaweed Gracilariopsis chorda and identified 3,098 rhythmic genes. Here, we characterized possible cryptochrome-based regulation and photosynthetic/cytosolic carbon metabolism in this species. We found a large family of cryptochrome genes in G. chorda that display rhythmic expression over the diurnal cycle and may compensate for the lack of phytochromes in this species. The input pathway gates regulatory networks of carbon metabolism which results in a compact and efficient energy metabolism during daylight hours. The system in G. chorda is distinct from energy metabolism in most plants, which activates in the dark. The green lineage, in particular, land plants, balance water loss and CO2 capture in terrestrial environments. In contrast, red seaweeds maintain a reduced set of photoreceptors and a compact cytosolic carbon metabolism to thrive in the harsh abiotic conditions typical of intertidal zones.

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Section: Resultsmentioning

confidence: 99%

Diurnal Rhythms in the Red Seaweed Gracilariopsis chorda are Characterized by Unique Regulatory Networks of Carbon Metabolism

Lee,

Yang,

Weber

et al. 2024

Molecular Biology and Evolution

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“…The precise mechanism behind the transfers is currently unknown, although many have been proposed (Dunning et al ., 2019; Christin et al ., 2012; Hibdige et al ., 2021). Based on current evidence, the most mechanisms likely involve reproductive contamination through illegitimate pollination (Christin et al ., 2012; Pereira et al ., 2022). This would potentially mirror plant transformation techniques such as repeated pollination (Shan et al ., 2005) or pollen tube pathway‐mediated transformation (Ali et al ., 2015) where the reproductive process is effectively contaminated with DNA from a third individual.…”

Section: Discussionmentioning

confidence: 99%

“…This would potentially mirror plant transformation techniques such as repeated pollination (Shan et al ., 2005) or pollen tube pathway‐mediated transformation (Ali et al ., 2015) where the reproductive process is effectively contaminated with DNA from a third individual. These transformation methods require minimal human intervention and could therefore occur naturally in wind‐pollinated species, driving the observed grass‐to‐grass LGT through reproductive contamination (Pereira et al ., 2022).…”

Section: Discussionmentioning

confidence: 99%

Lateral gene transfer generates accessory genes that accumulate at different rates within a grass lineage

Raimondeau,

Bianconi,

Pereira

et al. 2023

New Phytologist

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Summary Lateral gene transfer (LGT) is the movement of DNA between organisms without sexual reproduction. The acquired genes represent genetic novelties that have independently evolved in the donor's genome. Phylogenetic methods have shown that LGT is widespread across the entire grass family, although we know little about the underlying dynamics. We identify laterally acquired genes in five de novo reference genomes from the same grass genus (four Alloteropsis semialata and one Alloteropsis angusta). Using additional resequencing data for a further 40 Alloteropsis individuals, we place the acquisition of each gene onto a phylogeny using stochastic character mapping, and then infer rates of gains and losses. We detect 168 laterally acquired genes in the five reference genomes (32–100 per genome). Exponential decay models indicate that the rate of LGT acquisitions (6–28 per Ma) and subsequent losses (11–24% per Ma) varied significantly among lineages. Laterally acquired genes were lost at a higher rate than vertically inherited loci (0.02–0.8% per Ma). This high turnover creates intraspecific gene content variation, with a preponderance of them occurring as accessory genes in the Alloteropsis pangenome. This rapid turnover generates standing variation that can ultimately fuel local adaptation.

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“…Most of these genes are of ancient provenance, with many acquired over a billion years ago in the ancestor of this lineage. Whereas HGT in the prokaryotic domains is understood to be widespread and continual (Jain et al, 1999; Koonin, 2016; Rivera et al, 1998), only in recent studies has eukaryotic HGT also been shown to be a common and continuous process, for example, in grasses (Pereira et al, 2022), and various microbial eukaryotes (Alsmark et al, 2013; Huang, 2013; Nowack et al, 2016). Therefore, the principles underlying the process of prokaryote HGT and gene retention may also apply to eukaryotes.…”

Section: Introductionmentioning

confidence: 99%

Diverse fates of ancient horizontal gene transfers in extremophilic red algae

Van Etten,

Stephens,

Chille

et al. 2024

Environmental Microbiology

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Horizontal genetic transfer (HGT) is a common phenomenon in eukaryotic genomes. However, the mechanisms by which HGT‐derived genes persist and integrate into other pathways remain unclear. This topic is of significant interest because, over time, the stressors that initially favoured the fixation of HGT may diminish or disappear. Despite this, the foreign genes may continue to exist if they become part of a broader stress response or other pathways. The conventional model suggests that the acquisition of HGT equates to adaptation. However, this model may evolve into more complex interactions between gene products, a concept we refer to as the ‘Integrated HGT Model’ (IHM). To explore this concept further, we studied specialized HGT‐derived genes that encode heavy metal detoxification functions. The recruitment of these genes into other pathways could provide clear examples of IHM. In our study, we exposed two anciently diverged species of polyextremophilic red algae from the Galdieria genus to arsenic and mercury stress in laboratory cultures. We then analysed the transcriptome data using differential and coexpression analysis. Our findings revealed that mercury detoxification follows a ‘one gene‐one function’ model, resulting in an indivisible response. In contrast, the arsH gene in the arsenite response pathway demonstrated a complex pattern of duplication, divergence and potential neofunctionalization, consistent with the IHM. Our research sheds light on the fate and integration of ancient HGTs, providing a novel perspective on the ecology of extremophiles.

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The mechanisms underpinning lateral gene transfer between grasses

Cited by 6 publications

References 100 publications

Diurnal Rhythms in the Red Seaweed Gracilariopsis chorda are Characterized by Unique Regulatory Networks of Carbon Metabolism

Diurnal Rhythms in the Red Seaweed Gracilariopsis chorda are Characterized by Unique Regulatory Networks of Carbon Metabolism

Lateral gene transfer generates accessory genes that accumulate at different rates within a grass lineage

Diverse fates of ancient horizontal gene transfers in extremophilic red algae

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