Evolution and regulation of complex life cycles: a brown algal perspective

Cock, J. Mark; Godfroy, Olivier; Macaisne, Nicolas; Peters, Akira F.; Coelho, Susana M.

doi:10.1016/j.pbi.2013.09.004

Cited by 63 publications

(55 citation statements)

References 35 publications

(29 reference statements)

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“…Brown algae, although only distantly related to plants and animals, have convergently evolved plant-like body plans and reproductive cycles including male and female gametogenesis (Charrier et al, 2012). Furthermore, many brown algae have an alternative life cycle with two life stages, termed gametophytes (1N) and sporophytes (2N) (Charrier et al, 2012;Cock et al, 2014). Gametophytes from some kelp species, such as Saccharina japonica, can even develop into larger multicellular organisms but rarely reach tissue differentiation (Ye et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

Single‐base methylome profiling of the giant kelp Saccharina japonica reveals significant differences in DNA methylation to microalgae and plants

et al. 2019

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Summary Brown algae have convergently evolved plant‐like body plans and reproductive cycles, which in plants are controlled by differential DNA methylation. This contribution provides the first single‐base methylome profiles of haploid gametophytes and diploid sporophytes of a multicellular alga. Although only c. 1.4% of cytosines in Saccharina japonica were methylated mainly at CHH sites and characterized by 5‐methylcytosine (5mC), there were significant differences between life‐cycle stages. DNA methyltransferase 2 (DNMT2), known to efficiently catalyze tRNA methylation, is assumed to methylate the genome of S. japonica in the structural context of tRNAs as the genome does not encode any other DNA methyltransferases. Circular and long noncoding RNA genes were the most strongly methylated regulatory elements in S. japonica. Differential expression of genes was negatively correlated with DNA methylation with the highest methylation levels measured in both haploid gametophytes. Hypomethylated and highly expressed genes in diploid sporophytes included genes involved in morphogenesis and halogen metabolism. The data herein provide evidence that cytosine methylation, although occurring at a low level, is significantly contributing to the formation of different life‐cycle stages, tissue differentiation and metabolism in brown algae.

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Section: Introductionmentioning

confidence: 99%

Single‐base methylome profiling of the giant kelp Saccharina japonica reveals significant differences in DNA methylation to microalgae and plants

et al. 2019

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“…Recently, the filamentous alga Ectocarpus sp has emerged as a genetic model for the brown algae (Coelho et al, 2012c;Cock et al, 2014). A high-quality genome sequence is available for this species Cormier et al, 2017), together with extensive transcriptomic data Luthringer et al, 2015) and genetic tools including a dense genetic map (Heesch et al, 2010;Avia et al, 2017).…”

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DISTAG/TBCCd1 Is Required for Basal Cell Fate Determination in Ectocarpus

et al. 2017

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Brown algae are one of the most developmentally complex groups within the eukaryotes. As in many land plants and animals, their main body axis is established early in development, when the initial cell gives rise to two daughter cells that have apical and basal identities, equivalent to shoot and root identities in land plants, respectively. We show here that mutations in the Ectocarpus DISTAG (DIS) gene lead to loss of basal structures during both the gametophyte and the sporophyte generations. Several abnormalities were observed in the germinating initial cell in dis mutants, including increased cell size, disorganization of the Golgi apparatus, disruption of the microtubule network, and aberrant positioning of the nucleus. DIS encodes a TBCCd1 protein, which has a role in internal cell organization in animals, Chlamydomonas reinhardtii, and trypanosomes. Our study highlights the key role of subcellular events within the germinating initial cell in the determination of apical/basal cell identities in a brown alga and emphasizes the remarkable functional conservation of TBCCd1 in regulating internal cell organization across extremely distant eukaryotic groups.

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“…First, the persistence of both haploid and diploid stages in a variety of taxa suggests that haploid-diploid life cycles are not a transitional state but an evolutionarily stable strategy (e.g., among the eukaryotic algae, Klinger 1993). Second, lengthening of the haploid phase accompanied by reduction of the diploid phase was also observed in certain groups-an unlikely scenario if diploidy were evolutionarily favored (e.g., within the green algae, Otto 1996; and the brown algae, Bell 1997;Cock et al 2014). Consequently, further research focused on the evolutionary stability of such diverse life cycles rather than on the evolution of diploidy as the sole successful strategy.…”

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Evolution and maintenance of haploid-diploid life cycles in natural populations: The case of the marine brown algaEctocarpus

et al. 2015

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The evolutionary stability of haploid-diploid life cycles is still controversial. Mathematical models indicate that niche differences between ploidy phases may be a necessary condition for the evolution and maintenance of these life cycles. Nevertheless, experimental support for this prediction remains elusive. In the present work, we explored this hypothesis in natural populations of the brown alga Ectocarpus. Consistent with the life cycle described in culture, Ectocarpus crouaniorum in NW France and E. siliculosus in SW Italy exhibited an alternation between haploid gametophytes and diploid sporophytes. Our field data invalidated, however, the long-standing view of an isomorphic alternation of generations. Gametophytes and sporophytes displayed marked differences in size and, conforming to theoretical predictions, occupied different spatiotemporal niches. Gametophytes were found almost exclusively on the alga Scytosiphon lomentaria during spring whereas sporophytes were present year-round on abiotic substrata. Paradoxically, E. siliculosus in NW France exhibited similar habitat usage despite the absence of alternation of ploidy phases. Diploid sporophytes grew both epilithically and epiphytically, and this mainly asexual population gained the same ecological advantage postulated for haploid-diploid populations. Consequently, an ecological interpretation of the niche differences between haploid and diploid individuals does not seem to satisfactorily explain the evolution of the Ectocarpus life cycle.

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Evolution and regulation of complex life cycles: a brown algal perspective

Cited by 63 publications

References 35 publications

Single‐base methylome profiling of the giant kelp Saccharina japonica reveals significant differences in DNA methylation to microalgae and plants

Single‐base methylome profiling of the giant kelp Saccharina japonica reveals significant differences in DNA methylation to microalgae and plants

DISTAG/TBCCd1 Is Required for Basal Cell Fate Determination in Ectocarpus

Evolution and maintenance of haploid-diploid life cycles in natural populations: The case of the marine brown algaEctocarpus

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