Kenny A. Bogaert

Brown Algae as a Model for Plant Organogenesis

Brown algae are an extremely interesting, but surprisingly poorly explored, group of organisms. They are one of only five eukaryotic lineages to have independently evolved complex multicellularity, which they express through a wide variety of morphologies ranging from uniseriate branched filaments to complex parenchymatous thalli with multiple cell types. Despite their very distinct evolutionary history, brown algae and land plants share a striking amount of developmental features. This has led to an interest in several aspects of brown algal development, including embryogenesis, polarity, cell cycle, asymmetric cell division and a putative role for plant hormone signalling. This review describes how investigations using brown algal models have helped to increase our understanding of the processes controlling early embryo development, in particular polarization, axis formation and asymmetric cell division. Additionally, the diversity of life cycles in the brown lineage and the emergence of Ectocarpus as a powerful model organism, are affording interesting insights on the molecular mechanisms underlying haploid-diploid life cycles. The use of these and other emerging brown algal models will undoubtedly add to our knowledge on the mechanisms that regulate development in multicellular photosynthetic organisms.

Seaweed reproductive biology: environmental and genetic controls

Abstract Knowledge of life cycle progression and reproduction of seaweeds transcends pure academic interest. Successful and sustainable seaweed exploitation and domestication will indeed require excellent control of the factors controlling growth and reproduction. The relative dominance of the ploidy-phases and their respective morphologies, however, display tremendous diversity. Consequently, the ecological and endogenous factors controlling life cycles are likely to be equally varied. A vast number of research papers addressing theoretical, ecological and physiological aspects of reproduction have been published over the years. Here, we review the current knowledge on reproductive strategies, trade-offs of reproductive effort in natural populations, and the environmental and endogenous factors controlling reproduction. Given that the majority of ecophysiological studies predate the “-omics” era, we examine the extent to which this knowledge of reproduction has been, or can be, applied to further our knowledge of life cycle control in seaweeds.

Two-step cell polarization in algal zygotes

In most complex eukaryotes, development starts with the establishment of cell polarity determining the first axis of the body plan. This polarity axis is established by the asymmetrical distribution of intrinsic factors1–3, which breaks the symmetry in a single step. Zygotes of the brown alga Fucus, which unlike land plant and animal zygotes4,5 do not possess a maternally predetermined polarity axis, serve as models to study polarity establishment6,7. Here, we studied this process in Dictyota, and concluded that sense and direction of the cell polarization vector are established in two mechanistically and temporally distinct phases that are under control of different life cycle stages. On egg activation, the zygote elongates rapidly according to a maternally predetermined direction expressing the first phase of cell polarization. Which of the two poles of the resulting prolate spheroidal zygote will acquire the basal cell fate is subsequently environmentally determined. The second phase is accompanied by and dependent on zygotic transcription instead of relying uniquely on maternal factors8. Cell polarization, whereby determination of direction and sense of the polarization vector are temporally and mechanistically uncoupled, is unique and represents a favourable system to gain insight into the processes underlying cell polarity establishment in general.

The Plastid Genome In Cladophorales Green Algae Is Encoded By Hairpin Plasmids

Chloroplast genomes, relics of an endosymbiotic cyanobacterial genome, are circular double-stranded DNA molecules. While fragmented mitochondrial genomes evolved several times during the evolution of eukaryotes, fragmented plastid genomes are only known in dinoflagellates. Here we show that the chloroplast genome of the green alga Boodlea composita (Cladophorales) is reduced and fragmented into hairpin plasmids. Extensive sequencing of DNA and RNA demonstrated that the chloroplast genome is fragmented into 1-7 kb, GC-rich DNA contigs, each containing a long inverted repeat with protein-coding genes and conserved non-coding region. These contigs correspond to linear single-stranded DNA molecules that fold onto themselves to form hairpin plasmids. An elevated transfer of chloroplast genes to the nucleus coincided to Boodlea chloroplast genome reduction. The genes retained in the chloroplast are highly divergent from their corresponding orthologs. A chloroplast genome that is composed only of linear DNA molecules is unprecedented among eukaryotes. One Sentence Summary Chloroplast genome in Cladophorales green algae is reduced and fragmented into multiple linear single-stranded DNA molecules.

Photopolarization of Fucus zygotes is determined by time sensitive vectorial addition of environmental cues during axis amplification

Fucoid zygotes have been extensively used to study cell polarization and asymmetrical cell division. Fertilized eggs are responsive to different environmental cues (e.g., light, gravity) for a long period before the polarity is fixed and the cells germinate accordingly. First, it is commonly believed that the direction and sense of the polarization vector are established simultaneously as indicated by the formation of an F-actin patch. Secondly, upon reorientation of the zygote, a new polar gradient is formed and it is assumed that the position of the future rhizoid pole is only influenced by the latter. Here we tested these two hypotheses investigating photopolarization in Fucus zygotes by reorienting zygotes 90° relative to a unilateral light source at different time points during the first cell cycle. We conclude that fixation of direction and sense of the polarization vector is indeed established simultaneously. However, the experiments yielded a distribution of polarization axes that cannot be explained if only the last environmental cue is supposed to determine the polarization axis. We conclude that our observations, together with published findings, can only be explained by assuming imprinting of the different polarization vectors and their integration as a vectorial sum at the moment of axis fixation. This way cells will average different serially perceived cues resulting in a polarization vector representative of the dynamic intertidal environment, instead of betting exclusively on the perceived vector at the moment of axis fixation.

Corrigendum: Two-step cell polarization in algal zygotes

Nature Plants 3, 16221 (2017); published 23 January 2017; corrected 13 February 2017. In the version of this Letter originally published, the first affiliation for Tom Beeckman should have read: VIB-UGent Center for Plant Systems Biology, Technologiepark 927, B-9052 Ghent, Belgium. This has been corrected in all versions of the Letter.

Egg activation-triggered shape change in the Dictyota dichotoma (Phaeophyceae) zygote is actin-myosin and secretion dependent

Background and Aims Cellular morphogenesis in land plants and brown algae is typically a slow process involving growth established by an interplay of turgor pressure and cell wall rigidity. However, a recent study showed that zygotes of the brown alga Dictyota dichotoma undergo a rapid shape change from a sphere to an elongated spheroid in about 90 s, establishing the first body axis. Methods Using a combination of pharmacology, staining techniques, membrane depolarization and microscopy techniques (brightfield, transmission electron microscopy and confocal laser scanning microscopy), egg activation and the shape change of the egg cell of D. dichotoma was studied. Key Results It was established that elongation of the zygote does not involve growth, i.e. a positive change in size. The elongation is dependent on F-actin and myosin but independent of microtubules. Secretion was also found to be necessary for elongation after addition of brefeldin A. Moreover, a temporal correlation between extracellular matrix secretion and elongation was observed. Ionomycin and high potassium seawater are capable of triggering the onset of elongation, suggesting a role for membrane depolarization and calcium influx in the signalling mechanism. The elongated cells are shorter in the presence of ionomycin, suggesting a role for calcium in elongation. Conclusions A model is proposed in which the fast elongation of the fertilized egg in Dictyota is accomplished by a force generated by F-actin and myosin, regulated by cytoplasmic calcium concentrations and by secretion during elongation lowering the antagonistic force. The finding of early extracellular matrix secretion, membrane depolarization and ionophore-triggered egg activation suggest significant differences in the mechanism of egg activation signalling between D. dichotoma and the oogamous brown algal model system Fucus .