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1.
Plant J ; 119(2): 1091-1111, 2024 Jul.
Artículo en Inglés | MEDLINE | ID: mdl-38642374

RESUMEN

Green feather algae (Bryopsidales) undergo a unique life cycle in which a single cell repeatedly executes nuclear division without cytokinesis, resulting in the development of a thallus (>100 mm) with characteristic morphology called coenocyte. Bryopsis is a representative coenocytic alga that has exceptionally high regeneration ability: extruded cytoplasm aggregates rapidly in seawater, leading to the formation of protoplasts. However, the genetic basis of the unique cell biology of Bryopsis remains poorly understood. Here, we present a high-quality assembly and annotation of the nuclear genome of Bryopsis sp. (90.7 Mbp, 27 contigs, N50 = 6.7 Mbp, 14 034 protein-coding genes). Comparative genomic analyses indicate that the genes encoding BPL-1/Bryohealin, the aggregation-promoting lectin, are heavily duplicated in Bryopsis, whereas homologous genes are absent in other ulvophyceans, suggesting the basis of regeneration capability of Bryopsis. Bryopsis sp. possesses >30 kinesins but only a single myosin, which differs from other green algae that have multiple types of myosin genes. Consistent with this biased motor toolkit, we observed that the bidirectional motility of chloroplasts in the cytoplasm was dependent on microtubules but not actin in Bryopsis sp. Most genes required for cytokinesis in plants are present in Bryopsis, including those in the SNARE or kinesin superfamily. Nevertheless, a kinesin crucial for cytokinesis initiation in plants (NACK/Kinesin-7II) is hardly expressed in the coenocytic part of the thallus, possibly underlying the lack of cytokinesis in this portion. The present genome sequence lays the foundation for experimental biology in coenocytic macroalgae.


Asunto(s)
Genoma de Planta , Genoma de Planta/genética , Filogenia , Chlorophyta/genética , Chlorophyta/fisiología , Regeneración/genética , Bryopsida/genética , Bryopsida/fisiología , Bryopsida/citología , Cinesinas/genética , Cinesinas/metabolismo , Miosinas/genética , Miosinas/metabolismo
2.
Biotechnol Lett ; 46(3): 373-383, 2024 Jun.
Artículo en Inglés | MEDLINE | ID: mdl-38493279

RESUMEN

OBJECTIVE: Currently, there is lack of a consistent and highly enriched source for docosapentaenoic acid (n-3 DPA, C22:5), and this work report the isolation of microorganism that naturally produces n-3 DPA. RESULTS: In this work, we screened microorganisms in our culture collections with the goal to isolate a strain with high levels of n-3 DPA. We isolated a strain of Sphaeroforma arctica that produces up to 11% n-3 DPA in total fatty acid and has a high n-3 DPA to DHA/EPA ratio. The cell growth of the isolated strain was characterized using microscopy imaging and flow cytometer technologies to confirm the coenocytic pattern of cell divisions previously described in S. arctica. Our novel isolate of S. arctica grew more robustly and produced significantly more n-3 DPA compared to previously isolated and described strains indicating the uniqueness of the discovered strain. CONCLUSION: Overall, this work reports a first isolate n-3 DPA producing microorganism and establishes the foundation for future strain improvement and elucidation of the physiological function of this LC-PUFA for human nutrition and health.


Asunto(s)
Ácidos Grasos Insaturados , Ácidos Grasos Insaturados/metabolismo , Estramenopilos/metabolismo , Estramenopilos/aislamiento & purificación
3.
Am J Bot ; 101(8): 1259-74, 2014 Aug.
Artículo en Inglés | MEDLINE | ID: mdl-25104551

RESUMEN

UNLABELLED: • PREMISE OF THE STUDY: Given the worldwide economic importance of maize endosperm, it is surprising that its development is not the most comprehensively studied of the cereals. We present detailed morphometric and cytological descriptions of endosperm development in the maize inbred line B73, for which the genome has been sequenced, and compare its growth with four diverse Nested Association Mapping (NAM) founder lines.• METHODS: The first 12 d of B73 endosperm development were described using semithin sections of plastic-embedded kernels and confocal microscopy. Longitudinal sections were used to compare endosperm length, thickness, and area.• KEY RESULTS: Morphometric comparison between Arizona- and Michigan-grown B73 showed a common pattern. Early endosperm development was divided into four stages: coenocytic, cellularization through alveolation, cellularization through partitioning, and differentiation. We observed tightly synchronous nuclear divisions in the coenocyte, elucidated that the onset of cellularization was coincident with endosperm size, and identified a previously undefined cell type (basal intermediate zone, BIZ). NAM founders with small mature kernels had larger endosperms (0-6 d after pollination) than lines with large mature kernels.• CONCLUSIONS: Our B73-specific model of early endosperm growth links developmental events to relative endosperm size, while accounting for diverse growing conditions. Maize endosperm cellularizes through alveolation, then random partitioning of the central vacuole. This unique cellularization feature of maize contrasts with the smaller endosperms of Arabidopsis, barley, and rice that strictly cellularize through repeated alveolation. NAM analysis revealed differences in endosperm size during early development, which potentially relates to differences in timing of cellularization across diverse lines of maize.


Asunto(s)
Diferenciación Celular , Endospermo/crecimiento & desarrollo , Zea mays/crecimiento & desarrollo , Endospermo/anatomía & histología , Endospermo/citología , Fertilización , Células Vegetales , Polinización , Especificidad de la Especie , Zea mays/anatomía & histología , Zea mays/citología
4.
Am J Bot ; 101(1): 6-25, 2014 Jan.
Artículo en Inglés | MEDLINE | ID: mdl-24363320

RESUMEN

Multicellularity has evolved at least once in every major eukaryotic clade (in all ploidy levels) and numerous times among the prokaryotes. According to a standard multilevel selection (MLS) model, in each case, the evolution of multicellularity required the acquisition of cell-cell adhesion, communication, cooperation, and specialization attended by a compulsory alignment-of-fitness phase and an export-of-fitness phase to eliminate cell-cell conflict and to establish a reproductively integrated phenotype. These achievements are reviewed in terms of generalized evolutionary developmental motifs (or "modules") whose overall logic constructs were mobilized and executed differently in bacteria, plants, fungi, and animals. When mapped onto a matrix of theoretically possible body plan morphologies (i.e., a morphospace), these motifs and the MLS model identify a "unicellular ⇒ colonial ⇒ multicellular" transformation series of body plans that mirrors trends observed in the majority of algae (i.e., a polyphyletic collection of photoautotrophic eukaryotes) and in the land plants, fungi, and animals. However, an alternative, more direct route to multicellularity theoretically exists, which may account for some aspects of fungal and algal evolution, i.e., a "siphonous ⇒ multicellular" transformation series. This review of multicellularity attempts to show that natural selection typically acts on functional traits rather than on the mechanisms that generate them ("Many roads lead to Rome.") and that genome sequence homologies do not invariably translate into morphological homologies ("Rome isn't what it used to be.").


Asunto(s)
Evolución Biológica , Células Eucariotas/citología , Crecimiento y Desarrollo , Adhesión Celular , Filogenia
5.
BMC Ecol Evol ; 21(1): 54, 2021 04 12.
Artículo en Inglés | MEDLINE | ID: mdl-33845757

RESUMEN

BACKGROUND: Placentation has evolved multiple times among both chordates and invertebrates. Although they are structurally less complex, invertebrate placentae are much more diverse in their origin, development and position. Aquatic colonial suspension-feeders from the phylum Bryozoa acquired placental analogues multiple times, representing an outstanding example of their structural diversity and evolution. Among them, the clade Cyclostomata is the only one in which placentation is associated with viviparity and polyembryony-a unique combination not present in any other invertebrate group. RESULTS: The histological and ultrastructural study of the sexual polymorphic zooids (gonozooids) in two cyclostome species, Crisia eburnea and Crisiella producta, revealed embryos embedded in a placental analogue (nutritive tissue) with a unique structure-comprising coenocytes and solitary cells-previously unknown in animals. Coenocytes originate via nuclear multiplication and cytoplasmic growth among the cells surrounding the early embryo. This process also affects cells of the membranous sac, which initially serves as a hydrostatic system but later becomes main part of the placenta. The nutritive tissue is both highly dynamic, permanently rearranging its structure, and highly integrated with its coenocytic 'elements' being interconnected via cytoplasmic bridges and various cell contacts. This tissue shows evidence of both nutrient synthesis and transport (bidirectional transcytosis), supporting the enclosed multiple progeny. Growing primary embryo produces secondary embryos (via fission) that develop into larvae; both the secondary embyos and larvae show signs of endocytosis. Interzooidal communication pores are occupied by 1‒2 specialized pore-cells probably involved in the transport of nutrients between zooids. CONCLUSIONS: Cyclostome nutritive tissue is currently the only known example of a coenocytic placental analogue, although syncytial 'elements' could potentially be formed in them too. Structurally and functionally (but not developmentally) the nutritive tissue can be compared with the syncytial placental analogues of certain invertebrates and chordates. Evolution of the cyclostome placenta, involving transformation of the hydrostatic apparatus (membranous sac) and change of its function to embryonic nourishment, is an example of exaptation that is rather widespread among matrotrophic bryozoans. We speculate that the acquisition of a highly advanced placenta providing massive nourishment might support the evolution of polyembryony in cyclostomes. In turn, massive and continuous embryonic production led to the evolution of enlarged incubating polymorphic gonozooids hosting multiple progeny.


Asunto(s)
Briozoos , Animales , Femenino , Peces , Invertebrados , Placenta , Placentación , Embarazo
6.
Genome Biol Evol ; 13(7)2021 07 06.
Artículo en Inglés | MEDLINE | ID: mdl-33963405

RESUMEN

Modern accounts of eukaryogenesis entail an endosymbiotic encounter between an archaeal host and a proteobacterial endosymbiont, with subsequent evolution giving rise to a unicell possessing a single nucleus and mitochondria. The mononucleate state of the last eukaryotic common ancestor (LECA) is seldom, if ever, questioned, even though cells harboring multiple (syncytia, coenocytes, and polykaryons) are surprisingly common across eukaryotic supergroups. Here, we present a survey of multinucleated forms. Ancestral character state reconstruction for representatives of 106 eukaryotic taxa using 16 different possible roots and supergroup sister relationships, indicate that LECA, in addition to being mitochondriate, sexual, and meiotic, was multinucleate. LECA exhibited closed mitosis, which is the rule for modern syncytial forms, shedding light on the mechanics of its chromosome segregation. A simple mathematical model shows that within LECA's multinucleate cytosol, relationships among mitochondria and nuclei were neither one-to-one, nor one-to-many, but many-to-many, placing mitonuclear interactions and cytonuclear compatibility at the evolutionary base of eukaryotic cell origin. Within a syncytium, individual nuclei and individual mitochondria function as the initial lower-level evolutionary units of selection, as opposed to individual cells, during eukaryogenesis. Nuclei within a syncytium rescue each other's lethal mutations, thereby postponing selection for viable nuclei and cytonuclear compatibility to the generation of spores, buffering transitional bottlenecks at eukaryogenesis. The prokaryote-to-eukaryote transition is traditionally thought to have left no intermediates, yet if eukaryogenesis proceeded via a syncytial common ancestor, intermediate forms have persisted to the present throughout the eukaryotic tree as syncytia but have so far gone unrecognized.


Asunto(s)
Evolución Biológica , Eucariontes , Archaea/genética , Eucariontes/genética , Células Eucariotas , Filogenia , Células Procariotas
7.
Curr Biol ; 31(18): 4104-4110.e5, 2021 09 27.
Artículo en Inglés | MEDLINE | ID: mdl-34293333

RESUMEN

The evolutionary path from protists to multicellular animals remains a mystery. Recent work on the genomes of several unicellular relatives of animals has shaped our understanding of the genetic changes that may have occurred in this transition.1-3 However, the specific cellular modifications that took place to accommodate these changes remain unclear. To address this, we need to compare metazoan cells with those of their extant relatives, which are choanoflagellates, filastereans, ichthyosporeans, and corallochytreans/pluriformeans. Interestingly, these lineages display a range of developmental patterns potentially homologous to animal ones. Genetic tools have already been established in three of those lineages.4-7 However, there are no genetic tools available for Corallochytrea. We here report the development of stable transfection in the corallochytrean Corallochytrium limacisporum. Using these tools, we discern previously unknown biological features of C. limacisporum. In particular, we identify two different paths for cell division-binary fission and coenocytic growth-that reveal a non-linear life cycle. Additionally, we found that C. limacisporum is binucleate for most of its life cycle, and that, contrary to what happens in most eukaryotes, nuclear division is decoupled from cellular division. Moreover, its actin cytoskeleton shares characteristics with both fungal and animal cells. The establishment of these tools in C. limacisporum fills an important gap in the unicellular relatives of animals, opening up new avenues of research to elucidate the specific cellular changes that occurred in the evolution of animals.


Asunto(s)
Eucariontes , Hongos , Animales , División del Núcleo Celular , Eucariontes/genética , Hongos/genética , Filogenia , Transfección
8.
Elife ; 92020 05 11.
Artículo en Inglés | MEDLINE | ID: mdl-32392127

RESUMEN

Chytrids are early-diverging fungi that share features with animals that have been lost in most other fungi. They hold promise as a system to study fungal and animal evolution, but we lack genetic tools for hypothesis testing. Here, we generated transgenic lines of the chytrid Spizellomyces punctatus, and used fluorescence microscopy to explore chytrid cell biology and development during its life cycle. We show that the chytrid undergoes multiple rounds of synchronous nuclear division, followed by cellularization, to create and release many daughter 'zoospores'. The zoospores, akin to animal cells, crawl using actin-mediated cell migration. After forming a cell wall, polymerized actin reorganizes into fungal-like cortical patches and cables that extend into hyphal-like structures. Actin perinuclear shells form each cell cycle and polygonal territories emerge during cellularization. This work makes Spizellomyces a genetically tractable model for comparative cell biology and understanding the evolution of fungi and early eukaryotes.


Asunto(s)
Quitridiomicetos/citología , Quitridiomicetos/crecimiento & desarrollo , Quitridiomicetos/genética , Actinas/metabolismo , Evolución Biológica , Ciclo Celular , Movimiento Celular , Proteínas Fúngicas/metabolismo , Genoma Fúngico , Microorganismos Modificados Genéticamente , Mitosis , Morfogénesis , Esporas Fúngicas/fisiología , Transformación Genética
9.
Elife ; 82019 11 14.
Artículo en Inglés | MEDLINE | ID: mdl-31724951

RESUMEN

Two unicellular relatives of animals reveal that coordinated contractions of groups of cells using actomyosin predated animal multicellularity during evolution.


Asunto(s)
Citoesqueleto de Actina , Actomiosina , Animales
10.
Elife ; 82019 10 28.
Artículo en Inglés | MEDLINE | ID: mdl-31647412

RESUMEN

In animals, cellularization of a coenocyte is a specialized form of cytokinesis that results in the formation of a polarized epithelium during early embryonic development. It is characterized by coordinated assembly of an actomyosin network, which drives inward membrane invaginations. However, whether coordinated cellularization driven by membrane invagination exists outside animals is not known. To that end, we investigate cellularization in the ichthyosporean Sphaeroforma arctica, a close unicellular relative of animals. We show that the process of cellularization involves coordinated inward plasma membrane invaginations dependent on an actomyosin network and reveal the temporal order of its assembly. This leads to the formation of a polarized layer of cells resembling an epithelium. We show that this stage is associated with tightly regulated transcriptional activation of genes involved in cell adhesion. Hereby we demonstrate the presence of a self-organized, clonally-generated, polarized layer of cells in a unicellular relative of animals.


Asunto(s)
Actomiosina/metabolismo , Membrana Celular/metabolismo , Polaridad Celular , Mesomycetozoea/fisiología , Animales , Regulación de la Expresión Génica
11.
Methods Mol Biol ; 1924: 83-120, 2019.
Artículo en Inglés | MEDLINE | ID: mdl-30694469

RESUMEN

The coenocytic tip-growing alga Vaucheria exhibits positive and negative phototropism, apical expansion, polarotropism, and branch induction from the illuminated region of the cell, all of which are caused by blue light. The bending response of Vaucheria is a blue light-mediated growth response. Differently from diffuse-growing cells or organs, the apical hemispherical dome of the Vaucheria cell is the site of not only maximum growth activity but also the site of blue light perception. Thence the phototropic response is initiated by the bulging mechanism: that is, a quick shift of the growth center to the adjacent subapical flank region. Since tip growth is driven by localized exocytosis, both phototropic bending and branch induction are considered to be closely related blue light-responses. Here I describe first how to prepare a highly useful culture medium for most freshwater algae, to establish unialgal and axenic culture of Vaucheria, and then describe several simple illumination systems using ordinary and/or inverted microscopes for the measurements of tip growth and for analyses of phototropism, polarotropism, and blue light-induced branching. Brief information is also included concerning the nature and function of aureochrome, the newly discovered, ochrophyte-specific blue light receptor. Aureochrome mediates blue light-induced branching, but its role in the phototropic response is still not elucidated.


Asunto(s)
Luz , Fototropismo/fisiología , Raíces de Plantas/fisiología , Raíces de Plantas/efectos de la radiación
12.
Curr Biol ; 28(12): 1964-1969.e2, 2018 06 18.
Artículo en Inglés | MEDLINE | ID: mdl-29887314

RESUMEN

Coordination of the cell division cycle with the growth of the cell is critical to achieve cell size homeostasis [1]. Mechanisms coupling the cell division cycle with cell growth have been described across diverse eukaryotic taxa [2-4], but little is known about how these processes are coordinated in organisms that undergo more complex life cycles, such as coenocytic growth. Coenocytes (multinucleate cells formed by sequential nuclear divisions without cytokinesis) are commonly found across the eukaryotic kingdom, including in animal and plant tissues and several lineages of unicellular eukaryotes [5]. Among the organisms that form coenocytes are ichthyosporeans, a lineage of unicellular holozoans that are of significant interest due to their phylogenetic placement as one of the closest relatives of animals [6]. Here, we characterize the coenocytic cell division cycle in the ichthyosporean Sphaeroforma arctica. We observe that, in laboratory conditions, S. arctica cells undergo a uniform and easily synchronizable coenocytic cell cycle, reaching up to 128 nuclei per cell before cellularization and release of daughter cells. Cycles of nuclear division occur synchronously within the coenocyte and in regular time intervals (11-12 hr). We find that the growth of cell volume is dependent on concentration of nutrients in the media; in contrast, the rate of nuclear division cycles is constant over a range of nutrient concentrations. Together, the results suggest that nuclear division cycles in the coenocytic growth of S. arctica are driven by a timer, which ensures periodic and synchronous nuclear cycles independent of the cell size and growth.


Asunto(s)
División del Núcleo Celular/fisiología , Tamaño de la Célula , Mesomycetozoea/fisiología , Animales , Ciclo Celular , Mesomycetozoea/crecimiento & desarrollo
13.
Front Plant Sci ; 6: 287, 2015.
Artículo en Inglés | MEDLINE | ID: mdl-25964794

RESUMEN

Multicellularity has independently evolved numerous times throughout the major lineages of life. Often, multicellularity can enable complex, macroscopic organismal architectures but it is not required for the elaboration of morphology. Several alternative cellular strategies have arisen as solutions permitting exquisite forms. The green algae class Ulvophyceae, for example, contains truly multicellular organisms, as well as macroscopic siphonous cells harboring one or multiple nuclei, and siphonocladous species, which are multinucleate and multicellular. These diverse cellular organizations raise a number of questions about the evolutionary and molecular mechanisms underlying complex organismal morphology in the green plants. Importantly, how does morphological patterning arise in giant coenocytes, and do nuclei, analogous to cells in multicellular organisms, take on distinct somatic and germline identities? Here, we comparatively explore examples of patterning and differentiation in diverse coenocytic and single-cell organisms and discuss possible mechanisms of development and nuclear differentiation in the siphonous algae.

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