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Plant leaves feature epidermal stomata that are organized in stereotyped patterns. How does the pattern originate? We provide transcriptomic, imaging, and genetic evidence that Arabidopsis embryos engage known stomatal fate and patterning factors to create regularly spaced stomatal precursor cells. Analysis of embryos from 36 plant species indicates that this trait is widespread among angiosperms. Embryonic stomatal patterning in Arabidopsis is established in three stages: first, broad SPEECHLESS (SPCH) expression; second, coalescence of SPCH and its targets into discrete domains; and third, one round of asymmetric division to create stomatal precursors. Lineage progression is then halted until after germination. We show that the embryonic stomatal pattern enables fast stomatal differentiation and photosynthetic activity upon germination, but it also guides the formation of additional stomata as the leaf expands. In addition, key stomatal regulators are prevented from driving the fate transitions they can induce after germination, identifying stage-specific layers of regulation that control lineage progression during embryogenesis.

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As many multicellular organisms, land plants start their life as a single cell, which forms an embryo. Embryo morphology is relatively simple, yet comprises basic tissues and organs, as well as stem cells that sustain post-embryonic development. Being condensed in both time and space, early plant embryogenesis offers an excellent window to study general principles of plant development. However, it has been technically challenging to obtain high spatial microscopic resolution, or to perform live imaging, that would enable an in-depth investigation. Recent advances in sample preparation and microscopy now allow studying the detailed cellular morphology of plant embryos in 3D. When coupled to quantitative image analysis and computational modelling, this allows resolving the temporal and spatial interactions between cellular patterning and genetic networks. In this review, we discuss examples of interdisciplinary studies that showcase the potential of the early plant embryo for revealing principles underlying plant development.

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During plant embryogenesis, regardless of whether it begins with a fertilized egg cell (zygotic embryogenesis) or an induced somatic cell (somatic embryogenesis), significant epigenetic reprogramming occurs with the purpose of parental or vegetative transcript silencing and establishment of a next-generation epigenetic patterning. To ensure genome stability of a developing embryo, large-scale transposon silencing occurs by an RNA-directed DNA methylation (RdDM) pathway, which introduces methylation patterns de novo and as such potentially serves as a global mechanism of transcription control during developmental transitions. RdDM is controlled by a two-armed mechanism based around the activity of two RNA polymerases. While PolIV produces siRNAs accompanied by protein complexes comprising the methylation machinery, PolV produces lncRNA which guides the methylation machinery toward specific genomic locations. Recently, RdDM has been proposed as a dominant methylation mechanism during gamete formation and early embryo development in Arabidopsis thaliana, overshadowing all other methylation mechanisms. Here, we bring an overview of current knowledge about different roles of DNA methylation with emphasis on RdDM during plant zygotic and somatic embryogenesis. Based on published chromatin immunoprecipitation data on PolV binding sites within the A. thaliana genome, we uncover groups of auxin metabolism, reproductive development and embryogenesis-related genes, and discuss possible roles of RdDM at the onset of early embryonic development via targeted methylation at sites involved in different embryogenesis-related developmental mechanisms.

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Premitotic control of cell division orientation is critical for plant development, as cell walls prevent extensive cell remodeling or migration. While many divisions are proliferative and add cells to existing tissues, some divisions are formative and generate new tissue layers or growth axes. Such formative divisions are often asymmetric in nature, producing daughters with different fates. We have previously shown that, in the Arabidopsis thaliana embryo, developmental asymmetry is correlated with geometric asymmetry, creating daughter cells of unequal volume. Such divisions are generated by division planes that deviate from a default "minimal surface area" rule. Inhibition of auxin response leads to reversal to this default, yet the mechanisms underlying division plane choice in the embryo have been unclear. Here, we show that auxin-dependent division plane control involves alterations in cell geometry, but not in cell polarity axis or nuclear position. Through transcriptome profiling, we find that auxin regulates genes controlling cell wall and cytoskeleton properties. We confirm the involvement of microtubule (MT)-binding proteins in embryo division control. Organization of both MT and actin cytoskeleton depends on auxin response, and genetically controlled MT or actin depolymerization in embryos leads to disruption of asymmetric divisions, including reversion to the default. Our work shows how auxin-dependent control of MT and actin cytoskeleton properties interacts with cell geometry to generate asymmetric divisions during the earliest steps in plant development.

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Epigenetic reprogramming occurs during gametogenesis as well as during embryogenesis to reset the genome for early development. In flowering plants, many heterochromatic marks are maintained in sperm, but asymmetric DNA methylation is mostly lost. Asymmetric DNA methylation is dependent on small RNA but the re-establishment of silencing in embryo is not well understood. Here we demonstrate that small RNAs direct the histone H3 lysine 9 dimethylation during Arabidopsis thaliana embryonic development, together with asymmetric DNA methylation. This de novo silencing mechanism depends on the catalytic domain of SUVH9, a Su(Var)3-9 homolog thought to be catalytically inactive.

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Phenotypic diversity of flowering plants stems from common basic features of the plant body pattern with well-defined body axes, organs and tissue organisation. Cell division and cell specification are the two processes that underlie the formation of a body pattern. As plant cells are encased into their cellulosic walls, directional cell division through precise positioning of division plane is crucial for shaping plant morphology. Since many plant cells are pluripotent, their fate establishment is influenced by their cellular environment through cell-to-cell signaling. Recent studies show that apart from biochemical regulation, these two processes are also influenced by cell and tissue morphology and operate under mechanical control. Finding a proper model system that allows dissecting the relationship between these aspects is the key to our understanding of pattern establishment. In this review, we present the Arabidopsis embryo as a simple, yet comprehensive model of pattern formation compatible with high-throughput quantitative assays.

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BACKGROUND: Eukaryotic genomes are partitioned into euchromatic and heterochromatic domains to regulate gene expression and other fundamental cellular processes. However, chromatin is dynamic during growth and development and must be properly re-established after its decondensation. Small interfering RNAs (siRNAs) promote heterochromatin formation, but little is known about how chromatin regulates siRNA expression. RESULTS: We demonstrate that thousands of transposable elements (TEs) produce exceptionally high levels of siRNAs in Arabidopsis thaliana embryos. TEs generate siRNAs throughout embryogenesis according to two distinct patterns depending on whether they are located in euchromatic or heterochromatic regions of the genome. siRNA precursors are transcribed in embryos, and siRNAs are required to direct the re-establishment of DNA methylation on TEs from which they are derived in the new generation. Decondensed chromatin also permits the production of 24-nt siRNAs from heterochromatic TEs during post-embryogenesis, and siRNA production from bipartite-classified TEs is controlled by their chromatin states. CONCLUSIONS: Decondensation of heterochromatin in response to developmental, and perhaps environmental, cues promotes the transcription and function of siRNAs in plants. Our results indicate that chromatin-mediated siRNA transcription provides a cell-autonomous homeostatic control mechanism to help reconstitute pre-existing chromatin states during growth and development including those that ensure silencing of TEs in the future germ line.

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In many flowering plants, asymmetric division of the zygote generates apical and basal cells with different fates. In Arabidopsis thaliana, the apical cell generates the embryo while the basal cell divides anticlinally, leading to a suspensor of six to nine cells that remain extra-embryonic and eventually senesce. In some genetic backgrounds, or upon ablation of the embryo, suspensor cells can undergo periclinal cell divisions and eventually form a second twin embryo. Likewise, embryogenesis can be induced from somatic cells by various genes, but the relationship with suspensor-derived embryos is unclear. Here, we addressed the nature of the suspensor to embryo fate transformation and its genetic triggers. We expressed most known embryogenesis-inducing genes specifically in suspensor cells. We next analyzed morphology and fate-marker expression in embryos in which suspensor division was activated by different triggers to address the developmental paths towards reprogramming. Our results show that reprogramming of Arabidopsis suspensor cells towards embryonic identity is a specific cellular response that is triggered by defined regulators, follows a conserved developmental trajectory and shares similarity to the process of somatic embryogenesis from post-embryonic tissues.

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The APETALA2 (AP2) subfamily of transcription factors are key regulators of angiosperm root, shoot, flower and embryo development. The broad diversity of anatomical and morphological structures is potentially associated with the genomic dynamics of the AP2 subfamily. However, a comprehensive phylogenomic analysis of the AP2 subfamily across angiosperms is lacking. We combined phylogenetic and synteny analysis of distinct AP2 subclades in the completed genomes of 107 angiosperm species. We identified major changes in copy number variation and genomic context within subclades across lineages, and discuss how these changes may have contributed to the evolution of lineage-specific traits. Multiple AP2 subclades show highly conserved patterns of copy number and synteny across angiosperms, while others are more dynamic and show distinct lineage-specific patterns. As examples of lineage-specific morphological divergence due to AP2 subclade dynamics, we hypothesize that loss of PLETHORA1/2 in monocots correlates with the absence of taproots, whereas independent lineage-specific changes of PLETHORA4/BABY BOOM and WRINKLED1 genes in Brassicaceae and monocots point towards regulatory divergence of embryogenesis between these lineages. Additionally, copy number expansion of TOE1 and TOE3/AP2 in asterids is implicated with differential regulation of flower development. Moreover, we show that the genomic context of AP2s is in general highly specialized per angiosperm lineage. To our knowledge, this study is the first to shed light on the evolutionary divergence of the AP2 subfamily subclades across major angiosperm lineages and emphasizes the need for lineage-specific characterization of developmental networks to understand trait variability further.

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During embryogenesis in plants, cell identities are specified de novo, starting from a single cell. By combining imaging, genomic profiling, and genetics, principles of early plant development have been unraveled in the dicotyledonous plant Arabidopsis. A central emerging question, however, is how well zygotic embryogenesis in Arabidopsis reflects homologous processes in other plant species, including early diverging, non-flowering, and non-seed plants. Here, we consider plant embryogenesis with an emphasis on its evolutionary history, the diverse modes of its initiation, and the concepts in pattern formation among morphologically distinct plant groups. Furthermore, we explore challenges and future directions in plant embryogenesis research.

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Heat-shock protein of 90 kDa (Hsp90) is a key molecular chaperone involved in folding the synthesized protein and controlling protein quality. Conformational dynamics coupled to ATPase activity in N-terminal domain is essential for Hsp90's function. However, the relevant process is still largely unknown in plant Hsp90s, especially those required for plant embryogenesis which is inextricably tied up with human survival. Here, AtHsp90.6, a member of Hsp90 family in Arabidopsis, was firstly identified as a protein essential for embryogenesis. Thus we modelled AtHsp90.6 in its functionally closed 'lid-down' and open 'lid-up' states, exploring the nucleotide binding mechanism in these two states. Free energy landscape and electrostatic potential analysis revealed the switching mechanism between these two states. Collectively, this study quantitatively analysed the conformational changes of AtHsp90.6 bound to ATP or ADP. This result may help us understand the mechanism of action of AtHsp90.6 in future.

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Plastids in plants and algae evolved from the endosymbiotic integration of a cyanobacterium by a heterotrophic eukaryote. New plastids can only emerge through fission; thus, the synchronization of bacterial division with the cell cycle of the eukaryotic host was vital to the origin of phototrophic eukaryotes. Most of the sampled algae house a single plastid per cell and basal-branching relatives of polyplastidic lineages are all monoplastidic, as are some non-vascular plants during certain stages of their life cycle. In this Review, we discuss recent advances in our understanding of the molecular components necessary for plastid division, including those of the peptidoglycan wall (of which remnants were recently identified in moss), in a wide range of phototrophic eukaryotes. Our comparison of the phenotype of 131 species harbouring plastids of either primary or secondary origin uncovers that one prerequisite for an algae or plant to house multiple plastids per nucleus appears to be the loss of the bacterial genes minD and minE from the plastid genome. The presence of a single plastid whose division is coupled to host cytokinesis was a prerequisite of plastid emergence. An escape from such a monoplastidic bottleneck succeeded rarely and appears to be coupled to the evolution of additional layers of control over plastid division and a complex morphology. The existence of a quality control checkpoint of plastid transmission remains to be demonstrated and is tied to understanding the monoplastidic bottleneck.

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Land plants can grow to tremendous body sizes, yet even the most complex architectures are the result of iterations of the same developmental processes: organ initiation, growth, and pattern formation. A central question in plant biology is how these processes are regulated and coordinated to allow for the formation of ordered, 3D structures. All these elementary processes first occur in early embryogenesis, during which, from a fertilized egg cell, precursors for all major tissues and stem cells are initiated, followed by tissue growth and patterning. Here we discuss recent progress in our understanding of this phase of plant life. We consider the cellular basis for multicellular development in 3D and focus on the genetic regulatory mechanisms that direct specific steps during early embryogenesis.

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