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The amphipod crustacean Parhyale hawaiensis: An emerging comparative model of arthropod development, evolution, and regeneration

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Abstract Recent advances in genetic manipulation and genome sequencing have paved the way for a new generation of research organisms. The amphipod crustacean Parhyale hawaiensis is one such system. Parhyale are easy to rear and offer large broods of embryos amenable to injection, dissection, and live imaging. Foundational work has described Parhyale embryonic development, while advancements in genetic manipulation using CRISPR‐Cas9 and other techniques, combined with genome and transcriptome sequencing, have enabled its use in studies of arthropod development, evolution, and regeneration. This study introduces Parhyale development and life history, a catalog of techniques and resources for Parhyale research, and two case studies illustrating its power as a comparative research system. This article is categorized under: Comparative Development and Evolution > Evolutionary Novelties Adult Stem Cells, Tissue Renewal, and Regeneration > Regeneration Comparative Development and Evolution > Model Systems Comparative Development and Evolution > Body Plan Evolution
Transgenesis in Parhyale using the Minos transposase system. (a) A basic Minos transposase donor plasmid and a schematic diagram of the transgenesis experiment. (b) Fluorescence image of a Minos‐transformed female Parhyale that exhibits transformation in one‐half of the body, with fully transgenic hatchlings in the brood pouch. (c) An example of transgenic animal in which GFP expression is specified by a Parhylale muscle enhancer. (d) Same as in c, but using DsRed that contains a nuclear localization signal (NLS). The bright signal that runs the length of the body is autofluorescence
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Germ layer compensation and germ layer interactions in Parhyale. For ease of comprehension, in this figure, embryos are illustrated with the dorsal side facing towards the reader. During actual development, the dorsal side of the embryo faces the yolk, while the ventral side is superficial and clearly visible. (a) Left column: illustration of wild‐type lineage patterns and morphology for ectoderm‐lineage blastomeres. Middle and right columns: illustrations of ablation experiments, demonstrating intra‐germ layer compensation in the ectoderm. Ablation of any two cells from the ectoderm lineage results in embryonic lethality. (b) Ablation of ectoderm lineage cells after the start of germband elongation. Germ layer compensation does not occur after the start of the germband stage. (c) Left column: illustration of wild‐type lineage patterns and morphology for mesoderm‐lineage blastomeres. Middle and right columns: illustrations of ablation experiments demonstrating intra‐germ layer compensation in the mesoderm. (d) Ablation of mesoderm lineage cells after the start of germband elongation. Germ layer compensation does not occur after the start of the germband stage. (e) Ablation of the mesoderm after the start of germband elongation does not affect ectodermal segmentation. (f) Ablation of the ectoderm after the start of germband elongation leads to defects in mesoblast division and migration
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Parhyale cell lineage and development. (a) Following fertilization, the embryo undergoes a series of stereotyped holoblastic cleavages. At the 4‐cell stage, the embryo can either undergo left or right cleavage, characterized by the position of the Mv+g cell. (b) Lineage tracing has revealed that descendants of cells of the eight‐cell stage display germ layer restriction. The eight‐cell embryo contains four macromeres (El, Er, Ep, Mav) and four micromeres (ml, mr, en, g). During the transition from S6 to S7, cells extrude their yolk to separate the cytoplasm from the yolk. The cells in the rosette of the S7 stage migrate beneath a layer of ectodermal cells in a process associated with gastrulation to generate the S8 germ cap stage. (c) Illustration of cell migrations during gastrulation. (d) Illustration of the contributions of El, Er, and Ep cells to the ectoderm at the germband stage. (e) Illustration of the contributions of ml, mr, and Mav cells to the mesoderm and the position of the germ cells at the germband stage. (f) Left, schematic diagram of the cell division cycles that give rise to the embryonic parasegments. Unorganized cells in the posterior of the embryo organize to form PSPRs, which then divide once to generate a/b and c/d cells, then again to generate a, b, c, and d cells. These divisions occur as mediolateral waves of division, beginning with the cells immediately next to the midline, and then spreading laterally. The midline cells divide shortly after the cells that are adjacent to them. Right, illustration of the organization of cells at the germband stage. (g) Migrations of the mesoteloblasts and mesoblasts during germband elongation. Illustration represents a subset of the mesoteloblasts. Mesoteloblasts migrate posteriorly and divide to deposit mesoblasts. Mesoblasts then migrate anteriorly to pair with their specified ectodermal parasegments. (h) Trunk ectodermal parasegments and their corresponding out‐of‐phase morphological segments. The “a” cell in each parasegment expresses engrailed, which marks the posterior of each morphological segment. (i) Gene expression markers and morphological markers in Parhyale development. At S17‐S19, engrailed marks the anterior of each parasegment, while distalless marks the developing limb buds. At S21, engrailed marks the parasegments, and at S23, mef‐2 marks the developing mesoderm. The gut anlagen, which sequesters the yolk and develops into the gut, is a prominent feature of embryos, and is useful in classifying embryonic stages. A, anterior; P, posterior; D, dorsal; V, ventral; L, left; R, right; An, antenna; Mn, mandible; Mx1, maxillule; Mx2, maxilla; Mxp, maxilliped
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Phylogeny and development of Parhyale hawaiensis. (a) P. hawaiensis is a malacostracan crustacean, and is within a clade with lobsters, crabs, and shrimp. Crustaceans are one of the four major groups of arthropods. The three remaining groups are chelicerates, including spiders and scorpions; myriapods, including millipedes and centipedes; and hexapods, including insects. (Schwentner, Combosch, Pakes Nelson, & Giribet, ). (b) Parhyale development takes place over ~10 days. The early embryo undergoes rounds of holoblastic cleavage (Stage 1–Stage 4) and cells eventually coalesce into a germ cap (Stage 8). Much of the embryo develops on the surface of the yolk during germband elongation. Parasegment formation can be visualized by the expression of engrailed (red). Over the course of embryogenesis, the Parhyale Hox genes (yellow) initiate expression over different regions of the body in a collinear anterior–posterior temporal sequence. The hatchling emerges as a miniature version of the adult. Sexually mature adults display sexual dimorphism: females are smaller and have visible ovaries, while males are larger and have larger chelipeds on T3. hpf, hours post‐fertilization; Dfd, deformed; Scr, sex combs reduced; Antp, antennapedia; Ubx, ultrabithorax; AbdA, abdominal‐A
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Homeotic transformations of segment identity in Parhyale through Hox gene knockout. CRISPR‐Cas9 knockout of Hox genes induces a range of different homeotic transformations, revealing the roles of these genes in specifying segment identity
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Body plan organization and Hox gene expression of Parhyale and other representative arthropods. (a) Body plan of Parhyale. (b) Body plan and Hox gene expression of Parhyale and several representative arthropods. The expression of Hox genes correlates strongly with differing segment identities across the arthropods. Thermobia, Lithobius, and Cupiennius patterns were reprinted with permission from Hughes and Kaufman (). Copyright 2002 Elsevier Ltd
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CRISPR‐Cas9 mutagenesis and transgenesis in Parhyale. (a) Bilateral CRISPR‐Cas9 knockout of Abd‐B. Left panel shows a wild‐type Parhyale hatching. Right panel shows a CRISPR‐Cas9 mutant for Abd‐B. The abdominal appendages in the mutant are transformed to thoracic walking and jumping leg identities. (b) CRISPR‐Cas9 homologous recombination plasmid and strategy to insert GFP into the Antp locus. (c) CRISPR‐Cas9 homologous combination‐mediated transgenesis. Transgenic embryo wherein GFP is expressed in segments that express Antp (Reprinted with permission from Martin et al. (2015). Copyright 2016 Elsevier Ltd.)
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