Epigenetic dynamics shaping melanophore and iridophore cell fate in zebrafish

Jang, Hyo Sik; Chen, Yujie; Ge, Jiaxin; Wilkening, Alicia N; Hou, Yiran; Lee, Hyung Joo; Choi, You Rim; Lowdon, Rebecca F.; Li, Daofeng; Kaufman, Charles; Johnson, Stephen L.; Wang, Ting

doi:10.1186/s13059-021-02493-x

Cited by 11 publications

(6 citation statements)

References 79 publications

(63 reference statements)

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“…It is recognized that open chromatin reorganization occurs during major developmental phase transitions in plants ( 69 , 70 ) and animals ( 71 , 72 ), but open chromatin dynamics during genome polyploidization, as a common and crucial event in the evolution of flowering plants, is still poorly understood. Here, we report that the DHS landscape, which was different between two diploid ancestors, showed convergent distributions in domesticated tetraploid cotton.…”

Section: Discussionmentioning

confidence: 99%

Genome-wide chromatin accessibility analysis unveils open chromatin convergent evolution during polyploidization in cotton

Han

López‐Arredondo

et al. 2022

Proc. Natl. Acad. Sci. U.S.A.

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Allopolyploidization, resulting in divergent genomes in the same cell, is believed to trigger a “genome shock”, leading to broad genetic and epigenetic changes. However, little is understood about chromatin and gene-expression dynamics as underlying driving forces during allopolyploidization. Here, we examined the genome-wide DNase I-hypersensitive site (DHS) and its variations in domesticated allotetraploid cotton ( Gossypium hirsutum and Gossypium barbadense , AADD) and its extant AA ( Gossypium arboreum ) and DD ( Gossypium raimondii ) progenitors. We observed distinct DHS distributions between G. arboreum and G. raimondii . In contrast, the DHSs of the two subgenomes of G. hirsutum and G. barbadense showed a convergent distribution. This convergent distribution of DHS was also present in the wild allotetraploids Gossypium darwinii and G. hirsutum var. yucatanense , but absent from a resynthesized hybrid of G. arboreum and G. raimondii , suggesting that it may be a common feature in polyploids, and not a consequence of domestication after polyploidization. We revealed that putative cis -regulatory elements (CREs) derived from polyploidization-related DHSs were dominated by several families, including Dof, ERF48, and BPC1. Strikingly, 56.6% of polyploidization-related DHSs were derived from transposable elements (TEs). Moreover, we observed positive correlations between DHS accessibility and the histone marks H3K4me3, H3K27me3, H3K36me3, H3K27ac, and H3K9ac, indicating that coordinated interplay among histone modifications, TEs, and CREs drives the DHS landscape dynamics under polyploidization. Collectively, these findings advance our understanding of the regulatory architecture in plants and underscore the complexity of regulome evolution during polyploidization.

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Section: Discussionmentioning

confidence: 99%

Genome-wide chromatin accessibility analysis unveils open chromatin convergent evolution during polyploidization in cotton

Han

López‐Arredondo

et al. 2022

Proc. Natl. Acad. Sci. U.S.A.

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“…26 At 4.43 mm (9 dpf), the fin fold had not yet developed rays and expressed alx4a mostly in iridophore pigment cells (Figure 5A). 27 By 5.41 mm (12 dpf), we observed strong alx4a:DsRed2 expression at the posterior end of the ventral melanophore stripe before the caudal fin condensation region (Figure 5B) 28 and faint expression just below the notochord distal tip (Figure 5B, white arrowhead). By 5.74 mm (13 dpf), ventral and dorsal alx4a:DsRed2 expression intensity increased (Figure 5C).…”

Section: Transgenic Markers Show Distinct Emergence Of Two Sets Of Tw...mentioning

confidence: 88%

Coordinated patterning of zebrafish caudal fin symmetry by a central and two peripheral organizers

Desvignes

Robbins

Carey

et al. 2022

Developmental Dynamics

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Background: Caudal fin symmetry characterizes teleosts and likely contributes to their evolutionary success. However, the coordinated development and patterning of skeletal elements establishing external symmetry remains incompletely understood. We explore the spatiotemporal emergence of caudal skeletal elements in zebrafish to consider evolutionary and developmental origins of caudal fin symmetry. Results: Transgenic reporters and skeletal staining reveal that the hypural diastema-defining gap between hypurals 2 and 3 forms early and separates progenitors of two plates of connective tissue. Two sets of central principal rays (CPRs) synchronously, sequentially, and symmetrically emerge around the diastema. The two dorsal-and ventral-most rays (peripheral principal rays, PPRs) arise independently and earlier than adjacent CPRs. Muscle and tendon markers reveal that different muscles attach to CPR and PPR sets. Conclusions: We propose that caudal fin symmetry originates from a central organizer that establishes the hypural diastema and bidirectionally patterns surrounding tissue into two plates of connective tissue and two mirrored sets of CPRs. Further, two peripheral organizers unidirectionally specify PPRs, forming a symmetric "composite" fin derived from three fields. Distinct CPR and PPR ontogenies may represent developmental modules conferring ray identities, muscle connections, and biomechanical properties. Our model contextualizes mechanistic studies of teleost fin morphological variation.

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“…For instance, in rodents, a specific ALX gene has been shown to control pigmentation outcomes [ 16 ]. Meanwhile, in fish, several ALX genes have been shown to specify pigmented cell types [ 12 , 13 ]. In these systems, like in butterflies, aristaless duplications appear to be relevant for the origin/control of color patterning.…”

Section: Discussionmentioning

confidence: 99%

“…In these systems, like in butterflies, aristaless duplications appear to be relevant for the origin/control of color patterning. Furthermore, for ALX in fish, both ancestral functions and novel pigmentation roles appear functional across multiple duplicates [ 13 ]. Future work should explore the expression, function, and cellular basis across other related systems with a single al or alx copy.…”

Section: Discussionmentioning

confidence: 99%

“…Within echinoderms and vertebrates, Alx activity regulates skeletogenesis and limb patterning [ 11 , 22 ]. Interestingly, several duplication events have happened across vertebrates from which novel roles, like the regulation of neurogenesis and pigmentation, have evolved for one or more copies of the gene across rodents and fishes [ 12 , 13 , 16 ].…”

Section: Introductionmentioning

confidence: 99%

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Divergent expression of aristaless1 and aristaless2 during embryonic appendage and pupal wing development in butterflies

et al. 2023

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Background Gene duplication events are critical for the evolution of new gene functions. Aristaless is a major regulator of distinct developmental processes. It is most known for its role during appendage development across animals. However, more recently other distinct biological functions have been described for this gene and its duplicates. Butterflies and moths have two copies of aristaless, aristaless1 (al1) and aristaless2 (al2), as a result of a gene duplication event. Previous work in Heliconius has shown that both copies appear to have novel functions related to wing color patterning. Here we expand our knowledge of the expression profiles associated with both ancestral and novel functions of Al1 across embryogenesis and wing pigmentation. Furthermore, we characterize Al2 expression, providing a comparative framework between gene copies within the same species, allowing us to understand the origin of new functions following gene duplication. Results Our work shows that the expression of both Al1 and Al2 is associated with the ancestral function of sensory appendage (leg, mouth, spines, and eyes) development in embryos. Interestingly, Al1 exhibits higher expression earlier in embryogenesis while the highest levels of Al2 expression are shifted to later stages of embryonic development. Furthermore, Al1 localization appears extranuclear while Al2 co-localizes tightly with nuclei earlier, and then also expands outside the nucleus later in development. Cellular expression of Al1 and Al2 in pupal wings is broadly consistent with patterns observed during embryogenesis. We also describe, for the first time, how Al1 localization appears to correlate with zones of anterior/posterior elongation of the body during embryonic growth, showcasing a possible new function related to Aristaless’ previously described role in appendage extension. Conclusions Overall, our data suggest that while both gene copies play a role in embryogenesis and wing pigmentation, the duplicates have diverged temporally and mechanistically across those functions. Our study helps clarify principles behind sub-functionalization and gene expression evolution associated with developmental functions following gene duplication events.

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Epigenetic dynamics shaping melanophore and iridophore cell fate in zebrafish

Cited by 11 publications

References 79 publications

Genome-wide chromatin accessibility analysis unveils open chromatin convergent evolution during polyploidization in cotton

Genome-wide chromatin accessibility analysis unveils open chromatin convergent evolution during polyploidization in cotton

Coordinated patterning of zebrafish caudal fin symmetry by a central and two peripheral organizers

Divergent expression of aristaless1 and aristaless2 during embryonic appendage and pupal wing development in butterflies

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