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Article: Spatial transcriptomics reveals a conserved segment polarity program that governs muscle patterning in

He, Shuonan / Shao, Wanqing / Chen, Shiyuan Cynthia / Wang, Ting / Gibson, Matthew C

bioRxiv : the preprint server for biology

2023

Abstract: During early animal evolution, the emergence of axially-polarized segments was central to the diversification of complex bilaterian body plans. Nevertheless, precisely how and when segment polarity pathways arose remains obscure. Here we demonstrate the ... ...

Abstract	During early animal evolution, the emergence of axially-polarized segments was central to the diversification of complex bilaterian body plans. Nevertheless, precisely how and when segment polarity pathways arose remains obscure. Here we demonstrate the molecular basis for segment polarization in developing larvae of the pre-bilaterian sea anemone Highlights: Nematostella
Language	English
Publishing date	2023-01-10
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.01.09.523347
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Article ; Online: Spatial transcriptomics reveals a cnidarian segment polarity program in Nematostella vectensis.

He, Shuonan / Shao, Wanqing / Chen, Shiyuan Cynthia / Wang, Ting / Gibson, Matthew C

Current biology : CB

2023 Volume 33, Issue 13, Page(s) 2678–2689.e5

Abstract: During early animal evolution, the emergence of axially polarized segments was central to the diversification of complex bilaterian body plans. Nevertheless, precisely how and when segment polarity pathways arose remains obscure. Here, we demonstrate the ...

Abstract	During early animal evolution, the emergence of axially polarized segments was central to the diversification of complex bilaterian body plans. Nevertheless, precisely how and when segment polarity pathways arose remains obscure. Here, we demonstrate the molecular basis for segment polarization in developing larvae of the sea anemone Nematostella vectensis. Utilizing spatial transcriptomics, we first constructed a 3D gene expression atlas of developing larval segments. Capitalizing on accurate in silico predictions, we identified Lbx and Uncx, conserved homeodomain-containing genes that occupy opposing subsegmental domains under the control of both bone morphogenetic protein (BMP) signaling and the Hox-Gbx cascade. Functionally, Lbx mutagenesis eliminated all molecular evidence of segment polarization at the larval stage and caused an aberrant mirror-symmetric pattern of retractor muscles (RMs) in primary polyps. These results demonstrate the molecular basis for segment polarity in a non-bilaterian animal, suggesting that polarized metameric structures were present in the Cnidaria-Bilateria common ancestor over 600 million years ago.
MeSH term(s)	Animals ; Sea Anemones/genetics ; Transcriptome ; Genes, Homeobox ; Signal Transduction ; Phylogeny
Language	English
Publishing date	2023-06-13
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	1071731-6
ISSN	1879-0445 ; 0960-9822
ISSN (online)	1879-0445
ISSN	0960-9822
DOI	10.1016/j.cub.2023.05.044
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Article ; Online: Manipulation of Gene Activity in the Regenerative Model Sea Anemone, Nematostella vectensis.

Hill, Eric M / Chen, Cheng-Yi / Del Viso, Florencia / Ellington, Lacey R / He, Shuonan / Karabulut, Ahmet / Paulson, Ariel / Gibson, Matthew C

Methods in molecular biology (Clifton, N.J.)

2022 Volume 2450, Page(s) 437–465

Abstract: With a surprisingly complex genome and an ever-expanding genetic toolkit, the sea anemone Nematostella vectensis has become a powerful model system for the study of both development and whole-body regeneration. Here we provide the most current protocols ... ...

Abstract	With a surprisingly complex genome and an ever-expanding genetic toolkit, the sea anemone Nematostella vectensis has become a powerful model system for the study of both development and whole-body regeneration. Here we provide the most current protocols for short-hairpin RNA (shRNA )-mediated gene knockdown and CRISPR/Cas9-targeted mutagenesis in this system. We further show that a simple Klenow reaction followed by in vitro transcription allows for the production of gene-specific shRNAs and single guide RNAs (sgRNAs) in a fast, affordable, and readily scalable manner. Together, shRNA knockdown and CRISPR/Cas9-targeted mutagenesis allow for rapid screens of gene function as well as the production of stable mutant lines that enable functional genetic analysis throughout the Nematostella life cycle.
MeSH term(s)	Animals ; Gene Knockdown Techniques ; Genome ; Mutagenesis ; RNA, Small Interfering/genetics ; Sea Anemones/genetics
Chemical Substances	RNA, Small Interfering
Language	English
Publishing date	2022-03-25
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-0716-2172-1_23
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Article: Cnidofest 2018: the future is bright for cnidarian research.

He, Shuonan / Grasis, Juris A / Nicotra, Matthew L / Juliano, Celina E / Schnitzler, Christine E

EvoDevo

2019 Volume 10, Page(s) 20

Abstract: The 2018 Cnidarian Model Systems Meeting (Cnidofest) was held September 6-9th at the University of Florida Whitney Laboratory for Marine Bioscience in St. Augustine, FL. Cnidofest 2018, which built upon the momentum of Hydroidfest 2016, brought together ... ...

Abstract	The 2018 Cnidarian Model Systems Meeting (Cnidofest) was held September 6-9th at the University of Florida Whitney Laboratory for Marine Bioscience in St. Augustine, FL. Cnidofest 2018, which built upon the momentum of Hydroidfest 2016, brought together research communities working on a broad spectrum of cnidarian organisms from North America and around the world. Meeting talks covered diverse aspects of cnidarian biology, with sessions focused on genomics, development, neurobiology, immunology, symbiosis, ecology, and evolution. In addition to interesting biology, Cnidofest also emphasized the advancement of modern research techniques. Invited technology speakers showcased the power of microfluidics and single-cell transcriptomics and demonstrated their application in cnidarian models. In this report, we provide an overview of the exciting research that was presented at the meeting and discuss opportunities for future research.
Language	English
Publishing date	2019-09-04
Publishing country	England
Document type	Journal Article
ZDB-ID	2563566-9
ISSN	2041-9139
ISSN	2041-9139
DOI	10.1186/s13227-019-0134-5
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Article ; Online: Electroporation of short hairpin RNAs for rapid and efficient gene knockdown in the starlet sea anemone, Nematostella vectensis.

Karabulut, Ahmet / He, Shuonan / Chen, Cheng-Yi / McKinney, Sean A / Gibson, Matthew C

Developmental biology

2019 Volume 448, Issue 1, Page(s) 7–15

Abstract: A mechanistic understanding of evolutionary developmental biology requires the development of novel techniques for the manipulation of gene function in phylogenetically diverse organismal systems. Recently, gene-specific knockdown by microinjection of ... ...

Abstract	A mechanistic understanding of evolutionary developmental biology requires the development of novel techniques for the manipulation of gene function in phylogenetically diverse organismal systems. Recently, gene-specific knockdown by microinjection of short hairpin RNA (shRNA) was applied in the sea anemone Nematostella vectensis, demonstrating that the shRNA approach can be used for efficient and robust sequence-specific knockdown of a gene of interest. However, the time- and labor-intensive process of microinjection limits access to this technique and its application in large scale experiments. To address this issue, here we present an electroporation protocol for shRNA delivery into Nematostella eggs. This method leverages the speed and simplicity of electroporation, enabling users to manipulate gene expression in hundreds of eggs or embryos within minutes. We provide a detailed description of the experimental procedure, including reagents, electroporation conditions, preparation of Nematostella eggs, and follow-up care of experimental animals. Finally, we demonstrate the knockdown of several endogenous and exogenous genes with known phenotypes and discuss the potential applications of this method.
MeSH term(s)	Anemone ; Animals ; Electroporation/methods ; Embryo, Nonmammalian/cytology ; Embryo, Nonmammalian/embryology ; Gene Knockdown Techniques/methods ; Oocytes/cytology ; Oocytes/metabolism ; RNA, Small Interfering/biosynthesis ; RNA, Small Interfering/genetics
Chemical Substances	RNA, Small Interfering
Language	English
Publishing date	2019-01-11
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1114-9
ISSN	1095-564X ; 0012-1606
ISSN (online)	1095-564X
ISSN	0012-1606
DOI	10.1016/j.ydbio.2019.01.005
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Article ; Online: Topological structures and syntenic conservation in sea anemone genomes.

Zimmermann, Bob / Montenegro, Juan D / Robb, Sofia M C / Fropf, Whitney J / Weilguny, Lukas / He, Shuonan / Chen, Shiyuan / Lovegrove-Walsh, Jessica / Hill, Eric M / Chen, Cheng-Yi / Ragkousi, Katerina / Praher, Daniela / Fredman, David / Schultz, Darrin / Moran, Yehu / Simakov, Oleg / Genikhovich, Grigory / Gibson, Matthew C / Technau, Ulrich

Nature communications

2023 Volume 14, Issue 1, Page(s) 8270

Abstract: There is currently little information about the evolution of gene clusters, genome architectures and karyotypes in early branching animals. Slowly evolving anthozoan cnidarians can be particularly informative about the evolution of these genome features. ...

Abstract	There is currently little information about the evolution of gene clusters, genome architectures and karyotypes in early branching animals. Slowly evolving anthozoan cnidarians can be particularly informative about the evolution of these genome features. Here we report chromosome-level genome assemblies of two related anthozoans, the sea anemones Nematostella vectensis and Scolanthus callimorphus. We find a robust set of 15 chromosomes with a clear one-to-one correspondence between the two species. Both genomes show chromosomal conservation, allowing us to reconstruct ancestral cnidarian and metazoan chromosomal blocks, consisting of at least 19 and 16 ancestral linkage groups, respectively. We show that, in contrast to Bilateria, the Hox and NK clusters of investigated cnidarians are largely disintegrated, despite the presence of staggered hox/gbx expression in Nematostella. This loss of microsynteny conservation may be facilitated by shorter distances between cis-regulatory sequences and their cognate transcriptional start sites. We find no clear evidence for topologically associated domains, suggesting fundamental differences in long-range gene regulation compared to vertebrates. These data suggest that large sets of ancestral metazoan genes have been retained in ancestral linkage groups of some extant lineages; yet, higher order gene regulation with associated 3D architecture may have evolved only after the cnidarian-bilaterian split.
MeSH term(s)	Animals ; Sea Anemones/genetics ; Phylogeny ; Synteny/genetics ; Gene Expression Regulation ; Genome/genetics
Language	English
Publishing date	2023-12-13
Publishing country	England
Document type	Journal Article
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-023-44080-7
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Article ; Online: An adaptable chromosome preparation methodology for use in invertebrate research organisms.

Guo, Longhua / Accorsi, Alice / He, Shuonan / Guerrero-Hernández, Carlos / Sivagnanam, Shamilene / McKinney, Sean / Gibson, Matthew / Sánchez Alvarado, Alejandro

BMC biology

2018 Volume 16, Issue 1, Page(s) 25

Abstract: Background: The ability to efficiently visualize and manipulate chromosomes is fundamental to understanding the genome architecture of organisms. Conventional chromosome preparation protocols developed for mammalian cells and those relying on species- ... ...

Abstract	Background: The ability to efficiently visualize and manipulate chromosomes is fundamental to understanding the genome architecture of organisms. Conventional chromosome preparation protocols developed for mammalian cells and those relying on species-specific conditions are not suitable for many invertebrates. Hence, a simple and inexpensive chromosome preparation protocol, adaptable to multiple invertebrate species, is needed. Results: We optimized a chromosome preparation protocol and applied it to several planarian species (phylum Platyhelminthes), the freshwater apple snail Pomacea canaliculata (phylum Mollusca), and the starlet sea anemone Nematostella vectensis (phylum Cnidaria). We demonstrated that both mitotically active adult tissues and embryos can be used as sources of metaphase chromosomes, expanding the potential use of this technique to invertebrates lacking cell lines and/or with limited access to the complete life cycle. Simple hypotonic treatment with deionized water was sufficient for karyotyping; growing cells in culture was not necessary. The obtained karyotypes allowed the identification of differences in ploidy and chromosome architecture among otherwise morphologically indistinguishable organisms, as in the case of a mixed population of planarians collected in the wild. Furthermore, we showed that in all tested organisms representing three different phyla this protocol could be effectively coupled with downstream applications, such as chromosome fluorescent in situ hybridization. Conclusions: Our simple and inexpensive chromosome preparation protocol can be readily adapted to new invertebrate research organisms to accelerate the discovery of novel genomic patterns across the branches of the tree of life.
MeSH term(s)	Animals ; Chromosomes/chemistry ; Chromosomes/genetics ; Embryo, Nonmammalian/chemistry ; Embryo, Nonmammalian/physiology ; Invertebrates ; Karyotyping/methods ; Mollusca/chemistry ; Mollusca/genetics ; Planarians/chemistry ; Planarians/genetics ; Platyhelminths/chemistry ; Platyhelminths/genetics ; Sea Anemones/chemistry ; Sea Anemones/genetics ; Snails/chemistry ; Snails/genetics
Language	English
Publishing date	2018-02-26
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1741-7007
ISSN (online)	1741-7007
DOI	10.1186/s12915-018-0497-4
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Article ; Online: An axial Hox code controls tissue segmentation and body patterning in

He, Shuonan / Del Viso, Florencia / Chen, Cheng-Yi / Ikmi, Aissam / Kroesen, Amanda E / Gibson, Matthew C

Science (New York, N.Y.)

2018 Volume 361, Issue 6409, Page(s) 1377–1380

Abstract: Hox genes encode conserved developmental transcription factors that govern anterior-posterior (A-P) pattering in diverse bilaterian animals, which display bilateral symmetry. Although Hox genes are also present within Cnidaria, these simple animals lack ... ...

Abstract	Hox genes encode conserved developmental transcription factors that govern anterior-posterior (A-P) pattering in diverse bilaterian animals, which display bilateral symmetry. Although Hox genes are also present within Cnidaria, these simple animals lack a definitive A-P axis, leaving it unclear how and when a functionally integrated Hox code arose during evolution. We used short hairpin RNA (shRNA)-mediated knockdown and CRISPR-Cas9 mutagenesis to demonstrate that a Hox-Gbx network controls radial segmentation of the larval endoderm during development of the sea anemone
MeSH term(s)	Animals ; Bacterial Proteins ; Body Patterning/genetics ; CRISPR-Cas Systems ; Endoderm/cytology ; Endoderm/growth & development ; Endonucleases ; Gene Expression Regulation, Developmental ; Gene Knockdown Techniques/methods ; Genes, Homeobox/genetics ; Genes, Homeobox/physiology ; Larva/cytology ; Larva/genetics ; Larva/growth & development ; Mutagenesis ; RNA, Small Interfering/genetics ; Sea Anemones/cytology ; Sea Anemones/genetics ; Sea Anemones/growth & development ; Transcription Factors/genetics ; Transcription Factors/physiology
Chemical Substances	Bacterial Proteins ; RNA, Small Interfering ; Transcription Factors ; Cas9 endonuclease Streptococcus pyogenes (EC 3.1.-) ; Endonucleases (EC 3.1.-)
Language	English
Publishing date	2018-09-27
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	128410-1
ISSN	1095-9203 ; 0036-8075
ISSN (online)	1095-9203
ISSN	0036-8075
DOI	10.1126/science.aar8384
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Article: Urban green spaces as potential habitats for introducing a native endangered plant, Calycanthus chinensis

Pan, Kaixuan / Lu, Yijun / He, Shuonan / Yang, Guofu / Chen, Yi / Fan, Xing / Ren, Yuan / Wang, Meng / Zhu, Kangdi / Shen, Qi / Jiang, Yueping / Shi, Yan / Meng, Panpan / Tang, Yuli / Chang, Jie / Ge, Ying

Urban forestry & urban greening. 2019 Dec., v. 46

2019

Abstract: Ex situ conservation in urban areas is an essential complementary approach to in situ conservation in wild areas. In this study, we combined multiple approaches, including vegetation investigations for both natural habitats and urban green spaces, eco- ... ...

Abstract	Ex situ conservation in urban areas is an essential complementary approach to in situ conservation in wild areas. In this study, we combined multiple approaches, including vegetation investigations for both natural habitats and urban green spaces, eco-physiological experiments and remote sensing investigations for urban green spaces, to identify potential habitats for introducing the endangered plant species Calycanthus chinensis to urban green spaces. The results showed that (1) C. chinensis prefer living under sparse forests with canopy densities of 20–60%; (2) C. chinensis was not a shade tolerant species due to its chlorophyll a/b ratio (2.58) being higher than the threshold (2.3) for shade tolerant species; (3) the large and thin leaves of C. chinensis are easily damaged by strong wind, so this species can only live under moderate canopy cover; (4) to maintain a sparse crown for the well-being of C. chinensis, the upper layer trees in urban green spaces need to be thinned slightly; and (5) introducing this endangered species increases biodiversity and ecosystem services of urban green spaces. Finally, this study provides a framework and a case study for using urban green spaces as micro-refuges for endangered species.
Keywords	Calycanthus chinensis ; biodiversity ; canopy ; case studies ; chlorophyll ; ecophysiology ; ecosystem services ; endangered species ; ex situ conservation ; forests ; green infrastructure ; habitats ; in situ conservation ; indigenous species ; leaves ; remote sensing ; shade tolerance ; trees ; urban areas ; wind speed
Language	English
Dates of publication	2019-12
Publishing place	Elsevier GmbH
Document type	Article
ISSN	1618-8667
DOI	10.1016/j.ufug.2019.126444
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Article ; Online: Capicua controls Toll/IL-1 signaling targets independently of RTK regulation.

Papagianni, Aikaterini / Forés, Marta / Shao, Wanqing / He, Shuonan / Koenecke, Nina / Andreu, María José / Samper, Núria / Paroush, Ze'ev / González-Crespo, Sergio / Zeitlinger, Julia / Jiménez, Gerardo

Proceedings of the National Academy of Sciences of the United States of America

2018 Volume 115, Issue 8, Page(s) 1807–1812

Abstract: The HMG-box protein Capicua (Cic) is a conserved transcriptional repressor that functions downstream of receptor tyrosine kinase (RTK) signaling pathways in a relatively simple switch: In the absence of signaling, Cic represses RTK-responsive genes by ... ...

Abstract	The HMG-box protein Capicua (Cic) is a conserved transcriptional repressor that functions downstream of receptor tyrosine kinase (RTK) signaling pathways in a relatively simple switch: In the absence of signaling, Cic represses RTK-responsive genes by binding to nearly invariant sites in DNA, whereas activation of RTK signaling down-regulates Cic activity, leading to derepression of its targets. This mechanism controls gene expression in both
MeSH term(s)	Animals ; Basic Helix-Loop-Helix Transcription Factors/genetics ; Basic Helix-Loop-Helix Transcription Factors/metabolism ; Cell Nucleus/genetics ; Cell Nucleus/metabolism ; Drosophila/embryology ; Drosophila/enzymology ; Drosophila/genetics ; Drosophila/metabolism ; Drosophila Proteins/genetics ; Drosophila Proteins/metabolism ; Female ; Gene Expression Regulation, Developmental ; HMGB Proteins/genetics ; HMGB Proteins/metabolism ; Male ; Nuclear Proteins/genetics ; Nuclear Proteins/metabolism ; Phosphoproteins/genetics ; Phosphoproteins/metabolism ; Promoter Regions, Genetic ; Receptor Protein-Tyrosine Kinases/genetics ; Receptor Protein-Tyrosine Kinases/metabolism ; Repressor Proteins/genetics ; Repressor Proteins/metabolism ; Signal Transduction ; Toll-Like Receptors/genetics ; Toll-Like Receptors/metabolism ; Transcription Factors/genetics ; Transcription Factors/metabolism
Chemical Substances	Basic Helix-Loop-Helix Transcription Factors ; Drosophila Proteins ; HMGB Proteins ; Nuclear Proteins ; Phosphoproteins ; Repressor Proteins ; Tl protein, Drosophila ; Toll-Like Receptors ; Transcription Factors ; cic protein, Drosophila ; dl protein, Drosophila ; gro protein, Drosophila ; Receptor Protein-Tyrosine Kinases (EC 2.7.10.1) ; tor protein, Drosophila (EC 2.7.10.1)
Language	English
Publishing date	2018-02-05
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	209104-5
ISSN	1091-6490 ; 0027-8424
ISSN (online)	1091-6490
ISSN	0027-8424
DOI	10.1073/pnas.1713930115
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