CaltechAUTHORS
  A Caltech Library Service

Hmx gene conservation identifies the origin of vertebrate cranial ganglia

Papdogiannis, Vasileios and Pennati, Alessandro and Parker, Hugo J. and Rothbächer, Ute and Patthey, Cedric and Bronner, Marianne E. and Shimeld, Sebastian M. (2022) Hmx gene conservation identifies the origin of vertebrate cranial ganglia. Nature, 605 (7911). pp. 701-705. ISSN 0028-0836. doi:10.1038/s41586-022-04742-w. https://resolver.caltech.edu/CaltechAUTHORS:20200909-144305477

[img] PDF - Submitted Version
Creative Commons Attribution Non-commercial No Derivatives.

1MB
[img] PDF (Reporting Summary) - Supplemental Material
See Usage Policy.

4MB
[img] MS Word (Supplementary Information cover sheet) - Supplemental Material
See Usage Policy.

14kB
[img] MS Word (Supplementary Table 1) - Supplemental Material
See Usage Policy.

13kB
[img] Archive (ZIP) (Supplementary Files 1–9) - Supplemental Material
See Usage Policy.

2MB
[img] Image (JPEG) (Extended Data Fig. 1: Expression of jawed vertebrate Hmx genes in neural derivatives) - Supplemental Material
See Usage Policy.

299kB
[img] Image (JPEG) (Extended Data Fig. 2: Schematics of experimental strategies for reporter assays and Ciona Hmx CNE identification) - Supplemental Material
See Usage Policy.

139kB
[img] Image (JPEG) (Extended Data Fig. 3: CRISPR-Cas9 knockout of Ciona Hmx and Ciona Ngn) - Supplemental Material
See Usage Policy.

296kB
[img] Image (JPEG) (Extended Data Fig. 4: Early developmental expression of Hmx and Ngn in C. intestinalis (Type B)) - Supplemental Material
See Usage Policy.

102kB
[img] Image (JPEG) (Extended Data Fig. 5: Molecular phylogenetic analysis of chordate Hmx sequences and alignment of lamprey Hmx sequences) - Supplemental Material
See Usage Policy.

297kB
[img] Image (JPEG) (Extended Data Fig. 6: Model of evolution of vertebrate Hmx uCNE and dCNE from an ancestral udCNE) - Supplemental Material
See Usage Policy.

61kB
[img] Image (JPEG) (Extended Data Fig. 7: Assessment of background deriving from the vector used to generate lamprey transgenics) - Supplemental Material
See Usage Policy.

303kB
[img]
Preview
Image (JPEG) (Extended Data Table 1 Quantification of BTN signal in control and Hmx CRISPR knockout embryos using the Ngn or Asic markers) - Supplemental Material
See Usage Policy.

36kB
[img]
Preview
Image (JPEG) (Extended Data Table 2 Quantification of Ciona Hmx CNE activity in control and Ngn CRISPR knockout embryos) - Supplemental Material
See Usage Policy.

31kB
[img]
Preview
Image (JPEG) (Extended Data Table 3 Full count data for Ciona Hmx -2kb transgenic reporter analysis (Fig. 2e–g) and for dCNE reporter analysis in Ciona transgenic embryos (Fig. 4h)) - Supplemental Material
See Usage Policy.

88kB

Use this Persistent URL to link to this item: https://resolver.caltech.edu/CaltechAUTHORS:20200909-144305477

Abstract

The evolutionary origin of vertebrates included innovations in sensory processing associated with the acquisition of a predatory lifestyle. Vertebrates perceive external stimuli through sensory systems serviced by cranial sensory ganglia, whose neurons arise predominantly from cranial placodes; however, the understanding of the evolutionary origin of placodes and cranial sensory ganglia is hampered by the anatomical differences between living lineages and the difficulty in assigning homology between cell types and structures. Here we show that the homeobox transcription factor Hmx is a constitutive component of vertebrate sensory ganglion development and that in the tunicate Ciona intestinalis, Hmx is necessary and sufficient to drive the differentiation programme of bipolar tail neurons, cells previously thought to be homologues of neural crest. Using Ciona and lamprey transgenesis, we demonstrate that a unique, tandemly duplicated enhancer pair regulated Hmx expression in the stem-vertebrate lineage. We also show notably robust vertebrate Hmx enhancer function in Ciona, demonstrating that deep conservation of the upstream regulatory network spans the evolutionary origin of vertebrates. These experiments demonstrate regulatory and functional conservation between Ciona and vertebrate Hmx, and point to bipolar tail neurons as homologues of cranial sensory ganglia.


Item Type:Article
Related URLs:
URLURL TypeDescription
nhttps://doi.org/10.1038/s41586-022-04742-wDOIArticle
https://rdcu.be/cOac9PublisherFree ReadCube access
https://doi.org/10.1101/2020.09.07.281501DOIDiscussion Paper
https://www.ncbi.nlm.nih.gov/gquery/?term=MN264670Related ItemData
https://www.ncbi.nlm.nih.gov/gquery/?term=MN264672Related ItemData
http://www.ncbi.nlm.nih.gov/sra?term=GSE141046Related ItemData
http://odr.stowers.org/websimr/Related ItemStowers Original Data Repository
ORCID:
AuthorORCID
Pennati, Alessandro0000-0002-2766-2966
Parker, Hugo J.0000-0001-7646-2007
Rothbächer, Ute0000-0002-9989-6139
Patthey, Cedric0000-0002-2627-9578
Bronner, Marianne E.0000-0003-4274-1862
Shimeld, Sebastian M.0000-0003-0195-7536
Alternate Title:Hmx gene conservation identifies the evolutionary origin of vertebrate cranial ganglia
Additional Information:© 2022 Nature Publishing Group. Received 14 November 2019; Accepted 07 April 2022; Published 18 May 2022. We thank A. Stolfi and R. Zeller for sharing plasmids used in the Ciona CRISPR and overexpression studies, respectively; H. Escriva for hosting C.P. and for access to his amphioxus facility; and S. Green for lamprey husbandry assistance. V.P. was supported by a Natural Motion scholarship. V.P. and S.M.S. acknowledge the Elizabeth Hannah Jenkinson fund for financial support. V.P. also thanks T. Manousaki and C. Tsigenopoulos for their support while based in HCMR. A.P. was supported by the Accademia Nazionale dei Lincei while working in Oxford and by the H2020 Marie Sklodowska-Curie COFUND ARDRE to U.R. while working in Innsbruck. C.P. was supported by an EMBO Long Term Fellowship while working in Oxford. M.E.B. acknowledges support from award R35NS111564 from the NIH. H.J.P. was supported by funds from the Stowers Institute (grant no. 1001). Data availability: Cloned Hmx gene sequences have been deposited in Genbank accessions MN264670–MN264672. RNA-seq data have been deposited in SRA accession GSE141046. Original data underlying Fig. 4b, c of this manuscript can be accessed from the Stowers Original Data Repository at http://odr.stowers.org/websimr/. Contributions: V.P., C.P and S.M.S. conceived the study. V.P. conducted lamprey gene expression analysis, CNE identification, analysis of lamprey reporter gene experiments, Ciona Hmx expression analysis, Ciona Hmx overexpression analysis and RNA-seq and the molecular phylogenetic analyses. A.P. conducted Ciona CNE identification and reporter gene experiments, tests of lamprey CNE activity in Ciona, CRISPR and overexpression reporter analyses, and analysis of Ciona Hmx and Ngn gene expression. C.P. conducted the amphioxus in situ hybridization and participated in RNA-seq data analysis. H.J.P. conducted the lamprey reporter construct injections and analysis. U.R., M.E.B. and S.M.S. supervised the work. All authors contributing to drafting and editing the manuscript. The authors declare no competing interests. Peer review information: Nature thanks Noriyuki Satoh and the other, anonymous reviewers for their contribution to the peer review of this work.
Funders:
Funding AgencyGrant Number
Natural Motion ScholarshipUNSPECIFIED
Elizabeth Hannah Jenkinson FundUNSPECIFIED
Accademia Nazionale dei LinceiUNSPECIFIED
Marie Curie FellowshipUNSPECIFIED
European Molecular Biology Organization (EMBO)UNSPECIFIED
NIHR35NS111564
Stowers Institute1001
Subject Keywords:Embryology; Evolutionary developmental biology
Issue or Number:7911
DOI:10.1038/s41586-022-04742-w
Record Number:CaltechAUTHORS:20200909-144305477
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20200909-144305477
Official Citation:Papadogiannis, V., Pennati, A., Parker, H.J. et al. Hmx gene conservation identifies the origin of vertebrate cranial ganglia. Nature 605, 701–705 (2022). https://doi.org/10.1038/s41586-022-04742-w
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:105301
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:09 Sep 2020 21:55
Last Modified:07 Jun 2022 22:14

Repository Staff Only: item control page