Cited by 9Marine Invertebrate Physiology and EcologyDevelopmental Biology and Gene RegulationNeurogenesis and neuroplasticity mechanisms

Early evolution of the LIM homeobox gene family

Open access
Srivastava, Mansi, Larroux, Claire, Lu, Daniel R, Mohanty, Kareshma, Chapman, Jarrod, Degnan, Bernard M, Rokhsar, Daniel S·2010·BMC Biology

Abstract

BACKGROUND: LIM homeobox (Lhx) transcription factors are unique to the animal lineage and have patterning roles during embryonic development in flies, nematodes and vertebrates, with a conserved role in specifying neuronal identity. Though genes of this family have been reported in a sponge and a cnidarian, the expression patterns and functions of the Lhx family during development in non-bilaterian phyla are not known. RESULTS: We identified Lhx genes in two cnidarians and a placozoan and report the expression of Lhx genes during embryonic development in Nematostella and the demosponge Amphimedon. Members of the six major LIM homeobox subfamilies are represented in the genomes of the starlet sea anemone, Nematostella vectensis, and the placozoan Trichoplax adhaerens. The hydrozoan cnidarian, Hydra magnipapillata, has retained four of the six Lhx subfamilies, but apparently lost two others. Only three subfamilies are represented in the haplosclerid demosponge Amphimedon queenslandica. A tandem cluster of three Lhx genes of different subfamilies and a gene containing two LIM domains in the genome of T. adhaerens (an animal without any neurons) indicates that Lhx subfamilies were generated by tandem duplication. This tandem cluster in Trichoplax is likely a remnant of the original chromosomal context in which Lhx subfamilies first appeared. Three of the six Trichoplax Lhx genes are expressed in animals in laboratory culture, as are all Lhx genes in Hydra. Expression patterns of Nematostella Lhx genes correlate with neural territories in larval and juvenile polyp stages. In the aneural demosponge, A. queenslandica, the three Lhx genes are expressed widely during development, including in cells that are associated with the larval photosensory ring. CONCLUSIONS: The Lhx family expanded and diversified early in animal evolution, with all six subfamilies already diverged prior to the cnidarian-placozoan-bilaterian last common ancestor. In Nematostella, Lhx gene expression is correlated with neural territories in larval and juvenile polyp stages. This pattern is consistent with a possible role in patterning the Nematostella nervous system. We propose a scenario in which Lhx genes play a homologous role in neural patterning across eumetazoans.

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  • The study examined expression patterns of several transcription factor families (Fox, Klf, Lhx, Nkx, Nr, Pax, Pou, Prdm, Sox, Tbx), all of which have been shown to have important roles in spatial patterning, cell-type specification and differentiation during development.

    “We examined the expression patterns of several transcription factor families (Extended Data Fig. 13), including forkhead box (Fox), Krüppel-like factor (Klf), LIM homeobox (Lhx), NKX-homeodomain (Nkx), nuclear receptor (Nr), Paired box (Pax), POU domain (Pou), positive regulatory domain (Prdm), SRY-related HMG-box (Sox), and T-box (Tbx), all of which have been shown to have important roles in”

    From A high-resolution transcriptomic and spatial atlas of cell types in the whole mouse brain (2023) · cites this paper as [106]

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  • The grouping of Lhx members based on their gene expression patterns exactly matches their phylogeny tree based on their coding sequences and aligns with the sub-family definition.

    “The grouping of Lhx members based on their gene expression patterns exactly matches their phylogeny tree based on their coding sequences106 and aligns with the sub-family definition.”

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Research works printed but not linked: 3

  1. Greenspan RJ An introduction to nervous systems 2007 Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press
  2. Lentz TL Primitive Nervous Systems 1968 New Haven: Yale University Press
  3. Bürglin TR Duboule D A comprehensive classification of homeobox genes Guidebook to the Homeobox Genes 1994 New York: Oxford University Press 35 72

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Authors
Srivastava, M., Larroux, C., Lu, D. R., Mohanty, K., Chapman, J., Degnan, B. M., & Rokhsar, D. S.
Affiliations
  • University of California, Berkeley (US)
  • The University of Queensland (AU)
  • Joint Genome Institute (US)
Corresponding author
Srivastava, Mansi
Venue
BMC Biology
Published
2010-01-18
Volume
8
Issue
1
Pages
4-4
ISSN
1741-7007 (ISSN-L)
OpenAlex
W60522037
Cited by
1
References
67
Citations by year
2015: 1
FWCI
0.00
Type
journal article
Language
en
Open access
Locations
  • BMC Biology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
  • University of North Texas Digital Library (University of North Texas) (submittedVersion)
  • eScholarship (California Digital Library) (submittedVersion)
  • Lawrence Berkeley National Laboratory
Funders
Australian Research Council
Topics
  • Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Keywords
LIM homeobox genes, gene family evolution, Cnidaria, placozoans, Nematostella vectensis, Amphimedon queenslandica, Trichoplax adhaerens, Hydra magnipapillata, tandem duplication, neural patterning, embryonic development, gene expression patterns
MeSH terms
Animals, Hydra, Introns, Phylogeny, Sea Anemones, Homeodomain Proteins, Evolution, Molecular, Synteny, Hydrozoa, Embryonic Development, Placozoa

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