Ancient origins of axial patterning genes: Hox genes and ParaHox genes in the Cnidaria
Abstract
Among the bilaterally symmetrical, triploblastic animals (the Bilateria), a conserved set of developmental regulatory genes are known to function in patterning the anterior-posterior (AP) axis. This set includes the well-studied Hox cluster genes, and the recently described genes of the ParaHox cluster, which is believed to be the evolutionary sister of the Hox cluster (Brooke et al. 1998). The conserved role of these axial patterning genes in animals as diverse as frogs and flies is believed to reflect an underlying homology (i.e., all bilaterians derive from a common ancestor which possessed an AP axis and the developmental mechanisms responsible for patterning the axis). However, the origin and early evolution of Hox genes and ParaHox genes remain obscure. Repeated attempts have been made to reconstruct the early evolution of Hox genes by analyzing data from the triphoblastic animals, the Bilateria (Schubert et al. 1993; Zhang and Nei 1996). A more precise dating of Hox origins has been elusive due to a lack of sufficient information from outgroup taxa such as the phylum Cnidaria (corals, hydras, jellyfishes, and sea anemones). In combination with outgroup taxa, another potential source of information about Hox origins is outgroup genes (e.g., the genes of the ParaHox cluster). In this article, we present cDNA sequences of two Hox-like genes (anthox2 and anthox6) from the sea anemone, Nematostella vectensis. Phylogenetic analysis indicates that anthox2 (= Cnox2) is homologous to the GSX class of ParaHox genes, and anthox6 is homologous to the anterior class of Hox genes. Therefore, the origin of Hox genes and ParaHox genes occurred prior to the evolutionary split between the Cnidaria and the Bilateria and predated the evolution of the anterior-posterior axis of bilaterian animals. Our analysis also suggests that the central Hox class was invented in the bilaterian lineage, subsequent to their split from the Cnidaria.
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Hox genes in Nematostella and other cnidarians are expressed in spatial patterns consistent with an ancient role in embryonic development.
“Hox genes in Nematostella and other cnidarians are also expressed in spatial patterns consistent with an ancient role in embryonic development (54)(55)(56).”
From Sea Anemone Genome Reveals Ancestral Eumetazoan Gene Repertoire and Genomic Organization (2007) · cites this paper as [55]
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Self-citationExpansion of the SOX gene family predated the emergence of the Bilateria
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“Cathepsin is a protease that functions in phagolysosomes to aid in the destruction of phagocytosed pathogens and is broadly expressed in pigment cells, glia, and undetermined mesenchymal cells in planaria.(40,84,85) Additionally, cathepsin is considered an important modulator during wound healing by the degradation of…”
BackgroundHox and Wnt pattern the primary body axis of an anthozoan cnidarian before gastrulation
DuBuc, T. Q., Stephenson, T. B., Rock, A. Q., & Martindale, M. Q. (2018) · Nature Communications · doi:10.1038/s41467-018-04184-x · Cited by 73 · see citing works
Self-citationThe genetic factors of bilaterian evolution
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Sanetra, M., Begemann, G., Becker, M.-B., & Meyer, A. (2005) · Frontiers in Zoology · doi:10.1186/1742-9994-2-15 · Cited by 58 · see citing works
“In another example, the use of homologous genes to achieve bilateral symmetry in larvae of sea anemones was used to infer that bilaterality originated before the split of Cnidaria and Bilateria [82] (Fig.”
BackgroundInfluentialSchaffer, A., Bazarsky, M., Levy, K., Caspi, V. C., & Gat, U. (2016) · BMC Genomics · doi:10.1186/s12864-016-3027-1 · Cited by 58 · see citing works
Origin and evolution of the metazoan non-coding regulatory genome
Gaiti, F., Calcino, A., Tanurdžić, M., & Degnan, B. M. (2016) · Developmental Biology · doi:10.1016/j.ydbio.2016.11.013 · Cited by 58 · see citing works
Conserved and divergent genes in apex and axis development of cnidarians
Galliot, B. (2000) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(00)00141-6 · Cited by 56 · see citing works
Dunlap, W. C., Starčević, A., Baranas̆ić, D., Diminić, J., Žučko, J., Gaćeša, R., van Oppen, M. J. H., Hranueli, D., Cullum, J., & Long, P. F. (2013) · BMC Genomics · doi:10.1186/1471-2164-14-509 · Cited by 55 · see citing works
“Hox genes are well characterised in cnidarians and, given their importance in embryonic development, it is not surprising that molecular evidence from the Cnidaria reveal that the genetic origins of Hox genes predate the cnidarian-bilaterian divergence [83-85] yet had evolved after divergence of the sponge and eumetaz…”
BackgroundEvo-Devo: the long and winding road
Baguñà, J., & García‐Fernàndez, J. (2003) · The International Journal of Developmental Biology · doi:10.1387/ijdb.14756346 · Cited by 55 · see citing works
Genesis and evolution of the Evx and Moxgenes and the extended Hox and ParaHox gene clusters
Minguillón, C., & García‐Fernàndez, J. (2003) · Genome biology · doi:10.1186/gb-2003-4-2-r12 · Cited by 55 · see citing works
“The clustering of the Antennapedia superclass of homeobox genes in contemporary genomes is proposed to be the outcome of tandem gene duplication and cluster duplications from an ancestral UrArcheHox gene during metazoan evolution [2,3].”
BackgroundCombined-method phylogenetic analysis of Hox and ParaHox genes of the metazoa
Kourakis, M. J., & Martindale, M. Q. (2000) · Journal of Experimental Zoology · doi:10.1002/1097-010x(20000815)288:2 · Cited by 51 · see citing works
Self-citationCurrent problems with the zootype and the early evolution of Hox genes
Schierwater, B., & DeSalle, R. (2001) · Journal of Experimental Zoology · doi:10.1002/jez.1066 · Cited by 49 · see citing works
“This hypothesis is readily tested given recent studies on Hox genes and their function in cnidarian and more basal diploblastic animals (Martinez et al., ’98; Schierwater and Kuhn, ’98; Finnerty and Martindale, ’99).”
BackgroundHox and ParaHox genes in Nemertodermatida, a basal bilaterian clade
Jiménez-Guri, E., Paps, J., García‐Fernàndez, J., & Saló, E. (2006) · The International Journal of Developmental Biology · doi:10.1387/ijdb.062167ej · Cited by 47 · see citing works
“…genes) implies the genesis, by tandem duplication, of the central Hox gene in the Hox cluster, after the duplication of the ProtoHox cluster (Finnerty and Martindale, 1999; Ferrier and Holland, 2001); the 2-gene cluster model (one anterior, one posterior) implies the genesis, after the…”
BackgroundEvidence for a Dispersed Hox Gene Cluster in the Platyhelminth Parasite Schistosoma mansoni
Pierce, R. J., Wu, W., Hirai, H., Ivens, A. C., Murphy, L., Noël, C. J., Johnston, D. A., Artiguenave, F., Adams, M., Cornette, J., et al. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msi239 · Cited by 46 · see citing works
“…analysis and Southern blotting provided evidence for the existence of a Hox cluster in N. vectensis (Finnerty 2001), and the presence of both Hox and ParaHox genes (Finnerty and Martindale 1999) further supports the hypothesis that the Hox cluster originated before the emergence of cnidarians.”
BackgroundMechanisms of tentacle morphogenesis in the sea anemone Nematostella vectensis
Fritz, A. E., Ikmi, A., Seidel, C. W., Paulson, A., & Gibson, M. C. (2013) · Development · doi:10.1242/dev.088260 · Cited by 45 · see citing works
“Accordingly, the genome encodes many proteins known to be involved in appendage development of arthropods and vertebrates, including a Hox gene cluster (Finnerty and Martindale, 1999; Chourrout et al., 2006), Fibroblast growth factors (FGFs) (Matus et al.”
BackgroundPhylogenetic Context and Basal Metazoan Model Systems
Collins, A. G. (2005) · Integrative and Comparative Biology · doi:10.1093/icb/45.4.585 · Cited by 45 · see citing works
“This gene, along with the Trichoplax gene Trox-2, has been proposed to be either a gsx parahox homolog (Finnerty and Martindale, 1999; Finnerty et al., 2003) or a protohox gene belonging to the Diplox-2 gene family, which also contains the Trichoplax gene Trox-2 (Schierwater and Kuhn, 1998; Jakob et al.”
Agarwal, N., Guerra, J. C., Gala, N. B., Agarwal, P., Zouzias, A. D., Gandhi, C. D., & Prestigiacomo, C. J. (2013) · World Neurosurgery · doi:10.1016/j.wneu.2013.01.031 · Cited by 44 · see citing works
“0 DTD and Martindale determined that pregnancy does not increase the risk of hemorrhage (21).”
BackgroundKulakova, M. A., Cook, C. E., & Andreeva, T. F. (2008) · BMC Developmental Biology · doi:10.1186/1471-213x-8-61 · Cited by 44 · see citing works
“Holland [10] suggested that this function has been lost for Gsh because the position of the mouth has changed in this branch of the Bilateria.”
InfluentialFossils, genes, and the origin of novelty
Shubin, N. H., & Marshall, C. R. (2000) · Paleobiology · doi:10.1666/0094-8373(2000)26[324:fgatoo]2.0.co;2 · Cited by 45 · see citing works
The Precambrian emergence of animal life: a geobiological perspective
Gaidos, E. J., DuBuc, T. Q., Dunford, M. D., MCANDREW, P., PADILLA‐GAMIÑO, J., STUDER, B., Weersing, K., & Stanley, S. M. (2007) · Geobiology · doi:10.1111/j.1472-4669.2007.00125.x · Cited by 38 · see citing works
“The picture has been complicated by the discovery of the ParaHox sister group (Brooke et al., 1998) and the finding that cnidarians, diploblasts with only rudimentary (or vestigial) symmetry, possess both Hox and ParaHox genes (Finnerty & Martindale, 1999).”
BackgroundDating branches on the tree of life using DNA.
Wray, G. A. (2001) · Genome biology · doi:10.1186/gb-2001-3-1-reviews0001 · Cited by 37 · see citing works
“For instance, the idea that the origin of the Hox cluster of homeobox-containing developmental control genes directly triggered the diversification of bilaterian animals is not supported, as the Hox cluster predates the appearance of most metazoan body plans by a substantial interval [25].”
BackgroundMore constraint on ParaHox than Hox gene families in early metazoan evolution
Quiquand, M., Yanze, N., Schmich, J., Schmid, V. J., Galliot, B., & Piraino, S. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.01.022 · Cited by 37 · see citing works
“The A-3-P three-gene model is based on evolutionary parsimony (Finnerty and Martindale, 1999; Ferrier and Holland, 2001a): The apparent absence of central ParaHox genes in bilaterians and cnidarians, coupled with the lack of central Hox genes in cnidarians, suggested a simpler, three-gene composition of the original P…”
MethodThe cell specificity of gene expression in the response to heat stress in corals
Traylor‐Knowles, N., Rose, N. H., & Palumbi, S. R. (2017) · Journal of Experimental Biology · doi:10.1242/jeb.155275 · Cited by 37 · see citing works
“Within cnidarians, this method has been primarily used in the model systems Hydra and Nematostella vectensis (Finnerty and Martindale, 1999; Kurz et al., 1991; Wolenski et al., 2013a,b).”
MethodOsborne, P. W., Benoit, G., Laudet, V., Schubert, M., & Ferrier, D. E. K. (2008) · Developmental Biology · doi:10.1016/j.ydbio.2008.11.027 · Cited by 36 · see citing works
“The three ParaHox gene families, Gsx (or Gsh or ind), Xlox (or Xlhbox8, IPF1, PDX1, IDX1, STF1 or Lox3) and Cdx (or caudal/cad) are widespread within Bilateria (Ferrier and Holland, 2001a) and at the origin of chordates the ParaHox genes were linked in a tight cluster with Xlox located between Gsx and Cdx (Brooke et a…”
BackgroundSamadi, L., & Steiner, G. (2010) · BMC Developmental Biology · doi:10.1186/1471-213x-10-74 · Cited by 35 · see citing works
“Thus, they are considered evolutionary sister (or paralogue) clusters [1-7].”
BackgroundThomas‐Chollier, M., Ledent, V., Leyns, L., & Vervoort, M. (2010) · BMC Evolutionary Biology · doi:10.1186/1471-2148-10-73 · Cited by 33 · see citing works
“Gsx genes have been reported to be closer to Hox Anterior group genes, Xlox to PG3 genes, and Cdx to Hox Posterior genes [13,25-27].”
Hox and ParaHox Genes in Flatworms: Characterization and Expression1
Saló, E., Tauler, J., Jiménez-Guri, E., Bayascas, J. R., González-Linares, J., García‐Fernàndez, J., & Baguñà, J. (2001) · American Zoologist · doi:10.1668/0003-1569(2001)041[0652:hapgif]2.0.co;2 · Cited by 31 · see citing works
“Phylogenetic evidence suggests that Hox and ParaHox cluster are sister clusters, both being descendants from an ancestral ProtoHox cluster (Brooke et al., 1998; Finnerty and Martindale, 1999).”
BackgroundIs the evolution of Cnox-2 Hox/ParaHox genes “multicolored” and “polygenealogical?”
Schierwater, B., Dellaporta, S. L., & DeSalle, R. (2002) · Molecular Phylogenetics and Evolution · doi:10.1016/s1055-7903(02)00238-5 · Cited by 31 · see citing works
“Up to five Hox genes have been found in a single cnidarian (Finnerty and Martindale, 1999; Kuhn et al., 1996, 1999).”
BackgroundChanging Hydrozoan Bauplans by Silencing Hox-Like Genes
Jakob, W., & Schierwater, B. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000694 · Cited by 29 · see citing works
“, 2004 [56,45,17]”
Cnidarians Reveal Intermediate Stages in the Evolution of Hox Clusters and Axial Complexity
Finnerty, J. R. (2001) · American Zoologist · doi:10.1093/icb/41.3.608 · Cited by 27 · see citing works
Self-citationIsolation of Hox and ParaHox genes in the bivalve Pecten maximus
Canapa, A., Biscotti, M. A., Olmo, E., & Barucca, M. (2005) · Gene · doi:10.1016/j.gene.2004.12.039 · Cited by 25 · see citing works
Conserved and novel roles for the Gsh2 transcription factor in primary neurogenesis
Winterbottom, E. F., Illes, J. C., Faas, L., & Isaacs, H. V. (2010) · Development · doi:10.1242/dev.047159 · Cited by 24 · see citing works
“ParaHox genes have been identified both in cnidarian species and in all major branches of bilaterians (Brooke et al., 1998; Finnerty and Martindale, 1999; Frobius and Seaver, 2006; Hui et al., 2009; Ryan et al., 2007), and their products play conserved roles in the regulation of tissue patterning and differentiation d…”
Developmental Insights into the Origin of Complex Colonial Hydrozoans
Cartwright, P. (2003) · Integrative and Comparative Biology · doi:10.1093/icb/43.1.82 · Cited by 23 · see citing works
“Cnox-2 has been classified as an ortholog of the ParaHox gene GSX (Finnerty and Martindale, 1999).”
BackgroundSullivan, J. C., Reitzel, A. M., & Finnerty, J. R. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm941 · Cited by 23 · see citing works
“The emergence of Nematostella vectensis as a model system began with the developmental and field studies of Hand and Uhlinger in the early 1990s (16–18), and it gained momentum with the publication of the first molecular studies (19, 20 ), which demonstrated that the starlet sea anemone could yield key insights into e…”
BackgroundSelf-citationGene Loss may have Shaped the Cnidarian and Bilaterian Hox and ParaHox Complement
Steinworth, B. M., Martindale, M. Q., & Ryan, J. F. (2022) · Genome Biology and Evolution · doi:10.1093/gbe/evac172 · Cited by 22 · see citing works
Self-citationHox and paraHox genes in bivalve molluscs
Barucca, M., Olmo, E., & Canapa, A. (2003) · Gene · doi:10.1016/s0378-1119(03)00657-7 · Cited by 21 · see citing works
Coral biodiversity and evolution: recent molecular contributions
Uri Frank, A., & Mokady, O. (2002) · Canadian Journal of Zoology · doi:10.1139/z02-131 · Cited by 20 · see citing works
Beyond the Hox: how widespread is homeobox gene clustering?
Holland, P. W. H. (2001) · Journal of Anatomy · doi:10.1046/j.1469-7580.2001.19910013.x · Cited by 20 · see citing works
Missing link in the evolution of Hox clusters
Ogishima, S., & Tanaka, H. (2006) · Gene · doi:10.1016/j.gene.2006.08.011 · Cited by 20 · see citing works
Ferrier, D. E. K. (2010) · Advances in experimental medicine and biology · doi:10.1007/978-1-4419-6673-5_6 · Cited by 19 · see citing works
Expression of aGsx parahox gene,Cnox-2, in colony ontogeny inHydractinia (Cnidaria: Hydrozoa)
Cartwright, P., Schierwater, B., & Buss, L. W. (2006) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.21106 · Cited by 19 · see citing works
The Role of Hox Genes in Axial Patterning in Hydra1
Bode, H. R. (2001) · American Zoologist · doi:10.1668/0003-1569(2001)041[0621:trohgi]2.0.co;2 · Cited by 18 · see citing works
“References for the several eh1/GEH domains are Xgsc: Blumberg et al., 1991; Dgsc: Goriely et al., 1996; Cngsc: Broun et al., 1999; en (DM): Poole et al., 1985; en (Ce): Wilson et al., 1994; NK2: Kim and Nirenberg, 1989; CnNK2: Grens et al., 1996; Cnox-2; Shenk et al., 1993a; Anthox2: Finnerty and Martindale, 1999; Gsh…”
BackgroundInfluentialStatistical Tests between Competing Hypotheses of Hox Cluster Evolution
Lanfear, R., & Bromham, L. D. (2008) · Systematic Biology · doi:10.1080/10635150802430079 · Cited by 16 · see citing works
“Second, observations from the recently sequenced cnidarian Nematostella vectensis suggest that the Cnidaria may contain only two groups of Hox and ParaHox genes, which has led to the suggestion that the ProtoHox cluster may have contained either two or three genes, rather than four (Finnerty and Martindale, 1999; Ferr…”
BackgroundDeutsch, J. S. (2010) · Advances in experimental medicine and biology · doi:10.1007/978-1-4419-6673-5 · Cited by 15 · see citing works
Dewel, R. A., Dewel, W. C., & McKinney, F. K. (2001) · Historical Biology · doi:10.1080/10292380109380592 · Cited by 14 · see citing works
“In fact, they have both Hox genes, which in bilaterians regulate colinear development of ectoderm or neuroectoderm, and ParaHox genes, which are similarly expressed in structures derived from endoderm (Brooke et al, 1998; Finnerty and Martindale, 1999; Gauchat et al, 2000; Kourakis and Martindale, 2000).”
BackgroundMoiseeva, E., Rabinowitz, C., Paz, G., & Rinkevich, B. (2017) · PLoS ONE · doi:10.1371/journal.pone.0182677 · Cited by 12 · see citing works
Evolution of Hox Gene Clusters
Ferrier, D. E. K. (2007) · Springer eBooks · doi:10.1007/978-0-387-68990-6_4 · Cited by 12 · see citing works
Hox and paraHox genes from the anthozoan Parazoanthus parasiticus
Hill, A., Wagner, A., & Hill, M. S. (2003) · Molecular Phylogenetics and Evolution · doi:10.1016/s1055-7903(03)00062-9 · Cited by 9 · see citing works
“Thus, there appear to be two distinct anterior Hox groupings in the Cnidaria, as has been suggested previously (Finnerty, 1998; Finnerty and Martindale, 1997; Finnerty and Martindale, 1999; Kourakis and Martindale, 2000), but one of the groupings may be anthozoanspecific (see Ppox4 group in Fig.”
BackgroundEstablishing a model organism: A report from the first annual Nematostella meeting
Reitzel, A. M., Ryan, J. F., & Tarrant, A. M. (2011) · BioEssays · doi:10.1002/bies.201100145 · Cited by 8 · see citing works
“Magie C, Daly M, Martindale MQ. 2007.”
BackgroundInfluentialSchmidt‐Rhaesa, A. (2007) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780198566687.003.0001 · Cited by 7 · see citing works
Hox and ParaHox Genes in Flatworms: Characterization and Expression
Saló, E., Tauler, J., Jiménez-Guri, E., Bayascas, J. R., González-Linares, J., García‐Fernàndez, J., & Baguñà, J. (2001) · American Zoologist · doi:10.1093/icb/41.3.652 · Cited by 5 · see citing works
Hox, Parahox, Ehgbox, and NK Genes in Bivalve Molluscs: Evolutionary Implications
Pérez‐Parallé, M. L., Pazos, A. J., Mesías-Gansbiller, C., & Sánchez, J. L. (2016) · Journal of Shellfish Research · doi:10.2983/035.035.0119 · Cited by 5 · see citing works
Are the Deuterostome Posterior Hox Genes a Fast-Evolving Class?
Lanfear, R. (2010) · Advances in experimental medicine and biology · doi:10.1007/978-1-4419-6673-5_8 · Cited by 5 · see citing works
Seeing ghosts: Neoproterozoic bilaterian body plans
Valentine, J. W. (2007) · Geological Society London Special Publications · doi:10.1144/sp286.26 · Cited by 5 · see citing works
“As Hox genes are known in Radiata (but not in choanoflagellates or sponges), they were presumably present in the last common ancestor of Radiata and Bilateria (see, for example, Finnerty & Martindale 1999).”
Background
- Authors
- Finnerty, J. R., & Martindale, M. Q.
- Affiliations
- University of Chicago (US)
- Corresponding author
- Martindale, Mark Q.
- Venue
- Evolution & Development
- Publisher
- Wiley
- Published
- 1999-07
- Volume
- 1
- Issue
- 1
- Pages
- 16-23
- ISSN
- 1520-541X (ISSN-L)
- 1525-142X
- OpenAlex
- W2099219158
- Cited by
- 152
- References
- 31
- Citations by year
- 2025: 1 · 2024: 6 · 2023: 1 · 2022: 1 · 2020: 3 · 2018: 2 · 2017: 2 · 2016: 5 · 2014: 3 · 2013: 4
- FWCI
- 4.59
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Evolution & Development (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- Hox genes, ParaHox genes, axial patterning, anterior-posterior axis, Cnidaria, Nematostella vectensis, outgroup taxa, sea anemone
- MeSH terms
- Amino Acid Sequence, Animals, Base Sequence, Cnidaria, DNA, Genes, Homeobox, Molecular Sequence Data, Phylogeny, Sequence Homology, Amino Acid, Body Patterning
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