Expression of the Hox gene complex in the indirect development of a sea urchin
Open accessAbstract
Hox complex genes control spatial patterning mechanisms in the development of arthropod and vertebrate body plans. Hox genes are all expressed during embryogenesis in these groups, which are all directly developing organisms in that embryogenesis leads at once to formation of major elements of the respective adult body plans. In the maximally indirect development of a large variety of invertebrates, the process of embryogenesis leads only to a free-living, bilaterally organized feeding larva. Maximal indirect development is exemplified in sea urchins. The 5-fold radially symmetric adult body plan of the sea urchin is generated long after embryogenesis is complete, by a separate process occurring within imaginal tissues set aside in the larva. The single Hox gene complex of Strongylocentrotus purpuratus contains 10 genes, and expression of eight of these genes was measured by quantitative methods during both embryonic and larval developmental stages and also in adult tissues. Only two of these genes are used significantly during the entire process of embryogenesis per se , although all are copiously expressed during the stages when the adult body plan is forming in the imaginal rudiment. They are also all expressed in various combinations in adult tissues. Thus, development of a microscopic, free-living organism of bilaterian grade, the larva, does not appear to require expression of the Hox gene cluster as such, whereas development of the adult body plan does. These observations reflect on mechanisms by which bilaterian metazoans might have arisen in Precambrian evolution.
AI snapshot
Written from the paper’s full text.
TL;DR
In the indirect development of the sea urchin *Strongylocentrotus purpuratus*, only two of eight assayed Hox complex genes are significantly expressed during embryogenesis, while all eight are expressed during postembryonic formation of the adult body plan in the imaginal rudiment. The authors argue that the Hox cluster is not required for building the free-living bilaterian larva but is deployed for adult body plan development.
Key findings
- Of the 10 genes in the *S. purpuratus* Hox complex, eight were measured; only SpHox7 and SpHox11/13b were significantly expressed during embryogenesis, whereas SpHox2, SpHox3, SpHox4/5, SpHox8, SpHox9/10, and SpHox11/13a were not significantly expressed at any embryonic stage.
- At 48 h in the 1,000-cell embryo, transcript numbers were approximately SpHox2 ≈330, SpHox4/5 ≈250, SpHox6 ≈150, SpHox9/10 ≈190, and SpHox11/13a ≈130 per embryo, with SpHox3 undetectable; SpHox7 had 30–100 transcripts per active cell between 48 and 72 h, and SpHox11/13b had ≥30–40 transcripts per active cell.
- By 2–3 weeks, when the adult rudiment is forming, all eight Hox genes studied were expressed at levels from a few thousand to more than 20,000 molecules per larva, and levels were even higher in newly emergent juveniles.
- Adult tissues showed combinatorial Hox expression: coelomocytes expressed SpHox8 far more than other genes; ovary and testis expressed SpHox2, 3, 7, 8, 9/10, and 11/13b but much less SpHox4/5 and SpHox11/13a; body wall preferentially expressed SpHox3.
Methods
- Probe excess RNA titrations with antisense RNA probes were used to quantify transcript numbers for eight Hox genes across embryonic stages, 2-week and 3-week larvae, emergent juveniles, and adult tissues; controls included SpZ12–1 and CyIIIa mRNAs.
- Whole-mount in situ hybridization (WMISH) was used for spatial expression, including SpHox3 in the larval rudiment.
- Larvae were raised in the laboratory and harvested at stages including egg, blastula, 48–72 h pluteus, 2 weeks, 3 weeks, and after metamorphosis at about 5–6 weeks.
Limitations
- The paper states that negative WMISH data are not informative, motivating the titration approach; it also notes that much additional work is required to understand the roles of these genes in rudiment development, with detailed expression studies in progress.
- The authors state that for most genes they cannot exclude the possibility that low transcript levels are confined to a few cells, and they suggest low numbers may represent rare nuclear RNAs that are not processed in the embryo.
- Evident from the text: only eight of the 10 Hox complex genes were assayed, and the study reports expression patterns rather than functional perturbation, so roles in larval or adult development are inferred from transcript abundance and localization.
Model-written summary. Check it against the paper before relying on it.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
0 of 20 cited sources checked · 0 supported · 0 flagged
- Findingown data§ RESULTS
Hox gene transcript levels in newly emergent juveniles are higher than in larvae.
“Levels in newly emergent juveniles are in every case even higher.”
Quote in the paperSubstantial claim - Findingown data§ RESULTS
SpHox3 is expressed in five patches of cells in the ventral region of the rudiment, apparently in the somatocoelar mesoderm of the nascent tooth sacs.
“This gene was expressed in five patches of cells in the ventral region of the rudiment, apparently in the somatocoelar mesoderm of the nascent tooth sacs.”
Quote in the paperSubstantial claim - Findingown data§ RESULTS
There is no obvious difference in adult tissue expression patterns of Hox genes according to their positions in the cluster.
“Furthermore there was no obvious difference in the patterns of expression in adult tissues of these genes according to their positions in the cluster.”
Quote in the paperSubstantial claim - Findingown data§ DISCUSSION
In 48-h embryos, transcript numbers for SpHox2, SpHox3, SpHox4/5, SpHox6, SpHox9/10, and SpHox11/13a are low (undetectable to approximately 330 per embryo).
“In the 48-h 1,000 cell embryo, the numbers of transcripts are, for SpHox2, ≈330 per embryo; for SpHox3, undetectable; for SpHox4/5, ≈250; for SpHox6, ≈150, for SpHox9/10, ≈190; for SpHox11/13a, ≈130; and the same or lower values obtain for earlier embryos.”
Quote in the paperSubstantial claim - Findingown data§ Abstract
Among the eight S. purpuratus Hox genes studied, only SpHox7 and SpHox11/13b are expressed significantly during embryogenesis.
“Only two of these genes are used significantly during the entire process of embryogenesis per se”
- Also stated in: § RESULTS · plain
“only SpHox7 and SpHox11/13b, as previously shown (23, 24), are expressed significantly in the embryo.”
- Also stated in: § RESULTS · plain
“SpHox2, SpHox3, SpHox4/5, SpHox8, SpHox9/10, and SpHox11/13a are not expressed significantly at any stage of embryogenesis.”
Quote in the paperSubstantial claim - Also stated in: § RESULTS · plain
- Findingown data§ Abstract
All eight studied Hox genes are expressed at significant levels during the stages when the adult body plan is forming in the imaginal rudiment.
“although all are copiously expressed during the stages when the adult body plan is forming in the imaginal rudiment”
- Also stated in: § RESULTS · plain
“transcripts of all of the eight Hox cluster genes studied are present at significant levels”
- Also stated in: § RESULTS · plain
“all represented by transcripts at levels ranging from a few thousand to more than 20,000 molecules per larva during the stages of rudiment formation.”
Quote in the paperSubstantial claim - Also stated in: § RESULTS · plain
- Findingown data§ Abstract
The eight Hox genes are expressed in various combinations in adult sea urchin tissues.
“They are also all expressed in various combinations in adult tissues.”
- Also stated in: § RESULTS · plain
“Each of the eight genes is expressed in a certain pattern in these adult tissues, and conversely each tissue expresses a certain pattern of Hox complex genes.”
Quote in the paperSubstantial claim - Also stated in: § RESULTS · plain
- Premisecitation§ DISCUSSION
Lophotrochozoans have a homologous set of Hox genes.
“These animals have a homologous set of Hox genes (34)”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [34]
Not checked in the free run.
- Premisecitation§ Abstract
In maximal indirect development, the adult body plan forms within the larva from special patches of cells set aside during embryogenesis.
“In maximal indirect development, the adult body plan instead forms within the larva by a complex secondary process from special patches of cells set aside during embryogenesis (1).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [1] 1. Peterson K J, Cameron R A, Davidson E H. BioEssays. 1997;19:623–631. doi: 10.1002/bies.950190713. [DOI] [PubMed] [Google Scholar] 2.Salser S J, Kenyon C. Trends Genet. 1994;10:159–164. doi: 10.1016/0168-9525(94)90092-2. [DOI] [PubMed] [Google Scholar] 3.Kourakis M J, Master V A, Lokhorst D K, Nardelli-Haefliger D, Weeden C J, Martindale M Q, Shankland M. Dev Biol. 1997;190:284–300. doi: 10.1006/dbio.1997.8689. [DOI] [PubMed] [Google Scholar] 4.Wong V Y, Aisemberg G O, Macagno E R. J Neurosci. 1995;15:5551–5559. doi: 10.1523/JNEUROSCI.15-08-05551.1995. [DOI] [PMC free article] [PubMed] [Goog source
Not checked in the free run.
- Premisecitation§ DISCUSSION
Indirect development is primitive for bilaterians.
“We have discussed elsewhere evidence that has led us and our colleagues to conclude that indirect development is primitive for bilaterians (1, 5).”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites [1] 1. Peterson K J, Cameron R A, Davidson E H. BioEssays. 1997;19:623–631. doi: 10.1002/bies.950190713. [DOI] [PubMed] [Google Scholar] 2.Salser S J, Kenyon C. Trends Genet. 1994;10:159–164. doi: 10.1016/0168-9525(94)90092-2. [DOI] [PubMed] [Google Scholar] 3.Kourakis M J, Master V A, Lokhorst D K, Nardelli-Haefliger D, Weeden C J, Martindale M Q, Shankland M. Dev Biol. 1997;190:284–300. doi: 10.1006/dbio.1997.8689. [DOI] [PubMed] [Google Scholar] 4.Wong V Y, Aisemberg G O, Macagno E R. J Neurosci. 1995;15:5551–5559. doi: 10.1523/JNEUROSCI.15-08-05551.1995. [DOI] [PMC free article] [PubMed] [Goog source
Not checked in the free run.
- cites [5] source
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- Interpretationreasoning§ RESULTS
Hox gene expression occurs throughout the period of adult body plan formation.
“Thus, Hox gene expression occurs throughout the period of adult body plan formation.”
Quote in the paperSubstantial claim - Premisecitation§ RESULTS
By late embryogenesis, SpHox11/13b products are confined to subregions of the oral ectoderm, the larval arms, and the foregut.
“and to subregions of the oral ectoderm, the larval arms, and the foregut (24).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [24]
Not checked in the free run.
- Interpretationown data§ RESULTS
SpHox3 expression is specific to the 5-fold radially symmetric organization of the adult body plan.
“SpHox3 was expressed specifically in the 5-fold radially symmetric organization of the adult body plan.”
Quote in the paperSubstantial claim - Interpretationown data§ DISCUSSION
The low numbers of transcripts of the other six Hox genes in the embryo before feeding do not appear to indicate expression of functional significance for embryogenesis.
“the small number of transcripts of the other six Hox cluster genes found in the embryo before feeding do not appear to indicate expression that is of functional significance for the processes of embryogenesis.”
Quote in the paperSubstantial claim- Rests on an assumption: Regional specification processes in the sea urchin embryo are essentially complete by 48 h.
- Rests on an assumption: The structures of the late embryo (gut, oral ectoderm, skeletal structures) are composed of much larger populations of cells than two to eight cells.
- Interpretationcitation§ DISCUSSION
The low transcript numbers measured for the six Hox genes likely represent ubiquitously distributed, rare nuclear RNAs that may not ever be processed in the embryo.
“It is not unlikely that the low numbers of transcripts measured represent ubiquitously distributed, rare nuclear RNAs that may not ever be processed in the embryo (33), which are present at any given time at levels of 0.05–1 molecule per cell (22).”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites [33] source
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- cites [22]
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- Interpretationreasoning§ DISCUSSION
Regulatory utilization of all Hox complex genes is an integral aspect of the later set of regulatory inventions leading to adult body plans of large animals.
“Regulatory utilization of all of the genes of the Hox gene complex appears now as an integral aspect of the later set of regulatory inventions, that leading to the adult body plans of large animals.”
Quote in the paperSubstantial claim - Interpretationown data§ DISCUSSION
Except for SpHox7 and SpHox11/13b, the studied Hox genes play no significant role in formation of the embryo/larva, exclusive of set-aside cell progeny contributing to the imaginal rudiment.
“our evidence indicates that, except for SpHox7 and SpHox11/13b, the Hox genes we studied play no significant role in the formation of the embryo/larva, i.e., in the development of larval structures, exclusive of the set-aside cell progeny that contribute to the imaginal rudiment from which the juvenile sea urchin derives.”
Quote in the paperSubstantial claim - Interpretationown data§ DISCUSSION
The genetic regulatory apparatus needed to build micrometazoan organisms is qualitatively simpler than that needed for development of any known adult bilaterian body plan.
“The present work adds to the discussion of metazoan origins experimental evidence that the genetic regulatory apparatus needed to build such micrometazoan organisms is indeed qualitatively simpler than that needed for the development of any known adult bilaterian body plan.”
Quote in the paperSubstantial claim - Study design and conductcitation§ RESULTS
The probe excess titration method is extremely sensitive, permitting reliable detection of <0.05 mRNA molecules per average embryonic cell.
“it is extremely sensitive, permitting reliable detection of <0.05 mRNA molecules per average embryonic cell”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [20] source
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- Classified as probably not a substantial claim. 7
- May combine two claims. 6
Probably not a substantial claim: may not pass S3 (load-bearing).
Findingnone given§ AbstractThe single Hox gene complex of Strongylocentrotus purpuratus contains 10 genes.
“The single Hox gene complex of Strongylocentrotus purpuratus contains 10 genes”
Quote in the paperNot a substantial claimMay combine two claims.
Findingcitation§ DISCUSSIONSpHox7 and SpHox11/13b transcripts are present at respectable levels for transcription factor genes: 30-100 SpHox7 transcripts per active cell between 48 and 72 h, and at least 30-40 SpHox11/13b transcripts per active cell.
“Thus, there are 30–100 SpHox7 transcripts per active cell between 48 and 72 h (23), and for SpHox11/13b, there are ≥30–40 transcripts per active cell (Fig. 3 and ref. 24).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites [23]
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- cites [24]
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Probably not a substantial claim: may not pass S3 (load-bearing).
Premisecitation§ AbstractIn C. elegans, an almost normal embryo and first-stage larva are formed irrespective of mutation of the genes of the reduced Hox gene cluster.
“in C. elegans an almost normal embryo and first-stage larva are formed irrespective of mutation of the genes of the reduced Hox gene cluster of this organism (18).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [18]
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May combine two claims.
Interpretationreasoning§ DISCUSSIONIt is not likely that SpHox7 or SpHox11/13b participate in regional embryonic specification functions.
“It is not even likely that SpHox7 or SpHox11/13b participate in regional embryonic specification functions.”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
Premisecitation§ AbstractHox cluster genes play key roles in many aspects of spatial patterning in modern bilaterians.
“The Hox cluster genes operate within this system and play key roles in many aspects of spatial patterning (14, 15).”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites [14] source
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- cites [15]
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Classified as probably not a substantial claim.
Premisecitation§ AbstractIn the leech, Hox genes are activated only after the segmented body plan has formed by elaboration of the germ band.
“In the leech the Hox genes are activated only after the formation of the segmented body plan has occurred by elaboration of the germ band, the cells of which are previously segmentally specified, at their birth (19).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [19]
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Probably not a substantial claim: may not pass S3 (load-bearing).
Premisecitation§ RESULTSBy late embryogenesis, SpHox7 products are confined to the vertex region of the aboral ectoderm.
“by late embryogenesis their products are confined, respectively, to the vertex region of the aboral ectoderm (23)”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [23]
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Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.
Premisecitation§ RESULTSSpHox7 and SpHox11/13b are activated before gastrulation.
“The SpHox7 and SpHox11/13b genes had been found to be activated before gastrulation”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites [23]
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- cites [24]
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May combine two claims.
Interpretationown data§ DISCUSSIONNone of the embryo-wide specification functions, and in the limit none but the finishing touches of embryonic morphogenesis, could possibly require most of the genes of the Hox cluster.
“We conclude that none of the embryo-wide specification functions, and in the limit none but the finishing touches of embryonic morphogenesis, could possibly require most of the genes of the Hox cluster.”
Quote in the paperSubstantial claim- Rests on an assumption: Regional specification processes in the sea urchin embryo are essentially complete by 48 h.
- Rests on an assumption: The structures of the late embryo (gut, oral ectoderm, skeletal structures) are composed of much larger populations of cells than two to eight cells.
Probably not a substantial claim: may not pass S3 (load-bearing).
Study design and conductown data§ RESULTSControl titrations for SpZ12-1 and CyIIIa mRNAs gave values close to those previously published.
“As controls for the measurement procedures and calculations, titrations were carried out for mRNAs of the transcription factor gene SpZ12–1 (25) and of the cytoskeletal actin CyIIIa (26, 27), the same RNAs as used for estimation of Hox gene transcripts. The values observed were close to those previously published.”
Quote in the paperNot a substantial claim0 of 3 sources checked- cites [25]
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- cites [26] source
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- cites [27]
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May combine two claims.
Interpretationown data§ AbstractDevelopment of the sea urchin larva does not appear to require expression of the Hox gene cluster as such, whereas development of the adult body plan does.
“Thus, development of a microscopic, free-living organism of bilaterian grade, the larva, does not appear to require expression of the Hox gene cluster as such, whereas development of the adult body plan does.”
Quote in the paperSubstantial claimMay combine two claims.
Interpretationreasoning§ DISCUSSIONThe Hox cluster is not a definitive and essential component of the genetic regulatory apparatus underlying development of every free-living metazoan organism of bilaterian grade, although it is likely essential for development of adult body plans of all macroscopic bilaterian organisms.
“It is not true, therefore, that the Hox cluster is a definitive and essential component of the genetic regulatory apparatus that underlies development of every free-living metazoan organism of bilaterian grade, although it is likely to be essential for the development of the adult body plans of all macroscopic bilaterian organisms.”
Quote in the paperSubstantial claim
The paper relies on this without support.
Regional specification processes in the sea urchin embryo are essentially complete by 48 h.
“However, regional specification processes in this embryo are essentially complete by 48 h, although further elaboration of some differentiated cells and further morphogenetic progression takes place in archenteron, skeleton, ciliated band, and stomodaeum.”
The paper relies on this without support.
The structures of the late embryo (gut, oral ectoderm, skeletal structures) are composed of much larger populations of cells than two to eight cells.
“the structures that constitute the late embryo, e.g., gut, oral ectoderm, skeletal structures, are all composed of much larger populations of cells.”
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the sea urchin Strongylocentrotus purpuratus, only two posterior Hox genes are used to build the embryo.
“In Strongylocentrotus purpuratus (sea urchin), only two posterior Hox genes are used to build the embryo (Arenas-Mena et al., 1998).”
From Conservation of Hox/ParaHox-Related Genes in the Early Development of a Cnidarian (2001) · cites this paper as Arenas-Mena et al., 1998
All Hox cluster genes so far investigated by in situ hybridization are expressed in the progeny of set-aside cells.
“More importantly, all of those Hox cluster genes so far investigated by in situ hybridization are indeed expressed in the progeny of the set-side cells, i.e., as elements that will give rise to structures of the juvenile”
From Bilaterian Origins: Significance of New Experimental Observations (2000) · cites this paper as Arenas-Mena et al., 1998
Six of the eight Hox cluster genes examined are not significantly expressed until embryogenesis is complete.
“So far no real surprises: the more shocking observation that emerged from this study was that 6 of the 8 Hox cluster genes examined by Arenas-Mena et al. (1998) are not significantly expressed at all until embryogenesis is complete.”
From Bilaterian Origins: Significance of New Experimental Observations (2000) · cites this paper as Arenas-Mena et al. (1998)
All eight Hox genes examined so far are expressed copiously during adult body plan formation.
“All of the eight Hox genes so far examined are expressed copiously during adult body plan formation (Arenas-Mena et al., 1998).”
From Bilaterian Origins: Significance of New Experimental Observations (2000) · cites this paper as Arenas-Mena et al., 1998
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
Each contradiction between two passages listed here was confirmed by an independent check.
Fertilization is said to begin at three weeks
MinorThe paper describes two- and three-week-old larvae, so fertilization cannot begin at three weeks. The surrounding discussion appears to concern rudiment development rather than fertilization.
“By 3 weeks fertilization has begun and the picture has changed completely.”
“The larvae were harvested at 2 weeks and 3 weeks (Fig. 2 B and C), when the rudiment has advanced to the point where the five primary podia and tooth sacs are already beginning to protrude from the ventral surface”
Embryonic transcript list substitutes SpHox6 for SpHox8
MinorThe paper identifies SpHox8 as one of the six tested genes with little embryonic expression, but its subsequent list of embryonic transcript counts gives SpHox6 instead and omits SpHox8.
“for SpHox4/5, ≈250; for SpHox6, ≈150, for SpHox9/10, ≈190; for SpHox11/13a, ≈130”
“SpHox2, SpHox3, SpHox4/5, SpHox8, SpHox9/10, and SpHox11/13a are not expressed significantly at any stage of embryogenesis.”
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Cited by
Sorted by citations
Modulating Hox gene functions during animal body patterning
Pearson, J. C., Lemons, D., & McGinnis, W. (2005) · Nature Reviews Genetics · doi:10.1038/nrg1726 · Cited by 879 · see citing works
Early animal evolution: emerging views from comparative biology and geology
Knoll, A. H., & Carroll, S. B. (1999) · Science · doi:10.1126/science.284.5423.2129 · Cited by 821 · see citing works
Peterson, K. J., & Eernisse, D. J. (2001) · Evolution & Development · doi:10.1046/j.1525-142x.2001.003003170.x · Cited by 529 · see citing works
The last common bilaterian ancestor
Erwin, D. H., & Davidson, E. H. (2002) · Development · doi:10.1242/dev.129.13.3021 · Cited by 320 · see citing works
Self-citationOn the Independent Origins of Complex Brains and Neurons
Moroz, L. L. (2009) · Brain, Behavior and Evolution · doi:10.1159/000258665 · Cited by 209 · see citing works
Regulatory evolution and the origin of the bilaterians
Peterson, K. J., & Davidson, E. H. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.9.4430 · Cited by 139 · see citing works
Self-citationBilaterian Origins: Significance of New Experimental Observations
Peterson, K. J., Cameron, R. A., & Davidson, E. H. (2000) · Developmental Biology · doi:10.1006/dbio.1999.9475 · Cited by 133 · see citing works
Self-citationOrganization of an echinoderm <i>Hox</i> gene cluster
Martinez, P., Rast, J. P., Arenas-Mena, C., & Davidson, E. H. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.4.1469 · Cited by 85 · see citing works
Self-citationAn integrated view of precambrian eumetazoan evolution
Davidson, E. H., & Erwin, D. H. (2009) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2009.74.042 · Cited by 48 · see citing works
Self-citationPeterson, K. J., Irvine, S. Q., Cameron, R. A., & Davidson, E. H. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.9.4487 · Cited by 47 · see citing works
Self-citation
- Authors
- Arenas-Mena, C., Martinez, P., Cameron, R. A., & Davidson, E. H.
- Affiliations
- Division of Biology, California Institute of Technology, Pasadena, CA 901125; and Stowers Institute for Medical Research, Kansas City, MO 64110
- Stowers Institute for Medical Research (US)
- ORCID
- Cameron, R. Andrew
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 1998-10-27
- Volume
- 95
- Issue
- 22
- Pages
- 13062-13067
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC23710
- OpenAlex
- W2039007955
- Semantic Scholar
- 11b1b340276a77c3718394f97f5368e2287fd940
- Cited by
- 137
- References
- 28
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 5 · 2023: 7 · 2022: 5 · 2021: 2 · 2020: 2 · 2019: 2 · 2018: 5 · 2016: 3 · 2015: 6 · 2014: 5 · 2013: 3 · 2012: 3
- FWCI
- 4.07
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion)
- Funders
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD05753)
- 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 › Agricultural and Biological Sciences › Aquatic Science › Echinoderm biology and ecology
- Keywords
- Hox genes, Strongylocentrotus purpuratus, sea urchin development, indirect development, larval development, spatial patterning, gene expression, bilaterian evolution, Precambrian evolution
- MeSH terms
- Animals, Embryo, Nonmammalian, Embryonic Induction, Genes, Homeobox, Multigene Family, Larva, Sea Urchins, Gene Expression Regulation, Developmental, Body Patterning
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-06.
Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-06.
Statistics and arithmetic are recomputed, not judged.
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