Evolution of vertebrate central nervous system is accompanied by novel expression changes of duplicate genes

Chen, Yuan; Ding, Yun; Zhang, Zuming; Wang, Wen; Chen, Jun-Yuan; Ueno, Naoto; Mao, Bingyu

doi:10.1016/j.jgg.2011.10.004

Cited by 9 publications

(9 citation statements)

References 53 publications

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“…Before this study, amphioxus bHLH-PAS genes, including Ncoa of B. belcheri [58], Hifα of B. belcheri tsingtauense ( B. japonicum ) [59], Bmal of B. lanceolatum [60], and Sim of B. floridae [55], had been identified. The present study has confirmed the Ncoa , Hifα , and Bmal homologs of B. floridae , and identified six additional bHLH-PAS genes.…”

Section: Discussionmentioning

confidence: 99%

“…In the developing mouse embryo, Ncoa1 ( SRC-1 ) is highly expressed in olfactory epithelium, brain, anterior pituitary, and other organs [66,67]; mouse Ncoa2 ( SRC-2 ) is expressed in the developing anterior pituitary [68]. Similarly, Xenopus NCOA paralogs are expressed in various parts of the CNS [58]. These findings suggest that these vertebrate NCOA paralogs contribute to CNS development.…”

Section: Discussionmentioning

confidence: 99%

“…These findings suggest that these vertebrate NCOA paralogs contribute to CNS development. In a previous study using the Asian amphioxus B. belcheri , Ncoa expression was not detected in the CNS, and it was proposed that NCOA expression may have shifted from non-CNS to CNS only in the vertebrate lineage (supplementary figure 4 in [58]). By contrast, our results clearly show that BfNcoa is indeed expressed in CNS during B. floridae embryogenesis.…”

Section: Discussionmentioning

confidence: 99%

“…The difference between our results and those of Chen et al . [58] may stem from differences in species, experimental protocols, riboprobe sensitivity, or the developmental stage examined. In any event, our results suggest that NCOA function in the CNS is likely conserved in chordates.…”

Section: Discussionmentioning

confidence: 99%

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Genome-wide survey and expression analysis of the bHLH-PAS genes in the amphioxus Branchiostoma floridae reveal both conserved and diverged expression patterns between cephalochordates and vertebrates

2014

EvoDevo

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BackgroundThe bHLH-PAS transcription factors are found in both protostomes and deuterostomes. They are involved in many developmental and physiological processes, including regional differentiation of the central nervous system, tube-formation, hypoxia signaling, aromatic hydrocarbon sensing, and circadian rhythm regulation. To understand the evolution of these genes in chordates, we analyzed the bHLH-PAS genes of the basal chordate amphioxus (Branchiostoma floridae).ResultsFrom the amphioxus draft genome database, we identified ten bHLH-PAS genes, nine of which could be assigned to known orthologous families. The tenth bHLH-PAS gene could not be assigned confidently to any known bHLH family; however, phylogenetic analysis clustered this gene with arthropod Met family genes and two spiralian bHLH-PAS-containing sequences, suggesting that they may share the same ancestry. We examined temporal and spatial expression patterns of these bHLH-PAS genes in developing amphioxus embryos. We found that BfArnt, BfNcoa, BfSim, and BfHifα were expressed in the central nervous system in patterns similar to those of their vertebrate homologs, suggesting that their functions may be conserved. By contrast, the amphioxus BfAhr and BfNpas4 had expression patterns distinct from those in vertebrates. These results imply that there were changes in gene regulation after the divergence of cephalochordates and vertebrates.ConclusionsWe have identified ten bHLH-PAS genes from the amphioxus genome and determined the embryonic expression profiles for these genes. In addition to the nine currently recognized bHLH-PAS families, our survey suggests that the BfbHLHPAS-orphan gene along with arthropod Met genes and the newly identified spiralian bHLH-PAS-containing sequences represent an ancient group of genes that were lost in the vertebrate lineage. In a comparison with the expression patterns of the vertebrate bHLH-PAS paralogs, which are the result of whole-genome duplication, we found that although several members seem to retain conserved expression patterns during chordate evolution, many duplicated paralogs may have undergone subfunctionalization and neofunctionalization in the vertebrate lineage. In addition, our survey of amphioxus bHLH-PAS gene models from genome browser with experimentally verified cDNA sequences calls into question the accuracy of the current in silico gene annotation of the B. floridae genome.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

See 2 more Smart Citations

Genome-wide survey and expression analysis of the bHLH-PAS genes in the amphioxus Branchiostoma floridae reveal both conserved and diverged expression patterns between cephalochordates and vertebrates

2014

EvoDevo

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“…Even though all the genes are encoded in the same genome in a multicellular organism, different sets of genes are expressed in different developmental stages and in different cell types. It is generally believed that diversification of tissue/cell distribution patterns of paralogous proteins is vital for evolutionary emergence and maintenance of multicellularity (6,7). However, a concise quantitative framework to describe, and to explain, the relationship between paralog enrichment and multicellularity remains yet to be developed.…”

Section: Introductionmentioning

confidence: 99%

Duplicate gene enrichment and expression pattern diversification in multicellularity

Padawer

Leighty

Wang

2012

Nucleic Acids Research

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The enrichment of duplicate genes, and therefore paralogs (proteins coded by duplicate genes), in multicellular versus unicellular organisms enhances genomic functional innovation. This study quantitatively examined relationships among paralog enrichment, expression pattern diversification and multicellularity, aiming to better understand genomic basis of multicellularity. Paralog abundance in specific cells was compared with those in unicellular proteomes and the whole proteomes of multicellular organisms. The budding yeast, Saccharomyces cerevisiae and the nematode, Caenorhabditis elegans, for which the gene sets expressed in specific cells are available, were used as uni and multicellular models, respectively. Paralog count (K) distributions [P(k)] follow a power-law relationship [P(k) ∝ k−α] in the whole proteomes of both species and in specific C. elegans cells. The value of the constant α can be used as a gauge of paralog abundance; the higher the value, the lower the paralog abundance. The α-value is indeed lower in the whole proteome of C. elegans (1.74) than in S. cerevisiae (2.34), quantifying the enrichment of paralogs in multicellular species. We also found that the power-law relationship applies to the proteomes of specific C. elegans cells. Strikingly, values of α in specific cells are higher and comparable to that in S. cerevisiae. Thus, paralog abundance in specific cells is lower and comparable to that in unicellular species. Furthermore, how much the expression level of a gene fluctuates across different C. elegans cells correlates positively with its paralog count, which is further confirmed by human gene-expression patterns across different tissues. Taken together, these results quantitatively and mechanistically establish enrichment of paralogs with diversifying expression patterns as genomic and evolutionary basis of multicellularity.

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Evolution of new characters after whole genome duplications: Insights from amphioxus

Holland

2013

Seminars in Cell & Developmental Biology

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Evolution of vertebrate central nervous system is accompanied by novel expression changes of duplicate genes

Cited by 9 publications

References 53 publications

Genome-wide survey and expression analysis of the bHLH-PAS genes in the amphioxus Branchiostoma floridae reveal both conserved and diverged expression patterns between cephalochordates and vertebrates

Genome-wide survey and expression analysis of the bHLH-PAS genes in the amphioxus Branchiostoma floridae reveal both conserved and diverged expression patterns between cephalochordates and vertebrates

Duplicate gene enrichment and expression pattern diversification in multicellularity

Evolution of new characters after whole genome duplications: Insights from amphioxus

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