Reproduction-associated pathways in females of gibel carp
(Carassius gibelio) shed light on the molecular mechanisms of
the coexistence of asexual and sexual reproduction

J 2024

Reproduction-associated pathways in females of gibel carp (Carassius gibelio) shed light on the molecular mechanisms of the coexistence of asexual and sexual reproduction

JACQUES, Florian, Tomáš TICHOPÁD, Martin DEMKO, Vojtěch BYSTRÝ, Kristína KŘÍŽOVÁ et. al.

Basic information

Original name

Reproduction-associated pathways in females of gibel carp (Carassius gibelio) shed light on the molecular mechanisms of the coexistence of asexual and sexual reproduction

Authors

JACQUES, Florian (250 France, guarantor, belonging to the institution), Tomáš TICHOPÁD, Martin DEMKO (703 Slovakia, belonging to the institution), Vojtěch BYSTRÝ (203 Czech Republic, belonging to the institution), Kristína KŘÍŽOVÁ (703 Slovakia, belonging to the institution), Mária SEIFERTOVÁ (703 Slovakia, belonging to the institution), Kristýna VOŘÍŠKOVÁ (203 Czech Republic, belonging to the institution), Md Mehedi Hasan FUAD (50 Bangladesh, belonging to the institution), Lukáš VETEŠNÍK (203 Czech Republic, belonging to the institution) and Andrea VETEŠNÍKOVÁ ŠIMKOVÁ (203 Czech Republic, belonging to the institution)

Edition

BMC Genomics, London, BioMed Central Ltd, 2024, 1471-2164

Other information

Language

English

Type of outcome

Článek v odborném periodiku

Field of Study

10603 Genetics and heredity

Country of publisher

United Kingdom of Great Britain and Northern Ireland

Confidentiality degree

není předmětem státního či obchodního tajemství

References:

URL

Impact factor

Impact factor: 4.400 in 2022

Organization unit

Faculty of Science

DOI

http://dx.doi.org/10.1186/s12864-024-10462-4

UT WoS

001236839800006

Keywords in English

Carassius gibelio; Reproduction; Gynogenesis; Asexual reproduction; Evolution of sexual reproduction; Meiosis; Differential expression analysis; Oogenesis; Transcriptomics

Abstract

V originále

Gibel carp (Carassius gibelio) is a cyprinid fish that originated in eastern Eurasia and is considered as invasive in European freshwater ecosystems. The populations of gibel carp in Europe are mostly composed of asexually reproducing triploid females (i.e., reproducing by gynogenesis) and sexually reproducing diploid females and males. Although some cases of coexisting sexual and asexual reproductive forms are known in vertebrates, the molecular mechanisms maintaining such coexistence are still in question. Both reproduction modes are supposed to exhibit evolutionary and ecological advantages and disadvantages. To better understand the coexistence of these two reproduction strategies, we performed transcriptome profile analysis of gonad tissues (ovaries) and studied the differentially expressed reproduction-associated genes in sexual and asexual females. We used high-throughput RNA sequencing to generate transcriptomic profiles of gonadal tissues of triploid asexual females and males, diploid sexual males and females of gibel carp, as well as diploid individuals from two closely-related species, C. auratus and Cyprinus carpio. Using SNP clustering, we showed the close similarity of C. gibelio and C. auratus with a basal position of C. carpio to both Carassius species. Using transcriptome profile analyses, we showed that many genes and pathways are involved in both gynogenetic and sexual reproduction in C. gibelio; however, we also found that 1500 genes, including 100 genes involved in cell cycle control, meiosis, oogenesis, embryogenesis, fertilization, steroid hormone signaling, and biosynthesis were differently expressed in the ovaries of asexual and sexual females. We suggest that the overall downregulation of reproduction-associated pathways in asexual females, and their maintenance in sexual ones, allows the populations of C. gibelio to combine the evolutionary and ecological advantages of the two reproductive strategies. However, we showed that many sexual-reproduction-related genes are maintained and expressed in asexual females, suggesting that gynogenetic gibel carp retains the genetic toolkits for meiosis and sexual reproduction. These findings shed new light on the evolution of this asexual and sexual complex.

Links

GA22-27023S, research and development project

Name: Evoluční a ekologické mechanizmy koexistence asexuální a sexuální reprodukce u ryb

Investor: Czech Science Foundation

Citovat

JACQUES, Florian, Tomáš TICHOPÁD, Martin DEMKO, Vojtěch BYSTRÝ, Kristína KŘÍŽOVÁ, Mária SEIFERTOVÁ, Kristýna VOŘÍŠKOVÁ, Md Mehedi Hasan FUAD, Lukáš VETEŠNÍK and Andrea VETEŠNÍKOVÁ ŠIMKOVÁ. Reproduction-associated pathways in females of gibel carp (Carassius gibelio) shed light on the molecular mechanisms of the coexistence of asexual and sexual reproduction. BMC Genomics. London: BioMed Central Ltd, 2024, vol. 25, No 1, p. 1-22. ISSN 1471-2164. Available from: https://dx.doi.org/10.1186/s12864-024-10462-4.

@article{2422337,
   author = {Jacques, Florian and Tichopád, Tomáš and Demko, Martin and Bystrý, Vojtěch and Křížová, Kristína and Seifertová, Mária and Voříšková, Kristýna and Fuad, Md Mehedi Hasan and Vetešník, Lukáš and Vetešníková Šimková, Andrea},
   article_location = {London},
   article_number = {1},
   doi = {http://dx.doi.org/10.1186/s12864-024-10462-4},
   keywords = {Carassius gibelio; Reproduction; Gynogenesis; Asexual reproduction; Evolution of sexual reproduction; Meiosis; Differential expression analysis; Oogenesis; Transcriptomics},
   language = {eng},
   issn = {1471-2164},
   journal = {BMC Genomics},
   title = {Reproduction-associated pathways in females of gibel carp (Carassius gibelio) shed light on the molecular mechanisms of the coexistence of asexual and sexual reproduction},
   url = {https://doi.org/10.1186/s12864-024-10462-4},
   volume = {25},
   year = {2024}
}

TY  - JOUR
ID  - 2422337
AU  - Jacques, Florian - Tichopád, Tomáš - Demko, Martin - Bystrý, Vojtěch - Křížová, Kristína - Seifertová, Mária - Voříšková, Kristýna - Fuad, Md Mehedi Hasan - Vetešník, Lukáš - Vetešníková Šimková, Andrea
PY  - 2024
TI  - Reproduction-associated pathways in females of gibel carp (Carassius gibelio) shed light on the molecular mechanisms of the coexistence of asexual and sexual reproduction
JF  - BMC Genomics
VL  - 25
IS  - 1
SP  - 1-22
EP  - 1-22
PB  - BioMed Central Ltd
SN  - 14712164
KW  - Carassius gibelio
KW  - Reproduction
KW  - Gynogenesis
KW  - Asexual reproduction
KW  - Evolution of sexual reproduction
KW  - Meiosis
KW  - Differential expression analysis
KW  - Oogenesis
KW  - Transcriptomics
UR  - https://doi.org/10.1186/s12864-024-10462-4
N2  - Gibel carp (Carassius gibelio) is a cyprinid fish that originated in eastern Eurasia and is considered as invasive in European freshwater ecosystems. The populations of gibel carp in Europe are mostly composed of asexually reproducing triploid females (i.e., reproducing by gynogenesis) and sexually reproducing diploid females and males. Although some cases of coexisting sexual and asexual reproductive forms are known in vertebrates, the molecular mechanisms maintaining such coexistence are still in question. Both reproduction modes are supposed to exhibit evolutionary and ecological advantages and disadvantages. To better understand the coexistence of these two reproduction strategies, we performed transcriptome profile analysis of gonad tissues (ovaries) and studied the differentially expressed reproduction-associated genes in sexual and asexual females. We used high-throughput RNA sequencing to generate transcriptomic profiles of gonadal tissues of triploid asexual females and males, diploid sexual males and females of gibel carp, as well as diploid individuals from two closely-related species, C. auratus and Cyprinus carpio. Using SNP clustering, we showed the close similarity of C. gibelio and C. auratus with a basal position of C. carpio to both Carassius species. Using transcriptome profile analyses, we showed that many genes and pathways are involved in both gynogenetic and sexual reproduction in C. gibelio; however, we also found that 1500 genes, including 100 genes involved in cell cycle control, meiosis, oogenesis, embryogenesis, fertilization, steroid hormone signaling, and biosynthesis were differently expressed in the ovaries of asexual and sexual females. We suggest that the overall downregulation of reproduction-associated pathways in asexual females, and their maintenance in sexual ones, allows the populations of C. gibelio to combine the evolutionary and ecological advantages of the two reproductive strategies. However, we showed that many sexual-reproduction-related genes are maintained and expressed in asexual females, suggesting that gynogenetic gibel carp retains the genetic toolkits for meiosis and sexual reproduction. These findings shed new light on the evolution of this asexual and sexual complex.
ER  -

JACQUES, Florian, Tomáš TICHOPÁD, Martin DEMKO, Vojtěch BYSTRÝ, Kristína KŘÍŽOVÁ, Mária SEIFERTOVÁ, Kristýna VOŘÍŠKOVÁ, Md Mehedi Hasan FUAD, Lukáš VETEŠNÍK and Andrea VETEŠNÍKOVÁ ŠIMKOVÁ. Reproduction-associated pathways in females of gibel carp (Carassius gibelio) shed light on the molecular mechanisms of the coexistence of asexual and sexual reproduction. \textit{BMC Genomics}. London: BioMed Central Ltd, 2024, vol.~25, No~1, p.~1-22. ISSN~1471-2164. Available from: https://dx.doi.org/10.1186/s12864-024-10462-4.

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