Sequential loading of cohesin subunits during the first meiotic prophase of grasshoppers.

The cohesin complexes play a key role in chromosome segregation during both mitosis and meiosis. They establish sister chromatid cohesion between duplicating DNA molecules during S-phase, but they also have an important role during postreplicative double-strand break repair in mitosis, as well as du...

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Main Authors: Ana M Valdeolmillos, Alberto Viera, Jesús Page, Ignacio Prieto, Juan L Santos, María Teresa Parra, Margarete M S Heck, Carlos Martínez-A, José L Barbero, José A Suja, Julio S Rufas
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2007-02-01
Series:PLoS Genetics
Online Access:http://europepmc.org/articles/PMC1802827?pdf=render
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author Ana M Valdeolmillos
Alberto Viera
Jesús Page
Ignacio Prieto
Juan L Santos
María Teresa Parra
Margarete M S Heck
Carlos Martínez-A
José L Barbero
José A Suja
Julio S Rufas
author_facet Ana M Valdeolmillos
Alberto Viera
Jesús Page
Ignacio Prieto
Juan L Santos
María Teresa Parra
Margarete M S Heck
Carlos Martínez-A
José L Barbero
José A Suja
Julio S Rufas
author_sort Ana M Valdeolmillos
collection DOAJ
description The cohesin complexes play a key role in chromosome segregation during both mitosis and meiosis. They establish sister chromatid cohesion between duplicating DNA molecules during S-phase, but they also have an important role during postreplicative double-strand break repair in mitosis, as well as during recombination between homologous chromosomes in meiosis. An additional function in meiosis is related to the sister kinetochore cohesion, so they can be pulled by microtubules to the same pole at anaphase I. Data about the dynamics of cohesin subunits during meiosis are scarce; therefore, it is of great interest to characterize how the formation of the cohesin complexes is achieved in order to understand the roles of the different subunits within them. We have investigated the spatio-temporal distribution of three different cohesin subunits in prophase I grasshopper spermatocytes. We found that structural maintenance of chromosome protein 3 (SMC3) appears as early as preleptotene, and its localization resembles the location of the unsynapsed axial elements, whereas radiation-sensitive mutant 21 (RAD21) (sister chromatid cohesion protein 1, SCC1) and stromal antigen protein 1 (SA1) (sister chromatid cohesion protein 3, SCC3) are not visualized until zygotene, since they are located in the synapsed regions of the bivalents. During pachytene, the distribution of the three cohesin subunits is very similar and all appear along the trajectories of the lateral elements of the autosomal synaptonemal complexes. However, whereas SMC3 also appears over the single and unsynapsed X chromosome, RAD21 and SA1 do not. We conclude that the loading of SMC3 and the non-SMC subunits, RAD21 and SA1, occurs in different steps throughout prophase I grasshopper meiosis. These results strongly suggest the participation of SMC3 in the initial cohesin axis formation as early as preleptotene, thus contributing to sister chromatid cohesion, with a later association of both RAD21 and SA1 subunits at zygotene to reinforce and stabilize the bivalent structure. Therefore, we speculate that more than one cohesin complex participates in the sister chromatid cohesion at prophase I.
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spelling doaj.art-06bbc122a4c84ac2bade051eb638400c2022-12-21T23:01:24ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042007-02-0132e2810.1371/journal.pgen.0030028Sequential loading of cohesin subunits during the first meiotic prophase of grasshoppers.Ana M ValdeolmillosAlberto VieraJesús PageIgnacio PrietoJuan L SantosMaría Teresa ParraMargarete M S HeckCarlos Martínez-AJosé L BarberoJosé A SujaJulio S RufasThe cohesin complexes play a key role in chromosome segregation during both mitosis and meiosis. They establish sister chromatid cohesion between duplicating DNA molecules during S-phase, but they also have an important role during postreplicative double-strand break repair in mitosis, as well as during recombination between homologous chromosomes in meiosis. An additional function in meiosis is related to the sister kinetochore cohesion, so they can be pulled by microtubules to the same pole at anaphase I. Data about the dynamics of cohesin subunits during meiosis are scarce; therefore, it is of great interest to characterize how the formation of the cohesin complexes is achieved in order to understand the roles of the different subunits within them. We have investigated the spatio-temporal distribution of three different cohesin subunits in prophase I grasshopper spermatocytes. We found that structural maintenance of chromosome protein 3 (SMC3) appears as early as preleptotene, and its localization resembles the location of the unsynapsed axial elements, whereas radiation-sensitive mutant 21 (RAD21) (sister chromatid cohesion protein 1, SCC1) and stromal antigen protein 1 (SA1) (sister chromatid cohesion protein 3, SCC3) are not visualized until zygotene, since they are located in the synapsed regions of the bivalents. During pachytene, the distribution of the three cohesin subunits is very similar and all appear along the trajectories of the lateral elements of the autosomal synaptonemal complexes. However, whereas SMC3 also appears over the single and unsynapsed X chromosome, RAD21 and SA1 do not. We conclude that the loading of SMC3 and the non-SMC subunits, RAD21 and SA1, occurs in different steps throughout prophase I grasshopper meiosis. These results strongly suggest the participation of SMC3 in the initial cohesin axis formation as early as preleptotene, thus contributing to sister chromatid cohesion, with a later association of both RAD21 and SA1 subunits at zygotene to reinforce and stabilize the bivalent structure. Therefore, we speculate that more than one cohesin complex participates in the sister chromatid cohesion at prophase I.http://europepmc.org/articles/PMC1802827?pdf=render
spellingShingle Ana M Valdeolmillos
Alberto Viera
Jesús Page
Ignacio Prieto
Juan L Santos
María Teresa Parra
Margarete M S Heck
Carlos Martínez-A
José L Barbero
José A Suja
Julio S Rufas
Sequential loading of cohesin subunits during the first meiotic prophase of grasshoppers.
PLoS Genetics
title Sequential loading of cohesin subunits during the first meiotic prophase of grasshoppers.
title_full Sequential loading of cohesin subunits during the first meiotic prophase of grasshoppers.
title_fullStr Sequential loading of cohesin subunits during the first meiotic prophase of grasshoppers.
title_full_unstemmed Sequential loading of cohesin subunits during the first meiotic prophase of grasshoppers.
title_short Sequential loading of cohesin subunits during the first meiotic prophase of grasshoppers.
title_sort sequential loading of cohesin subunits during the first meiotic prophase of grasshoppers
url http://europepmc.org/articles/PMC1802827?pdf=render
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