Inter-homolog crossing-over and synapsis in Arabidopsis meiosis are dependent on the chromosome axis protein AtASY3.
In this study we have analysed AtASY3, a coiled-coil domain protein that is required for normal meiosis in Arabidopsis. Analysis of an Atasy3-1 mutant reveals that loss of the protein compromises chromosome axis formation and results in reduced numbers of meiotic crossovers (COs). Although the frequency of DNA double-strand breaks (DSBs) appears moderately reduced in Atasy3-1, the main recombination defect is a reduction in the formation of COs. Immunolocalization studies in wild-type meiocytes indicate that the HORMA protein AtASY1, which is related to Hop1 in budding yeast, forms hyper-abundant domains along the chromosomes that are spatially associated with DSBs and early recombination pathway proteins. Loss of AtASY3 disrupts the axial organization of AtASY1. Furthermore we show that the AtASY3 and AtASY1 homologs BoASY3 and BoASY1, from the closely related species Brassica oleracea, are co-immunoprecipitated from meiocyte extracts and that AtASY3 interacts with AtASY1 via residues in its predicted coiled-coil domain. Together our results suggest that AtASY3 is a functional homolog of Red1. Since studies in budding yeast indicate that Red1 and Hop1 play a key role in establishing a bias to favor inter-homolog recombination (IHR), we propose that AtASY3 and AtASY1 may have a similar role in Arabidopsis. Loss of AtASY3 also disrupts synaptonemal complex (SC) formation. In Atasy3-1 the transverse filament protein AtZYP1 forms small patches rather than a continuous SC. The few AtMLH1 foci that remain in Atasy3-1 are found in association with the AtZYP1 patches. This is sufficient to prevent the ectopic recombination observed in the absence of AtZYP1, thus emphasizing that in addition to its structural role the protein is important for CO formation.
School of Biosciences, University of Birmingham, United Kingdom.
Maheen
M
Ferdous
James D
JD
Higgins
Kim
K
Osman
Christophe
C
Lambing
Elisabeth
E
Roitinger
Karl
K
Mechtler
Susan J
SJ
Armstrong
Ruth
R
Perry
Mónica
M
Pradillo
Nieves
N
Cuñado
F Chris H
FC
Franklin
D017360:Arabidopsis / Q000166:cytology / Q000235:genetics*; D029681:Arabidopsis Proteins / Q000235:genetics; D001937:Brassica / Q000235:genetics; D023902:Chromosome Pairing; D032461:Chromosomes, Plant / Q000235:genetics; D003434:Crossing Over, Genetic; D053903:DNA Breaks, Double-Stranded; D004268:DNA-Binding Proteins / Q000235:genetics*; D008540:Meiosis / Q000235:genetics*; D009154:Mutation; D011995:Recombination, Genetic; D029701:Saccharomyces cerevisiae Proteins / Q000235:genetics; D013573:Synaptonemal Complex / Q000235:genetics*
C411742:ASY1 protein, Arabidopsis; C572933:ASY3 protein, Arabidopsis; D029681:Arabidopsis Proteins; D004268:DNA-Binding Proteins; C086672:HOP1 protein, S cerevisiae; C086673:RED1 protein, S cerevisiae; D029701:Saccharomyces cerevisiae Proteins