Interference-mediated synaptonemal complex formation with embedded crossover designation.
Biological systems exhibit complex patterns at length scales ranging from the molecular to the organismic. Along chromosomes, events often occur stochastically at different positions in different nuclei but nonetheless tend to be relatively evenly spaced. Examples include replication origin firings, formation of chromatin loops along chromosome axes and, during meiosis, localization of crossover recombination sites ("crossover interference"). We present evidence in the fungus Sordaria macrospora that crossover interference is part of a broader pattern that includes synaptonemal complex (SC) nucleation. This pattern comprises relatively evenly spaced SC nucleation sites, among which a subset are crossover sites that show a classical interference distribution. This pattern ensures that SC forms regularly along the entire length of the chromosome as required for the maintenance of homolog pairing while concomitantly having crossover interactions locally embedded within the SC structure as required for both DNA recombination and structural events of chiasma formation. This pattern can be explained by a threshold-based designation and spreading interference process. This model can be generalized to give diverse types of related and/or partially overlapping patterns, in two or more dimensions, for any type of object.
Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA 02138;
Liangran
L
Zhang
Institut de Génétique et Microbiologie, Unité Mixte de Recherche 8621, Université Paris-Sud, 91405 Orsay, France; and.
Eric
E
Espagne
Institut de Génétique et Microbiologie, Unité Mixte de Recherche 8621, Université Paris-Sud, 91405 Orsay, France; and Institut Curie, 75248 Paris Cedex 05, France.
Arnaud
A
de Muyt
Institut de Génétique et Microbiologie, Unité Mixte de Recherche 8621, Université Paris-Sud, 91405 Orsay, France; and.
Denise
D
Zickler
Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA 02138; kleckner@fas.harvard.edu.
Nancy E
NE
Kleckner
D003434:Crossing Over, Genetic; D005800:Genes, Fungal; D020037:Sordariales / Q000235:genetics*; D013573:Synaptonemal Complex / Q000502:physiology*
crossover designation; recombination/synapsis; spatial patterning; synapsis initiation site