Multiple roles of Spo11 in meiotic chromosome behavior

Abstract

Spo11, a type II topoisomerase, is likely to be required universally for initiation of meiotic recombination. However, a dichotomy exists between budding yeast and the animals Caenorhabditis elegans and Drosophila melanogaster with respect to additional roles of Spo11 in meiosis. In Saccharomyces cerevisiae, Spo11 is required for homolog pairing, as well as axial element (AE) and synaptonemal complex (SC) formation. All of these functions are Spo11 independent in C.elegans and D.melanogaster. We examined Spo11 function in a multicellular fungus, Coprinus cinereus. The C.cinereus spo11‐1 mutant shows high levels of homolog pairing and occasionally forms full‐length AEs, but no SC. In C.cinereus, Spo11 is also required for maintenance of meiotic chromosome condensation and proper spindle formation. Meiotic progression in spo11‐1 is aberrant; late in meiosis basidia undergo programmed cell death (PCD). To our knowledge, this is the first example of meiotic PCD outside the animal kingdom. Ionizing radiation can partially rescue spo11‐1 for both AE and SC formation and viable spore production, suggesting that the double‐strand break function of Spo11 is conserved and is required for these functions.

Local chromosome context is a major determinant of crossover pathway biochemistry during budding yeast meiosis

“…This suggests that Spo11-DSBs form in an environment that is refractory to Rad53 recruitment and modification, but that there also are environments where exogenouslyinduced damage can trigger the mitotic DNA damage response. In light of this suggestion, it is interesting that the meiotic defects of spo11 mutants in a variety of organisms are often only partially rescued by DSBs caused by exogenous agents (Bowring et al, 2006;Celerin et al, 2000;Dernburg et al, 1998;Loidl and Mochizuki, 2009;Pauklin et al, 2009;Storlazzi et al, 2003;Thorne and Byers, 1993). While other factors may be responsible for the limited rescue observed, we suggest that it reflects the random location of exogenously-induced DSBs, with only a subset Figure 6.…”

Tying synaptonemal complex initiation to the formation and programmed repair of DNA double-strand breaks

“…The DNA double-strand breaks (DSBs) that initiate recombination occur before synapsis begins in budding yeast (3), and cytological features (e.g., histone H2AX phosphorylation and formation of strand exchange protein complexes) indicate that the same is true in other fungi, higher plants, and mammals (4)(5)(6)(7)(8). DSBs are created by the Spo11 protein (9,10), and spo11 null mutants in many organisms are defective for SC formation (11)(12)(13)(14)(15)(16). In some cases, exogenous DSBs can at least partially substitute for Spo11 in SC formation (15)(16)(17).…”

“…DSBs are created by the Spo11 protein (9,10), and spo11 null mutants in many organisms are defective for SC formation (11)(12)(13)(14)(15)(16). In some cases, exogenous DSBs can at least partially substitute for Spo11 in SC formation (15)(16)(17). Moreover, mutations that block processing of DSBs once they are formed (e.g., rad50S, dmc1) also cause defects in SC formation (18)(19)(20).…”

Wood production, wood technology, and biotechnological impacts

“…White cap mutants (Fig. 4B) lacking any basidiospores helped to clone the gene spo11 for a type II topoisomerase active in meiosis (Cummings et al 1999, Celerin et al 2000. Two further genes have been identified by mutant analysis that act in the A mating type pathway.…”