RESEARCH ARTICLE Altered distribution of MLH1 foci is associated with changes in cohesins and chromosome axis compaction in an asynaptic mutant of tomato Huanyu Qiao & Hildo H. Offenberg & Lorinda K. Anderson Received: 6 October 2011 / Revised: 3 January 2012 / Accepted: 21 January 2012 / Published online: 17 February 2012 # Springer-Verlag 2012 Abstract In most multicellular eukaryotes, synapsis [synapto- nemal complex (SC) formation] between pairs of homologous chromosomes during prophase I of meiosis is closely linked with crossing over. Asynaptic mutants in plants have reduced synapsis and increased univalent frequency, often resulting in genetically unbalanced gametes and reduced fertility. Surpris- ingly, some asynaptic mutants (like as1 in tomato) have wild- type or increased levels of crossing over. To investigate, we examined SC spreads from as1/as1 microsporocytes using both light and electron microscopic immunolocalization. We observed increased numbers of MLH1 foci (a crossover mark- er) per unit length of SC in as1 mutants compared to wild-type. These changes are associated with reduced levels of detectable cohesin proteins in the axial and lateral elements (AE/LEs) of SCs, and the AE/LEs of as1 mutants are also significantly longer than those of wild-type or another asynaptic mutant. These results indicate that chromosome axis structure, synap- sis, and crossover control are all closely linked in plants. Synapsis is defined as the formation of a unique structure called the synaptonemal complex (SC) between pairs of homologous chromosomes during prophase I of meiosis (Zickler and Kleckner 1999; Page and Hawley 2004). Each SC is composed of a central element and two lateral ele- ments [LEs, called axial elements (AEs) before SC forma- tion] that are linked together by transverse filaments (TFs). Different stages in the pairing and synapsis of homologous chromosomes can be monitored using SC components. Dur- ing leptotene of prophase I, AEs form between the two sister chromatids of each chromosome. In zygotene, homologous chromosomes are in the process of synapsis when TFs begin to link together the two LEs. At pachytene, an SC extends along the length of each synapsed pair of homologs (biva- lents). Finally, at diplotene, SCs breakdown (desynapse), and bivalents that are now held together by chiasmata con- dense. In a number of organisms, including budding yeast, mammals, and higher plants, synapsis of homologous chro- mosomes during prophase I of meiosis depends on prior formation of programmed DNA double-strand breaks (DSBs; Keeney 2001). In higher plants, the relationship between synapsis and crossing over has been examined using mutants that do not complete synapsis (Beadle 1933; Rhoades 1947; Miller 1963; Nel 1979; Kitada and Omura 1984; Kaul and Murthy 1985; Havekes et al. 1994). Many of the asynaptic mutants arose spontaneously, and the specific defect is unknown (as indicated by the general as designation of the mutations). These mutants were initially identified by their reduced fertility that is usually accompanied by incomplete synapsis, the presence of univalents at metaphase I, random segregation of univalents, and aneuploid spores and gametes (Rhoades 1947; Miller 1963; Nel 1979; Havekes et al. 1994). Given the close relationship between synapsis and crossing over (Zickler and Kleckner 1999), one might expect that limited synapsis Responsible Editor: Erich Nigg Electronic supplementary material The online version of this article (doi:10.1007/s00412-012-0363-z) contains supplementary material, which is available to authorized users. H. Qiao : L. K. Anderson (*) Department of Biology and Program in Molecular Plant Biology, Colorado State University, Fort Collins, CO 80523, USA e-mail: lorinda.anderson@colostate.edu H. H. Offenberg Johannes Poststraat 49, 5348, TL Oss, The Netherlands Present Address: H. Qiao Department of Microbiology, University of California, Davis, CA 95616, USA Chromosoma (2012) 121:291–305 DOI 10.1007/s00412-012-0363-z