Meiotic crossovers characterized by haplotype-specific chromosome painting in maize

Authors: DO VALE MARTINS, LIVIA - Michigan State University; YU, FAN - Michigan State University; ZHAO, HAINAN - Michigan State University; DENNISON, TESIA - Iowa State University; Lauter, Nicholas; WANG, HAIYAN - Michigan State University; DENG, ZUHU - Fujian Agriculture And Forest University; THOMPSON, ADDIE - Michigan State University; SEMRAU, KASSANDRA - Arbor Biosciences; ROUILLARD, JEAN-MARIE - Arbor Biosciences; BIRCHLER, JAMES - University Of Missouri; JIANG, JIMING - University Of Michigan

Submitted to: Nature Communications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/10/2019
Publication Date: 10/10/2019
Citation: Do Vale Martins, L., Yu, F., Zhao, H., Dennison, T., Lauter, N.C., Wang, H., Deng, Z., Thompson, A., Semrau, K., Rouillard, J., Birchler, J.A., Jiang, J. 2019. Meiotic crossovers characterized by haplotype-specific chromosome painting in maize. Nature Communications. 10:4604. https://doi.org/10.1038/s41467-019-12646-z.
DOI: https://doi.org/10.1038/s41467-019-12646-z

Interpretive Summary: Plant genomes are much more flexible than animal genomes because they readily tolerate additions and losses of genetic material, including single- and multi-gene sized pieces (presence-absence variation), whole chromosomes (aneuploidy), and chromosome sets (polyploidy). During breeding for crop improvement, some of the new and useful genetic variation occurs at these levels, which can be difficult to characterize because they break the normal cytogenetic rules. It is essential to understand how useful cytogenetic variation arises, as well as how frequently the normal rules of inheritance are violated. To this end, we report the successful development and application of an improved set of genome-painting tools, allowing visual examination of chromosome structures. The improvement is based on the simultaneous use of thousands of colored reporter molecules that are engineered to differentiate the parental origins of the DNA segments that they "paint". The proof-of-concept work was performed on a single chromosome of the corn genome for which other detailed genetic resources were already available, making the findings definitive and efficient to obtain.

Technical Abstract: Meiotic crossovers (COs) play a critical role in generating genetic variation and maintaining faithful segregation of homologous chromosomes during meiosis. We developed a technique that allows visualization of COs directly on metaphase chromosomes. We computationally identified oligonucleotides (oligos) specific to chromosome 10 of maize inbreds B73 and Mo17. The haplotype-specific oligos, based on presence-absence variation (PAV) or single nucleotide polymorphism (SNP) between the two inbreds, were synthesized in parallel and labeled as probes for fluorescence in situ hybridization (FISH). The parental chromosome 10 in B73 x Mo17 hybrids can be differentially painted by FISH using the haplotype-specific oligo probes. We were able to cytologically characterize COs derived from the two homologous chromosomes 10 in progenies derived from the B73 x Mo17 hybrids. Chromosome painting of 58 F2 plants derived from the B73 x Mo17 hybrids revealed the lack of COs in the entire proximal half of chromosome 10. However, we detected COs located in proximal regions very close to the centromere in several recombinant inbred lines from an intermated B73 x Mo17 population, suggesting the effective accumulation of COs in recombination-suppressed chromosomal regions through intermating. Potential applications of haplotype-specific chromosome painting are discussed.