Maize Genome Structure Variation: Interplay between Retrotransposon Polymorphisms and Genic Recombination[W]

Although maize (Zea mays) retrotransposons are recombinationally inert, the highly polymorphic structure of maize haplotypes raises questions regarding the local effect of intergenic retrotransposons on recombination. To examine this effect, we compared recombination in the same genetic interval with and without a large retrotransposon cluster. We used three different bz1 locus haplotypes, McC, B73, and W22, in the same genetic background. We analyzed recombination between the bz1 and stc1 markers in heterozygotes that differ by the presence and absence of a 26-kb intergenic retrotransposon cluster. To facilitate the genetic screen, we used Ds and Ac markers that allowed us to identify recombinants by their seed pigmentation. We sequenced 239 recombination junctions and assigned them to a single nucleotide polymorphism–delimited interval in the region. The genetic distance between the markers was twofold smaller in the presence of the retrotransposon cluster. The reduction was seen in bz1 and stc1, but no recombination occurred in the highly polymorphic intergenic region of either heterozygote. Recombination within genes shuffled flanking retrotransposon clusters, creating new chimeric haplotypes and either contracting or expanding the physical distance between markers. Our findings imply that haplotype structure will profoundly affect the correlation between genetic and physical distance for the same interval in maize.

[1]  C. Williams,et al.  Comparative recombination distances among Zea mays L. inbreds, wide crosses and interspecific hybrids. , 1995, Genetics.

[2]  R. A. Brink,et al.  A Genetic Change Associated with the R Locus in Maize Which Is Directed and Potentially Reversible. , 1956, Genetics.

[3]  D. Grant,et al.  Expanding the genetic map of maize with the intermated B73 × Mo17 (IBM) population , 2002, Plant Molecular Biology.

[4]  J. Mottinger.  Unstable mutants of bronze induced by pre-meiotic X-ray treatment in maize , 2004, Theoretical and Applied Genetics.

[5]  H. Dooner,et al.  Remarkable variation in maize genome structure inferred from haplotype diversity at the bz locus , 2006, Proceedings of the National Academy of Sciences.

[6]  E. Buckler,et al.  Using Crossover Breakpoints in Recombinant Inbred Lines to Identify Quantitative Trait Loci Controlling the Global Recombination Frequency , 2007, Genetics.

[7]  H. Tsujimoto,et al.  Tetrad-FISH analysis reveals recombination suppression by interstitial heterochromatin sequences in rye (Secale cereale) , 2002, Molecular Genetics and Genomics.

[8]  H. Fu,et al.  The highly recombinogenic bz locus lies in an unusually gene-rich region of the maize genome , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[9]  E. Ganko,et al.  Retrotransposon-gene associations are widespread among D. melanogaster populations. , 2004, Molecular biology and evolution.

[10]  Patrick S Schnable,et al.  Cis-effects on Meiotic Recombination Across Distinct a1-sh2 Intervals in a Common Zea Genetic Background Sequence data from this article have been deposited with the EMBL/GenBank Data Libraries under accession nos. AY656756, AY656757, AY656758 and AY662984, AY662985, AY662986, AY662987. , 2005, Genetics.

[11]  B. Mcclintock.  Topographical relations between elements of control systems in maize , 1962 .

[12]  P. Schnable,et al.  Molecular characterization of meiotic recombination across the 140-kb multigenic a1-sh2 interval of maize , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[13]  W. Zacheus Cande,et al.  Mapping a new frontier; development of integrated cytogenetic maps in plants , 2000, Functional & Integrative Genomics.

[14]  Phillip SanMiguel,et al.  The paleontology of intergene retrotransposons of maize , 1998, Nature Genetics.

[15]  S. Hake,et al.  Mutator insertions in an intron of the maize knotted1 gene result in dominant suppressible mutations. , 1994, Genetics.

[16]  Joachim Messing,et al.  Gene expression of a gene family in maize based on noncollinear haplotypes , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[17]  T. Petes,et al.  Meiotic recombination hot spots and cold spots , 2001, Nature Reviews Genetics.

[18]  Z. Zheng,et al.  A maize sesquiterpene cyclase gene induced by insect herbivory and volicitin: characterization of wild-type and mutant alleles. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[19]  Michael Black,et al.  Role of transposable elements in heterochromatin and epigenetic control , 2004, Nature.

[20]  Agnes P Chan,et al.  Uneven chromosome contraction and expansion in the maize genome. , 2006, Genome research.

[21]  E. Ralston,et al.  A Single Genetic Unit Specifies Two Transposition Functions in the Maize Element Activator , 1986, Science.

[22]  H. Fu,et al.  A gene-enriched BAC library for cloning large allele-specific fragments from maize: isolation of a 240-kb contig of the bronze region. , 2000, Genome research.

[23]  Michele Morgante,et al.  Evolution of DNA Sequence Nonhomologies among Maize Inbredsw⃞ , 2005, The Plant Cell Online.

[24]  H. Dooner,et al.  Genetic Fine Structure of the BRONZE Locus in Maize. , 1986, Genetics.

[25]  E. Ralston,et al.  Sequence of three bronze alleles of maize and correlation with the genetic fine structure. , 1988, Genetics.

[26]  H. Fu,et al.  Intraspecific violation of genetic colinearity and its implications in maize , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[27]  Steven G. Schroeder,et al.  Development and mapping of SSR markers for maize , 2002, Plant Molecular Biology.

[28]  C. Mézard,et al.  Meiotic recombination hotspots in plants. , 2006, Biochemical Society transactions.

[29]  H. Fu,et al.  Recombination rates between adjacent genic and retrotransposon regions in maize vary by 2 orders of magnitude , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[30]  G. Reuter,et al.  Recombinogenic effects of suppressors of position-effect variegation in Drosophila. , 2002, Genetics.

[31]  C. Poneleit,et al.  Variability of recombination frequencies in the Iowa Stiff Stalk Synthetic (Zea mays L.) , 1993, Theoretical and Applied Genetics.

[32]  H. Dooner,et al.  Recombination occurs uniformly within the bronze gene, a meiotic recombination hotspot in the maize genome. , 1997, The Plant cell.

[33]  Jianxin Ma,et al.  Rapid recent growth and divergence of rice nuclear genomes. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[34]  D. Grant,et al.  A linkage map based on information from four F2 populations of maize (Zea mays L.) , 1991, Theoretical and Applied Genetics.

[35]  Phillip SanMiguel,et al.  Evidence that a Recent Increase in Maize Genome Size was Caused by the Massive Amplification of Intergene Retrotransposons , 1998 .

[36]  H. Dooner.  Extensive Interallelic Polymorphisms Drive Meiotic Recombination into a Crossover Pathway Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.001271. , 2002, The Plant Cell Online.

[37]  R. Phillips,et al.  Complex structure of knob DNA on maize chromosome 9. Retrotransposon invasion into heterochromatin. , 1998, Genetics.

[38]  P. Schnable,et al.  Unequal Sister Chromatid and Homolog Recombination at a Tandem Duplication of the a1 Locus in Maize , 2006, Genetics.

[39]  W. K. Baker.  Crossing Over in Heterochromatin , 1958, The American Naturalist.