Comparative physical mapping links conservation of microsynteny to chromosome structure and recombination in grasses

Abstract

Nearly finished sequences for model organisms provide a foundation from which to explore genomic diversity among other taxonomic groups. We explore genome-wide microsynteny patterns between the rice sequence and two sorghum physical maps that integrate genetic markers, bacterial artificial chromosome (BAC) fingerprints, and BAC hybridization data. The sorghum maps largely tile a genomic component containing 41% of BACs but 80% of single-copy genes that shows conserved microsynteny with rice and partially tile a nonsyntenic component containing 46% of BACs but only 13% of single-copy genes. The remaining BACs are centromeric (4%) or unassigned (8%). The two genomic components correspond to cytologically discernible ''euchromatin'' and ''heterochromatin.'' Gene and repetitive DNA distributions support this classification. Greater microcolinearity in recombinogenic (euchromatic) than nonrecombinogenic (heterochromatic) regions is consistent with the hypothesis that genomic rearrangements are usually deleterious, thus more likely to persist in nonrecombinogenic regions by virtue of Muller's ratchet. Interchromosomal centromeric rearrangements may have fostered diploidization of a polyploid cereal progenitor. Model plant sequences better guide studies of related genomes in recombinogenic than nonrecombinogenic regions. Bridging of 35 physical gaps in the rice sequence by sorghum BAC contigs illustrates reciprocal benefits of comparative approaches that extend at least across the cereals and perhaps beyond.comparative genomics ͉ Oryza ͉ synteny T he grasses (Poaceae) provide most of mankind's caloric intake and a growing share of our fuel. The best-studied grasses, leading cereal crops, shared a common paleopolyploid ancestor Ϸ42-47 million years ago (mya) (1). Cereals show much colinearity of genetic maps and often have important traits controlled by quantitative trait loci at corresponding locations (2). Despite these similarities, the cereals have diverged remarkably in genome size from Ϸ430 million base pairs (MBP) in rice (3) to 15,966 MBP in wheat (3), largely due to differential repetitive DNA amplification and elimination.As a model for tropical grasses, sorghum [Sorghum bicolor (SB)] is a logical complement to rice (Oryza), in that it has biochemical and morphological specializations to improve carbon assimilation at high temperatures (C4 photosynthesis). By contrast, rice uses C3 photosynthesis more typical of temperate grasses. The Ϸ760-MBP (3) sorghum genome is a logical bridge to the Ϸ2,500-MBP (3) maize genome, and the Ϸ4,000-MBP (3) genome of sugarcane, the world's leading biomass͞biofuels crop. Sorghum shared common ancestry with maize (12 mya) and sugarcane (5 mya), much more recently than rice (42-47 mya). The most recent whole-genome duplication in sorghum appears to be Ϸ70 mya (1) vs. Ϸ12 mya in maize (4) and Ͻ5 mya in sugarcane (5), promising a higher success rate in relating sorghum genes to phenotypes by knockouts than either maize or sugarcane genes. Comparison of SB and closely related Sorghum...

Evolutionary fate of rhizome-specific genes in a non-rhizomatous Sorghum genotype

“…BAC clones corresponding to RT-enriched genes from S. propinquum and S. bicolor By hybridization of gene-specific overgos, we have identified the BAC clones and number of contigs (genetic loci) at which family members of each gene are represented in the physical maps of both S. bicolor and S. propinquum (Bowers et al, 2005). A total of 24 genes of S. proqinquum were anchored to only one locus, whereas 17 genes occurred at 2-10 loci and 9 genes at more than 10 loci.…”

“…Six clones that were enriched in RT relative to RMI were also RT-enriched relative to AG, resulting in a total of 54 clones that were further analyzed herein. Overgo probes were designed from the sequences of each of 54 RT-enriched genes by BLAST comparison against other plant species to identify the most-conserved 40 bp sequences as described (Bowers et al, 2005). For gene sequences with no matches to any other plant species, arbitrary 40 bp sequences were used as overgo probes.…”

“…For gene sequences with no matches to any other plant species, arbitrary 40 bp sequences were used as overgo probes. Individual overgo probes were radioactively labeled (Yuksel and Paterson, 2005) and then hybridized to seven BAC filters including 40 957 BACs of S. propinquum and 69 545 BACs of S. bicolor as described (Bowers et al, 2005).…”

Comparative Genomics of Grasses Promises a Bountiful Harvest

“…In mammals, gene order conservation has been associated with the regulation of gene expression (Semon and Duret, 2006;Gierman et al, 2007), replication, and chromatin structure (Huvet et al, 2007). Nonrandom patterns of gene expression are found among proximally located rice (Ma et al, 2005) and Arabidopsis (Ren et al, 2007) genes. While a comparative study to date found no microsynteny between the two species in these domains (Ren et al, 2007), inferences about monocot-dicot synteny are much more complicated than was realized before the availability of whole-genome sequences (Paterson et al, 1996), due largely to multiple paleopolyploidies and associated gene losses.…”

“…While the Oryza-Sorghum-Brachypodium group is still viewed as having evolved relatively slowly, grasses that have been through recent genome duplications have undergone substantial fractionation of ancestral gene orders across multiple chromosomes. For example, there is greater similarity of gene order between the genomes of sorghum and rice, diverged by 40 to 50 million years Bowers et al, 2005), than between the genomes of sorghum and maize, diverged by 10 to 15 million years (Bowers et al, 2003). As yet unknown factors other than polyploidy also influence grass genome stability.…”