Gene expression of a gene family in maize based on noncollinear haplotypes

Abstract

Genomic regions of nearly every species diverged into different haplotypes, mostly based on point mutations, small deletions, and insertions that do not affect the collinearity of genes within a species. However, the same genomic interval containing the z1C gene cluster of two inbred lines of Zea mays significantly lost their gene collinearity and also differed in the regulation of each remaining gene set. Furthermore, when inbreds were reciprocally crossed, hybrids exhibited an unexpected shift of expression patterns so that ''overdominance'' instead of ''dominance complementation'' of allelic and nonallelic gene expression occurred. The same interval also differed in length (360 vs. 263 kb). Segmental rearrangements led to sequence changes, which were further enhanced by the insertion of different transposable elements. Changes in gene order affected not only z1C genes but also three unrelated genes. However, the orthologous interval between two subspecies of rice (not rice cultivars) was conserved in length and gene order, whereas changes between two maize inbreds were as drastic as changes between maize and sorghum. Given that chromosomes could conceivably consist of intervals of haplotypes that are highly diverged, one could envision endless breeding opportunities because of their linear arrangement along a chromosome and their expression potential in hybrid combinations (''binary'' systems). The implication of such a hypothesis for heterosis is discussed. z1C zein gene cluster ͉ heterosis ͉ genomic organization ͉ overdominance ͉ transposition C orn or Zea mays is one of the most important crops in the world.Although wheat and rice surpass it as a staple and in acreage, no crop rivals its total grain yield and the diversity of its uses as processed food, for animal feed and sweetener in soft drinks, and its industrial applications such as fuel and adhesives. The preference of corn over other grains or legumes for such applications is because of the unusual properties of hybrids. When distant inbred lines are crossed, the resulting hybrids exhibit an unusual vigor (heterosis) that results in higher yields per acre than the parental lines would produce themselves (1). The premium exercised for the breeding of steadily improved maize inbreds customized for different geographic areas has generated a huge enterprise worldwide, particularly in the United States, yet the underlying molecular mechanism for hybrid vigor is not well understood. To decide between two models explaining ''dominance complementation'' or ''overdominance'' of heterozygotes, it will therefore be necessary to compare not only the genomic architecture of genes within an interval of several hundred kilobases but also the expression of these genes of two parental inbreds and their reciprocal hybrids.The fact that some gene families are highly clustered within such lengthy intervals rather than spread over the entire genome is the springboard for our study. One such interval encodes the 22-kDa ␣-zein storage proteins. These proteins accumulate d...

Comparative Genomics of Grasses Promises a Bountiful Harvest

“…This finding, while important, is not unprecedented. For example, the major seed storage proteins of maize (zein) and sorghum (kafirin) are encoded by genes that appear to have evolved since the divergence of the panicoids from the oryzoids, being absent in rice (Song and Messing, 2003). Mechanisms that may lead to the creation of new genes by juxtaposition of existing gene fragments are now well known.…”

Identification of a Gene in the Process of Being Lost from the Genus Agrostis

“…Gain of the Crs-1 locus from another species is thus a formal possibility. The haplotype noncolinearity for some genes observed between maize inbreds (Fu and Dooner, 2002;Song and Messing, 2003;Brunner et al, 2005) was proposed to occur largely from insertion events rather than deletion events (Brunner et al, 2005). In that study, the nonshared genes were truncated versions of homologs present elsewhere in the genome (Brunner et al, 2005), suggesting insertion originated from genomic elements within the individual genome, not from introgression from another genome.…”

“…The genes missing in B73 are obviously not essential, and paralogs present in other regions of the genome likely compensate for their loss (Fu and Dooner, 2002). A similar situation of differences in gene content in the zein 21C genomic region was observed in the maize inbreds B73 and BSSS53 (Song and Messing, 2003). Recent information suggests that the apparent gene loss and haplotype noncolinearity observed between maize inbreds is actually a result of insertion of gene segments from elsewhere in the genome (Brunner et al, 2005;H.…”

“…Apparently, some genomic event occurred that resulted in a haplotype in which the Crs-1 locus was lost and this haplotype has come to predominate in the population. As discussed above, the haplotype noncolinearity observed between maize inbreds (Fu and Dooner, 2002;Song and Messing, 2003;Brunner et al, 2005) likely originated from gene insertion events from elsewhere in the genome, rather that deletion events, and so is different from the situation with Crs-1.…”

Helitrons: Their Impact on Maize Genome Evolution and Diversity

“…Intriguingly, data emerging from analysis of multiple regions of the genome indicate that significant differences in gene composition and colinearity are widely prevalent among different maize inbred lines. (Fu and Dooner 2002;Song and Messing 2003;. This so-called, "intraspecific violation of gene colinearity" or "+/-polymorphism"" has been shown to be primarily due to the presence/absence of gene piece rich fragments between different inbred lines.…”