Intraspecific violation of genetic colinearity and its implications in maize

Abstract

Although allelic sequences can vary extensively, it is generally assumed that each gene in one individual will have an allelic counterpart in another individual of the same species. We report here that this assumption does not hold true in maize. We have sequenced over 100 kb from the bz genomic region of two different maize lines and have found dramatic differences between them. First, the retrotransposon clusters, which comprise most of the repetitive DNA in maize, differ markedly in make-up and location relative to the genes in the bz region. Second, and more importantly, the genes themselves differ between the two lines, demonstrating that genetic microcolinearity can be violated within the same species. Our finding has bearing on the underlying genetic basis of hybrid vigor in maize, and possibly other organisms, and on the measurement of genetic distances.

Figure 1

Organization of genes and transposons in the bz genomic region of two different maize lines, McC and B73. The proximal end is at 0 kb; the distal end is at 151 kb in McC and at 110 kb in B73. Genes are shown as pentagons pointing in the direction of transcription; exons are in bronze, and introns are in yellow. Each transposon is in a different color. To facilitate the identification of interrupted retrotransposons, LTRs and encoded proteins of the same element are in the same color. Where a sequence in one line cannot be aligned with a sequence at the corresponding position in the other line, a dotted line is used to show the lack of alignment. The paired sequences of McC and B73 can be aligned only at the genes that they have in common: stk1, bz, stc1, rpl35A, tac6058, hypro1, znf, tac7077, and uce2. The McC chromosome contains three retrotransposon blocks, proximal to stk1, znf, and tac7077, respectively. The B73 chromosome contains two completely different retrotransposon blocks at the first and third of those locations plus a third cluster between bz and stc1, genes that are separated by less than 1 kb in McC. In addition, the genes cdl1, hypro2, hypro3, and rlk, which are found distal to hypro1 in McC, are missing entirely from B73. The location of cleavable NotI sites in McC and B73 genomic DNA is marked with an N. The McC sequence (GenBank accession no. AF391808) is a composite from two adjacent BAC clones centered around the NotI site in the Bz-McC allele (16). The B73 sequence (GenBank accession no. AF448416) is derived from two overlapping BACs isolated from a commercial library by using a bz probe.

Figure 2

Composition of the bz genomic region in different maize lines. NotI-digested genomic DNA from 10 different maize lines was separated by CHEF gel electrophoresis, blotted to Nylon membranes, hybridized to the four probes shown, and washed under high-stringency conditions. (A) bz. (B) tac7077. (C) rlk. (D) hypro2.