Nearly identical paralogs: implications for maize (Zea mays L.) genome evolution

Abstract

As an ancient segmental tetraploid, the maize (Zea mays L.) genome contains large numbers of paralogs that are expected to have diverged by a minimum of 10% over time. Nearly identical paralogs (NIPs) are defined as paralogous genes that exhibit > or = 98% identity. Sequence analyses of the "gene space" of the maize inbred line B73 genome, coupled with wet lab validation, have revealed that, conservatively, at least approximately 1% of maize genes have a NIP, a rate substantially higher than that in Arabidopsis. In most instances, both members of maize NIP pairs are expressed and are therefore at least potentially functional. Of evolutionary significance, members of many NIP families also exhibit differential expression. The finding that some families of maize NIPs are closely linked genetically while others are genetically unlinked is consistent with multiple modes of origin. NIPs provide a mechanism for the maize genome to circumvent the inherent limitation that diploid genomes can carry at most two "alleles" per "locus." As such, NIPs may have played important roles during the evolution and domestication of maize and may contribute to the success of long-term selection experiments in this important crop species.

Figure 1.—

Strategy used for determining whether a CP is indicative of residual heterozygosity or the existence of a NIP. Because alleles segregate during meiosis, CPs associated with residual heterozygosity are expected to segregate in a 1:2:1 ratio among selfed progeny. In contrast, NIPs would not be expected to segregate among the selfed progeny of an inbred line.

Figure 2.—

An example of a validated NIP (MAGI_21152). The membership and layout of MF GSSs, a CP-competent interval (∼900 bp), and the trace file for a 150-bp subinterval of the CP-competent interval (the bottom chromatograph) are shown relative to the two paramorphisms highlighted.

Figure 3.—

Mechanisms of gene duplication for (A) genetically linked (i–iii) and (B) genetically unlinked (i–iii) NIPs. Unequal pairing between flanking repeats (A, ii) can occur between homologs or sister chromatids, but probably at a lower rate. Transposon-mediated duplication can generate genetically tightly linked (A, i) and unlinked (B, i) NIPs. Unlinked NIPs could reside on separate chromosomes as depicted in (B, i) or could be at least 50 cM apart on the same chromosome. (B) Genetically unlinked NIPs are shown on two separate chromosomes (I and II). Unlinked NIPs can result from duplications of entire chromosomes (B, ii) or large segments of chromosomes that subsequently diverge (i.e., chromosomal rearrangements and gene loss or gain). Unlinked NIPs might also be generated by chromosomal rearrangements between duplicates that were originally genetically linked. Both linked and unlinked gene duplications might also occur by currently uncharacterized mechanisms. Boxes, thick lines, and solid circles represent genes, nongenic repeats, and centromeres, respectively.

Figure 4.—

A proposed mechanism for the evolution of gene duplications and the generation of NIPs and totally identical paralogs (TIPs). Genetically linked (A) and unlinked (B) duplication events generate TIPs that can diverge over time to produce NIPs. NIPs can be homogenized back into TIPs via nonallelic gene conversion or can further diverge. More diverged paralogs might also be homogenized into TIPs, but likely at a lower rate (dashed line). Shaded boxes represent genes and vertical lines within the boxes represent paramorphisms.