Nearly Identical Paralogs: Implications for Maize (Zea mays L.) Genome Evolution

Genetics, Jan 2007 by Emrich, Scott J, Li, Li, Wen, Tsui-Jung, Yandeau-Nelson, Marna D, Et al

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 ≥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 ~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.

THE grasses (Poaceae) are a highly adaptable family of monocotyledonous plants that have been independently domesticated by several human civilizations. Maize (Zea mays L.) is a hypothesized ancient segmental tetraploid, and it is estimated that nearly one-third of all modern maize genes have a paralogous sequence (BLANC and WOLFE 2004). More recently, the expected divergence of the segmental allotetraploid event has been revised from the original 15-30% (GAUT and DOEBLEY 1997) to 10-20% (BLANC and WOLFE 2004) on the basis of maize ESTs.

Genomewide duplications are generally believed to provide raw material for evolutionary innovation (OHNO 1970) and as such they have played important roles in the evolution of both plants and vertebrates (reviewed by DURAND 2003; MOORE and PURUGGANAN 2005). In contrast to the diverged paralogs produced via ancient duplications, detailed analyses of the human genome have identified nearly identical sequences that were inadvertently collapsed, or condensed into a single contiguous region, during genome assembly (BAILEY et al. 2002; CHEUNG et al. 2003; SHE et al. 2004).

Tandem duplications are common among plant species (ZHANG and GAUT 2003). Indeed, MESSING et al. (2004) have estimated that approximately onethird of maize genes are tandemly duplicated. Few of these tandem duplications are similar enough that they would collapse during genome assembly. Several tandem duplications of maize have been well characterized, including, R-r (ROBBINS et al. 1991), Rp1 (RICHTER et al. 1995), P1 (ZHANG and Peterson 2005), and A1-b (YANDEAU-NELSON et al. 2006). Such duplications can be generated via unequal recombination (RICHTER et al. 1995; YANDEAU-NELSON et al. 2006). In contrast, the transposition of Mu-like transposons in rice (Pack-MULEs; JIANG et al. 2004; JURETIC et al. 2005) and Helitrons in maize (LAL et al. 2003; BRUNNER et al. 2005; LAI et al. 2005; LAL and HANNAH 2005; MORGANTE et al. 2005), which have incorporated fragments of unrelated genes, can generate dispersed genic duplications. Although as many as 11% of all maize gene fragments are unique to a specific inbred line (MORGANTE et al. 2005), the extent to which these gene duplications are functional is not known.

Because the maize inbred line B73 is homozygous at essentially all loci and its "gene space" has been extensively sequenced, it is an ideal candidate for beginning to study the extent, causes, and evolutionary significance of recent duplications in this complex genome. Toward this end, assemblies of B73 ESTs and geneenriched Genome Survey Sequences (GSSs) were examined for the appearance of "polymorphic" nucleotide positions, which we term candidate paramorphisms (CPs; EMRICH et al. 2004; FU et al. 2004). If a specific CP site is not due to a sequencing error or residual heterozygosity, we term this site a paramorphism (PM; FU et al. 2004). A paramorphism provides evidence of the existence of highly similar genomic loci and is strong evidence of a recent duplication without respect to the underlying duplication mechanism. We have termed a subset of such regions nearly identical paralogs (NIPs) if they exhibit$98% identity, are genic, and are not transposons or other repetitive sequences.

On the basis of highly conservative criteria, we estimate that ~1% of genes in the B73 maize genome have at least one NIP, and nearly all of these exhibit .99% identity. In addition, we determined that many of these highly similar loci in the maize genome are genetically linked. BecauseMuelements do not preferentially move to linked sites (LISCH et al. 1995), this result implies either that Helitrons preferentially insert into neighboring locations or that other mechanisms were involved in the origins of these genetically linked NIPs. The observed frequency of NIPs is substantially higher in maize than in the model dicotyledon, Arabidopsis thaliana, suggesting that this phenomenon is not universal in plants. Most importantly, we also report that members of many NIP families are differentially expressed. We hypothesize that the high frequency of NIPs in combination with their diverse expression patterns may have provided a selective advantage during the domestication and the genetic improvement ofmaize by classical plant breeders and may play a fundamental role in the success of long-term selection experiments (e.g., LAURIE et al. 2004).