The amplification and evolution of orthologous 22-kDa α-prolamin tandemly arrayed genes in coix, sorghum and maize genomes

Abstract

Tandemly arrayed genes (TAGs) account for about one-third of the duplicated genes in eukaryotic genomes. They provide raw genetic material for biological evolution, and play important roles in genome evolution. The 22-kDa prolamin genes in cereal genomes represent typical TAG organization, and provide the good material to investigate gene amplification of TAGs in closely related grass genomes. Here, we isolated and sequenced the Coix 22-kDa prolamin (coixin) gene cluster (283 kb), and carried out a comparative analysis with orthologous 22-kDa prolamin gene clusters from maize and sorghum. The 22-kDa prolamin gene clusters descended from orthologous ancestor genes, but underwent independent gene amplification paths after the separation of these species, therefore varied dramatically in sequence and organization. Our analysis indicated that the gene amplification model of 22-kDa prolamin gene clusters can be divided into three major stages. In the first stage, rare gene duplications occurred from the ancestor gene copy accidentally. In the second stage, rounds of gene amplification occurred by unequal crossing over to form tandem gene array(s). In the third stage, gene array was further diverged by other genomic activities, such as transposon insertions, segmental rearrangements, etc. Unlike their highly conserved sequences, the amplified 22-kDa prolamin genes diverged rapidly at their expression capacities and expression levels. Such processes had no apparent correlation to age or order of amplified genes within TAG cluster, suggesting a fast evolving nature of TAGs after gene amplification. These results provided insights into the amplification and evolution of TAG families in grasses.

Structure, Organization, and Expression of the Alpha Prolamin Multigenic Family Bring New Insights into the Evolutionary Relationships among Grasses

“…Contigs were aligned to each other, and those possessing nucleotide sequence identity lower than 97% over the entire sequence were treated as unique. This analysis resulted in the identification of 10 α‐coixin sequences from which 9 presented 99% similarity with a cluster of 22 kDa α‐prolamins described by Zhou et al (2010; Supplemental Table S2 and Supplemental Fig. S2).…”

“…The difference between the 19 and 22 kDa α‐zeins is the number of tandem α‐helix repeats, as the former has 9 repeats, while the latter has 10 repeats (Argos et al, 1982; Garrat et al, 1993). In coix, only the 22 kDa α‐coixin has been described thus far (Ottoboni et al, 1993; Zhou et al, 2010). However, inspection of the sequenced sorghum genome revealed 19 kDa α‐kafirin‐related sequences that contain 10 instead of 9 α‐helix repeats (Figueira et al, 2008).…”

“…Sugarcane also harbors orthologous genes encoding the 19 kDa α‐canein (Figueira et al, 2008). A common characteristic of the α‐prolamin in maize, sorghum, coix, sugarcane, and millet is its multigenic family architecture (Figueira et al, 2008; Zhou et al, 2010; Xu et al, 2012). This is true for the 22 kDa subclass in the five species and the 19 kDa α‐zein and 19 kDa α‐canein; however, in sorghum, there are only few copies of the 19 kDa α‐kafirin‐related sequence (Xu et al, 2012).…”

Evolution of orthologous tandemly arrayed gene clusters

“…As this phenomenon is facilitated by the presence of repetitive sequences, a single duplication can induce a chain reaction leading to further duplications, eventually creating large Tandemly Arrayed Gene ( TAG ) clusters: groups of paralogous genes that are adjacent on a chromosome. TAGs account for about one-third of the duplicated genes in eukaryotes [9]. In human, they represent about 15% of all genes [10].…”

“…In most biology-oriented studies, a gene tree is obtained by applying a classical phylogenetic method to an alignment of the amino acid sequences corresponding to the collected gene sequences, and a duplication scenario is proposed for the gene family, based on a careful analysis of this gene tree (see for example [9] for the study of the 22-kDA prolamin gene amplification in grass genomes). Although such manual analysis may be useful to propose amplification scenarios for families of limited size and simple organization, it is usually impractical to infer more general evolutionary scenarios for large TAG clusters affected, in addition to duplications, by other events such as segmental deletion, that may lead to gene loss, and rearrangements (such as inversions or inverted duplications), that may affect gene order and transcriptional orientations.…”