Expansion of PIM family by tandem and segmental duplication of
PIM1
PIM1 , a member of the PIM gene family composed of three
single-copy genes (PIM1, PIM2, PIM3 ) and highly evolutionarily
conserved in multicellular organism, was originally identified as a
common proviral insertion site for the Moloney murine leukemia virus
(Selten et al., 1985) and has been known as a proto-oncogene and
implicated in the control of cancer cell proliferation, migration and
apoptosis (Narlik-Grassow et al., 2014). In contrast to other amniotic
genomes (including chicken) that harbor only single copy of PIM1gene, large expansion of PIM1 which have been reported in zebra
finch (Taeniopygia guttata ) (Kong et al., 2010), another species
of songbird, is also found in tree sparrow when PIM3 keeps one
single copy. Out of a total of 449 initially predicted PIM1genes, only 142 are found to be complete for the conserved protein
kinase domain which related with the protein kinase catalytic activity.
To deduce the evolutionary relationship of the PIM family, we
construct a phylogenetic tree containing 154 PIM (2 of chicken, 3 of
human, 6 of zebra finch and 143 of tree sparrow) proteins and divided
the expanded PIM1 genes of tree sparrow into 2 subgroups based on
the constructed phylogenetic tree (Figure 2A). All subgroup I PIM1
proteins are found to have similar conserved motifs (motif 6-10) with
the chicken and human PIM1 when subgroup II PIM1 have at most 5 excess
motifs (motif 1-5) which also appear in the zebra finch (Figure 2A;
Figure S5). The structural variation of subgroup II PIM1 proteins may be
derived from an insertion event during duplication.
Notably, besides the structural difference, the two subgroups show
different chromosomal distribution pattern and duplication mechanism.
All subgroup I PIM1 are centered in chromosome 7 and 24 when
subgroup II have more decentralized distribution (Table S7). The
centered distribution pattern of subgroup I is mainly owing to the
tandem duplication events involved in the expansion of subgroup IPIM1 genes and the more dispersed subgroup II PIM1 genes
are derived from segmental duplication (Figure S6). The dispersed
duplicates of PIM1 are noticed to be always adjacent to genes of
several other families including C2H2zinc finger (C2H2ZNF ) protein,
olfactory receptor (OR ), p21-activated kinase (PAK ),
maestro heat-like repeat containing protein family member (MROH ),
hydrocephalus-inducing protein homolog (HYDIN ) and inositol
1,4,5-trisphosphate receptor-interacting protein-like (ITPRIPL )
which result in these 6 gene families expand simultaneously but at
different degree in tree sparrow genome (Figure 2B; Figure S6).
Furthermore, we find that the genomic regions contained these 7 families
mainly distribute across chromosomes Z and 18-36, and these regions also
contain high density of long terminal repeat (LTR) retrotransposons
(Figure 2C; Figure S7), the same distribution pattern of these 7
families members and LTR retrotransposons may indicate that the
expansion of these 7 families and LTR retrotransposons happened in tree
sparrow genome simultaneously. Based on these results, we assume that
large, interspersed segmental duplication of genomic regions contained
random members of these 7 gene families occurred multiple times at
different time points during evolution, and these replication events may
be the strong driving force of the evolution of tree sparrow genome.
As so far, the expansion events of PIM1 are only found in
passerine (zebra finch and tree sparrow). To find out if the expansion
of PIM1 is songbird-specific, the PIM gene family members
are identified and counted for all available avian genome in Ensembl,
including 47 species covered 12 avian orders (Table S8). By comparing
the number of PIM1 in the 47 genomes, the expansion ofPIM1 is detected in 18 species of 3 orders (Figure 2C; Table S9).
This result show that the expansion of PIM gene family caused by
duplicated PIM1 genes occurred not only in the order
Passeriformes, but also in Psittaciformes and Strigiformes (Figure 2C)
which may indicate the PIM1 genes duplicate independently in
several avian lineages.