Glycosyltransferase Family 61 in Liliopsida (Monocot): The Story of a Gene Family Expansion

Abstract

Plant cell walls play a fundamental role in several plant traits and also influence crop use as livestock nutrition or biofuel production. The Glycosyltransferase family 61 (GT61) is involved in the synthesis of cell wall xylans. In grasses (Poaceae), a copy number expansion was reported for the GT61 family, and raised the question of the evolutionary history of this gene family in a broader taxonomic context. A phylogenetic study was performed on GT61 members from 13 species representing the major angiosperm clades, in order to classify the genes, reconstruct the evolutionary history of this gene family and study its expansion in monocots. Four orthogroups (OG) were identified in angiosperms with two of them displaying a copy number expansion in monocots. These copy number expansions resulted from both tandem and segmental duplications during the genome evolution of monocot lineages. Positive selection footprints were detected on the ancestral branch leading to one of the orthogroups suggesting that the gene number expansion was accompanied by functional diversification, at least partially. We propose an OG-based classification framework for the GT61 genes at different taxonomic levels of the angiosperm useful for any further functional or translational biology study.

Keywords: Liliopsida; gene family expansion; glycosyltransferase family 61; orthologous genes; phylogeny; positive selection footprints.

FIGURE 1

(A) Number of GT61 family members annotated in 37 plant genomes from the GreenPhyl database. Monocot species span from Musa acuminata to Sorghum bicolor; dicot species span from Coffea canephora to Cajanus cajan. (B) Dendrogram of phylogenetic relationships among the studied species.

FIGURE 2

Phylogenetic tree obtained with 219 GT61 sequences [sequences from clade C of Anders et al. (2012) were not analyzed] from 13 species representing angiosperms. Dicot and monocot sequence names are in dark green and purple, respectively. 253 aligned positions were used to build the tree. Branches of sequences assigned to A, D, F, and G orthogroups are indicated in red, blue, fuchsia and green, respectively. Branch aLRT support was indicated only for main branches (complete data are available in Supplementary Data S3).

FIGURE 3

Phylogenetic tree obtained with 55 GT61 sequences from clade D, F, and G. Species origin of sequences was indicated by a five digit code [A. comosus (ANACO), A. officinalis (ASPOF), B. distachyon (BRADI), E. guineensis (ELAGV), M. acuminata (MUSAC), O. sativa (ORYSA), P. dactylifera (PHODA), S. italica (SETIT), A. trichopoda (AMBTC), A. thaliana (ARATH), C. canephora (COFCA), T. cacao (THECC), and V. vinifera (VITVI)]. Dicot and monocot sequence names are in dark green and purple, respectively.

FIGURE 4

Phylogenetic tree obtained with 164 GT61 sequences from clade A. Clades corresponding to orthogroups are collapsed. The fully expanded representation of the tree is in Supplementary Figure S1.

FIGURE 5

Model for tandem expansion of GT61 genes (symbolized by arrows) belonging to OG-GT61-A in the Commelinid lineage. Blue color indicates tandem duplication, red color indicates inversions. The first step was the tandem triplication of the common GT61-A ancestor followed by inversion of central copy that finally underwent to additional tandem duplication. Succession of second (inversion) and third step (tandem duplication) could be inverted, making the A2, [A3, A4] and A5 amplification predating the inversion of their common ancestor.

FIGURE 6

Phylogenetic tree used for PAML analyses. Length is reported for each tested branch. Clades corresponding to orthogroups are collapsed.