Genomic analysis of NAC transcription factors in banana (Musa acuminata) and definition of NAC orthologous groups for monocots and dicots

Abstract

Identifying the molecular mechanisms underlying tolerance to abiotic stresses is important in crop breeding. A comprehensive understanding of the gene families associated with drought tolerance is therefore highly relevant. NAC transcription factors form a large plant-specific gene family involved in the regulation of tissue development and responses to biotic and abiotic stresses. The main goal of this study was to set up a framework of orthologous groups determined by an expert sequence comparison of NAC genes from both monocots and dicots. In order to clarify the orthologous relationships among NAC genes of different species, we performed an in-depth comparative study of four divergent taxa, in dicots and monocots, whose genomes have already been completely sequenced: Arabidopsis thaliana, Vitis vinifera, Musa acuminata and Oryza sativa. Due to independent evolution, NAC copy number is highly variable in these plant genomes. Based on an expert NAC sequence comparison, we propose forty orthologous groups of NAC sequences that were probably derived from an ancestor gene present in the most recent common ancestor of dicots and monocots. These orthologous groups provide a curated resource for large-scale protein sequence annotation of NAC transcription factors. The established orthology relationships also provide a useful reference for NAC function studies in newly sequenced genomes such as M. acuminata and other plant species.

Fig. 1

Inference of the orthologous groups with similarity-based approach. Empty and filled shapes indicate orthologous copies in two different species. a Schematic representation of the amplification of a multi-copy family in two species. Arrows connect copies of an OG in a species with the less divergent copy of the other species. b Expected Blastp results for an OG. Arrows connect copies of a species with the best Blastp hit in the other species

Fig. 2

Comparison between expert versus OrthoMCL automatic analysis for OG detection. Clusters obtained by OrthoMCL with three increasing inflation parameter and the OG member included in each cluster

Fig. 3

Exon/intron structure of NAC genes according to the orthologous groups

Fig. 4

Maximum Likelihood phylogenetic tree of NAC proteins. Phylogenetic analysis was carried with protein sequences from A. thaliana (ARATH), V. vinifera (VITVI), O. sativa (ORYSA) and M. acuminata (MUSAC) as described in the “Methods”. Branch support values correspond to approximate likelihood ratio test (a-LRT) results. The 26 clusters supporting the grouping were indicated on the figure with the numbering proposed in this work. Leaf colors of the gene tree are colored according to their species. PhyloXML format of this gene tree and phylogenetic trees of the groups are provided as Online Resources 4

Fig. 5

Evolutionary reconstruction of the fate of an ancestral locus having NAC genes of divergent OGs in tandem position. Blue and red arrowheads indicate NAC genes included in OGs 3c and 1g, respectively; green arrowheads indicate RicinB-lectin_2 genes; grey arrowheads indicate other genes

Fig. 6

Hierarchical clustering of the 40 NAC OGs analysed in the four species (V. vinifera, A thaliana, O. sativa and M. acuminata). The colour gradient from green to red indicates whether a particular group is significantly smaller or bigger based on Z-score for all genes across the four species. The figure was generated using PermutMatrix (Caraux and Pinloche 2004) with the euclidean distance and the McQuitty clustering parameters