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Phylogenomics of the benzoxazinoid biosynthetic pathway of Poaceae: gene duplications and origin of the Bx cluster.

ABSTRACT: BACKGROUND:The benzoxazinoids 2,4-dihydroxy-1,4-benzoxazin-3-one (DIBOA) and 2,4-dihydroxy-7- methoxy-1,4-benzoxazin-3-one (DIMBOA), are key defense compounds present in major agricultural crops such as maize and wheat. Their biosynthesis involves nine enzymes thought to form a linear pathway leading to the storage of DI(M)BOA as glucoside conjugates. Seven of the genes (Bx1-Bx6 and Bx8) form a cluster at the tip of the short arm of maize chromosome 4 that includes four P450 genes (Bx2-5) belonging to the same CYP71C subfamily. The origin of this cluster is unknown. RESULTS:We show that the pathway appeared following several duplications of the TSA gene (?-subunit of tryptophan synthase) and of a Bx2-like ancestral CYP71C gene and the recruitment of Bx8 before the radiation of Poaceae. The origins of Bx6 and Bx7 remain unclear. We demonstrate that the Bx2-like CYP71C ancestor was not committed to the benzoxazinoid pathway and that after duplications the Bx2-Bx5 genes were under positive selection on a few sites and underwent functional divergence, leading to the current specific biochemical properties of the enzymes. The absence of synteny between available Poaceae genomes involving the Bx gene regions is in contrast with the conserved synteny in the TSA gene region. CONCLUSIONS:These results demonstrate that rearrangements following duplications of an IGL/TSA gene and of a CYP71C gene probably resulted in the clustering of the new copies (Bx1 and Bx2) at the tip of a chromosome in an ancestor of grasses. Clustering favored cosegregation and tip chromosomal location favored gene rearrangements that allowed the further recruitment of genes to the pathway. These events, a founding event and elongation events, may have been the key to the subsequent evolution of the benzoxazinoid biosynthetic cluster.

SUBMITTER: Dutartre L

PROVIDER: S-EPMC3449204 | biostudies-literature | 2012 May

REPOSITORIES: biostudies-literature

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Phylogenomics of the benzoxazinoid biosynthetic pathway of Poaceae: gene duplications and origin of the Bx cluster.

Dutartre Leslie L Hilliou Frédérique F Feyereisen René R

BMC evolutionary biology 20120511

<h4>Background</h4>The benzoxazinoids 2,4-dihydroxy-1,4-benzoxazin-3-one (DIBOA) and 2,4-dihydroxy-7- methoxy-1,4-benzoxazin-3-one (DIMBOA), are key defense compounds present in major agricultural crops such as maize and wheat. Their biosynthesis involves nine enzymes thought to form a linear pathway leading to the storage of DI(M)BOA as glucoside conjugates. Seven of the genes (Bx1-Bx6 and Bx8) form a cluster at the tip of the short arm of maize chromosome 4 that includes four P450 genes (Bx2-5 ...[more]

PMID: 22577841

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Project description:Chloridoideae is one of the largest subfamilies of Poaceae, containing many species of great economic and ecological value; however, phylogenetic relationships among the subtribes and genera of Cynodonteae are controversial. In the present study, we combined 111 plastomes representing all five tribes, including 25 newly sequenced plastomes that are mostly from Cynodonteae. Phylogenetic analyses supported the five monophyletic tribes of Chloridoideae, including Centropodieae, Triraphideae, Eragrostideae, Zoysieae and Cynodonteae. Simultaneously, nine monophyletic lineages were revealed in Cynodonteae: supersubtribe Boutelouodinae, subtribes Tripogoninae, Aeluropodinae, Eleusininae, Dactylocteniinae, supersubtribe Gouiniodinae, Cleistogenes and Orinus, and subtribe Triodiinae. Within the tribe of Cynodonteae, the basal lineage is supersubtribe Boutelouodinae and Tripogoninae is sister to the remaining lineages. The clade formed of Aeluropodinae and Eleusininae is sister to the clade composed of Dactylocteniinae, supersubtribe Gouiniodinae, Cleistogenes and Orinus, and subtribe Triodiinae. The clade comprising Dactylocteniinae and supersubtribe Gouiniodinae is sister to the clade comprising Cleistogenes, Orinus, and Triodiinae. Acrachne is a genus within Eleusininae but not within Dactylocteniinae. Molecular evidence determined that Diplachne is not clustered with Leptochloa, which indicated that Diplachne should not be combined into Leptochloa. Cleistogenes is sister to a clade composed of Orinus and Triodia, whereas the recently proposed subtribe Orininae was not supported. Cynodonteae was estimated to have experienced rapid divergence within a short period, which could be a major obstacle in resolving its phylogenetic relationships. Ancestral state reconstructions of morphological characters showed that the most recent common ancestor (MRCA) of Chloridoideae has a panicle, multiple florets in each spikelet, the peaked type of stomatal subsidiary cells, and a saddle-shaped phytoliths, while the ancestral morphological characters of Cynodonteae are the panicle, peaked type of stomatal subsidiary cells, sharp-cap cell typed and equal-base-cell microhair, and square-shaped phytoliths. Overall, plastome phylogenomics provides new insights into the phylogenetic relationships and morphological character evolution of Chloridoideae.

Dataset Information

Phylogenomics of the benzoxazinoid biosynthetic pathway of Poaceae: gene duplications and origin of the Bx cluster.

Publications

Phylogenomics of the benzoxazinoid biosynthetic pathway of Poaceae: gene duplications and origin of the Bx cluster.

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