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The coffee genome provides insight into the convergent evolution of caffeine biosynthesis

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Science  05 Sep 2014:
Vol. 345, Issue 6201, pp. 1181-1184
DOI: 10.1126/science.1255274
  1. Fig. 1 Structure of the C. canephora genome.

    (A) Alignment of the pseudochromosome 1 sequence with the genetic map of C. canephora and genomic overview. Correspondences between the genetic linkage map and the DNA pseudomolecule are shown at left (oriented and nonoriented scaffolds are indicated in blue and green, respectively; gray lines denote consistent data; orange lines indicate markers with an approximate genetic location). The relative proportions (percentage of nucleotides) in sliding windows (1-Mb size, 500-kb step) of transposable elements (Copia in red, Gypsy in green) and genes (exons in blue, introns in dark blue) are shown at right. (B) Coffee chromosomal blocks descending from the seven ancestral core eudicot chromosomes. The three paralogous descendants of the seven ancestral chromosomes are shown in shared colors but different textures. (C) Comparison of three grapevine chromosomes (descendants of the prehexaploidization core eudicot chromosome) mapped to a single coffee chromosome and three regions in the tomato genome. (D) Phylogeny and genome duplication history of core eudicots. Arrowheads indicate tetraploidization (blue) or hexaploidization (green) events. Red lines trace lineages of six species that have not undergone further polyploidization. Bar graphs and colors reflect gene-order differences (table S17) between each of the six species (column labels) and the entire set, showing the gene order conservatism of coffee, especially among asterids, and of peach and cacao among rosids.

  2. Fig. 2 Evolution of caffeine biosynthesis.

    (A) The principal caffeine biosynthetic pathway. Three methylation steps are necessary to produce caffeine from xanthosine, involving the successive action of three NMTs: xanthosine methyltransferase (XMT), theobromine synthase [7-methylxanthine methyltransferase (MXMT)], and caffeine synthase [3,7-dimethylxanthine methyltransferase (DXMT)]. SAM, S-adenosylmethionine; SAH, S-adenosylhomocysteine. (B) Evolutionary position of caffeine-producing plants with respect to other eudicots (phylogeny adapted from www.mobot.org/MOBOT/research/APweb/). (C) ML phylogeny of coffee, tea, and cacao NMTs. Bootstrap support values (percentages) from 1000 replicates are shown next to relevant clades. Branch lengths are proportional to expected numbers of nucleotide substitutions per site. Colors identify genes assignable to the genomic blocks denoted in (D). (D) (Left) A model summarizing the duplication history of coffee NMT genes, following the phylogeny in (C). Three distinct tandem gene arrays evolved in situ on chromosome 1 from nearby gene duplicates (bold squares). The red and green blocks, colored as in (C), translocated (to chromosome 9) or rearranged (to elsewhere on chromosome 1) from their ancestral locus (blue region), respectively. (Right) Gene orders on modern chromosomes. Translocation of the red block, containing the putative caffeine NMT metabolic cluster, left the phylogenetically derived CcDXMT gene behind. Similarly, CcNMT19 is a derived gene within its own NMT clade that remained in place following movement of the green block. Numbers at branches indicate relative times since major duplication events or diversification times of the tandem arrays, calculated from approximately neutral synonymous substitution rates. (E) Expression profiles (reads per kilobase per million reads mapped) of known Coffea canephora NMTs. The genes in the putative metabolic cluster (along with CcDXMT and CcMXMT) exhibit similar expression patterns, higher in perisperm than endosperm. Data are plotted as log2 values. DAP, days after pollination.

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