Abstract
Functional gene clusters, containing two or more genes encoding different enzymes for the same pathway, are sometimes observed in plant genomes, most often when the genes specify the synthesis of specialized defensive metabolites. Here, we show that a cluster of genes in tomato (Solanum lycopersicum; Solanaceae) contains genes for terpene synthases (TPSs) that specify the synthesis of monoterpenes and diterpenes from cis-prenyl diphosphates, substrates that are synthesized by enzymes encoded by cis-prenyl transferase (CPT) genes also located within the same cluster. The monoterpene synthase genes in the cluster likely evolved from a diterpene synthase gene in the cluster by duplication and divergence. In the orthologous cluster in Solanum habrochaites, a new sesquiterpene synthase gene was created by a duplication event of a monoterpene synthase followed by a localized gene conversion event directed by a diterpene synthase gene. The TPS genes in the Solanum cluster encoding cis-prenyl diphosphate-utilizing enzymes are closely related to a tobacco (Nicotiana tabacum; Solanaceae) diterpene synthase encoding Z-abienol synthase (Nt-ABS). Nt-ABS uses the substrate copal-8-ol diphosphate, which is made from the all-trans geranylgeranyl diphosphate by copal-8-ol diphosphate synthase (Nt-CPS2). The Solanum gene cluster also contains an ortholog of Nt-CPS2, but it appears to encode a nonfunctional protein. Thus, the Solanum functional gene cluster evolved by duplication and divergence of TPS genes, together with alterations in substrate specificity to utilize cis-prenyl diphosphates and through the acquisition of CPT genes.
Highlights
Gene duplications provide the raw material for the evolution of genes with new functions by allowing selection to act on divergent sequences while maintaining the original function of the gene (Ohno, 1970)
While the released tomato genome sequence suggested that S. lycopersicum TPS18, TPS19, TPS20, TPS21, TPS41, and NERYL DIPHOSPHATE SYNTHASE1 (NDPS1) are present in the chromosome 8 cluster, the actual sequence assembly was poor, with many gaps and incomplete gene sequences
An apparently functional cytochrome P450 gene is situated between TPS21 and TPS20, and the cluster is flanked on one side by a gene for aldehyde oxidase and on the other side by a second cytochrome P450 gene that contains an insertion, followed by three alcohol acyl transferase genes, with the first having multiple deletions and mutations and the other two potentially functional (Figure 2; see Supplemental Figure 1 online)
Summary
Gene duplications provide the raw material for the evolution of genes with new functions by allowing selection to act on divergent sequences while maintaining the original function of the gene (Ohno, 1970). In a second wild tomato species, Solanum habrochaites accession LA1777, two homologous trichome-expressed genes on the same region of chromosome 8 were identified that encode proteins with different activities (Sallaud et al, 2009) One of these genes, the CPT gene CISFARNESYL DIPHOSPHATE SYNTHASE (zFPS), shows high identity to Sl-NDPS1 and encodes an enzyme that catalyzes the synthesis of the atypical TPS substrate 2Z,6Z-farnesyl diphosphate (Z,Z-FPP) (Figure 1A). Four additional TPS transcripts were identified, including those encoding a sesquiterpene synthase, ShZIS, which utilizes Z,Z-FPP to synthesize 7-epi-zingiberene, and three monoterpene synthases, Sh-PHS1, Sh-PIS, and Sh-LMS, which utilize NPP to synthesize b-phellandrene, a-pinene, and limonene, respectively (Figure 1B) Overall, these data suggest a diverse pattern of terpene biosynthesis in the trichomes of Solanum species. The combined data were used to determine the evolutionary trajectories of the genes in this cluster in Solanaceae and to further understand how functional clusters in specialized metabolism are formed and evolve over time
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