Plant biosynthetic gene clusters in the context of metabolic evolution

Smit, Samuel Jacobus; Lichman, Benjamin R.

doi:10.1039/d2np00005a

Cited by 42 publications

(24 citation statements)

References 153 publications

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“…Chromatin interaction maps revealed 3-D clustering of a subset of MIA pathway genes, some exhibiting organ-level specificity and interactions via chromatin loops, suggestive that TADs, in addition to physical colocalization, can be used to identify genes involved in specialized metabolism. The detection of TADs as well as chromatin loops of physically clustered genes is consistent with the co-regulation hypothesis on the origins of biosynthetic pathway gene clustering as the 3-D chromatin interactions serve key roles in gene regulation 57 . Application of techniques to probe chromatin accessibility such as Assay for Transposase-Accessible Chromatin coupled to high throughput sequencing will reveal cis-regulatory sequences including proximal transcription factor binding sites and distal enhancers.…”

Section: Discussionsupporting

confidence: 85%

Single-cell multi-omics enabled discovery of alkaloid biosynthetic pathway genes in the medical plant Catharanthus roseus

Wood

et al. 2022

Preprint

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Advances in omics technologies now permit generation of highly contiguous genome assemblies, detection of transcripts and metabolites at the level of single cells, and high-resolution determination of gene regulatory features including 3-dimensional chromatin interactions. Using a complementary, multi-omics approach, we interrogated the monoterpene indole alkaloid (MIA) biosynthetic pathway in Catharanthus roseus, a source of leading anti-cancer drugs. We identified not only new clusters of genes involved in MIA biosynthesis on the eight C. roseus chromosomes but also rampant gene duplication including paralogs of MIA pathway genes. Clustering was not limited to the linear genome and through chromatin interaction data, MIA pathway genes were shown to be present within the same topologically associated domain, permitting identification of a secologanin transporter. Single cell RNA-sequencing revealed exquisite and sequential cell-type specific partitioning of the leaf MIA biosynthetic pathway that, when coupled with a newly developed single cell metabolomics approach, permitted identification of a reductase that yields the bis-indole alkaloid anhydrovinblastine. Last, we revealed cell-type specific expression in the root MIA pathway that is conferred in part by neo- and sub-functionalization of paralogous MIA pathway genes. This study highlights how a suite of omic approaches, including single cell gene expression and metabolomics, can efficiently link sequence with function in complex, specialized metabolic pathways of plants.

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Section: Discussionsupporting

confidence: 85%

Single-cell multi-omics enabled discovery of alkaloid biosynthetic pathway genes in the medical plant Catharanthus roseus

Wood

et al. 2022

Preprint

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“…The organization of genes involved in specialized plant diterpenoid metabolism, including class I & II diTPSs and cytochrome P450s, in the form of biosynthetic gene clusters (BGCs) has been frequently reported (Polturak et al, 2022; Smit and Lichman, 2022; Zhan et al, 2022). In the region of the genome of S. barbata where the genes encoding CPS, MS and KLS/IKLS are located, there are also 8 genes encoding cytochromes P450 (CYP), most of them annotated as ferruginol synthase (FS).…”

Section: Resultsmentioning

confidence: 99%

“…Consequently, the phylogenomic data from the genes encoding KLS activity support the polyphyletic origin of clerodane biosynthesis in the family Lamiaceae. (Polturak et al, 2022;Smit and Lichman, 2022;Zhan et al, 2022). In the region of the genome of S. barbata where the genes encoding CPS, MS and KLS/IKLS are located, there are also 8 genes encoding cytochromes P450 (CYP), most of them annotated as ferruginol synthase (FS).…”

Section: Mussini)mentioning

confidence: 99%

The genomes of medicinal skullcaps reveal the polyphyletic origins of clerodane diterpene biosynthesis in the family Lamiaceae

Lin

et al. 2022

Preprint

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The presence of anticancer clerodane diterpenoids is a chemotaxonomic marker for the traditional Chinese medicinal plant Scutellaria barbata, although the molecular mechanisms behind clerodane biosynthesis are unknown. Here, we report a high-quality assembly of the 414.98 Mb genome of S. barbata into thirteen pseudochromosomes. Using phylogenomic and biochemical data, we mapped the plastidial metabolism of kaurene (gibberellins), abietane and clerodane diterpenes in three species of the family Lamiaceae (Scutellaria barbata, Scutellaria baicalensis and Salvia splendens), facilitating the identification of genes involved in the biosynthesis of the clerodanes, kolavenol and isokolavenol. We show that clerodane biosynthesis evolved through recruitment and neofunctionalization of genes from gibberellin and abietane metabolism. Despite the assumed monophyletic origin of clerodane biosynthesis which is widespread in species of the Lamiaceae, our data show distinct evolutionary lineages and suggest polyphyletic origins of clerodane biosynthesis in the family Lamiaceae. Our study not only provides significant insights into the evolution of clerodane biosynthetic pathways in the mint family, Lamiaceae, but also will facilitate the elucidation of anticancer clerodanes biosynthesis and future metabolic engineering efforts to increase the production of these high-value chemicals.

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“…Gene duplication, neo‐functionalization and translocation have been considered as the primary routes to BGC assembling (Nützmann et al., 2018). The origination of MABGC has been extensively studied and discussed, particularly after the discovery of MABGCs in E. crus‐galli and bryophyte C. plumiforme (Guo et al., 2017; Kitaoka et al., 2021; Mao et al., 2020; Miyamoto et al., 2016; Peters, 2020; Smit & Lichman, 2022; Zhang & Peters, 2020). MABGC in bryophyte C. plumiforme was evolved independently and convergently (Mao et al., 2020) and it was speculated that the rice MABGC emerged within Oryza , first by the addition of CYP99A2/3 to the syntenic locus, followed by recruitment of CPS4 , KSL4 , and MAS1/2 (Miyamoto et al., 2016).…”

Section: Discussionmentioning

confidence: 99%

“…MABGC in bryophyte C. plumiforme was evolved independently and convergently (Mao et al., 2020) and it was speculated that the rice MABGC emerged within Oryza , first by the addition of CYP99A2/3 to the syntenic locus, followed by recruitment of CPS4 , KSL4 , and MAS1/2 (Miyamoto et al., 2016). MABGC in Echinochloa was considered to be transferred from Oryza presumably through hybridization and introgression (Peters, 2020; Smit & Lichman, 2022; Zhang & Peters, 2020). Our results appear not to support the introgression‐origin hypothesis for the Echinochloa MABGC.…”

Section: Discussionmentioning

confidence: 99%

Lateral transfers lead to the birth of momilactone biosynthetic gene clusters in grass

Akashi

et al. 2022

The Plant Journal

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SUMMARY Momilactone A, an important plant labdane‐related diterpenoid, functions as a phytoalexin against pathogens and an allelochemical against neighboring plants. The genes involved in the biosynthesis of momilactone A are found in clusters, i.e., momilactone A biosynthetic gene clusters (MABGCs), in the rice and barnyardgrass genomes. In addition, we know little about the origin and evolution of MABGCs. Here, we integrated results from comprehensive phylogeny and comparative genomic analyses of the core genes of MABGC‐like clusters and MABGCs in 40 monocot plant genomes, providing convincing evidence for the birth and evolution of MABGCs in grass species. The MABGCs found in the PACMAD clade of the core grass lineage (including Panicoideae and Chloridoideae) originated from a MABGC‐like cluster in Triticeae (BOP clade) via lateral gene transfer (LGT) and followed by recruitment of MAS1/2 and CYP76L1 genes. The MABGCs in Oryzoideae originated from PACMAD through another LGT event and lost CYP76L1 afterwards. The Oryza MABGC and another Oryza diterpenoid cluster c2BGC are two distinct clusters, with the latter originating from gene duplication and relocation within Oryzoideae. Further comparison of the expression patterns of the MABGC genes between rice and barnyardgrass in response to pathogen infection and allelopathy provides novel insights into the functional innovation of MABGCs in plants. Our results demonstrate LGT‐mediated origination of MABGCs in grass and shed lights into the evolutionary innovation and optimization of plant biosynthetic pathways.

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Plant biosynthetic gene clusters in the context of metabolic evolution

Abstract: A significant subset of plant specialised metabolism genes are arranged in biosynthetic gene clusters. Here, we review these clusters and discuss their possible roles within the context of genome dynamics and metabolic evolution.

Cited by 42 publications

References 153 publications

Single-cell multi-omics enabled discovery of alkaloid biosynthetic pathway genes in the medical plant Catharanthus roseus

Single-cell multi-omics enabled discovery of alkaloid biosynthetic pathway genes in the medical plant Catharanthus roseus

The genomes of medicinal skullcaps reveal the polyphyletic origins of clerodane diterpene biosynthesis in the family Lamiaceae

Lateral transfers lead to the birth of momilactone biosynthetic gene clusters in grass

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