Convergent evolution of caffeine in plants by co-option of exapted ancestral enzymes

Huang, Ruiqi; O’Donnell, Andrew J.; Barboline, Jessica J; Barkman, Todd J.

doi:10.1073/pnas.1602575113

Cited by 101 publications

(159 citation statements)

References 62 publications

(58 reference statements)

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“…The connection between apparent genomic homoplasy arising from ILS and apparent phenotypic homoplasy is probably strongest for traits with a simple genetic architecture (18), such as those involving the function or regulation of a single enzyme (21,68). In plants, enzymes in biosynthetic pathways for floral pigments or defensive compounds are good candidates (69,70). Notably, the taxonomic distribution of alkaloids, triterpenes, and sterols have played a role in the systematics of Pachycereeae (30).…”

Section: Resultsmentioning

confidence: 99%

Extensive gene tree discordance and hemiplasy shaped the genomes of North American columnar cacti

Copetti

Búrquez

Bustamante

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

108

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Few clades of plants have proven as difficult to classify as cacti. One explanation may be an unusually high level of convergent and parallel evolution (homoplasy). To evaluate support for this phylogenetic hypothesis at the molecular level, we sequenced the genomes of four cacti in the especially problematic tribe Pachycereeae, which contains most of the large columnar cacti of Mexico and adjacent areas, including the iconic saguaro cactus (Carnegiea gigantea) of the Sonoran Desert. We assembled a high-coverage draft genome for saguaro and lower coverage genomes for three other genera of tribe Pachycereeae (Pachycereus,Lophocereus, andStenocereus) and a more distant outgroup cactus,Pereskia. We used these to construct 4,436 orthologous gene alignments. Species tree inference consistently returned the same phylogeny, but gene tree discordance was high: 37% of gene trees having at least 90% bootstrap support conflicted with the species tree. Evidently, discordance is a product of long generation times and moderately large effective population sizes, leading to extensive incomplete lineage sorting (ILS). In the best supported gene trees, 58% of apparent homoplasy at amino sites in the species tree is due to gene tree-species tree discordance rather than parallel substitutions in the gene trees themselves, a phenomenon termed “hemiplasy.” The high rate of genomic hemiplasy may contribute to apparent parallelisms in phenotypic traits, which could confound understanding of species relationships and character evolution in cacti.

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Section: Resultsmentioning

confidence: 99%

Extensive gene tree discordance and hemiplasy shaped the genomes of North American columnar cacti

Copetti

Búrquez

Bustamante

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

108

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“…An analysis of the wild tobacco genomes of Nicotiana attenuata and Nicotiana obtusifolia allowed the direct association of genome evolution with the assembly of the nicotine biosynthesis pathway, showing that gene duplication and insertion of transposable elements were essential components of the establishment of this pathway (Xu et al, 2017). Caffeine, by contrast, surprisingly arose from two previously unknown biochemical pathways in coffee, citrus, chocolate, guaraná , and tea plants (Huang et al, 2016). Amazingly this occurred via the resurrection of extinct enzymes that ancient plants once possessed, and the novel pathways evolved rapidly because the ancestral enzymes were co-opted from previous biochemical roles to those of caffeine biosynthesis (Huang et al, 2016).…”

Section: Convergent and Divergent Evolution Of Metabolism: The Combinmentioning

confidence: 99%

The Structure and Function of Major Plant Metabolite Modifications

et al. 2019

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Plants produce a myriad of structurally and functionally diverse metabolites that play many different roles in plant growth and development and in plant response to continually changing environmental conditions as well as abiotic and biotic stresses. This metabolic diversity is, to a large extent, due to chemical modification of the basic skeletons of metabolites. Here, we review the major known plant metabolite modifications and summarize the progress that has been achieved and the challenges we are facing in the field. We focus on discussing both technical and functional aspects in studying the influences that various modifications have on biosynthesis, degradation, transport, and storage of metabolites, as well as their bioactivity and toxicity. Finally, we discuss some emerging insights into the evolution of metabolic pathways and metabolite functionality.

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“…Unfortunately, this information is hard to obtain for many taxa because there are still a large number of plants whose metabolomic composition has never been investigated. Recent studies revealed that convergent evolution can lead to identical specialized metabolites being biosynthesized through different unrelated pathways (Huang et al ., ; Zhao et al ., ). Therefore, researchers should consider the risk of drawing incorrect conclusions when they apply specialized metabolic pathways established in different plants.…”

Section: Resultsmentioning

confidence: 99%

Comprehensive mass spectrometry‐guided phenotyping of plant specialized metabolites reveals metabolic diversity in the cosmopolitan plant family Rhamnaceae

et al. 2019

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Plants produce a myriad of specialized metabolites to overcome their sessile habit and combat biotic as well as abiotic stresses. Evolution has shaped the diversity of specialized metabolites, which then drives many other aspects of plant biodiversity. However, until recently, large-scale studies investigating the diversity of specialized metabolites in an evolutionary context have been limited by the impossibility of identifying chemical structures of hundreds to thousands of compounds in a time-feasible manner. Here we introduce a workflow for large-scale, semi-automated annotation of specialized metabolites and apply it to over 1000 metabolites of the cosmopolitan plant family Rhamnaceae. We enhance the putative annotation coverage dramatically, from 2.5% based on spectral library matches alone to 42.6% of total MS/MS molecular features, extending annotations from well-known plant compound classes into dark plant metabolomics. To gain insights into substructural diversity within this plant family, we also extract patterns of co-occurring fragments and neutral losses, so-called Mass2Motifs, from the dataset; for example, only the Ziziphoid clade developed the triterpenoid biosynthetic pathway, whereas the Rhamnoid clade predominantly developed diversity in flavonoid glycosides, including 7-O-methyltransferase activity. Our workflow provides the foundations for the automated, high-throughput chemical identification of massive metabolite spaces, and we expect it to revolutionize our understanding of plant chemoevolutionary mechanisms.

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Convergent evolution of caffeine in plants by co-option of exapted ancestral enzymes

Cited by 101 publications

References 62 publications

Extensive gene tree discordance and hemiplasy shaped the genomes of North American columnar cacti

Extensive gene tree discordance and hemiplasy shaped the genomes of North American columnar cacti

The Structure and Function of Major Plant Metabolite Modifications

Comprehensive mass spectrometry‐guided phenotyping of plant specialized metabolites reveals metabolic diversity in the cosmopolitan plant family Rhamnaceae

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