Phytochemistry reflects different evolutionary history in traditional classes versus specialized structural motifs

• Published in: Scientific reports Vol. 11; no. 1; p. 17247
• Main Authors: Uckele, Kathryn A., Jahner, Joshua P., Tepe, Eric J., Richards, Lora A., Dyer, Lee A., Ochsenrider, Kaitlin M., Philbin, Casey S., Kato, Massuo J., Yamaguchi, Lydia F., Forister, Matthew L., Smilanich, Angela M., Dodson, Craig D., Jeffrey, Christopher S., Parchman, Thomas L.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 26.08.2021; Nature Publishing Group; Nature Portfolio
• Subjects: 631/181/757; 631/92/604; DNA sequencing; Evolution; Flavonoids; Humanities and Social Sciences; Hypotheses; Lability; Metabolites; multidisciplinary; NMR; Nuclear magnetic resonance; Phenols; Phylogenetics; Phylogeny; Phytochemicals; Science; Science (multidisciplinary)
• ISSN: 2045-2322; 2045-2322
• DOI: 10.1038/s41598-021-96431-3

Foundational hypotheses addressing plant–insect codiversification and plant defense theory typically assume a macroevolutionary pattern whereby closely related plants have similar chemical profiles. However, numerous studies have documented variation in the degree of phytochemical trait lability, raising the possibility that phytochemical evolution is more nuanced than initially assumed. We utilize proton nuclear magnetic resonance ( 1 H NMR) data, chemical classification, and double digest restriction-site associated DNA sequencing (ddRADseq) to resolve evolutionary relationships and characterize the evolution of secondary chemistry in the Neotropical plant clade Radula ( Piper ; Piperaceae). Sequencing data substantially improved phylogenetic resolution relative to past studies, and spectroscopic characterization revealed the presence of 35 metabolite classes. Metabolite classes displayed phylogenetic signal, whereas the crude 1 H NMR spectra featured little evidence of phylogenetic signal in multivariate tests of chemical resonances. Evolutionary correlations were detected in two pairs of compound classes (flavonoids with chalcones; p -alkenyl phenols with kavalactones), where the gain or loss of a class was dependent on the other’s state. Overall, the evolution of secondary chemistry in Radula is characterized by strong phylogenetic signal of traditional compound classes and weak phylogenetic signal of specialized chemical motifs, consistent with both classic evolutionary hypotheses and recent examinations of phytochemical evolution in young lineages.