Phylogenetic patterns suggest frequent multiple origins of secondary metabolites across the seed-plant 'tree of life'

Yongzeng Zhang; Tao Deng; Lu Sun; Jacob B Landis; Michael J Moore; Hengchang Wang; Yuehua Wang; Xiaojiang Hao; Jijun Chen; Shenghong Li; Maonian Xu; Pema-Tenzin Puno; Peter H Raven; Hang Sun

doi:10.1093/nsr/nwaa105

Phylogenetic patterns suggest frequent multiple origins of secondary metabolites across the seed-plant 'tree of life'

Natl Sci Rev. 2020 May 21;8(4):nwaa105. doi: 10.1093/nsr/nwaa105. eCollection 2021 Apr.

Authors

Yongzeng Zhang¹, Tao Deng¹, Lu Sun¹, Jacob B Landis², Michael J Moore³, Hengchang Wang⁴, Yuehua Wang⁵, Xiaojiang Hao⁶, Jijun Chen⁶, Shenghong Li⁶, Maonian Xu⁷, Pema-Tenzin Puno⁶, Peter H Raven⁸, Hang Sun¹

Affiliations

¹ CAS Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China.
² Department of Botany and Plant Sciences, University of California Riverside, Riverside, CA 92521, USA.
³ Department of Biology, Oberlin College, Oberlin, OH 44074, USA.
⁴ CAS Key Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Chinese Academy of Sciences, Wuhan 430074, China.
⁵ School of Life Science, Yunnan University, Kunming 650091, China.
⁶ State Key Laboratory of Phytochemistry and Plant Resources in West China, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China.
⁷ Pharmaceutical Sciences, University of Iceland, 107 Reykjavik, Iceland.
⁸ Missouri Botanical Garden, St. Louis, MO 63110, USA.

Abstract

To evaluate the phylogenetic patterns of the distribution and evolution of plant secondary metabolites (PSMs), we selected 8 classes of PSMs and mapped them onto an updated phylogenetic tree including 437 families of seed plants. A significant phylogenetic signal was detected in 17 of the 18 tested seed-plant clades for at least 1 of the 8 PSM classes using the D statistic. The phylogenetic signal, nevertheless, indicated weak clustering of PSMs compared to a random distribution across all seed plants. The observed signal suggests strong diversifying selection during seed-plant evolution and/or relatively weak evolutionary constraints on the evolution of PSMs. In the survey of the current phylogenetic distributions of PSMs, we found that multiple origins of PSM biosynthesis due to external selective forces for diverse genetic pathways may have played important roles. In contrast, a single origin of PSMs seems rather uncommon. The distribution patterns for PSMs observed in this study may also be useful in the search for natural compounds for medicinal purposes.

Keywords: bioprospecting; co-diversification; evolution; phylogenetic signal; phylogenetic tree; secondary metabolites; seed plants.