Comparative metabolomics of fruits and leaves in a hyperdiverse lineage suggests fruits are a key incubator of phytochemical diversification

Abstract

SummaryInteractions between plants and leaf herbivores have long been implicated as the major driver of plant secondary metabolite diversity. However, other plant-animal interactions, such as those between fruits and frugivores, may also be involved in phytochemical diversification.Using 12 species of Piper, we conducted untargeted metabolomics and molecular networking with extracts of fruits and leaves. We evaluated organ-specific secondary metabolite composition and compared multiple dimensions of phytochemical diversity across organs, including richness, structural complexity, and variability across samples at multiple scales within and across species.Plant organ identity significantly influenced secondary metabolite composition, both independent of and in interaction with species identity. Leaves and fruit shared a majority of compounds, but fruits contained more unique compounds and had higher total estimated chemical richness. While organ-level chemical richness and structural complexity varied substantially across species, fruit diversity exceeded leaf diversity in more species than the reverse. Furthermore, the variance in chemical composition across samples was higher for fruits than leaves. By documenting a broad pattern of high phytochemical diversity in fruits relative to leaves, this study lays groundwork for incorporating fruit into a comprehensive and integrative understanding of the ecological and evolutionary factors shaping secondary metabolite composition at the whole-plant level.

Diversity and Divergence: Evolution of defense chemistry in the tropical tree genusInga

“…S5). Second, it is possible that many compounds that are absent in leaves could be present in other tissues (70,71). Finally, because there are many more secondary metabolites than enzymes that produce them, it has been argued that a core set of enzymes with low substrate specificity is capable of producing a broad set of chemical structures (20,72).…”

Fruits, frugivores, and the evolution of phytochemical diversity

“…In sum, the existing data from P. reticulatum shows that fruits contain a higher diversity of secondary metabolites than leaves, and are particularly rich in amides (Whitehead et al 2013, Schneider et al 2021. Amides have multiple functional roles in fruits, affecting defense against fungal pathogens and insect seed predators (Whitehead and Bowers 2014) and the behavior and physiology of seed-dispersing bats (Baldwin andWhitehead 2015, Whitehead et al 2016).…”

“…Only one group of flavonoids show the opposite pattern, suggesting an evolutionary origin in leaves. Data are from Schneider et al (2021); refer to that study for further methodological details and interpretation. 11 of study systems.…”

“…Patterns were variable across species, but Piper reticulatum contained an estimated 588 total secondary metabolites across all tissue types. Many of these compounds (256 total) were shared across tissues, but at least 272 compounds spread across several classes were unique to fruits (found in fruit pulp or seeds but not in leaves), compared to only 60 that were unique to leaves (Schneider et al 2021, Fig. 4).…”

“…4). On average, samples of unripe fruit pulp, ripe fruit pulp, or seeds contained 23–34% higher chemical richness than leaves (Schneider et al 2021, Fig. 5).…”