Exploring allopolyploidy-mediated innovations of gain-of-function defenses in a plant-insect arms race

Plants are champion synthetic chemists! They harness their remarkable metabolic capabilities to produce an extraordinarily large repertoire of structurally diverse metabolites. The overarching objective of our team is to elucidate the biosynthesis, ecological functions, and evolutionary trajectories of metabolic pathways that contribute to plant adaptation to the environment. In this presentation, I will focus on the mechanisms that drive the evolution of key specialized metabolism-based defensive innovations against herbivorous insects and how these shape the plants’ arms race with herbivorous insects which have evolved biochemical and behavioral counter-adaptations.

The Nicotiana genus, with approximately half of its species being allopolyploids, offers a compelling framework to more specifically explore the role of allopolyploidization as an evolutionary driver of these processes. A recent evolutionary metabolomics study from our group investigated chemodiversity innovations associated with allopolyploidization in this genus, highlighting N-acyl-nornicotines (NANNs) -- derived from the ancestral nicotine state of the genus -- as defense compounds strongly influenced by allopolyploidization events (Elser et al., Science Advances, 2023; DOI: 10.1126/sciadv.ade8984). Nicotine is well known as a potent defense metabolite; however, certain herbivores, notably the tobacco hornworm, have evolved tolerance—likely through mechanisms such as efficient nicotine excretion. 

Using the evolutionary trajectory of NANNs as a case study, I will illustrate how allopolyploidization in the Nicotiana section Repandae has led to tissue- and chemotype-specific shifts, turning trichome-based NANN production into a highly potent gain-of-function defense against specialized insects. In particular, I will present findings on the discovery of NANN biosynthetic genes, their evolutionary origins in the context of allopolyploidy, and their novel mode of action in circumventing nicotine tolerance.

Complete list of authors:
Emmanuel Gaquerel^1,2, David Elser¹, Aura Navarro-Quezada², Remigius Groening², Laurence Herrgott¹, Monika Kupke², Ludivine Malherbe¹

¹ Institut de Biologie Moléculaire des Plantes (IBMP) du CNRS, Université de Strasbourg | Team Evolution & Diversity of Plant Metabolism, France
² Centre for Organismal Studies, University of Heidelberg, Germany