Independent evolution of ancestral and novel defenses in a genus of toxic plants (Erysimum, Brassicaceae)

Abstract

Phytochemical diversity is thought to result from coevolutionary cycles as specialization in herbivores imposes diversifying selection on plant chemical defenses. Plants in the speciose genus Erysimum (Brassicaceae) produce both ancestral glucosinolates and evolutionarily novel cardenolides as defenses. Here we test macroevolutionary hypotheses on co-expression, co-regulation, and diversification of these potentially redundant defenses across this genus. We sequenced and assembled the genome of E. cheiranthoides and foliar transcriptomes of 47 additional Erysimum species to construct a phylogeny from 9868 orthologous genes, revealing several geographic clades but also high levels of gene discordance. Concentrations, inducibility, and diversity of the two defenses varied independently among species, with no evidence for trade-offs. Closely related, geographically co-occurring species shared similar cardenolide traits, but not glucosinolate traits, likely as a result of specific selective pressures acting on each defense. Ancestral and novel chemical defenses in Erysimum thus appear to provide complementary rather than redundant functions.

Less Is More: A Mutation in the Chemical Defense Pathway ofErysimum cheiranthoides(Brassicaceae) Reduces Total Cardenolide Abundance but Increases Resistance to Insect Herbivores

“…This observation is consistent with a survey of 28 Erysimum species, where despite a vast diversity in cardenolide compounds, the total cardenolide HPLC-MS peak area was strongly correlated with Na + /K + -ATPase inhibition (r = 0.95, p<0.001; Züst et al 2020). The shift in cardenolide profile of the 454 mutant line also resulted in a more even cardenolide distribution ( Fig.…”

“…All experiments were conducted with the genomesequenced E. cheiranthoides var. Elbtalaue (Züst et al 2020 and were hatched on artificial diet (Southland Products, http://www.southlandproducts.net) in an incubator at 28 °C. A P. rapae colony, which was started with approximately 30 adults that were collected on the Cornell University campus in August, 2019, was maintained on Brassica oleracea L (Brassicaceae) cv.…”

“…Erysimum cheiranthoides L (Brassicaceae; wormseed wallflower), a widely distributed annual species, accumulates not only indole and aliphatic glucosinolates, but also cardenolides, steroid-derived specialized metabolites that function as inhibitors of essential Na + /K + -ATPases in animal cells (Züst et al 2020). This additional set of defensive compounds provides enhanced protection against crucifer-specialist herbivores that can tolerate or detoxify glucosinolates, including the glucosinolate-tolerant P. rapae (Dimock et al 1991;Renwick et al 1989;Sachdev-Gupta et al 1993;Sachdev-Gupta et al 1990).…”

“…Like glucosinolates, for which more than 120 different compounds have been identified across the Brassicaceae (Fahey et al 2001), cardenolides are a large group of chemically and functionally similar plant defensive metabolites. A recent analysis identified a total of 95 different cardenolide structures in 48 species of the Erysimum, the only cardenolide-producing genus within the Brassicaceae (Züst et al 2018;Züst et al 2020). This vast diversity is primarily generated by modifications to the core steroid structure of the molecules (the genin), and by glycosylation of the genin with various sugar moieties to form linear glycoside 'tails'.…”

“…This vast diversity is primarily generated by modifications to the core steroid structure of the molecules (the genin), and by glycosylation of the genin with various sugar moieties to form linear glycoside 'tails'. In E. cheiranthoides, the first Erysimum species to have its genome sequenced (Züst et al 2020), the most abundant cardenolides are glycosides of the three genins digitoxigenin, cannogenol, and strophanthidin ( Fig. 1).…”