Differential defensive and nutritional traits among cultivated tomato and its wild relatives shape their interactions with a specialist herbivore

Abstract

Cultivated tomato presented lower constitutive volatiles, reduced morphological and chemical defenses, and increased leaf nutritional quality that affect its resistance against the specialist herbivore Tuta absoluta compared to its wild relatives. Plant domestication process has selected desirable agronomic attributes that can both intentionally and unintentionally compromise other important traits, such as plant defense and nutritional value. However, the effect of domestication on defensive and nutritional traits of plant organs not exposed to selection and the consequent interactions with specialist herbivores are only partly known. Here, we hypothesized that the modern cultivated tomato has reduced levels of constitutive defense and increased levels of nutritional value compared with its wild relatives, and such differences affect the preference and performance of the South American tomato pinworm, Tuta absoluta-an insect pest that co-evolved with tomato. To test this hypothesis, we compared plant volatile emissions, leaf defensive (glandular and non-glandular trichome density, and total phenolic content), and nutritional traits (nitrogen content) among the cultivated tomato Solanum lycopersicum and its wild relatives S. pennellii and S. habrochaites. We also determined the attraction and ovipositional preference of female moths and larval performance on cultivated and wild tomatoes. Volatile emissions were qualitatively and quantitatively different among the cultivated and wild species. Glandular trichomes density and total phenolics were lower in S. lycopersicum. In contrast, this species had a greater non-glandular trichome density and leaf nitrogen content. Female moths were more attracted and consistently laid more eggs on the cultivated S. lycopersicum. Larvae fed on S. lycopersicum leaves had a better performance reaching shorter larval developmental times and increasing the pupal weight compared to those fed on wild tomatoes. Overall, our study documents that agronomic selection for increased yields has altered the defensive and nutritional traits in tomato plants, affecting their resistance to T. absoluta.

Keywords: Agronomic selection; Leaf nitrogen; Phenolics; Plant resistance; Plant volatiles; Trichomes; Tuta absoluta.