Parasitism by Cuscuta pentagona Attenuates Host Plant Defenses against Insect Herbivores

Abstract

Considerable research has examined plant responses to concurrent attack by herbivores and pathogens, but the effects of attack by parasitic plants, another important class of plant-feeding organisms, on plant defenses against other enemies has not been explored. We investigated how attack by the parasitic plant Cuscuta pentagona impacted tomato (Solanum lycopersicum) defenses against the chewing insect beet armyworm (Spodoptera exigua; BAW). In response to insect feeding, C. pentagona-infested (parasitized) tomato plants produced only one-third of the antiherbivore phytohormone jasmonic acid (JA) produced by unparasitized plants. Similarly, parasitized tomato, in contrast to unparasitized plants, failed to emit herbivore-induced volatiles after 3 d of BAW feeding. Although parasitism impaired antiherbivore defenses, BAW growth was slower on parasitized tomato leaves. Vines of C. pentagona did not translocate JA from BAW-infested plants: amounts of JA in parasite vines grown on caterpillar-fed and control plants were similar. Parasitized plants generally contained more salicylic acid (SA), which can inhibit JA in some systems. Parasitized mutant (NahG) tomato plants deficient in SA produced more JA in response to insect feeding than parasitized wild-type plants, further suggesting cross talk between the SA and JA defense signaling pathways. However, JA induction by BAW was still reduced in parasitized compared to unparasitized NahG, implying that other factors must be involved. We found that parasitized plants were capable of producing induced volatiles when experimentally treated with JA, indicating that resource depletion by the parasite does not fully explain the observed attenuation of volatile response to herbivore feeding. Collectively, these findings show that parasitic plants can have important consequences for host plant defense against herbivores.

Plant Interactions with Arthropod Herbivores: State of the Field

“…The phenomenon of signal cross talk in plant biology has gained increased attention as scientists seek to understand how plants respond to simultaneous attack by multiple herbivores and pathogens. A novel example of signal cross talk is described in an article by Runyon et al (2008), who examined how the parasitic plant Cuscuta pentagona affects induced defenses of tomato to insect attack.…”

Glucosinolates from Host Plants Influence Growth of the Parasitic Plant Cuscuta gronovii and Its Susceptibility to Aphid Feeding

“…Parasitic plants make their living by extracting resources from other plants and, therefore, share many of the same ecological challenges faced by other plantfeeding organisms, including the need to acquire appropriate hosts and overcome host defenses (Runyon et al, 2006(Runyon et al, , 2008(Runyon et al, , 2010Mescher et al, 2009;Smith et al, 2009). In the case of arthropod herbivores, many species are able not only to overcome the chemical defenses of their hosts but also to sequester plant toxins for use against their own natural enemies (Opitz and Mueller, 2009).…”

A holoparasitic plant severely reduces the vegetative and reproductive performance of its host plant in the Caatinga, a Brazilian seasonally dry forest

“…We emphasize that the parasitism of C. partita on Z. diphylla may act beyond the redirection of resources and the hormonal control of the host plant, as has been described for many interactions involving other species of parasitic plants (e.g., Knutson 1979;Puustinen & Salonen 1999;Pennings & Callaway 2002;Runyon et al 2008). In this sense, cell division processes during the development of vegetative and generative cells of pollen grains of Z. diphylla may also be affected by parasites.…”

“…Specifically, parasitic interactions associated with the establishment of haustoria may lead to changes in the photosynthetic parameters of host species, such as the average of CO 2 partial intracellular pressure and photosynthetic electron transport rates (e.g. Gomes & Fernandes 1994;Fernandes et al 1998;Runyon et al 2008;Prider et al 2009;Li et al 2012). Because of these changes, parasitized plants may exhibit a reduced number of leaves, branches, flowers and individual biomass, relative to non-parasitized plants, as may be the case for Z. diphylla in the Caatinga.…”

“…In addition to photosynthate reallocation, holoparasitic plants may stimulate the secretion of hormones by the host plant, directly inoculating the host structures with their own hormones or mRNA (Knutson 1979;Ihl et al 1984;Westwood et al 2010). In this sense, holoparasitic plants may negatively impact many metabolic and physiological aspects of their host plants, such as stomata opening, photosynthesis rate, transpiration, hormone secretion or water-use efficiency (Goldstein et al 1989;Fernandes et al 1998;Sala et al 2001;Runyon et al 2008;Prider et al 2009). …”