Stem parasitic plant Cuscuta australis (dodder) transfers herbivory-induced signals among plants

Abstract

spp. (i.e., dodders) are stem parasites that naturally graft to their host plants to extract water and nutrients; multiple adjacent hosts are often parasitized by one or more plants simultaneously, forming connected plant clusters. Metabolites, proteins, and mRNAs are known to be transferred from hosts to, and bridges even facilitate host-to-host virus movement. Whether bridges transmit ecologically meaningful signals remains unknown. Here we show that, when host plants are connected by bridges, systemic herbivory signals are transmitted from attacked plants to unattacked plants, as revealed by the large transcriptomic changes in the attacked local leaves, undamaged systemic leaves of the attacked plants, and leaves of unattacked but connected hosts. The interplant signaling is largely dependent on the jasmonic acid pathway of the damaged local plants, and can be found among conspecific or heterospecific hosts of different families. Importantly, herbivore attack of one host plant elevates defensive metabolites in the other systemic bridge-connected hosts, resulting in enhanced resistance against insects even in several consecutively -connected host plants over long distances (> 100 cm). By facilitating plant-to-plant signaling, provides an information-based means of countering the resource-based fitness costs to their hosts.

Aphid (Myzus persicae) feeding on the parasitic plant dodder (Cuscuta australis) activates defense responses in both the parasite and soybean host

“…Feeding of leafworm larvae on soybean hosts led to transcriptomic changes in C. australis (Hettenhausen et al ., ). Thus, we investigated whether leafworms or aphids feeding on soybean plants altered the resistance of C. australis to GPAs.…”

“…Previously, it was found that when two soybean hosts were simultaneously parasitized by the same C. australis plants, leafworms feeding on the leaves of one soybean host resulted in 904, 655 and 566 differentially expressed genes (DEGs) in the local leaves, systemic leaves of the insect‐attacked plant, and the leaves of the systemic plant; however, only 140 DEGs were identified in C. australis , most of which are related to primary metabolism (Hettenhausen et al ., ). Congruent with such a small number of DEGs, in the present study our bioassay indicated that leafworm feeding on soybean leaves did not change the resistance of C. australis to subsequent GPA infestation (Fig.…”

“…). Recently, we found that when a C. australis connects two hosts of different families, such as Arabidopsis (Brassicaceae) and tobacco ( Nicotiana tabacum , Solanaceae) or soybean (Fabaceae) and wild tomato ( Solanum pennellii , Solanaceae), caterpillar feeding on one host strongly induced transcriptional changes in the systemic untreated host plants, indicating that chewing insect feeding‐induced systemic signals also are well conserved (Hettenhausen et al ., ). Much research is still needed to reveal the nature of the aphid feeding‐induced mobile signals and whether these signal molecules have anything in common with the wounding‐ or caterpillar feeding‐induced ones.…”

“…Herbivory by the root‐feeding lined click beetle Agriotes lineatus (Elateridae, Coleoptera) led to an increase of terpenoid levels in roots as well as in leaves of cotton ( Gossypium herbaceum ), and the leaves exhibited highly increased resistance to beet armyworm (Bezemer et al ., ). Previously, it was found that C. australis haustorial connections transmitted inter‐plant systemic signals between different hosts, such as soybean plants, and it was found that these systemic signals also enhanced host resistance to leafworms (Hettenhausen et al ., ). Here, we show that GPA feeding on C. australis also positively affects the resistance of the soybean hosts to subsequent infestation from leafworms or aphids, likely through systemic signaling (Fig.…”

“…Certain host primary and secondary metabolites, such as sucrose, amino acids and glucosinolates (defensive metabolites in Brassicaceae), also can be translocated from hosts to Cuscuta (Birschwilks et al ., ; Smith et al ., ). Recently, it was found that when Cuscuta plants simultaneously parasitize multiple hosts and a host is attacked by caterpillars, Cuscuta can transmit herbivory‐induced systemic signals to the other host plants and activate defense‐related responses (Hettenhausen et al ., ). All of these lines of evidence demonstrate that Cuscuta and its hosts may extensively exchange molecules, including those having signaling functions.…”