Abstract

BackgroundDodder (Cuscuta spp., Convolvulaceae) species are obligate leaf- and rootless parasites that totally depend on hosts to survive. Dodders naturally graft themselves to host stems to form vascular fusion, from which they obtain nutrients and water. In addition, dodders and their hosts also exchange various other molecules, including proteins, mRNAs, and small RNAs. It is very likely that vascular fusion also allows inter-plant translocation of systemic signals between dodders and host plants and these systemic signals may have profound impacts on the physiology of dodder and host plants. Herbivory is a common biotic stress for plants. When a dodder parasite is attacked by lepidopteran insects, how dodder responds to caterpillar feeding and whether there are inter-plant communications between the host plants and the parasites is still poorly understood.ResultsHere, wild-type (WT) tobacco and a tobacco line in which jasmonic acid (JA) biosynthesis was silenced (AOC-RNAi) were used as the hosts, and the responses of dodders and their host plants to herbivory by Spodoptera litura caterpillars on the dodders were investigated. It was found that after caterpillar attack, dodders grown on AOC-RNAi tobacco showed much a smaller number of differentially expressed genes, although the genotypes of the tobacco plants did not have an effect on the simulated S. litura feeding-induced JA accumulation in dodders. We further show that S. litura herbivory on dodder also led to large changes in transcriptome and defensive metabolites in the host tobacco, leading to enhanced resistance to S. litura, and the JA pathway of tobacco host is critical for these systemic responses.ConclusionsOur findings indicate that during caterpillar attack on dodder, the JA pathway of host plant is required for the proper transcriptomic responses of both dodder and host plants. This study highlights the importance of the host JA pathway in regulating the inter-plant systemic signaling between dodder and hosts.

Highlights

  • Dodder (Cuscuta spp., Convolvulaceae) species are obligate leaf- and rootless parasites that totally depend on hosts to survive

  • Host jasmonic acid (JA) signaling seems to be involved in host defense against the dodder parasite [25], we did not observe differential growth of dodder C. campestris on WT and allene oxide cyclase (AOC)-RNA interference (RNAi) tobacco (Additional file 1: Figure S2)

  • We found 162 differentially expressed genes (DEGs) in the dodders grown on WT tobacco following CLW herbivory and more than 90% of these DEGs (150) were up-regulated; in contrast, in dodders parasitizing AOCRNAi tobacco, only 56 DEGs were detected (Fig. 1b; Additional file 3: Table S2), and these were all upregulated (Fig. 1b)

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Summary

Introduction

Dodder (Cuscuta spp., Convolvulaceae) species are obligate leaf- and rootless parasites that totally depend on hosts to survive. When a dodder parasite is attacked by lepidopteran insects, how dodder responds to caterpillar feeding and whether there are inter-plant communications between the host plants and the parasites is still poorly understood. Almost all parts of plants (leaves, roots, stems, flowers, and seeds) can be attacked by insects. Chewing insects, such as certain beetles and caterpillars, rapidly remove and ingest plant tissues. Wounding inflicted by insect feeding is recognized by plants; specific defense responses are triggered by herbivore-associated elicitors, such as fatty-acid amino acid conjugates (FACs) in the oral secretions (OS) of lepidopteran larvae, and certain components in the salivary fluids of piercing-sucking insects [3, 4]. Ca2+, mitogen-activated protein kinase (MAPK), and phytohormone signaling are involved in the regulation of subsequent transcriptomic reconfigurations, leading to accumulation of defensive metabolites [5, 6]

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