Integrated metabolomic and transcriptomic analyses of the parasitic plant Cuscuta japonica Choisy on host and non-host plants

Abstract

Background: Cuscuta japonica Choisy (Japanese dodder) is a parasitic weed that damages many plants and affects agricultural production. The haustorium of C. japonica plays a key role during parasitism in host plants; in contrast, some non-host plants effectively inhibit its formation. However, the metabolic differences between normal dodder in host plants and dodder inhibition in non-host plants are largely unknown. Here, we utilized an integrative analysis of transcriptomes and metabolomes to compare the differential regulatory mechanisms between C. japonica interacting with the host plant Ficus microcarpa and the non-host plant Mangifera indica.

Results: After parasitization for 24 h and 72 h, the differentially abundant metabolites between these two treatments were enriched in pathways associated with α-linolenic acid metabolism, linoleic acid metabolism, phenylpropanoid biosynthesis, and pyrimidine metabolism. At the transcriptome level, the flavor biosynthesis pathway was significantly enriched at 24 h, whereas the plant-pathogen interaction, arginine and proline metabolism, and MARK signaling-plant pathways were significantly enriched at 72 h, based on the differentially expressed genes between these two treatments. Subsequent temporal analyses identified multiple genes and metabolites that showed different trends in dodder interactions between the host and non-host plants. In particular, the phenylpropanoid biosynthesis pathway showed significant differential regulation between C. japonica in host and non-host plants.

Conclusions: These results provide insights into the metabolic mechanisms of dodder-host interactions, which will facilitate future plant protection from C. japonica parasitism.

Keywords: Cuscuta japonica Choisy; Host plant; Metabolome; Non-host plant; Parasitism; Phenylpropanoid biosynthesis; Transcriptome.

Fig. 1

Cuscuta japonica planted on non-host Mangifera indica (A) and host Ficus microcarpa ‘Golden Leaves’ (B) including close-up of a parasitic vine entwining and cross section through an infection site. CC. japonica attached to non-host (left) and host (right) plants after 15 days

Fig. 2

Distribution of identified metabolite classes (A); principal component analysis of samples (B); and heatmap of differentially accumulated metabolites in each sample (C). MTD, dodders attached to the stems of non-host plant; HTD, dodders attached to the stems of host plant

Fig. 3

Number of differentially accumulated metabolites (A); pathway enrichment analysis for differentially abundant metabolites at 24 h (B); at 72 h (C). MTD, dodders attached to the stems of non-host plant; HTD, dodders attached to the stems of host plant

Fig. 4

Gene expression analysis. Correlation across samples according to gene expression profiles (A). Differentially expressed genes in host and non-host plants at 24 h after attachment (B), Differentially expressed genes in hosts compared with those in non-hosts at 72 h after attachment (C). MTD, dodders attached to the stems of non-host plant; HTD, dodders attached to the stems of host plant

Fig. 5

KEGG pathway enrichment analysis. DEGs generated by the comparison of HTD and MTD at 24 h (A). DEGs produced by HTD vs MTD at 72 h (B). We obtained permission to use the KEGG software from the Kanehisa laboratory. MTD, dodders attached to the stems of non-host plant; HTD, dodders attached to the stems of host plant; DEGs, differentially expressed genes

Fig. 6

KEGG pathway enrichment analysis for metabolites in trend profiles of the HTD (A) and MTD (B) groups. We obtained permission to use the KEGG software from the Kanehisa laboratory. MTD, dodders attached to the stems of non-host plant; HTD, dodders attached to the stems of host plant

Fig. 7

KEGG pathway enrichment analysis for genes in trend profiles of the HTD (A) and MTD (B) groups. We obtained permission to use the KEGG software from the Kanehisa laboratory. MTD, dodders attached to the stems of non-host plant; HTD, dodders attached to the stems of host plant

Fig. 8

DEGs presented in phenylpropanoid biosynthesis pathway (A). Heatmap for DEGs and DAMs in phenylpropanoid biosynthesis pathway (B). MTD, dodders attached to the stems of non-host plant; HTD, dodders attached to the stems of host plant; DEGs, differentially expressed genes; DAMS, differentially abundant metabolites