Transcriptomic and Metabolomic Reprogramming from Roots to Haustoria in the Parasitic Plant, Thesium chinense

Abstract

Most plants show remarkable developmental plasticity in the generation of diverse types of new organs upon external stimuli, allowing them to adapt to their environment. Haustorial formation in parasitic plants is an example of such developmental reprogramming, but its molecular mechanism is largely unknown. In this study, we performed field-omics using transcriptomics and metabolomics to profile the molecular switch occurring in haustorial formation of the root parasitic plant, Thesium chinense, collected from its natural habitat. RNA-sequencing with de novo assembly revealed that the transcripts of very long chain fatty acid (VLCFA) biosynthesis genes, auxin biosynthesis/signaling-related genes and lateral root developmental genes are highly abundant in the haustoria. Gene co-expression network analysis identified a network module linking VLCFAs and the auxin-responsive lateral root development pathway. GC-TOF-MS analysis consistently revealed a unique metabolome profile with many types of fatty acids in the T. chinense root system, including the accumulation of a 25-carbon long chain saturated fatty acid in the haustoria. Our field-omics data provide evidence supporting the hypothesis that the molecular developmental machinery used for lateral root formation in non-parasitic plants has been co-opted into the developmental reprogramming of haustorial formation in the linage of parasitic plants.

Host-parasite tissue adhesion by a secreted type of β-1,4-glucanase in the parasitic plant Phtheirospermum japonicum

“…3b ). Numerous genes were highly upregulated during parasitism or grafting, including some genes previously known to be associated with wound healing processes, such as auxin action, procambial activity, and vascular formation 19 , 26 , 27 (Fig. 3b, c ).…”

“…Involvement of cell wall modification in parasitism has been reported in various parasitic plant lineages 13 , 14 , 19 , 20 . This study identified a part of responsive genes for cell wall modification and performed functional analysis.…”

“…Similarly, transcriptome analysis of dodder revealed increased expression of genes encoding cell wall-modifying enzymes, such as pectin lyase, pectin methyl esterase, cellulase, and expansins, in the infective stages 14 . A transcriptome analysis of Thesium chinense , a parasitic Santalaceae plant, also identified highly upregulated genes that encode proteins associated with cell wall organization as a peripheral module in the gene co-expression network during developmental reprogramming of haustorium 19 . In addition, upregulation of genes that encode cell wall-modifying enzymes was detected in the transcriptome of host–parasite interface in the model Triphysaria versicolor , using laser microdissection 20 .…”

Common Mechanisms of Developmental Reprogramming in Plants—Lessons From Regeneration, Symbiosis, and Parasitism

“…In addition, this study identified similar expression patterns of floral tissue such as pollen in the haustoria, suggesting that the penetration of the haustorium may have co-opted genes from the polarized invasive growth seen in pollen tubes (Yang et al, 2015). In terms of development and cellular morphology, recent transcriptome analyses in Striga hermonthica and Thesium chinense showed that the formation of haustoria and LR goes through a similar process: auxin accumulates at the initiation sites, cell proliferation is reactivated, and cell walls are dramatically remodeled (Yoshida et al, 2016;Ichihashi et al, 2018;Yoshida et al, 2019). Notably, the pericycle-derived lateral root primordia grow through their own endodermal, cortical, and epidermal layers, while the haustorium grows through the host cell layers, such as the epidermis, cortex, endodermis, and pericycle, to reach the host stele.…”

Orobanchaceae parasite–host interactions

“…Indeed, gene expression patterns in both lateral root development and haustorium development partly overlap (Yoshida et al, 2019). The key regulator may be LATERAL ORGAN BOUNDARIES DOMAIN (LBD) proteins that orchestrate auxin downstream signaling for induced development and are highly upregulated in haustorium development in several parasitic plant species (Ichihashi et al, 2018;Ichihashi et al, 2020).…”