Root-Knot and Cyst Nematodes Activate Procambium-Associated Genes in Arabidopsis Roots

Abstract

Developmental plasticity is one of the most striking features of plant morphogenesis, as plants are able to vary their shapes in response to environmental cues. Biotic or abiotic stimuli often promote organogenesis events in plants not observed under normal growth conditions. Root-knot nematodes (RKNs) are known to parasitize multiple species of rooting plants and to induce characteristic tissue expansion called galls or root-knots on the roots of their hosts by perturbing the plant cellular machinery. Galls contain giant cells (GCs) and neighboring cells, and the GCs are a source of nutrients for the parasitizing nematode. Highly active cell proliferation was observed in galls. However, the underlying mechanisms that regulate the symptoms triggered by the plant-nematode interaction have not yet been elucidated. In this study, we deciphered the molecular mechanism of gall formation with an in vitro infection assay system using RKN Meloidogyne incognita, and the model plant Arabidopsis thaliana. By taking advantages of this system, we performed next-generation sequencing-based transcriptome profiling, and found that the expression of procambium identity-associated genes were enriched during gall formation. Clustering analyses with artificial xylogenic systems, together with the results of expression analyses of the candidate genes, showed a significant correlation between the induction of gall cells and procambium-associated cells. Furthermore, the promoters of several procambial marker genes such as ATHB8, TDR and WOX4 were activated not only in M. incognita-induced galls, but similarly in M. javanica induced-galls and Heterodera schachtii-induced syncytia. Our findings suggest that phytoparasitic nematodes modulate the host’s developmental regulation of the vascular stem cells during gall formation.

Phytoparasitic Nematode Control of Plant Hormone Pathways

“…The TDIF-TDR-WOX4 pathway promotes procambial cell proliferation, whereas the TDIF-TDR-Glycogen Synthase Kinase3-BRI1-EMS SUPPRESSOR1 pathway inhibits xylem differentiation from procambial cells. Procambial-associated genes are activated in both CN and RKN feeding sites (Guo et al, 2017;Yamaguchi et al, 2017). The TDIF-TDR-WOX4 procambial cell proliferation pathway is required for CN feeding site formation (Guo et al, 2017); however, further research is needed to assess whether the TDIF-TDR-Glycogen Synthase Kinase3-BRI1-EMS SUPPRESSOR1 signaling is equally important.…”

A galling insect activates plant reproductive programs during gall development

“…Expression of the WOX, CLE, and PXY cambial activation pathway is also key to development of the gall-like structures elicited by root-knot and cyst nematodes and nodulation by Rhizobium in legumes 82 , suggesting that phylloxera and other parasites have converged on altering developmental regulation of vascular stem cells during gall elicitation. We are aware of no studies of CLE peptide production in phylloxera or other insects, as has been shown to be important for root-galling nematodes 82 .…”

Auxin Contributes to the Intraorgan Regulation of Gene Expression in Response to Shade

“…Phloem marker genes, such as SUC2, SEOR1 (AT3G01680), and APL (AT1G79430) (Kondo et al, 2016;Yamaguchi et al, 2017), were expressed at much higher levels in VS and almost not at all in MN ( Fig. 2; Supplemental Fig.…”