Overlapping Plant Signal Transduction Pathways Induced by a Parasitic Nematode and a Rhizobial Endosymbiont

Abstract

Root-knot nematodes and rhizobia establish interactions with roots characterized by the de novo induction of host structures, termed giant cells and nodules, respectively. Two transcription regulators, PHAN and KNOX, required for the establishment of meristems were previously shown to be expressed in tomato giant cells. We isolated the orthologues of PHAN and KNOX (Mt-phan and Mt-knox-1) from the model legume Medicago truncatula, and established the spatial distribution of their expression in situ. We confirmed that Mt-phan and Mt-knox-1 are expressed in lateral root initials and in nematode-induced giant cells and showed that they are expressed in nodules induced by Sinorhizobium meliloti. Expression of both genes becomes spatially restricted as the nodules develop. We further examined nematode feeding sites for the expression of two genes involved in nodule formation, ccs52 (encodes a mitotic inhibitor) and ENOD40 (encodes an early, nodulation mitogen), and found transcripts of both genes to be present in and around giant cells induced in Medicago. Collectively, these results reveal common elements of host responses to mutualistic and parasitic plant endosymbionts and imply that overlapping regulatory pathways lead to giant cells and nodules. We discuss these pathways in the context of phytohormones and parallels between beneficial symbiosis and disease.

Root-knot nematodes and bacterial Nod factors elicit common signal transduction events in Lotus japonicus

“…This strongly argues that the effect of these genes is exerted directly in the GC and not at some other stage of the RKN life cycle. The actual GC inductive process is accompanied by transcriptional events common to the early events of nodule formation by rhizobia (15,16), suggesting that the sequence of events initiated by NF might be similar to those events that lead to GC formation. Although the chemical nature of NemF remains unknown, in our model, the bacterial, fungal, and nematode signal molecules are sufficiently similar to be recognized by the same receptor complexes (20,21) and thus initiate similar downstream effects.…”

“…Migration into the vascular cylinder is intercellular and nondestructive and, once in the stele, RKN induce characteristic giant cells (GC), from which the developing larvae feed. GC formation invokes host pathways in common with those necessary for nitrogen-nodule formation, including induction of specific transcription regulators (14), early nodulation genes (15,16), and cytokinin-response pathways (17), suggesting that at the cellular level, RKN and rhizobia exploit a common strategy. Consistent with this, a beet cyst nematodeinducible resistance gene is induced during rhizobial invasion (11).…”

Transcriptional, Posttranscriptional, and Posttranslational Regulation of SHOOT MERISTEMLESS Gene Expression in Arabidopsis Determines Gene Function in the Shoot Apex

“…Interestingly, the pattern of lateral root distribution is altered in the mutant stm-1 (Casimiro et al, 2001). Indeed, the STM orthologs in tomato LYCOPERSICUM ESCULENTUM T6/TOMATO KNOTTED2 (LeT6/TKN2) and in M. truncatula MtKNOX1 are found to be expressed in lateral roots (Koltai and Bird, 2000;Koltai et al, 2001). The class I KNOX gene KNAT6 acts redundantly with STM in SAM maintenance and is expressed in roots (Dean et al, 2004;Belles-Boix et al, 2006).…”

“…supercontig_152.57; Populus trichocarpa gene Potri.011G011100; grape (Vitis vinifera) gene GSVIVG01004811001; tomato (Solanum lycopersicum) gene LeT6 (Solyc02g081120; Janssen et al, 1998); Medicago truncatula gene MtKNOX1 (Medtr5g085860; Koltai et al, 2001); soybean (Glycine max) gene Glyma09g01000; bean (Phaseolus vulgaris) gene Phvul.006G145800; and Ricinus communis gene 29842.t000028. All sequences were obtained from Phytozome (http://www.…”

Comprehensive Transcriptome Profiling in Tomato Reveals a Role for Glycosyltransferase in Mi-Mediated Nematode Resistance

“…Gheysen and Fenoll (2002) provide a detailed review of the approximately 50 genes known to be up-regulated and a few that are repressed. One emerging picture is that GCs share many features with rhizobial nodules, including coexpression of specific transcription regulators , early nodulation genes (Bird, 1996;Koltai et al, 2001;Favery et al, 2002), and cytokinin-responsive genes (Lohar et al, 2004); genetic data reinforce these similarities (Lohar and Bird, 2003;Bird, 2004;Weerasinghe et al, 2005). Numerous putative defense genes also are up-regulated during RKN infection, including peroxidases, chitinases, extensins, and proteinase inhibitors, perhaps as a global response to pathogen invasion.…”