Cytokinins play opposite roles in lateral root formation, and nematode and Rhizobial symbioses

Abstract

SummaryWe used the cytokinin-responsive Arabidopsis response regulator (ARR)5 gene promoter fused to a b-glucuronidase (GUS) reporter gene, and cytokinin oxidase (CKX) genes from Arabidopsis thaliana (AtCKX3) and maize (ZmCKX1) to investigate the roles of cytokinins in lateral root formation and symbiosis in Lotus japonicus. ARR5 expression was undetectable in the dividing initial cells at early stages of lateral root formation, but later we observed high expression in the base of the lateral root primordium. The root tip continues to express ARR5 during subsequent development of the lateral root. These results suggest a dynamic role for cytokinin in lateral root development. We observed ARR5 expression in curled/deformed root hairs, and also in nodule primordia in response to Rhizobial inoculation. This expression declined once the nodule emerged from the parent root. Root penetration and migration of root-knot nematode (RKN) second-stage larvae (L2) did not elevate ARR5 expression, but a high level of expression was induced when L2 reached the differentiating vascular bundle and during early stages of the nematode±plant interaction. ARR5 expression was speci®cally absent in mature giant cells (GCs), although dividing cells around the GCs continued to express this reporter. The same pattern was observed using a green¯uorescent protein (GFP) reporter driven by the ARR5 promoter in tomato. Overexpression of CKX genes rendered the transgenic hairy roots resistant to exogenous application of the cytokinin [N 6 -(D 2 isopentenyl) adenine riboside] (iPR). CKX roots have signi®cantly more lateral roots, but fewer nodules and nematode-induced root galls per plant, than control hairy roots.

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.…”

“…Various lines of evidence also have implicated auxin and cytokinin flux in the RKN-host interaction (Mathesius et al, 1998;Hutangura et al, 1999;Karczmarek et al, 2004;Lohar et al, 2004) as part of the regulation of root architecture. Thus, rather than focus on gene expression in GCs per se, we designed experiments to interrogate genes representative of the broader tomato root transcriptome during compatible and incompatible interactions with RKN.…”

“…Various approaches, including construction of subtractive cDNA libraries from individual GCs , promoter-trapping strategies (Sijmons et al, 1994;Barthels et al, 1997;Favery et al, 2004), and in situ hybridizations (Lohar et al, 2004;Gal et al, 2006), have examined gene expression patterns during RKN feeding site initiation. Collectively, these experiments have revealed that genes regulating the cell cycle (Niebel et al, 1996;de Almeida Engler et al, 1999), cell wall synthesis (Niebel et al, 1993;Goellner et al, 2001;Vercauteren et al, 2002), and transcription regulation are up-regulated in GCs.…”

Root system architecture: insights fromArabidopsisand cereal crops

“…Cytokinin is primarily synthesized in the root cap [69] and has a largely antagonistic effect to auxin in terms of root architecture: cytokinin has an inhibitory effect on lateral root branching, with mutants for cytokinin biosynthesis and sensitivity demonstrating increased numbers of lateral roots [70][71][72][73]. Auxin is synthesized primarily in young aerial tissues and undergoes polar transport towards the root tissues [74].…”

RNA Interference-Mediated Repression of S6 Kinase 1 Impairs Root Nodule Development in Soybean

“…Both kinases seem to become activated in early stages of nodules such as 2-day-old nodules in which nodule organogenesis including cortical cell division occurs (Oldroyd et al, 2011). The effects of phytohormones, especially auxin and cytokinin, have been reported to affect nodule organogenesis (Lohar et al, 2004;Oldroyd et al, 2011), and the activity of plant S6K1 was also found to be positively regulated by these hormones (Turck et al, 2004). Therefore, it seems probable that control of nodulation by these phytohormones is mediated through the activation of TOR signaling components.…”