Abstract
BackgroundAuxin and glucose are both essential elements in normal root development. The heterotrimeric G protein complex in Arabidopsis thaliana, defined as containing alpha (AtGPA1), beta (AGB1), and gamma (AGG) subunits and a GTPase accelerating protein called Regulator of G Signaling 1 protein (AtRGS1), are involved in glucose signaling and regulate auxin transport.Methodology/Principal FindingsA systems approach was used to show that formation of lateral roots, a process requiring coordinated cell division followed by targeted cell expansion, involves a signaling interaction between glucose and auxin. We dissected the relationship between auxin and glucose action using lateral root formation as the biological context. We found that auxin and glucose act synergistically to yield a complex output involving both stimulatory and antagonist glucose effects on auxin responsiveness. Auxin-induced, lateral-root formation becomes bimodal with regard to auxin dose in the presence of glucose. This bimodality is mediated, in part, by the G protein complex defined above.Conclusion/SignificanceAuxin and glucose are essential signals controlling the rate of cell proliferation and expansion in roots. Auxin promotes the formation of lateral roots and is consequently essential for proper root architecture. Glucose affects the activation state of the heterotrimeric G protein complex which regulates auxin distribution in the root. The bimodality of auxin-induced, lateral-root formation becomes prominent in the presence of glucose and in roots lacking the G protein complex. Bimodality is apparent without added glucose in all loss-of-function mutants for these G protein components, suggesting that the heterotrimeric G protein complex attenuates the bimodality and that glucose inhibits this attenuation through the complex. The bimodality can be further resolved into the processes of lateral root primordia formation and lateral root emergence, from which a model integrating these signals is proposed.
Highlights
The plant hormone auxin is morphogenic in the sense that its effect on cell behavior is a function of concentration
Both lateral-root primordium (LRP) and lateral roots (LR) were scored separately but for the initial set of experiments (Figs 1 and 2) the LRP and LR are combined for simplicity
Malamy and Benfey [13] classified several stages of LR formation and, for purposes here, scores are based on binning LRP as stages I to VI and binning LR as all emergent roots
Summary
The plant hormone auxin is morphogenic in the sense that its effect on cell behavior is a function of concentration. Bimodality in auxin-induced K+ flux in guard cells [3] and coleoptiles epidermal cells [4] was reported. Bimodality of auxin action in cooperation with sucrose was observed in cellular differentiation of the vascular cambium [5]. The modular action of AUXIN-RESPONSE FACTORS (ARF) and accessory proteins (IAA proteins) in lateral root formation was shown to be successive [6]. One possibility is that the levels of some transcription factors are controlled by auxin in a concentration and/or time-dependent manner. Auxin and glucose are both essential elements in normal root development. The heterotrimeric G protein complex in Arabidopsis thaliana, defined as containing alpha (AtGPA1), beta (AGB1), and gamma (AGG) subunits and a GTPase accelerating protein called Regulator of G Signaling 1 protein (AtRGS1), are involved in glucose signaling and regulate auxin transport
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