Glucose attenuation of auxin-mediated bimodality in lateral root formation is partly coupled by the heterotrimeric G protein complex

Abstract

Background: 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.

Methodology/principal findings: A 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/significance: Auxin 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.

Figure 1. Interaction between auxin and glucose in lateral root formation.

A. Acetocarmine-stained root with many lateral root (LR) and lateral root primordia (LRP, red cells). Inset: a single LRP (arrow). B. Acetocarmine-stained root grown with may lateral roots emerged. C. Three-dimensional representation of the effect of auxin and glucose on the formation of LR and LRP (combined). The data were fitted to a model as described in Methods. D. The auxin dose response for LR+LRP production at 4 concentrations of glucose. Inset, the same except expanded in range and number of auxin concentrations and performed with only 2 doses of glucose. E. The glucose dose response for LR+LRP production at 4 concentrations of auxin. The error bars represent the 95% Wald confidence intervals.

Figure 2. The role of the heterotrimeric G protein complex in the bimodality of auxin-induced lateral root formation.

A. 3-dimensional representation the effect of auxin and glucose on the formation of lateral root primordia and emergent lateral roots (LR+LRP) in wild type (light grey) and seedlings lacking an intact heterotrimeric G protein complex (dark grey). B. Expanded auxin dose response for LR+LRP production at 2 concentrations of glucose for wild type (Col, open squares) and the gpa1-4,agb1-2 double mutant (solid squares). C–E. Auxin dose response for LR+LRP production in wild type (Col, solid line) and seedlings lacking a single component of the G protein complex (dashed lines): gpa1-4 mutant (C), agb1-2 (D), and rgs1-2 (E). The error bars represent the 95% Wald confidence intervals.

Figure 3. The effect of glucose and the role of the heterotrimeric G protein on lateral root primordia formation (LRP) and lateral root (LR) emergence.

A–B. Auxin dose response for LRP production (A) and LR emergence (B) at 0% glucose (open circles) and 1% glucose (solid circles) for wild type (Col) seedlings. C–D. Auxin dose response for LRP production (C) and LR emergence (D) at 0% glucose for the double gpa1-4,agb1-2 mutant (solid circles) and for wild type (Col) seedlings (open circles). The error bars represent the 95% Wald confidence intervals E. A speculative model consistent with the present and published data. The gray box represents the data published by Mudgil and coworkers . The evidence for each of the signaling elements and the stimulatory and inhibitory arrows is described in the Discussion section. *GPA1, activated (GTP-bound) Gα subunit; GPA1/AGB1/AGG, heterotrimer.