Glucose Attenuation of Auxin-Mediated Bimodality in Lateral Root Formation Is Partly Coupled by the Heterotrimeric G Protein Complex

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.

Interaction between Glucose and Brassinosteroid during the Regulation of Lateral Root Development in Arabidopsis

“…The BR signaling pathway has been reported to influence the functions of auxin and vice versa during root growth and development (Nemhauser et al, 2004;Mouchel et al, 2006;Hardtke et al, 2007;Vert et al, 2008). Similarly, sugar signals are also reported to interact with the auxin signaling machinery (Moore et al, 2003;Gonzali et al, 2005;Ohto et al, 2006;Mishra et al, 2009;Mudgil et al, 2009;Booker et al, 2010;Sairanen et al, 2012;Yuan et al, 2014). Glc inhibits the G-protein complex-dependent Figure 10.…”

“…Previous studies suggested a prominent effect of Glc on root growth and development in Arabidopsis (Mishra et al, 2009;Booker et al, 2010;Kircher and Schopfer, 2012;Xiong et al, 2013;Yuan et al, 2014). Increasing Figure 1.…”

“…These and various other factors form a complex signal response network to bring about optimum growth changes to enable better fitness in plants. Glc and auxin can interact extensively to control many aspects of root architecture, such as root elongation, LR production, root hair development, and root directional growth (Mishra et al, 2009;Mudgil et al, 2009;Booker et al, 2010;Yuan et al, 2014). However, there are very few reports in the literature that either directly or indirectly link BR responses to sugar signaling (Laxmi et al, 2004;Rognoni et al, 2007;Gupta et al, 2012;Singh et al, 2014a).…”

Multiple Interactions between Glucose and Brassinosteroid Signal Transduction Pathways in Arabidopsis Are Uncovered by Whole-Genome Transcriptional Profiling

“…reports for sugar and auxin interaction during plant growth and development (Moore et al, 2003;Mishra et al, 2009;Mudgil et al, 2009;Booker et al, 2010). To determine any involvement of auxin machinery in Glc-BR control of etiolated hypocotyl elongation growth, we used well-established auxin reporter auxin responsive promoter DR5::GUS.…”

Cytokinin Interplay with Ethylene, Auxin, and Glucose Signaling Controls Arabidopsis Seedling Root Directional Growth

“…Increasing Glc concentrations can induce differential root length, lateral roots, gravitropism, and root hair elongation in auxin perception and signaling mutants, suggesting that auxin signaling is involved in controlling Glc-regulated root responses (Mishra et al, 2009). Glc has also been shown to act via G-protein signaling to attenuate auxin-mediated bimodality in controlling lateral root formation (Booker et al, 2010).…”