We tested whether a gene regulating nodule number in Medicago truncatula, Super Numeric Nodules (SUNN ), is involved in root architecture responses to carbon (C) and nitrogen (N) and whether this is mediated by changes in shoot-to-root auxin transport. Nodules and lateral roots are root organs that are under the control of nutrient supply, but how their architecture is regulated in response to nutrients is unclear. We treated wild-type and sunn-1 seedlings with four combinations of low or increased N (as nitrate) and C (as CO(2)) and determined responses in C/N partitioning, plant growth, root and nodule density, and changes in auxin transport. In both genotypes, nodule density was negatively correlated with tissue N concentration, while only the wild type showed significant correlations between N concentration and lateral root density. Shoot-to-root auxin transport was negatively correlated with shoot N concentration in the wild type but not in the sunn-1 mutant. In addition, the ability of rhizobia to alter auxin transport depended on N and C treatment as well as the SUNN gene. Nodule and lateral root densities were negatively correlated with auxin transport in the wild type but not in the sunn-1 mutant. Our results suggest that SUNN is required for the modulation of shoot-to-root auxin transport in response to altered N tissue concentrations in the absence of rhizobia and that this controls lateral root density in response to N. The control of nodule density in response to N is more likely to occur locally in the root.