Nodule number regulation in legumes is controlled by a feedback loop that integrates nutrient and rhizobia symbiont status signals to regulate nodule development. Signals from the roots are perceived by shoot receptors, including a CLV1-like receptor-like kinase known as SUNN inMedicago truncatula. In the absence of functional SUNN, the autoregulation feedback loop is disrupted, resulting in hypernodulation. To elucidate early autoregulation mechanisms disrupted in SUNN mutants, we searched for genes with altered expression in the loss-of-functionsunn-4mutant and included therdn1-2autoregulation mutant for comparison. We identified constitutively altered expression of small groups of genes insunn-4roots and insunn-4shoots. All genes with verified roles in nodulation that were induced in wild-type roots during the establishment of nodules were also induced insunn-4, including autoregulation genesTML2andTML1. Only an isoflavone-7-O-methyltransferase gene was induced in response to rhizobia in wild-type roots but not induced insunn-4. In shoot tissues of wild-type, eight rhizobia-responsive genes were identified, including a MYB family transcription factor gene that remained at a baseline level insunn-4; three genes were induced by rhizobia in shoots ofsunn-4but not wild-type. We cataloged the temporal induction profiles of many small secreted peptide (MtSSP) genes in nodulating root tissues, encompassing members of twenty-four peptide families, including the CLE and IRON MAN families. The discovery that expression ofTML2in roots, a key factor in inhibiting nodulation in response to autoregulation signals, is also triggered insunn-4in the section of roots analyzed, suggests that the mechanism of TML regulation of nodulation inM. truncatulamay be more complex than published models.