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Background  MADS-box transcription factors (TFs) are the key regulators of multiple developmental processes in plants; among them, a chrysanthemum MADS-box TF  CmANR1  has been isolated and described as functioning in root development in response to high nitrate concentration signals. However, how CmANR1 affects root and shoot development remains unclear.    Results  We report that CmANR1 plays a positive role in root system development in chrysanthemum throughout the developmental stages of in vitro tissue cultures. Metabolomics combined with transcriptomics assays show that  CmANR1  promotes robust root system development by facilitating nitrate assimilation, and influencing the metabolic pathways of amino acid, glycolysis, and the tricarboxylic acid cycle (TCA) cycle. Also, we found that the expression levels of TFs associated with the nitrate signaling pathways, such as  AGL8 ,  AGL21 , and  LBD29 , are significantly up-regulated in  CmANR1 -transgenic plants relative to the wild-type (WT) control; by contrast, the expression levels of  RHD3-LIKE ,  LBD37 , and  GATA23  were significantly down-regulated. These results suggest that these nitrate signaling associated TFs are involved in  CmANR1 -modulated control of root development. In addition,  CmANR1  also acts as a positive regulator to control shoot growth and development.    Conclusions  These findings provide potential mechanisms of MADS-box TF CmANR1 modulation of root and shoot development, which occurs by regulating a series of nitrate signaling associated TFs, and influencing the metabolic pathways of amino acid and glycolysis, as well as TCA cycle and nitrate assimilation.    Supplementary Information  The online version contains supplementary material available at 10.1186/s12870-021-02860-7.

New insights into the role of MADS-box transcription factor gene CmANR1 on root and shoot development in chrysanthemum (Chrysanthemum morifolium)