Inhibition of legume nodulation by Pi deficiency is dependent on the autoregulation of nodulation (AON) pathway

SUMMARY Inhibition of nodule development is one of the main adverse effects of phosphate (Pi) deficiency in legumes. Despite all of the efforts made over the last decades to understand how root nodules cope with Pi deficiency, the molecular mechanisms leading to the reduction in nodule number under Pi deficiency remain elusive. In the present study, we provide experimental evidence indicating that Pi deficiency activates the autoregulation of nodulation (AON) pathway, leading to a reduction in nodule numbers in both common bean and soybean. A transcriptional profile analysis revealed that the expression of the AON‐related genes PvNIN, PvRIC1, PvRIC2, and PvTML is upregulated under Pi deficiency conditions. The downregulation of the MYB transcription factor PvPHR1 in common bean roots significantly reduced the expression of these four AON‐related genes. Physiological analyses indicated that Pi deficiency does not affect the establishment of the root nodule symbiosis in the supernodulation mutant lines Pvnark and Gmnark. Reciprocal grafting and split‐roots analyses determined that the activation of the AON pathway was required for the inhibitory effect of Pi deficiency. Altogether, these data improve our understanding of the genetic mechanisms controlling the establishment of the root nodule symbiosis under Pi deficiency. Significance Statement Inhibition of nodule development is one of the main adverse effects of phosphate (Pi) deficiency in legumes. However, the molecular mechanisms leading to the reduction in nodule number under Pi deficiency remain elusive. We provide experimental evidence that Pi deficiency activates the autoregulation of nodulation (AON) pathway, leading to a reduction in nodule numbers in legumes. The activation of the AON pathway under Pi‐deficient conditions is likely by the transcription factor PHR1.