Spatial Divergence of <i>PHR-PHT1</i> Modules Maintains Phosphorus Homeostasis in Soybean Nodules

Abstract

Maintaining phosphorus (Pi) homeostasis in nodules is the key to nodule development and nitrogen fixation, an important source of nitrogen for agriculture and ecosystems. <i>PHOSPHATE-TRANSPORTER1</i> (<i>PHT1</i>) and its regulator <i>PHOSPHATE-STARVATION-RESPONSE1</i> (<i>PHR1</i>), which constitute the <i>PHR1-PHT1</i> module, play important roles in maintaining Pi homeostasis in different organs. However, the <i>PHR1-PHT1</i> module and its functions in nodules remain unknown. We identified one <i>PHT1</i> (<i>GmPHT1;11</i>) and four <i>PHR1</i> (<i>GmPHR1</i>) homologs in soybean (<i>Glycine max</i>) plants, which displayed specific expression patterns in different tissues in nodules, similar to previously reported <i>GmPHT1;1</i> and <i>GmPHT1;4</i> Through the integration of different approaches, <i>GmPHR-GmPHT1</i> modules were confirmed. Combining our results and previous reports, we established multiple <i>GmPHR-GmPHT1</i> modules acting in the infected or noninfected tissues in nodules. A single <i>GmPHR</i> had more than one <i>GmPHT1</i> target, and vice versa. Therefore, overlapping and cross-talking modules monitored the wave of available Pi to maintain Pi homeostasis in nodules, which sequentially regulated nodule initiation and development. High levels of <i>GmPHT1;11</i> enhanced Pi accumulation in nodules, increased nodule size, but decreased nodule number. Nitrogenase activity was also enhanced by <i>GmPHT1;11</i> Our findings uncover <i>GmPHR-GmPHT1</i> modules in nodules, which expands our understanding of the mechanism of maintaining Pi homeostasis in soybean plants.