Phosphorus is an essential macronutrient for plant development and metabolism. Plants have evolved ingenious mechanisms to overcome phosphate (Pi) starvation. However, the molecular mechanisms underlying regulation of shoot and root architectures as well as coordinated utilization of Pi and nitrogen remain largely unclear. Here, we show that Nodulation Signaling Pathway 1 (NSP1) and NSP2 regulate tiller number by promoting the biosynthesis of strigolactones (SLs), which are a class of phytohormones with fundamental effects on plant architecture and environmental responses. We found that in response to low-Pi stress, NSP1 and NSP2 are induced by Oryza sativa PHOSPHATE STARVATION RESPONSE2 (OsPHR2) and form a complex to directly bind the promoters of SL biosynthesis genes, leading to a great promotion on SL biosynthesis in rice. Interestingly, the NSP1/2-SL signaling module represses the expression of CROWN ROOTLESS 1 (CRL1), a newly identified early SL responsive gene in roots, to restrain lateral root density under Pi deficiency. Furthermore, we demonstrated that GR24^4DO treatment under normal conditions could repress the expression of OsNRTs and OsAMTs to suppress nitrogen absorption but enhance the expression of OsPTs to promote Pi absorption, thus facilitating the balance of nitrogen and phosphorus uptake in rice. Importantly, we found that the NSP1p:NSP1 and NSP2p:NSP2 transgenic plants showed improved agronomic traits and grain yield under low and medium phosphorus conditions. Taken together, these results uncovered the mechanisms of SL biosynthesis and signaling in response to Pi starvation stress, providing genetic resources for improving plant architecture and nutrient use efficiency under low Pi environments.

Phosphorus is an essential macronutrient for plant development and metabolism. Plants have evolved ingenious mechanisms to overcome phosphate (Pi) starvation. However, the molecular mechanisms underlying regulation of shoot and root architectures as well as coordinated utilization of Pi and nitrogen remain largely unclear. Here, we show that Nodulation Signaling Pathway 1 (NSP1) and NSP2 regulate tiller number by promoting the biosynthesis of strigolactones (SLs), which are a class of phytohormones with fundamental effects on plant architecture and environmental responses. We found that in response to low-Pi stress, NSP1 and NSP2 are induced by Oryza sativa PHOSPHATE STARVATION RESPONSE2 (OsPHR2) and form a complex to directly bind the promoters of SL biosynthesis genes, leading to a great promotion on SL biosynthesis in rice. Interestingly, the NSP1/2-SL signaling module represses the expression of CROWN ROOTLESS 1 (CRL1), a newly identified early SL responsive gene in roots, to restrain lateral root density under Pi deficiency. Furthermore, we demonstrated that GR24^4DO treatment under normal conditions could repress the expression of OsNRTs and OsAMTs to suppress nitrogen absorption but enhance the expression of OsPTs to promote Pi absorption, thus facilitating the balance of nitrogen and phosphorus uptake in rice. Importantly, we found that the NSP1p:NSP1 and NSP2p:NSP2 transgenic plants showed improved agronomic traits and grain yield under low and medium phosphorus conditions. Taken together, these results uncovered the mechanisms of SL biosynthesis and signaling in response to Pi starvation stress, providing genetic resources for improving plant architecture and nutrient use efficiency under low Pi environments.

Phosphorus is an essential macronutrient for plant development and metabolism. Plants have evolved ingenious mechanisms to overcome phosphate (Pi) starvation. However, the molecular mechanisms underlying regulation of shoot and root architectures as well as coordinated utilization of Pi and nitrogen remain largely unclear. Here, we show that Nodulation Signaling Pathway 1 (NSP1) and NSP2 regulate tiller number by promoting the biosynthesis of strigolactones (SLs), which are a class of phytohormones with fundamental effects on plant architecture and environmental responses. We found that in response to low-Pi stress, NSP1 and NSP2 are induced by Oryza sativa PHOSPHATE STARVATION RESPONSE2 (OsPHR2) and form a complex to directly bind the promoters of SL biosynthesis genes, leading to a great promotion on SL biosynthesis in rice. Interestingly, the NSP1/2-SL signaling module represses the expression of CROWN ROOTLESS 1 (CRL1), a newly identified early SL responsive gene in roots, to restrain lateral root density under Pi deficiency. Furthermore, we demonstrated that GR24^4DO treatment under normal conditions could repress the expression of OsNRTs and OsAMTs to suppress nitrogen absorption but enhance the expression of OsPTs to promote Pi absorption, thus facilitating the balance of nitrogen and phosphorus uptake in rice. Importantly, we found that the NSP1p:NSP1 and NSP2p:NSP2 transgenic plants showed improved agronomic traits and grain yield under low and medium phosphorus conditions. Taken together, these results uncovered the mechanisms of SL biosynthesis and signaling in response to Pi starvation stress, providing genetic resources for improving plant architecture and nutrient use efficiency under low Pi environments.