CsSPX‐PHR/PHL‐PHT1 and CsmiR399a‐PHO2‐PHT1/PHO1 Modules Orchestrate Pi Use Efficiency and Aluminium Tolerance in Tea Plants

High aluminium (Al) toxicity in acidic soils limits natural phosphate (Pi) nutrition to Al-hyperaccumulator tea plants, yet how they achieve Pi use efficiency (PUE) and Al tolerance remains elusive. Here, we deciphered Pi signalling networks and regulatory mechanisms underlying tea plant PUE, by functionally characterising Pi signalling components responding to Pi/N status changes and Al/H stress. CsPHT1.4 and CsPHT1.5 are PM-localised transporters expressed in tea root xylem and stem phloem for Pi uptake and redistribution. The physical interactions between CsSPX1a/2 and CsPHR1b/PHL1a under Pi supply repressed CsPHR1b/PHL1a activation of CsPHT1.4 transcription, but CsPHR1b/PHL1a were relieved from inhibition from the interactions for root Pi uptake under Pi deficiency or low Al conditions. Moreover, N-supply activated CsHHO6a suppressed CsSPX1a, and further activated CsPHR1b and CsPHT1.4 for Pi acquisition. High Al/H toxicity up-regulated CsSTOP1a/2a activated CsSPX1a transcription to repress CsPHR1b-CsPHT1.4 and inhibit Pi absorption and root growth. Meanwhile, Pi supply and high Al/H stress activated CsmiR399a to repress CsPHO2 and stabilise CsPHT1.5/CsPHO1 for Pi redistribution in tea plants. CsSPX1a-CsPHR1b-CsPHT1.4 and CsmiR399a-CsPHO2-CsPHT1.5 modules coordinately regulate Pi homoeostasis under Al/H stress and various N- and Pi- nutrition conditions, laying a foundation for genetic improvement of tea PUE and adaptation to stresses.