Spermine-mediated modulation of ethylene governs photosynthetic efficiency, nitrogen utilization, and heat stress tolerance in wheat (Triticum aestivum L.)

• Spermine and ethylene enhance antioxidant defense and upregulates psbA, psbB , and psbC . • Spermine enhances Rubisco activity, nitrogen metabolism and p-NUE. • Controlled ethylene levels are essential for optimal heat stress protection. • Spermine inhibits ACS/ACO expression, hence reducing ethylene overproduction. Global warming-induced heat stress (HS) limits wheat productivity by impairing photosynthesis and nitrogen metabolism. We evaluated the effect of spermine (Spm) and ethephon (ETH; an ethylene donor) in HS tolerance across eight cultivars, and selected PBW343 (heat-tolerant) and PBW17 (heat-sensitive) for a detailed study. Under HS, ROS accumulation and lipid peroxidation increased by 145.6%, while photosynthetic rate and photosynthetic nitrogen use efficiency (p-NUE) declined by 39.3% and 35%, respectively. Spm (100 μM) reduced ROS and lipid peroxidation by 33.9%, enhanced antioxidant enzymes (SOD, APX, GR), upregulated psbA, psbB, and psbC, and suppressed ACS/ACO expression, decreasing ethylene emission by 23.8%. HS increased oxidative stress by increasing H 2 O 2 and MDA levels, but ETH (200 µL L⁻¹) and Spm applied together most effectively reduced oxidative stress under control and heat stress conditions. Combining Spm with the ethylene inhibitor aminoethoxyvinylglycine (AVG; 50 μL L⁻¹) under HS reduced GR activity and photosynthesis, confirming that balanced ethylene signaling is essential for thermoprotection. Our findings reveal that Spm enhances HS tolerance by redirecting S-adenosylmethionine metabolism toward polyamine biosynthesis, stabilizing membranes, detoxifying ROS, and sustaining photosynthesis. This supports the Spm ethylene pathway modulation to improve wheat resilience to HS.