Methyl jasmonate mediates melatonin-induced cold tolerance of grafted watermelon plants

Root-shoot communication has a critical role in plant adaptation to environmental stress. Grafting is widely applied to enhance the abiotic stress tolerance of many horticultural crop species; however, the signal transduction mechanism involved in this tolerance remains unknown. Here, we show that pumpkin- or figleaf gourd rootstock-enhanced cold tolerance of watermelon shoots is accompanied by increases in the accumulation of melatonin, methyl jasmonate (MeJA), and hydrogen peroxide (H₂O₂). Increased melatonin levels in leaves were associated with both increased melatonin in rootstocks and MeJA-induced melatonin biosynthesis in leaves of plants under cold stress. Exogenous melatonin increased the accumulation of MeJA and H₂O₂ and enhanced cold tolerance, while inhibition of melatonin accumulation attenuated rootstock-induced MeJA and H₂O₂ accumulation and cold tolerance. MeJA application induced H₂O₂ accumulation and cold tolerance, but inhibition of JA biosynthesis abolished rootstock- or melatonin-induced H₂O₂ accumulation and cold tolerance. Additionally, inhibition of H₂O₂ production attenuated MeJA-induced tolerance to cold stress. Taken together, our results suggest that melatonin is involved in grafting-induced cold tolerance by inducing the accumulation of MeJA and H₂O₂. MeJA subsequently increases melatonin accumulation, forming a self-amplifying feedback loop that leads to increased H₂O₂ accumulation and cold tolerance. This study reveals a novel regulatory mechanism of rootstock-induced cold tolerance.