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.