Root-shoot communications play important roles in plant stress responses. Here, we examined the roles of root-sourced signals in the shoot response to heat in cucumber plants. Cucumber plants grafted onto their own roots and luffa roots were exposed to aerial and root-zone heat to examine their tolerance by assessing the levels of oxidative stress, PSII photoinhibition, accumulation of abscisic acid (ABA), H2 O2 and heat shock protein (HSP) 70 using immunoblotting, chlorophyll fluorescence, immunoassay, CeCl3 staining and Western blotting, respectively. Grafting onto the luffa rootstock enhanced the shoot tolerance to the heat. This enhanced tolerance was associated with increased accumulation of ABA and apoplastic H2 O2 , RBOH transcripts and HSP70 expression and a decrease in oxidative stress in the shoots. The increases in the ABA and H2 O2 concentrations in the shoots were attributed to an increase in ABA transport from roots and an increase in ABA biosynthesis in the shoots when the root-zone and shoots were heat stressed, respectively. Inhibition of H2 O2 accumulation compromised luffa rootstock-induced HSP70 expression and heat tolerance. These results suggest that, under heat stress, ABA triggers the expression of HSP70 in an apoplastic H2 O2 -dependent manner, implicating the role of an ABA-dependent H2 O2 -driven mechanism in a systemic response involving root-shoot communication.