AUREA maintains the balance between chlorophyll synthesis and adventitious root formation in tomato

Flooding tolerance is an important trait for tomato breeding. In this study, we obtained a recessive mutant exhibiting highly enhanced submergence resistance. Phenotypical analyses showed that this resistant to flooding (rf) mutant displays slightly chlorotic leaves and spontaneous initiation of adventitious roots (ARs) on stems. The mutation was mapped to the phytochromobilin synthase gene AUREA (AU), in which a single amino acid substitution from asparagine to tyrosine occurred. In addition to the classic function of AU in phytochrome and chlorophyll biogenesis in leaves, we uncovered its novel role in mediating AR formation on stems. We further observed temporal coincidence of the two phenotypes in the rf mutant: chlorosis and spontaneous AR formation and revealed that AU functions by maintaining heme homeostasis. Interestingly, our grafting results suggest that heme might play roles in AR initiation via long-distance transport from leaves to stems. Our results present genetic evidence for the involvement of the AU–heme oxygenase-1–heme pathway in AR initiation in tomato. As fruit production and yield in the rf mutant are minimally impacted, the mutation identified in this study may provide a target for biotechnological renovation of tomato germplasm in future breeding.