A two-step auxin-GA cross-talk regulates organ formation in tomato

Plant organ formation involves an initiation stage followed by growth, together determining organ shape. The plant hormone auxin regulates both initiation and growth. However, it is still not clear how auxin facilitates these two separate successive stages. Here, we show that in tomato compound-leaf development, auxin promotes leaflet initiation and growth via opposite effects on gibberellin (GA) metabolism. Short auxin treatment induced the expression of GA catabolism genes, while a longer increased auxin response induced the expression of GA biosynthesis genes. GA biosynthesis mutants suppressed auxin-induced blade growth. Leaflet number was reduced by increased GA activity, and local reduction of GA activity led to the formation of ectopic leaflets, indicating that leaflet initiation requires reduced GA. Expression of a GA catabolism gene in initiating leaflets was sufficient to induce ectopic leaflets in the adjacent intercalary region, suggesting a non-autonomous function of GA. Collectively, these results point to a context-dependent dual interaction between auxin and GA in organ formation: auxin reduces GA to enable initiation, and induces GA to promote growth.