Multiple Gibberellin Receptors Contribute to Phenotypic Stability under Changing Environments

Abstract

The pleiotropic and complex gibberellin (GA) response relies on targeted proteolysis of DELLA proteins mediated by a GA-activated GIBBERELLIN-INSENSITIVE DWARF1 (GID1) receptor. The tomato (<i>Solanum lycopersicum</i>) genome encodes for a single DELLA protein, PROCERA (PRO), and three receptors, SlGID1a (GID1a), GID1b1, and GID1b2, that may guide specific GA responses. In this work, clustered regularly interspaced short palindromic repeats (CRISPR) /CRISPR associated protein 9-derived <i>gid1</i> mutants were generated and their effect on GA responses was studied. The <i>gid1</i> triple mutant was extremely dwarf and fully insensitive to GA. Under optimal growth conditions, the three receptors function redundantly and the single <i>gid1</i> mutants exhibited very mild phenotypic changes. Among the three receptors, GID1a had the strongest effects on germination and growth. Yeast two-hybrid assays suggested that GID1a has the highest affinity to PRO. Analysis of lines with a single active receptor demonstrated a unique role for GID1a in protracted response to GA that was saturated only at high doses. When the <i>gid1</i> mutants were grown in the field under ambient changing environments, they showed phenotypic instability, the high redundancy was lost, and <i>gid1a</i> exhibited dwarfism that was strongly exacerbated by the loss of another <i>GID1b</i> receptor gene. These results suggest that multiple GA receptors contribute to phenotypic stability under environmental extremes.