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Evolution and diversification of the plant gibberellin receptor GID1

H. Yoshida,E. Tanimoto,Takaaki Hirai,Y. Miyanoiri,Rie Mitani,Mayuko Kawamura,M. Takeda,S. Takehara,K. Hirano,M. Kainosho,T. Akagi,M. Matsuoka,M. Ueguchi-Tanaka

Published 2018 in Proceedings of the National Academy of Sciences of the United States of America

ABSTRACT

Significance The plant gibberellin receptor GID1 shows sequence similarity to carboxylesterase, suggesting that it is derived from an enzyme. However, how GID1 evolved and was modified is unclear. We identified two amino acids that are essential for GID1 activity, and we found that adjustment of these residues caused GID1 to recognize novel GAs carrying 13-OH as active GAs and to strictly refuse inactive GAs. Phylogenetic analysis of 169 GID1s revealed seven subtypes, and the B-type in core eudicots showed unique characteristics. In fact, certain B-type GID1s showed a higher nonsynonymous-to-synonymous divergence ratio in the region determining GA affinity. Such B-type GID1s with higher affinity were preferentially expressed in the roots in some core eudicot plants and conferred adaptive growth under stress. The plant gibberellin (GA) receptor GID1 shows sequence similarity to carboxylesterase (CXE). Here, we report the molecular evolution of GID1 from establishment to functionally diverse forms in eudicots. By introducing 18 mutagenized rice GID1s into a rice gid1 null mutant, we identified the amino acids crucial for GID1 activity in planta. We focused on two amino acids facing the C2/C3 positions of ent-gibberellane, not shared by lycophytes and euphyllophytes, and found that adjustment of these residues resulted in increased GID1 affinity toward GA4, new acceptance of GA1 and GA3 carrying C13-OH as bioactive ligands, and elimination of inactive GAs. These residues rendered the GA perception system more sophisticated. We conducted phylogenetic analysis of 169 GID1s from 66 plant species and found that, unlike other taxa, nearly all eudicots contain two types of GID1, named A- and B-type. Certain B-type GID1s showed a unique evolutionary characteristic of significantly higher nonsynonymous-to-synonymous divergence in the region determining GA4 affinity. Furthermore, these B-type GID1s were preferentially expressed in the roots of Arabidopsis, soybean, and lettuce and might be involved in root elongation without shoot elongation for adaptive growth under low-temperature stress. Based on these observations, we discuss the establishment and adaption of GID1s during plant evolution.

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