The Arabidopsis IDD14, IDD15, and IDD16 Cooperatively Regulate Lateral Organ Morphogenesis and Gravitropism by Promoting Auxin Biosynthesis and Transport

Dayong Cui,Zhicai Wang,Yanjun Jing,Wei Xin,Jing Liu,Jingbo Zhao,Mingzhu Fan,Yuxin Hu,Hao Yu

doi:10.1371/journal.pgen.1003759

Abstract

The plant hormone auxin plays a critical role in regulating various aspects of plant growth and development, and the spatial accumulation of auxin within organs, which is primarily attributable to local auxin biosynthesis and polar transport, is largely responsible for lateral organ morphogenesis and the establishment of plant architecture. Here, we show that three Arabidopsis INDETERMINATE DOMAIN (IDD) transcription factors, IDD14, IDD15, and IDD16, cooperatively regulate auxin biosynthesis and transport and thus aerial organ morphogenesis and gravitropic responses. Gain-of-function of each IDD gene in Arabidopsis results in small and transversally down-curled leaves, whereas loss-of-function of these IDD genes causes pleiotropic phenotypes in aerial organs and defects in gravitropic responses, including altered leaf shape, flower development, fertility, and plant architecture. Further analyses indicate that these IDD genes regulate spatial auxin accumulation by directly targeting YUCCA5 (YUC5), TRYPTOPHAN AMINOTRANSFERASE of ARABIDOPSIS1 (TAA1), and PIN-FORMED1 (PIN1) to promote auxin biosynthesis and transport. Moreover, mutation or ectopic expression of YUC suppresses the organ morphogenic phenotype and partially restores the gravitropic responses in gain- or loss-of-function idd mutants, respectively. Taken together, our results reveal that a subfamily of IDD transcription factors plays a critical role in the regulation of spatial auxin accumulation, thereby controlling organ morphogenesis and gravitropic responses in plants.

Highlights

Auxin is a key plant hormone that plays critical roles in the regulation of plant growth and development
A yuc single mutant in Arabidopsis does not show an obvious phenotype, the mutation of multiple YUC genes leads to a diversity of auxin-related phenotypes, including reduced apical dominance, crinkled leaves, simple venation, and abnormal flower development, demonstrating that YUC-modulated local auxin biosynthesis is critical for plant morphogenesis and architecture formation [9,10]
We found that the three fragments containing a putative INDETERMINATE DOMAIN (IDD)-binding motif in YUC5, TRYPTOPHAN AMINOTRANSFERASE of ARABIDOPSIS1 (TAA1), or PIN1 were greatly enriched by IDD16 after GFP immunoprecipitation, whereas no binding activity was detected in the promoter regions of YUC2 or YUC3 (Figure 7B)

Summary

Introduction

Auxin is a key plant hormone that plays critical roles in the regulation of plant growth and development. A yuc single mutant in Arabidopsis does not show an obvious phenotype, the mutation of multiple YUC genes leads to a diversity of auxin-related phenotypes, including reduced apical dominance, crinkled leaves, simple venation, and abnormal flower development, demonstrating that YUC-modulated local auxin biosynthesis is critical for plant morphogenesis and architecture formation [9,10]. Such developmental defects in yuc mutants can be rescued by local expression of iaaM, a bacterial auxin biosynthetic gene, but not by the application of exogenous auxin [9]. The taa plant has a decreased level of endogenous IAA and displays defects in shade avoidance and root-specific ethylene sensitivity, and the simultaneous mutation of TAA1 and its close homologs (TAR1 and TAR2) results in phenotypes that are obviously auxin-related, such as reduced gravitropic response of

Author Summary

Results

Discussion

Findings

Materials and Methods