The cyclophilin A DIAGEOTROPICA gene affects auxin transport in both root and shoot to control lateral root formation

Maria G. Ivanchenko; Bangjun Wang; Eva Medvecká; Yunlong Du; Elisa Azzarello; Stefano Mancuso; Molly Megraw; Sergei Filichkin; Joseph G. Dubrovsky; Jiří Friml; Markus Geisler

doi:10.1242/dev.113225

journal article Jan 01, 2015

The cyclophilin A DIAGEOTROPICA gene affects auxin transport in both root and shoot to control lateral root formation

Maria G. Ivanchenko Bangjun Wang

Eva Medvecká Yunlong Du

Elisa Azzarello Stefano Mancuso Molly Megraw Sergei Filichkin Joseph G. Dubrovsky Jiří Friml

Markus Geisler

Development · The Company of Biologists

View at Publisher Save 10.1242/dev.113225

Abstract

Cyclophilin A is a conserved peptidyl-prolyl cis-trans isomerase (PPIase) best known as the cellular receptor of the immunosuppressant cyclosporine A. Despite significant effort, evidence of developmental functions of cyclophilin A in non-plant systems has remained obscure. Mutations in a tomato (Solanum lycopersicum) cyclophilin A ortholog, DIAGEOTROPICA (DGT), have been shown to abolish the organogenesis of lateral roots; however, a mechanistic explanation of the phenotype is lacking. Here, we show that the dgt mutant lacks auxin maxima relevant to priming and specification of lateral root founder cells. DGT is expressed in shoot and root, and localizes to both the nucleus and cytoplasm during lateral root organogenesis. Mutation of ENTIRE/IAA9, a member of the auxin-responsive Aux/IAA protein family of transcriptional repressors, partially restores the inability of dgt to initiate lateral root primordia but not the primordia outgrowth. By comparison, grafting of a wild-type scion restores the process of lateral root formation, consistent with participation of a mobile signal. Antibodies do not detect movement of the DGT protein into the dgt rootstock; however, experiments with radiolabeled auxin and an auxin-specific microelectrode demonstrate abnormal auxin fluxes. Functional studies of DGT in heterologous yeast and tobacco-leaf auxin-transport systems demonstrate that DGT negatively regulates PIN-FORMED (PIN) auxin efflux transporters by affecting their plasma membrane localization. Studies in tomato support complex effects of the dgt mutation on PIN expression level, expression domain and plasma membrane localization. Our data demonstrate that DGT regulates auxin transport in lateral root formation.

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Published: Jan 01, 2015

Authors

M

Maria G. Ivanchenko

Oregon State University, Department of Botany and Plant Pathology, 2082 Cordley Hall, Corvallis, OR 97331, USA

B

Bangjun Wang

University of Fribourg, Department of Biology – Plant Biology, CH-1700 Fribourg, Switzerland; School of Life Sciences, Southwest University, Chongqing 400715, China

E

Eva Medvecká

Institute of Science and Technology Austria, Am Campus 1, Klosterneuburg A-3400, Austria

Y

Yunlong Du

VIB Department of Plant Systems Biology and Department of Plant Biotechnology and Genetics, Ghent University, Gent 9052, Belgium; Key Laboratory of Agro-biodiversity and Pest Management of Education Ministry of China, Yunnan Agricultural University, Kunming 650201, China

E

Elisa Azzarello

LINV–DIPSAA–Università di Firenze, Viale delle idee 30, Sesto Fiorentino 50019, Italy

S

Stefano Mancuso

LINV–DIPSAA–Università di Firenze, Viale delle idee 30, Sesto Fiorentino 50019, Italy

M

Molly Megraw

Oregon State University, Department of Botany and Plant Pathology, 2082 Cordley Hall, Corvallis, OR 97331, USA

S

Sergei Filichkin

Oregon State University, Department of Botany and Plant Pathology, 2082 Cordley Hall, Corvallis, OR 97331, USA

J

Joseph G. Dubrovsky

Universidad Nacional Autónoma de México, Instituto de Biotecnología, Departamento de Biología Molecular de Plantas, Apartado Postal 510-3, 62210 Cuernavaca, Morelos, México

J

Jiří Friml

Institute of Science and Technology Austria, Am Campus 1, Klosterneuburg A-3400, Austria; VIB Department of Plant Systems Biology and Department of Plant Biotechnology and Genetics, Ghent University, Gent 9052, Belgium

M

Markus Geisler

University of Fribourg, Department of Biology – Plant Biology, CH-1700 Fribourg, Switzerland

Cite This Article

Maria G. Ivanchenko, Bangjun Wang, Eva Medvecká, et al. (2015). The cyclophilin A DIAGEOTROPICA gene affects auxin transport in both root and shoot to control lateral root formation. Development. https://doi.org/10.1242/dev.113225

The cyclophilin A DIAGEOTROPICA gene affects auxin transport in both root and shoot to control lateral root formation

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