Auxin-transporting ABC transporters are defined by a conserved D/E-P motif regulated by a prolylisomerase

Pengchao Hao; Jian Xia; Jie Liu; Martin Di Donato; Konrad Pakula; Aurélien Bailly; Michal Jasinski; Markus Geisler

doi:10.1074/jbc.RA120.014104

Auxin-transporting ABC transporters are defined by a conserved D/E-P motif regulated by a prolylisomerase

J Biol Chem. 2020 Sep 11;295(37):13094-13105. doi: 10.1074/jbc.RA120.014104. Epub 2020 Jul 22.

Authors

Pengchao Hao¹, Jian Xia¹, Jie Liu¹, Martin Di Donato¹, Konrad Pakula², Aurélien Bailly³, Michal Jasinski⁴, Markus Geisler⁵

Affiliations

¹ Department of Biology, University of Fribourg, Fribourg, Switzerland.
² Department of Plant Molecular Physiology, Institute of Bioorganic Chemistry, Polish Academy of Sciences, Poznan, Poland; NanoBioMedical Centre, Adam Mickiewicz University, Poznan, Poland.
³ Institute for Plant and Microbial Biology, Zurich, Switzerland.
⁴ Department of Plant Molecular Physiology, Institute of Bioorganic Chemistry, Polish Academy of Sciences, Poznan, Poland; Department of Biochemistry and Biotechnology, Poznan University of Life Sciences, Poznan, Poland.
⁵ Department of Biology, University of Fribourg, Fribourg, Switzerland. Electronic address: markus.geisler@unifr.ch.

Abstract

The plant hormone auxin must be transported throughout plants in a cell-to-cell manner to affect its various physiological functions. ABCB transporters are critical for this polar auxin distribution, but the regulatory mechanisms controlling their function is not fully understood. The auxin transport activity of ABCB1 was suggested to be regulated by a physical interaction with FKBP42/Twisted Dwarf1 (TWD1), a peptidylprolyl cis-trans isomerase (PPIase), but all attempts to demonstrate such a PPIase activity by TWD1 have failed so far. By using a structure-based approach, we identified several surface-exposed proline residues in the nucleotide binding domain and linker of Arabidopsis ABCB1, mutations of which do not alter ABCB1 protein stability or location but do affect its transport activity. P1008 is part of a conserved signature D/E-P motif that seems to be specific for auxin-transporting ABCBs, which we now refer to as ATAs. Mutation of the acidic residue also abolishes auxin transport activity by ABCB1. All higher plant ABCBs for which auxin transport has been conclusively proven carry this conserved motif, underlining its predictive potential. Introduction of this D/E-P motif into malate importer, ABCB14, increases both its malate and its background auxin transport activity, suggesting that this motif has an impact on transport capacity. The D/E-P1008 motif is also important for ABCB1-TWD1 interactions and activation of ABCB1-mediated auxin transport by TWD1. In summary, our data imply a new function for TWD1 acting as a putative activator of ABCB-mediated auxin transport by cis-trans isomerization of peptidyl-prolyl bonds.

Keywords: ABC transporter; ABCB; FKBP; PPIase; Twisted Dwarf1; auxin; auxin transport; membrane transport; plant biochemistry; post-transcriptional regulation.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

ATP Binding Cassette Transporter, Subfamily B, Member 1* / chemistry
ATP Binding Cassette Transporter, Subfamily B, Member 1* / genetics
ATP Binding Cassette Transporter, Subfamily B, Member 1* / metabolism
Amino Acid Motifs
Nicotiana* / chemistry
Nicotiana* / genetics
Nicotiana* / metabolism
Peptidylprolyl Isomerase* / chemistry
Peptidylprolyl Isomerase* / genetics
Peptidylprolyl Isomerase* / metabolism
Plant Proteins* / chemistry
Plant Proteins* / genetics
Plant Proteins* / metabolism
Tacrolimus Binding Proteins* / chemistry
Tacrolimus Binding Proteins* / genetics
Tacrolimus Binding Proteins* / metabolism

Substances

ATP Binding Cassette Transporter, Subfamily B, Member 1
Plant Proteins
Tacrolimus Binding Proteins
Peptidylprolyl Isomerase

Associated data

PDB/3G5U
PDB/5TSI