ABCB19/PGP19 stabilises PIN1 in membrane microdomains in Arabidopsis

Boosaree Titapiwatanakun, Joshua J. Blakeslee, Anindita Bandyopadhyay, Haibing Yang, Jozef Mravec, Michael Sauer, Yan Cheng, Jiri Adamec, Akitomo Nagashima, Markus Geisler, Tatsuya Sakai, Jiri Friml, Wendy Ann Peer, Angus S. Murphy

Research output: Contribution to journalArticle

159 Citations (Scopus)

Abstract

Auxin transport is mediated at the cellular level by three independent mechanisms that are characterised by the PIN-formed (PIN), P-glycoprotein (ABCB/PGP) and AUX/LAX transport proteins. The PIN and ABCB transport proteins, best represented by PIN1 and ABCB19 (PGP19), have been shown to coordinately regulate auxin efflux. When PIN1 and ABCB19 coincide on the plasma membrane, their interaction enhances the rate and specificity of auxin efflux and the dynamic cycling of PIN1 is reduced. However, ABCB19 function is not regulated by the dynamic cellular trafficking mechanisms that regulate PIN1 in apical tissues, as localisation of ABCB19 on the plasma membrane was not inhibited by short-term treatments with latrunculin B, oryzalin, brefeldin A (BFA) or wortmannin - all of which have been shown to alter PIN1 and/or PIN2 plasma membrane localisation. When taken up by endocytosis, the styryl dye FM4-64 labels diffuse rather than punctuate intracellular bodies in abcb19 (pgp19), and some aggregations of PIN1 induced by short-term BFA treatment did not disperse after BFA washout in abcb19. Although the subcellular localisations of ABCB19 and PIN1 in the reciprocal mutant backgrounds were like those in wild type, PIN1 plasma membrane localisation in abcb19 roots was more easily perturbed by the detergent Triton X-100, but not other non-ionic detergents. ABCB19 is stably associated with sterol/sphingolipid-enriched membrane fractions containing BIG/TIR3 and partitions into Triton X-100 detergent-resistant membrane (DRM) fractions. In the wild type, PIN1 was also present in DRMs, but was less abundant in abcb19 DRMs. These observations suggested a rationale for the observed lack of auxin transport activity when PIN1 is expressed in a non-plant heterologous system. PIN1 was therefore expressed in Schizosaccharomyces pombe, which has plant-like sterol-enriched microdomains, and catalysed auxin transport in these cells. These data suggest that ABCB19 stabilises PIN1 localisation at the plasma membrane in discrete cellular subdomains where PIN1 and ABCB19 expression overlaps.

Original languageEnglish (US)
Pages (from-to)27-44
Number of pages18
JournalPlant Journal
Volume57
Issue number1
DOIs
StatePublished - Jan 1 2009

Fingerprint

Membrane Microdomains
Indoleacetic Acids
Arabidopsis
auxins
brefeldin A
Brefeldin A
plasma membrane
Cell Membrane
detergents
Detergents
Octoxynol
transport proteins
sterols
Carrier Proteins
oryzalin
Phytosterols
sphingolipids
Sphingolipids
Membranes
Schizosaccharomyces

Keywords

  • Auxin transport
  • Detergent-resistant membrane
  • Lipid raft
  • Multi-drug resistance protein
  • P-glycoprotein
  • PIN1
  • Trafficking

ASJC Scopus subject areas

  • Genetics
  • Plant Science
  • Cell Biology

Cite this

Titapiwatanakun, B., Blakeslee, J. J., Bandyopadhyay, A., Yang, H., Mravec, J., Sauer, M., ... Murphy, A. S. (2009). ABCB19/PGP19 stabilises PIN1 in membrane microdomains in Arabidopsis. Plant Journal, 57(1), 27-44. https://doi.org/10.1111/j.1365-313X.2008.03668.x

ABCB19/PGP19 stabilises PIN1 in membrane microdomains in Arabidopsis. / Titapiwatanakun, Boosaree; Blakeslee, Joshua J.; Bandyopadhyay, Anindita; Yang, Haibing; Mravec, Jozef; Sauer, Michael; Cheng, Yan; Adamec, Jiri; Nagashima, Akitomo; Geisler, Markus; Sakai, Tatsuya; Friml, Jiri; Peer, Wendy Ann; Murphy, Angus S.

In: Plant Journal, Vol. 57, No. 1, 01.01.2009, p. 27-44.

Research output: Contribution to journalArticle

Titapiwatanakun, B, Blakeslee, JJ, Bandyopadhyay, A, Yang, H, Mravec, J, Sauer, M, Cheng, Y, Adamec, J, Nagashima, A, Geisler, M, Sakai, T, Friml, J, Peer, WA & Murphy, AS 2009, 'ABCB19/PGP19 stabilises PIN1 in membrane microdomains in Arabidopsis', Plant Journal, vol. 57, no. 1, pp. 27-44. https://doi.org/10.1111/j.1365-313X.2008.03668.x
Titapiwatanakun B, Blakeslee JJ, Bandyopadhyay A, Yang H, Mravec J, Sauer M et al. ABCB19/PGP19 stabilises PIN1 in membrane microdomains in Arabidopsis. Plant Journal. 2009 Jan 1;57(1):27-44. https://doi.org/10.1111/j.1365-313X.2008.03668.x
Titapiwatanakun, Boosaree ; Blakeslee, Joshua J. ; Bandyopadhyay, Anindita ; Yang, Haibing ; Mravec, Jozef ; Sauer, Michael ; Cheng, Yan ; Adamec, Jiri ; Nagashima, Akitomo ; Geisler, Markus ; Sakai, Tatsuya ; Friml, Jiri ; Peer, Wendy Ann ; Murphy, Angus S. / ABCB19/PGP19 stabilises PIN1 in membrane microdomains in Arabidopsis. In: Plant Journal. 2009 ; Vol. 57, No. 1. pp. 27-44.
@article{8329e01680d347db835cd0f6892325e3,
title = "ABCB19/PGP19 stabilises PIN1 in membrane microdomains in Arabidopsis",
abstract = "Auxin transport is mediated at the cellular level by three independent mechanisms that are characterised by the PIN-formed (PIN), P-glycoprotein (ABCB/PGP) and AUX/LAX transport proteins. The PIN and ABCB transport proteins, best represented by PIN1 and ABCB19 (PGP19), have been shown to coordinately regulate auxin efflux. When PIN1 and ABCB19 coincide on the plasma membrane, their interaction enhances the rate and specificity of auxin efflux and the dynamic cycling of PIN1 is reduced. However, ABCB19 function is not regulated by the dynamic cellular trafficking mechanisms that regulate PIN1 in apical tissues, as localisation of ABCB19 on the plasma membrane was not inhibited by short-term treatments with latrunculin B, oryzalin, brefeldin A (BFA) or wortmannin - all of which have been shown to alter PIN1 and/or PIN2 plasma membrane localisation. When taken up by endocytosis, the styryl dye FM4-64 labels diffuse rather than punctuate intracellular bodies in abcb19 (pgp19), and some aggregations of PIN1 induced by short-term BFA treatment did not disperse after BFA washout in abcb19. Although the subcellular localisations of ABCB19 and PIN1 in the reciprocal mutant backgrounds were like those in wild type, PIN1 plasma membrane localisation in abcb19 roots was more easily perturbed by the detergent Triton X-100, but not other non-ionic detergents. ABCB19 is stably associated with sterol/sphingolipid-enriched membrane fractions containing BIG/TIR3 and partitions into Triton X-100 detergent-resistant membrane (DRM) fractions. In the wild type, PIN1 was also present in DRMs, but was less abundant in abcb19 DRMs. These observations suggested a rationale for the observed lack of auxin transport activity when PIN1 is expressed in a non-plant heterologous system. PIN1 was therefore expressed in Schizosaccharomyces pombe, which has plant-like sterol-enriched microdomains, and catalysed auxin transport in these cells. These data suggest that ABCB19 stabilises PIN1 localisation at the plasma membrane in discrete cellular subdomains where PIN1 and ABCB19 expression overlaps.",
keywords = "Auxin transport, Detergent-resistant membrane, Lipid raft, Multi-drug resistance protein, P-glycoprotein, PIN1, Trafficking",
author = "Boosaree Titapiwatanakun and Blakeslee, {Joshua J.} and Anindita Bandyopadhyay and Haibing Yang and Jozef Mravec and Michael Sauer and Yan Cheng and Jiri Adamec and Akitomo Nagashima and Markus Geisler and Tatsuya Sakai and Jiri Friml and Peer, {Wendy Ann} and Murphy, {Angus S.}",
year = "2009",
month = "1",
day = "1",
doi = "10.1111/j.1365-313X.2008.03668.x",
language = "English (US)",
volume = "57",
pages = "27--44",
journal = "Plant Journal",
issn = "0960-7412",
publisher = "Wiley-Blackwell",
number = "1",

}

TY - JOUR

T1 - ABCB19/PGP19 stabilises PIN1 in membrane microdomains in Arabidopsis

AU - Titapiwatanakun, Boosaree

AU - Blakeslee, Joshua J.

AU - Bandyopadhyay, Anindita

AU - Yang, Haibing

AU - Mravec, Jozef

AU - Sauer, Michael

AU - Cheng, Yan

AU - Adamec, Jiri

AU - Nagashima, Akitomo

AU - Geisler, Markus

AU - Sakai, Tatsuya

AU - Friml, Jiri

AU - Peer, Wendy Ann

AU - Murphy, Angus S.

PY - 2009/1/1

Y1 - 2009/1/1

N2 - Auxin transport is mediated at the cellular level by three independent mechanisms that are characterised by the PIN-formed (PIN), P-glycoprotein (ABCB/PGP) and AUX/LAX transport proteins. The PIN and ABCB transport proteins, best represented by PIN1 and ABCB19 (PGP19), have been shown to coordinately regulate auxin efflux. When PIN1 and ABCB19 coincide on the plasma membrane, their interaction enhances the rate and specificity of auxin efflux and the dynamic cycling of PIN1 is reduced. However, ABCB19 function is not regulated by the dynamic cellular trafficking mechanisms that regulate PIN1 in apical tissues, as localisation of ABCB19 on the plasma membrane was not inhibited by short-term treatments with latrunculin B, oryzalin, brefeldin A (BFA) or wortmannin - all of which have been shown to alter PIN1 and/or PIN2 plasma membrane localisation. When taken up by endocytosis, the styryl dye FM4-64 labels diffuse rather than punctuate intracellular bodies in abcb19 (pgp19), and some aggregations of PIN1 induced by short-term BFA treatment did not disperse after BFA washout in abcb19. Although the subcellular localisations of ABCB19 and PIN1 in the reciprocal mutant backgrounds were like those in wild type, PIN1 plasma membrane localisation in abcb19 roots was more easily perturbed by the detergent Triton X-100, but not other non-ionic detergents. ABCB19 is stably associated with sterol/sphingolipid-enriched membrane fractions containing BIG/TIR3 and partitions into Triton X-100 detergent-resistant membrane (DRM) fractions. In the wild type, PIN1 was also present in DRMs, but was less abundant in abcb19 DRMs. These observations suggested a rationale for the observed lack of auxin transport activity when PIN1 is expressed in a non-plant heterologous system. PIN1 was therefore expressed in Schizosaccharomyces pombe, which has plant-like sterol-enriched microdomains, and catalysed auxin transport in these cells. These data suggest that ABCB19 stabilises PIN1 localisation at the plasma membrane in discrete cellular subdomains where PIN1 and ABCB19 expression overlaps.

AB - Auxin transport is mediated at the cellular level by three independent mechanisms that are characterised by the PIN-formed (PIN), P-glycoprotein (ABCB/PGP) and AUX/LAX transport proteins. The PIN and ABCB transport proteins, best represented by PIN1 and ABCB19 (PGP19), have been shown to coordinately regulate auxin efflux. When PIN1 and ABCB19 coincide on the plasma membrane, their interaction enhances the rate and specificity of auxin efflux and the dynamic cycling of PIN1 is reduced. However, ABCB19 function is not regulated by the dynamic cellular trafficking mechanisms that regulate PIN1 in apical tissues, as localisation of ABCB19 on the plasma membrane was not inhibited by short-term treatments with latrunculin B, oryzalin, brefeldin A (BFA) or wortmannin - all of which have been shown to alter PIN1 and/or PIN2 plasma membrane localisation. When taken up by endocytosis, the styryl dye FM4-64 labels diffuse rather than punctuate intracellular bodies in abcb19 (pgp19), and some aggregations of PIN1 induced by short-term BFA treatment did not disperse after BFA washout in abcb19. Although the subcellular localisations of ABCB19 and PIN1 in the reciprocal mutant backgrounds were like those in wild type, PIN1 plasma membrane localisation in abcb19 roots was more easily perturbed by the detergent Triton X-100, but not other non-ionic detergents. ABCB19 is stably associated with sterol/sphingolipid-enriched membrane fractions containing BIG/TIR3 and partitions into Triton X-100 detergent-resistant membrane (DRM) fractions. In the wild type, PIN1 was also present in DRMs, but was less abundant in abcb19 DRMs. These observations suggested a rationale for the observed lack of auxin transport activity when PIN1 is expressed in a non-plant heterologous system. PIN1 was therefore expressed in Schizosaccharomyces pombe, which has plant-like sterol-enriched microdomains, and catalysed auxin transport in these cells. These data suggest that ABCB19 stabilises PIN1 localisation at the plasma membrane in discrete cellular subdomains where PIN1 and ABCB19 expression overlaps.

KW - Auxin transport

KW - Detergent-resistant membrane

KW - Lipid raft

KW - Multi-drug resistance protein

KW - P-glycoprotein

KW - PIN1

KW - Trafficking

UR - http://www.scopus.com/inward/record.url?scp=58149117560&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=58149117560&partnerID=8YFLogxK

U2 - 10.1111/j.1365-313X.2008.03668.x

DO - 10.1111/j.1365-313X.2008.03668.x

M3 - Article

C2 - 18774968

AN - SCOPUS:58149117560

VL - 57

SP - 27

EP - 44

JO - Plant Journal

JF - Plant Journal

SN - 0960-7412

IS - 1

ER -