2.A.69 The Auxin Efflux Carrier (AEC) Family

Plants possess tissue-specific, pmf-driven, cellular, auxin efflux systems. These carriers are saturable, auxin-specific, and localized to the basal ends of auxin transport-competent cells. They may be found in various plant tissues including vascular tissues and roots. They are responsible for the polar (downwards) transport of auxins from the leaves to the roots. They also function in gravitropism. In fact, gravity-dependent relocation of auxin efflux carriers has been demonstrated (Ottenschläger et al., 2003). A single plant such as Arabidopsis thaliana possesses at least six such systems. Two isoforms in A. thaliana, one in vascular tissue (PIN1) and one in roots (REH1 or EIR1) have been functionally characterized as have homologues from Oryza sativa. These plant proteins are 600-700 amino acyl residues long and exhibit 8-12 transmembrane spanners.

The rate of auxin transport across the plasma membrane is regulated by the Auxin Binding Protein 1, ABP1, which influcences PIN activity at the plasma membrane (Čovanová et al. 2013).  This highlights the relevance of ABP1 for the formation of developmentally important, PIN-dependent auxin gradients.

Homologues of the AEC family are found in bacteria (E. coli, Klebsiella pneumoniae, Synechocystis, Aquifex aeolicus, Bacillus subtilis and Rickettsia prowazekii) as well as in archaea (Methanococcus jannaschii and Methanobacterium thermoautotrophicum.) The K. pneumoniae homologues (MdcF, 319 aas) has been implicated in malonate uptake. The O. oeni homologue, MleP, is a malate permease. The bacterial proteins are 300-400 aas in length (Young et al. 1999).

Yeast also possess homologues of the AEC family. Saccharomyces cerevisiae has three functionally uncharacterized AEC members (YL52, spP54072, 64.0 kDa; YNJ5, spP53930, 71.2 kDa; and YB8B, spP38355, 47.5 kDa), and Schizosaccharomyces pombe also has a sequenced homologue. It is thus clear that members of the AEC family are widespread, being found in Gram-negative, Gram-positive and cyanobacteria, in archaea, and in both fungi and plants. C. elegans, however, appears to lack identifiable homologues of the AEC family (Young et al. 1999).

Members of the AEC family are homologous to members of the BART superfamily (Mansour et al. 2007). Interestingly, the first halves of BASS family (TC# 2.A.28) members show extensive similarity with the second halves of AEC family members but not vice versa. Repeats of the basic 5 TMS element have not yet been demonstrated in members of the AEC family. 

The transport reaction probably catalyzed by the auxin efflux carrier is:

Auxin (in)  nH+ (out) → Auxin (out) nH+ (in)

This family belongs to the BART Superfamily.



Čovanová, M., M. Sauer, J. Rychtář, J. Friml, J. Petrášek, and E. Zažímalová. (2013). Overexpression of the auxin binding protein1 modulates PIN-dependent auxin transport in tobacco cells. PLoS One 8: e70050.

Carraro, N., T.E. Tisdale-Orr, R.M. Clouse, A.S. Knöller, and R. Spicer. (2012). Diversification and Expression of the PIN, AUX/LAX, and ABCB Families of Putative Auxin Transporters in Populus. Front Plant Sci 3: 17.

Costantini, A., E. Vaudano, K. Rantsiou, L. Cocolin, and E. Garcia-Moruno. (2011). Quantitative expression analysis of mleP gene and two genes involved in the ABC transport system in Oenococcus oeni during rehydration. Appl. Microbiol. Biotechnol. 91: 1601-1609.

Dueñas, E., C.R. Vazquez de Aldana, T. de Cos, C. Castro, and M. Henar Valdivieso. (1999). Generation of null alleles for the functional analysis of six genes from the right arm of Saccharomyces cerevisiae chromosome II. Yeast 15: 615-623.

Fiegler, H., J. Bassias, I. Jankovic, and R. Brückner. (1999). Identification of a gene in Staphylococcus xylosus encoding a novel glucose uptake protein. J. Bacteriol. 181: 4929-4936.

Friml, J., A. Vieten, M. Sauer, D. Weijers, H. Schwarz, T. Hamann, R. Offringa, and G. Jürgens. (2003). Efflux-dependent auxin gradients establish the apical-basal axis of Arabisopsis. Nature 426: 147-153.

Gälweiler, L., C. Guan, A. Müller, E. Wisman, K. Mendgen, A. Yephremov, and K. Palme. (1998). Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282: 2226-2230.

Hoenke, S., M. Schmid, and P. Dimroth. (1997). Sequence of a gene cluster from Klebsiella pneumoniae encoding malonate decarboxylase and expression of the enzyme in Escherichia coli. Eur. J. Biochem. 246: 530-538.

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Labarre, C., C. Divies, and J. Guzzo. (1996a). Genetic organization of the mle locus and identification of a mleR-like gene from Leuconostoc oenos. Appl. Env. Microbiol. 62: 4493-4498.

Labarre, C., J. Guzzo, J.F. Cavin, and C. Diviès. (1996). Cloning and characterization of the genes encoding the malolactic enzyme and the malate permease of Leuconostoc oenos. Appl. Environ. Microbiol. 62: 1274-1282.

Li, Y.L., Y.S. Lin, P.L. Huang, and Y.Y. Do. (2017). Two Paralogous Genes Encoding Auxin Efflux Carrier Differentially Expressed in Bitter Gourd (Momordica charantia). Int J Mol Sci 18:.

Luschnig, C., R.A. Gaxiola, P. Grisafi, and G.R. Fink. (1998). EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev. 12: 2175-2187.

Mansour, N.M., M. Sawhney, D.G. Tamang, C. Vogl, and M.H. Saier, Jr. (2007). The bile/arsenite/riboflavin transporter (BART) superfamily. FEBS J. 274: 612-629.

Mravec, J., P. Skůpa, A. Bailly, K. Hoyerová, P. Krecek, A. Bielach, J. Petrásek, J. Zhang, V. Gaykova, Y.D. Stierhof, P.I. Dobrev, K. Schwarzerová, J. Rolcík, D. Seifertová, C. Luschnig, E. Benková, E. Zazímalová, M. Geisler, and J. Friml. (2009). Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter. Nature 459: 1136-1140.

Nodzyński, T., S. Vanneste, M. Zwiewka, M. Pernisová, J. Hejátko, and J. Friml. (2016). Enquiry into the topology of plasma membrane localized PIN auxin transport components. Mol Plant. [Epub: Ahead of Print]

Ottenschläger, I., P. Wolff, C. Wolverton, R.P. Bhalerao, G. Sandberg, H. Ishikawa, M. Evans, and K. Palme. (2003). Gravity-regulated differential auxin transport from columella to lateral root cap cells. Proc. Natl. Acad. Sci. USA 100: 2987-2991.

Petrasek, J., J. Mravec, R. Bouchard, J.J. Blakeslee, M. Abas, D. Seifertova, J. Wisniewska, Z. Tadele, M. Kubes, M. Covanova, P. Dhonukshe, P. Skupa, E. Benkova, L. Perry, P. Krecek, O.R. Lee, G.R. Fink, M. Geisler, A.S. Murphy, C. Luschnig, E. Zazimalova, and J. Friml. (2006). PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312: 914-918.

Reinhardt, D., E.-R. Pesce, P. Stieger, T. Mandel, K. Baltensperger, M. Bennett, J. Traas, J. Friml, and C. Kuhlemeier. (2003). Regulation of phyllotaxis by polar auxin transport. Nature 426: 255-260.

Wang, P., T. Cheng, S. Wu, F. Zhao, G. Wang, L. Yang, M. Lu, J. Chen, and J. Shi. (2014). Phylogeny and Molecular Evolution Analysis of PIN-FORMED 1 in Angiosperm. PLoS One 9: e89289.

Watson, M.D. (2001). Disruption and basic phenotypic analysis of six novel genes from the right arm of chromosome XII of Saccharomyces cerevisiae. Yeast 18: 473-480.

Young, G.B., D.L. Jack, D.W. Smith, and M.H. Saier, Jr. (1999). The amino acid/auxin:proton symport permease family. Biochim. Biophys. Acta. 1415: 306-322.

Zhou, C., L. Han, and Z.Y. Wang. (2011). Potential but limited redundant roles of MtPIN4, MtPIN5 and MtPIN10/SLM1 in the development of Medicago truncatula. Plant Signal Behav 6: 1834-1836.


TC#NameOrganismal TypeExample

Auxin efflux carrier, PIN-FORMED 1 (PIN1) (Reinhardt et al., 2003; Carraro et al. 2012). Catalyzes auxin efflux without the participation of any other protein (Petrasek et al., 2006).  PIN1 determines the direction of intercellular auxin flow (Wang et al. 2014). It consists of two TMS bundles, each of 5 TMSs (Nodzyński et al. 2016), confirming previous bioinformatic predictions (Mansour et al. 2007).


PIN1 of Arabidopsis thaliana

2.A.69.1.2Auxin transporter, ethylene-insensitive root 1 (EIR1) auxin:H+ symporter Plants EIR1 of Arabidopsis thaliana
2.A.69.1.3Auxin efflux carrier, PIN7 (promotes embryonic axis formation) (Friml et al., 2003)PlantsPIN7 of Arabidopsis thaliana (NP_849923)
2.A.69.1.4Auxin efflux facilitator PIN3: functions in auxin redistribution through the root cap in response to the gravity sensors, ARL2 (Q6XL73) and ARG1 (Q9ZSY2). Both ARG1 and ARL2 are DnaJ homologues and show regions homologous to translocation proteins, NPL1 and Sec63 (3.A.5.8.1 and 3.A.5.9.1, respectively.)PlantsPIN3 of Arabidopsis thaliana

Auxin efflux carrier #10, PIN10/SLM1 (important for development; orthologous to A. thaliana PIN1 (Zhou et al., 2011)).


PIN10 of Medicago truncatula (Q673E5)

2.A.69.1.6Putative auxin efflux carrier component 8 (AtPIN8)PlantsPIN8 of Arabidopsis thaliana

Auxin efflux carrier, PIN5.  Regulates auxin homeostasis and metabolism.  Mediates auxin transport across the endoplasmic reticular membrane, for the cytosol to the ER lumen (Mravec et al. 2009).


PIN5 of Arabidopsis thaliana


The auxin efflux carrier, AEC3 or PIN1, of 634 aas and 10 TMSs, plays a role in fruit development (Li et al. 2017).

AEC3 of Momordica charantia (bitter gourd)


TC#NameOrganismal TypeExample

AEC family member


AEC family member of Trypanosoma cruzi (E7LII7)


Poorly characterized transporter YBR287w.  Deletion of the gene leads to poor growth on glucose-minimal medium at 15 degrees C in the FY 1679 genetic background, but is not involved in mating or sporulation (Dueñas et al. 1999).  


YBR287w of Saccharomyces cerevisiae


Auxin efflux carrier family member


AEC homologue of Aspergillus flavus (B8MZ51)


AEC family member


AEC family member of Entamoeba histolytica (C4MAS5)


Uncharacterized protein of 616 aas and 11 TMSs in a 5 + 6 arrangement

Rhodophyta (red algae)

UP of Cyanidioschyzon merolae


Uncharacterized transporter, nonessential for growth or sporulation, YLR152c, of 576 aas and 10 TMSs (Watson 2001).

UP of Saccharomyces cerevisiae


Uncharacterized protein of 442 aas and 10 TMSs in a 5 + 5 TMS arrangement.

UP of Citrus clementina


TC#NameOrganismal TypeExample

AEC homologue


AEC homologue of Streptomyces coelicolor


Malate transporter (MleP) homologue


MleP homologue of Dickeya dadantii (E0SFK1)

2.A.69.3.3Putative malonate transporter, MdcF Bacteria MdcF of Klebsiella pneumoniae

Putative malonate transporter, MdcF


MdcF of Rhizobium meliloti

2.A.69.3.5Uncharacterized transporter YfdV


YfdV of Escherichia coli O6:H1


Putative MdcF malonate transporter of 316 aas and 10 TMSs.


MdcF homologue of Rhizobium loti


TC#NameOrganismal TypeExample

Putative membrane permease-like protein. May belong to the BART superfamily (297aas; 10TMS)


permease-like protein of Chlorobium luteolum (Q3B5D8)

2.A.69.4.2Uncharacterized transporter MJ1031ArchaeaMJ1031 of Methanocaldococcus jannaschii
2.A.69.4.3Uncharacterized transporter MTH_1382


MTH_1382 of Methanothermobacter thermautotrophicus

AEC homologue


AEC homologue of Myxococcus xanthus


Malate permease, MleP (Labarre et al. 1996). Activated a few minutes after rehydration (Costantini et al. 2011).


MleP of Oenococcus (Leuconostoc) oeni


Putative auxin efflux carrier of 333 aas and 10 TMSs.

Auxin efflux carrier of Bifidobacterium longum


Uncharacterized protein of 308 aas and 10 TMSs (Hug et al. 2016).

UP of Candidatus Peribacter riflensis


Uncharacterized protein of 388 aas and 10 TMSs in a 5 + 5 TMS arrangement.

UP of Entamoeba histolytica