The proper distribution of the hormone auxin is essential for plant development. It is channeled by auxin efflux carriers of the PIN family, typically asymmetrically located on the plasma membrane (PM). Several studies demonstrated that some PIN transporters are also located at the endoplasmic reticulum (ER). From the PM-PINs, they differ in a shorter internal hydrophilic loop, which carries the most important structural features required for their subcellular localization, but their biological role is otherwise relatively poorly known. We discuss how ER-PINs take part in maintaining intracellular auxin homeostasis, possibly by modulating the internal levels of IAA; it seems that the exact identity of the metabolites downstream of ER-PINs is not entirely clear as well. We further review the current knowledge about their predicted structure, evolution and localization. Finally, we also summarize their role in plant development.

Department of Experimental Plant Biology Faculty of Science Charles University 12844 Prague Czech Republic

Laboratory of Hormonal Regulations in Plants Institute of Experimental Botany Czech Academy of Sciences 16502 Prague Czech Republic

Zobrazit více v PubMed

Zažímalová E., Petrášek J., Benková E., editors. Auxin and Its Role in Plant Development. Springer; Vienna, Austria: 2014.

Bielach A., Hrtyan M., Tognetti V.B. Plants under Stress: Involvement of Auxin and Cytokinin. Int. J. Mol. Sci. 2017;18:1427. doi: 10.3390/ijms18071427. PubMed DOI PMC

Zwiewka M., Bilanovičová V., Seifu Y.W., Nodzyński T. The Nuts and Bolts of PIN Auxin Efflux Carriers. Front. Plant Sci. 2019;10 doi: 10.3389/fpls.2019.00985. PubMed DOI PMC

Barbez E., Kleine-Vehn J. Divide Et Impera—cellular auxin compartmentalization. Curr. Opin. Plant Biol. 2013;16:78–84. doi: 10.1016/j.pbi.2012.10.005. PubMed DOI

Petrasek J., Friml J. Auxin transport routes in plant development. Development. 2009;136:2675–2688. doi: 10.1242/dev.030353. PubMed DOI

Geisler M., Aryal B., di Donato M., Hao P. A Critical View on ABC Transporters and Their Interacting Partners in Auxin Transport. Plant Cell Physiol. 2017;58:1601–1614. doi: 10.1093/pcp/pcx104. PubMed DOI

Krouk G., Lacombe B., Bielach A., Perrine-Walker F., Malinska K., Mounier E., Hoyerova K., Tillard P., Leon S., Ljung K., et al. Nitrate-Regulated Auxin Transport by NRT1.1 Defines a Mechanism for Nutrient Sensing in Plants. Dev. Cell. 2010;18:927–937. doi: 10.1016/j.devcel.2010.05.008. PubMed DOI

Swarup R., Friml J., Marchant A., Ljung K., Sandberg G., Palme K., Bennett M. Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. Genes Dev. 2001;15:2648–2653. doi: 10.1101/gad.210501. PubMed DOI PMC

Ranocha P., Dima O., Nagy R., Felten J., Corratgé-Faillie C., Novák O., Morreel K., Lacombe B., Martinez Y., Pfrunder S., et al. Arabidopsis WAT1 is a vacuolar auxin transport facilitator required for auxin homoeostasis. Nat. Commun. 2013;4:2625. doi: 10.1038/ncomms3625. PubMed DOI PMC

Barbez E., Kubeš M., Rolčík J., Béziat C., Pěnčík A., Wang B., Rosquete M.R., Zhu J., Dobrev P.I., Lee Y., et al. A novel putative auxin carrier family regulates intracellular auxin homeostasis in plants. Nature. 2012;485:119–122. doi: 10.1038/nature11001. PubMed DOI

Béziat C., Barbez E., Feraru M.I., Lucyshyn D., Kleine-Vehn J. Light triggers PILS-dependent reduction in nuclear auxin signalling for growth transition. Nat. Plants. 2017;3:1–9. doi: 10.1038/nplants.2017.105. PubMed DOI PMC

Mravec J., Skůpa P., Bailly A., Hoyerová K., Krecek P., Bielach A., Petrásek J., Zhang J., Gaykova V., Stierhof Y.-D., et al. Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter. Nature. 2009;459:1136–1140. doi: 10.1038/nature08066. PubMed DOI

Ding Z., Wang B., Moreno I., Dupláková N., Simon S., Carraro N., Reemmer J., Pěnčík A., Chen X., Tejos R., et al. ER-localized auxin transporter PIN8 regulates auxin homeostasis and male gametophyte development in Arabidopsis. Nat. Commun. 2012;3:941. doi: 10.1038/ncomms1941. PubMed DOI

Simon S., Skůpa P., Viaene T., Zwiewka M., Tejos R., Klíma P., Čarná M., Rolčík J., Rycke R.D., Moreno I., et al. PIN6 auxin transporter at endoplasmic reticulum and plasma membrane mediates auxin homeostasis and organogenesis in Arabidopsis. New Phytol. 2016;211:65–74. doi: 10.1111/nph.14019. PubMed DOI

Barbosa I.C.R., Hammes U.Z., Schwechheimer C. Activation and Polarity Control of PIN-FORMED Auxin Transporters by Phosphorylation. Trends Plant Sci. 2018;23:523–538. doi: 10.1016/j.tplants.2018.03.009. PubMed DOI

Adamowski M., Friml J. PIN-Dependent Auxin Transport: Action, Regulation, and Evolution. Plant Cell. 2015;27:20–32. doi: 10.1105/tpc.114.134874. PubMed DOI PMC

Kumar S., Stecher G., Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol. Biol. Evol. 2016;33:1870–1874. doi: 10.1093/molbev/msw054. PubMed DOI PMC

Skokan R., Medvecká E., Viaene T., Vosolsobě S., Zwiewka M., Müller K., Skůpa P., Karady M., Zhang Y., Janacek D.P., et al. PIN-driven auxin transport emerged early in streptophyte evolution. Nat. Plants. 2019;5:1114–1119. doi: 10.1038/s41477-019-0542-5. PubMed DOI

Křeček P., Skůpa P., Libus J., Naramoto S., Tejos R., Friml J., Zažímalová E. The PIN-FORMED (PIN) protein family of auxin transporters. Genome Biol. 2009;10:249. doi: 10.1186/gb-2009-10-12-249. PubMed DOI PMC

Nodzyński T., Vanneste S., Zwiewka M., Pernisová M., Hejátko J., Friml J. Enquiry into the Topology of Plasma Membrane-Localized PIN Auxin Transport Components. Mol. Plant. 2016;9:1504–1519. doi: 10.1016/j.molp.2016.08.010. PubMed DOI PMC

Paponov I.A., Teale W.D., Trebar M., Blilou I., Palme K. The PIN auxin efflux facilitators: Evolutionary and functional perspectives. Trends Plant Sci. 2005;10:170–177. doi: 10.1016/j.tplants.2005.02.009. PubMed DOI

Bennett T., Brockington S.F., Rothfels C., Graham S.W., Stevenson D., Kutchan T., Rolf M., Thomas P., Wong G.K.-S., Leyser O., et al. Paralogous Radiations of PIN Proteins with Multiple Origins of Noncanonical PIN Structure. Mol. Biol. Evol. 2014;31:2042–2060. doi: 10.1093/molbev/msu147. PubMed DOI PMC

Ludwig-Müller J. Auxin conjugates: Their role for plant development and in the evolution of land plants. J. Exp. Bot. 2011;62:1757–1773. doi: 10.1093/jxb/erq412. PubMed DOI

Bender R.L., Fekete M.L., Klinkenberg P.M., Hampton M., Bauer B., Malecha M., Lindgren K., Maki J.A., Perera M.A.D.N., Nikolau B.J., et al. PIN6 is required for nectary auxin response and short stamen development. Plant J. 2013;74:893–904. doi: 10.1111/tpj.12184. PubMed DOI

Sawchuk M.G., Edgar A., Scarpella E. Patterning of Leaf Vein Networks by Convergent Auxin Transport Pathways. PLOS Genet. 2013;9:e1003294. doi: 10.1371/journal.pgen.1003294. PubMed DOI PMC

Viaene T., Landberg K., Thelander M., Medvecka E., Pederson E., Feraru E., Cooper E.D., Karimi M., Delwiche C.F., Ljung K., et al. Directional Auxin Transport Mechanisms in Early Diverging Land Plants. Curr. Biol. 2014;24:2786–2791. doi: 10.1016/j.cub.2014.09.056. PubMed DOI

Ganguly A., Lee S.H., Cho M., Lee O.R., Yoo H., Cho H.-T. Differential auxin-transporting activities of PIN-FORMED proteins in Arabidopsis root hair cells. Plant Physiol. 2010;153:1046–1061. doi: 10.1104/pp.110.156505. PubMed DOI PMC

Huang F., Zago M.K., Abas L., van Marion A., Galván-Ampudia C.S., Offringa R. Phosphorylation of Conserved PIN Motifs Directs Arabidopsis PIN1 Polarity and Auxin Transport. Plant Cell. 2010;22:1129–1142. doi: 10.1105/tpc.109.072678. PubMed DOI PMC

Sasayama D., Ganguly A., Park M., Cho H.-T. The M3 phosphorylation motif has been functionally conserved for intracellular trafficking of long-looped PIN-FORMEDs in the Arabidopsis root hair cell. BMC Plant Biol. 2013;13:189. doi: 10.1186/1471-2229-13-189. PubMed DOI PMC

Benschop J.J., Mohammed S., O’Flaherty M., Heck A.J.R., Slijper M., Menke F.L.H. Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis. Mol. Cell Proteomics. 2007;6:1198–1214. doi: 10.1074/mcp.M600429-MCP200. PubMed DOI

Ditengou F.A., Gomes D., Nziengui H., Kochersperger P., Lasok H., Medeiros V., Paponov I.A., Nagy S.K., Nádai T.V., Mészáros T., et al. Characterization of auxin transporter PIN6 plasma membrane targeting reveals a function for PIN6 in plant bolting. New Phytol. 2018;217:1610–1624. doi: 10.1111/nph.14923. PubMed DOI

Ganguly A., Park M., Kesawat M.S., Cho H.-T. Functional Analysis of the Hydrophilic Loop in Intracellular Trafficking of Arabidopsis PIN-FORMED Proteins. Plant Cell. 2014;26:1570–1585. doi: 10.1105/tpc.113.118422. PubMed DOI PMC

Zhang Y., Hartinger C., Wang X., Friml J. Directional auxin fluxes in plants by intramolecular domain–domain coevolution of PIN auxin transporters. New Phytol. 2020;227:1406–1416. doi: 10.1111/nph.16629. PubMed DOI PMC

Hori K., Maruyama F., Fujisawa T., Togashi T., Yamamoto N., Seo M., Sato S., Yamada T., Mori H., Tajima N., et al. Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nat. Commun. 2014;5:3978. doi: 10.1038/ncomms4978. PubMed DOI PMC

Bao Y., Huang X., Rehman M., Wang Y., Wang B., Peng D. Identification and Expression Analysis of the PIN and AUX/LAX Gene Families in Ramie (Boehmeria nivea L. Gaud) Agronomy. 2019;9:435. doi: 10.3390/agronomy9080435. DOI

Lee H., Ganguly A., Lee R.D., Park M., Cho H.-T. Intracellularly Localized PIN-FORMED8 Promotes Lateral Root Emergence in Arabidopsis. Front. Plant Sci. 2020;10 doi: 10.3389/fpls.2019.01808. PubMed DOI PMC

Middleton A.M., Dal Bosco C., Chlap P., Bensch R., Harz H., Ren F., Bergmann S., Wend S., Weber W., Hayashi K.-I., et al. Data-Driven Modeling of Intracellular Auxin Fluxes Indicates a Dominant Role of the ER in Controlling Nuclear Auxin Uptake. Cell Rep. 2018;22:3044–3057. doi: 10.1016/j.celrep.2018.02.074. PubMed DOI

Bennett T.A., Liu M.M., Aoyama T., Bierfreund N.M., Braun M., Coudert Y., Dennis R.J., O’Connor D., Wang X.Y., White C.D., et al. Plasma membrane-targeted PIN proteins drive shoot development in a moss. Curr. Biol. 2014;24:2776–2785. doi: 10.1016/j.cub.2014.09.054. PubMed DOI PMC

Żabka A., Polit J.T., Winnicki K., Paciorek P., Juszczak J., Nowak M., Maszewski J. PIN2-like proteins may contribute to the regulation of morphogenetic processes during spermatogenesis in Chara vulgaris. Plant Cell Rep. 2016;35:1655–1669. doi: 10.1007/s00299-016-1979-x. PubMed DOI PMC

Bennett T. PIN proteins and the evolution of plant development. Trends Plant Sci. 2015;20:498–507. doi: 10.1016/j.tplants.2015.05.005. PubMed DOI

Vosolsobě S., Skokan R., Petrášek J. The evolutionary origins of auxin transport: What we know and what we need to know. J. Exp. Bot. 2020;71:3287–3295. doi: 10.1093/jxb/eraa169. PubMed DOI

Östin A., Kowalyczk M., Bhalerao R.P., Sandberg G. Metabolism of Indole-3-Acetic Acid in Arabidopsis. Plant Physiol. 1998;118:285–296. doi: 10.1104/pp.118.1.285. PubMed DOI PMC

Bosco C.D., Dovzhenko A., Liu X., Woerner N., Rensch T., Eismann M., Eimer S., Hegermann J., Paponov I.A., Ruperti B., et al. The endoplasmic reticulum localized PIN8 is a pollen-specific auxin carrier involved in intracellular auxin homeostasis. Plant J. 2012;71:860–870. doi: 10.1111/j.1365-313X.2012.05037.x. PubMed DOI

Hagen G., Guilfoyle T.J. Rapid induction of selective transcription by auxins. Mol. Cell. Biol. 1985;5:1197–1203. doi: 10.1128/MCB.5.6.1197. PubMed DOI PMC

Staswick P.E., Serban B., Rowe M., Tiryaki I., Maldonado M.T., Maldonado M.C., Suza W. Characterization of an Arabidopsis Enzyme Family That Conjugates Amino Acids to Indole-3-Acetic Acid. Plant Cell. 2005;17:616–627. doi: 10.1105/tpc.104.026690. PubMed DOI PMC

Ludwig-Müller J., Jülke S., Bierfreund N.M., Decker E.L., Reski R. Moss (Physcomitrella patens) GH3 proteins act in auxin homeostasis. New Phytol. 2009;181:323–338. doi: 10.1111/j.1469-8137.2008.02677.x. PubMed DOI

Di Mambro R., Svolacchia N., Dello Ioio R., Pierdonati E., Salvi E., Pedrazzini E., Vitale A., Perilli S., Sozzani R., Benfey P.N., et al. The Lateral Root Cap Acts as an Auxin Sink that Controls Meristem Size. Curr. Biol. 2019;29:1199–1205.e4. doi: 10.1016/j.cub.2019.02.022. PubMed DOI

Kong Q., Ma W., Yang H., Ma G., Mantyla J.J., Benning C. The Arabidopsis WRINKLED1 transcription factor affects auxin homeostasis in roots. J. Exp. Bot. 2017;68:4627–4634. doi: 10.1093/jxb/erx275. PubMed DOI PMC

Růžička K., Hejátko J. Auxin transport and conjugation caught together. J. Exp. Bot. 2017;68:4409–4412. doi: 10.1093/jxb/erx310. PubMed DOI PMC

Chen Y., Aung K., Rolčík J., Walicki K., Friml J., Brandizzi F. Inter-regulation of the unfolded protein response and auxin signaling. Plant J. 2014;77:97–107. doi: 10.1111/tpj.12373. PubMed DOI PMC

Fan L., Zhao L., Hu W., Li W., Novák O., Strnad M., Simon S., Friml J., Shen J., Jiang L., et al. Na+,K+/H+ antiporters regulate the pH of endoplasmic reticulum and auxin-mediated development. Plant Cell Environ. 2018;41:850–864. doi: 10.1111/pce.13153. PubMed DOI

Cazzonelli C.I., Vanstraelen M., Simon S., Yin K., Carron-Arthur A., Nisar N., Tarle G., Cuttriss A.J., Searle I.R., Benkova E., et al. Role of the Arabidopsis PIN6 Auxin Transporter in Auxin Homeostasis and Auxin-Mediated Development. PLoS ONE. 2013;8:e70069. doi: 10.1371/journal.pone.0070069. PubMed DOI PMC

Di Mambro R., De Ruvo M., Pacifici E., Salvi E., Sozzani R., Benfey P.N., Busch W., Novak O., Ljung K., Di Paola L., et al. Auxin minimum triggers the developmental switch from cell division to cell differentiation in the Arabidopsis root. Proc. Natl. Acad. Sci. USA. 2017;114:E7641–E7649. doi: 10.1073/pnas.1705833114. PubMed DOI PMC

Sanchez Carranza A.P., Singh A., Steinberger K., Panigrahi K., Palme K., Dovzhenko A., Dal Bosco C. Hydrolases of the ILR1-like family of Arabidopsis thaliana modulate auxin response by regulating auxin homeostasis in the endoplasmic reticulum. Sci. Rep. 2016;6:24212. doi: 10.1038/srep24212. PubMed DOI PMC

Lu G., Coneva V., Casaretto J.A., Ying S., Mahmood K., Liu F., Nambara E., Bi Y.-M., Rothstein S.J. OsPIN5b modulates rice (Oryza sativa) plant architecture and yield by changing auxin homeostasis, transport and distribution. Plant J. 2015;83:913–925. doi: 10.1111/tpj.12939. PubMed DOI

Verna C., Sawchuk M.G., Linh N.M., Scarpella E. Control of vein network topology by auxin transport. BMC Biol. 2015;13:94. doi: 10.1186/s12915-015-0208-3. PubMed DOI PMC

Benková E., Michniewicz M., Sauer M., Teichmann T., Seifertová D., Jürgens G., Friml J. Local, Efflux-Dependent Auxin Gradients as a Common Module for Plant Organ Formation. Cell. 2003;115:591–602. doi: 10.1016/S0092-8674(03)00924-3. PubMed DOI

Friml J., Vieten A., Sauer M., Weijers D., Schwarz H., Hamann T., Offringa R., Jürgens G. Efflux-dependent auxin gradients establish the apical–basal axis of Arabidopsis. Nature. 2003;426:147–153. doi: 10.1038/nature02085. PubMed DOI

Feng X.-L., Ni W.-M., Elge S., Mueller-Roeber B., Xu Z.-H., Xue H.-W. Auxin flow in anther filaments is critical for pollen grain development through regulating pollen mitosis. Plant Mol. Biol. 2006;61:215–226. doi: 10.1007/s11103-006-0005-z. PubMed DOI

Gan Z., Feng Y., Wu T., Wang Y., Xu X., Zhang X., Han Z. Downregulation of the auxin transporter gene SlPIN8 results in pollen abortion in tomato. Plant Mol. Biol. 2019;99:561–573. doi: 10.1007/s11103-019-00836-8. PubMed DOI

Mapping the membrane orientation of auxin homeostasis regulators PIN5 and PIN8 in Arabidopsis thaliana root cells reveals their divergent topology