Plasma Membrane Positioning Mechanism of Auxin Efflux Carrier PIN Proteins

doi:10.11983/CBB15017

Abstract

Abstract: Auxin concentration affects the morphological establishment of plant body and its organs, while PIN (PIN- FORMED) proteins determine the direction of auxin stream within tissues. The nature of lipid rafts of cellular plasma membrane underlies the uneven distribution of PINs in the plasma membrane. Meanwhile, clathrin-mediated endocytyosis, proteins phosphorylation/dephosphorylation and even genes transcriptional regulation affect this polar location of PINs. Additionally, at the time when multicellular plants emerge, PINs may undergo a transition from endoplasmic reticulum membrane to plasma membrane positioning.

Key words: auxin, PIN, endocytosis, phosphorylation, plant evolution

Wenjie Cao, Guisheng Li. Plasma Membrane Positioning Mechanism of Auxin Efflux Carrier PIN Proteins[J]. Chinese Bulletin of Botany, 2016, 51(2): 265-273.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.chinbullbotany.com/EN/10.11983/CBB15017

https://www.chinbullbotany.com/EN/Y2016/V51/I2/265

Figures/Tables 2

Figure 1 The cellular mechanism of the plasma membrane positioning of PINs The parts of plasma membrane connecting to cell wall (●) prevent the diffusion of PINs, and PID and PP2A located in plama membrane respectively phosphorylates and dephosphory- lates PINs. Clathrin mediates the endocytosis of PINs, however this process is inhibited by the binding of kinase TMK to ABP1-auxin complex. PINs already entering into cytoplasm ultimately arrive at TGN/EE, whereby they undergo regulation in recycling and reach certain parts of plasma membrane or enter into vacuole via degradation pathway. Actin mediates the apical movement of PINs while microtubuli mediates the reverse migration, and in the basal transportation GNOM is a key component; phosphorylated PINs will reach the apical membrane while dephosphorylated ones move to the basal. Mono-ubiquitylation promotes endocytosis of PINs while poly-ubiquitylation gets them into vacuole degeradation pathway. P: Phosphorylated PINs; U: Ubiquitylated PINs.

Figure 2 Representative phylogenetic relationships of PINs (A) Bootstrap values on branches are respectively from most parsimony tree of the first and second position of codons/ most likelihood tree of amino acid sequence/most likelihood tree of the first and second position of codons; (B) Bootstrap values are respectively from most parsimony tree of amino acid sequence/neighbour joining tree of the first and second position of codons; (C) Bootstrap values are from most likelihood tree of the second and third position of codons/ neighbour joining tree of amino acid sequence. - indicates values lower than 50; ? indicate incongruent topology between different methods; The length of the vertical bar on branches suggests the length of hydrophilic loop, and the grey colour means that the determination of PIN6 possessing a long hydrophilic loop is equivocal.

References 63

[1]	Ambrose C, Ruan Y, Gardiner J, Tamblyn LM, Catching A, Kirik V, Marc J, Overall R, Wasteneys GO (2013). CLASP interacts with sorting nexin 1 to link microtubules and auxin transport via PIN2 recycling in Arabidopsis tha- liana. Dev Cell 24, 649-659. DOI PMID
[2]	Bagnat M, Simons K (2002). Cell surface polarization during yeast mating. Proc Natl Acad Sci USA 99, 14183-14188. PMID
[3]	Barbez E, Lankova M, Parezova M, Maizel A, Zazimalova E, Petrasek J, Friml J, Kleine-Vehn J (2013). Single-cell-based system to monitor carrier driven cellular auxin homeostasis. BMC Plant Biol 13, 20. DOI PMID
[4]	Barbosa IC, Zourelidou M, Willige BC, Weller B, Sch- wechheimer C (2014). D6 PROTEIN KINASE activates auxin transport-dependent growth and PIN-FORMED ph- osphorylation at the plasma membrane. Dev Cell 29, 674-685. DOI PMID
[5]	Baster P, Robert S, Kleine-Vehn J, Vanneste S, Kania U, Grunewald W, De Rybel B, Beeckman T, Friml J (2012). SCF (TIR1/AFB)-auxin signaling regulates PIN vacuolar trafficking and auxin fluxes during root gravitropism. EMBO J 32, 260-274.
[6]	Bennett T, Brockington SF, Rothfels C, Graham SW, Stevenson D, Kutchan T, Rolf M, Thomas P, Wong GK, Leyser O, Glover BJ, Harrison CJ (2014). Paralogous radiations of PIN proteins with multiple origins of noncanonical PIN structure. Mol Biol Evol 31, 2042-2060. DOI PMID
[7]	Bhalerao RP, Bennett MJ (2003). The case for morphogens in plants. Nat Cell Biol 5, 939-943. DOI PMID
[8]	Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005). The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433, 39-44.
[9]	Boer DR, Freire-Rios A, van den Berg WA, Saaki T, Manfield IW, Kepinski S, Lopez-Vidrieo I, Franco-Zorrilla JM, de Vries SC, Solano R, Weijers D, Coll M (2014). Structural basis for DNA binding specificity by the auxin- dependent ARF transcription factors. Cell 156, 577-589.
[10]	Boot KJ, Libbenga KR, Hille SC, Offringa R, van Duijn B (2012). Polar auxin transport: an early invention. J Exp Bot 63, 4213-4218. DOI PMID
[11]	Busch M, Mayer U, Jurgens G (1996). Molecular analysis of the Arabidopsis pattern formation of gene GNOM: gene structure and intragenic complementation. Mol Gen Genet 250, 681-691.
[12]	Darwin C, Darwin F (1880). The Power of Movement in Plants. New York: D. Appleton and Company.
[13]	De Smet I, Voss U, Lau S, Wilson M, Shao N, Timme RE, Swarup R, Kerr I, Hodgman C, Bock R, Bennett M, Jurgens G, Beeckman T (2011). Unraveling the evolution of auxin signaling. Plant Physiol 155, 209-221. DOI PMID
[14]	Dhonukshe P (2009). Cell polarity in plants: linking PIN polarity generation mechanisms to morphogenic auxin gradients. Commun Integr Biol 2, 184-190. DOI PMID
[15]	Dhonukshe P, Aniento F, Hwang I, Robinson DG, Mravec J, Stierhof YD, Friml J (2007). Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr Biol 17, 520-527. DOI PMID
[16]	Donaldson JG, Jackson CL (2000). Regulators and effectors of the ARF GTPases. Curr Opin Cell Biol 12, 475-482. PMID
[17]	Fan L, Hao H, Xue Y, Zhang L, Song K, Ding Z, Botella MA, Wang H, Lin J (2013). Dynamic analysis of Arabidopsis AP2 sigma subunit reveals a key role in clathrin- mediated endocytosis and plant development. Development 140, 3826-3837.
[18]	Feraru E, Feraru MI, Kleine-Vehn J, Martiniere A, Mouille G, Vanneste S, Vernhettes S, Runions J, Friml J (2011). PIN polarity maintenance by the cell wall in Arabidopsis. Curr Biol 21, 338-343. DOI PMID
[19]	Feraru E, Vosolsobe S, Feraru MI, Petrasek J, Kleine- Vehn J (2012). Evolution and structural diversification of PILS putative auxin carriers in plants. Front Plant Sci 3, 227. DOI PMID
[20]	Friml J, Wisniewska J, Benkova E, Mendgen K, Palme K (2002). Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415, 806-809.
[21]	Friml J, Yang X, Michniewicz M, Weijers D, Quint A, Tietz O, Benjamins R, Ouwerkerk PB, Ljung K, Sandberg G, Hooykaas PJ, Palme K, Offringa R (2004). A PINOID- dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 306, 862-865. DOI PMID
[22]	Fujita T, Sakaguchi H, Hiwatashi Y, Wagstaff SJ, Ito M, Deguchi H, Sato T, Hasebe M (2008). Convergent evolution of shoots in land plants: lack of auxin polar transport in moss shoots. Evol Dev 10, 176-186. DOI PMID
[23]	Ganguly A, Park M, Kesawat MS, Cho HT (2014). Functional analysis of the hydrophilic loop in intracellular trafficking of Arabidopsis PIN-FORMED proteins. Plant Cell 26, 1570-1585.
[24]	Garrett JJ, Meents MJ, Blackshaw MT, Blackshaw LC, Hou H, Styranko DM, Kohalmi SE, Schultz EA (2012). A novel, semi-dominant allele of MONOPTEROS provides insight into leaf initiation and vein pattern formation. Plan- ta 236, 297-312.
[25]	Geldner N, Anders N, Wolters H, Keicher J, Kornberger W, Muller P, Delbarre A, Ueda T, Nakano A, Jurgens G (2003). The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112, 219-230. DOI PMID
[26]	Geldner N, Richter S, Vieten A, Marquardt S, Torres-Ruiz RA, Mayer U, Jurgens G (2004). Partial loss-of-function alleles reveal a role for GNOM in auxin transport-related, post-embryonic development of Arabidopsis. Development 131, 389-400. DOI PMID
[27]	Habets ME, Offringa R (2014). PIN-driven polar auxin transport in plant developmental plasticity: a key target for environmental and endogenous signals. New Phytol 203, 362-377. DOI PMID
[28]	Hofhuis H, Laskowski M, Du Y, Prasad K, Grigg S, Pinon V, Scheres B (2013). Phyllotaxis and rhizotaxis in Ara- bidopsis are modified by three PLETHORA transcription factors. Curr Biol 23, 956-962. DOI PMID
[29]	Huang F, Zago MK, Abas L, van Marion A, Galvan- Ampudia CS, Offringa R (2010). Phosphorylation of conserved PIN motifs directs Arabidopsis PIN1 polarity and auxin transport. Plant Cell 22, 1129-1142.
[30]	Kitakura S, Vanneste S, Robert S, Lofke C, Teichmann T, Tanaka H, Friml J (2011). Clathrin mediates endocytosis and polar distribution of PIN auxin transporters in Arabidopsis. Plant Cell 23, 1920-1931.
[31]	Kleine-Vehn J, Leitner J, Zwiewka M, Sauer M, Abas L, Luschnig C, Friml J (2008). Differential degradation of PIN2 auxin efflux carrier by retromer-dependent vacuolar targeting. Proc Natl Acad Sci USA 105, 17812-17817. DOI PMID
[32]	Kleine-Vehn J, Wabnik K, Martiniere A, Langowski L, Willig K, Naramoto S, Leitner J, Tanaka H, Jakobs S, Robert S, Luschnig C, Govaerts W, Hell SW, Runions J, Friml J (2011). Recycling, clustering, and endocytosis jointly maintain PIN auxin carrier polarity at the plasma membrane. Mol Syst Biol 7, 540. DOI PMID
[33]	Leitner J, Petrasek J, Tomanov K, Retzer K, Parezova M, Korbei B, Bachmair A, Zazimalova E, Luschnig C (2012). Lysine63-linked ubiquitylation of PIN2 auxin carrier protein governs hormonally controlled adaptation of Arabidopsis root growth. Proc Natl Acad Sci USA 109, 8322-8327. DOI PMID
[34]	Li H, Lin D, Dhonukshe P, Nagawa S, Chen D, Friml J, Scheres B, Guo H, Yang Z (2011). Phosphorylation switch modulates the interdigitated pattern of PIN1 locali- zation and cell expansion in Arabidopsis leaf epidermis. Cell Res 21, 970-978.
[35]	Li R, Liu P, Wan Y, Chen T, Wang Q, Mettbach U, Baluska F, Samaj J, Fang X, Lucas WJ, Lin J (2012). A membrane microdomain-associated protein, Arabidopsis Flot1, is involved in a clathrin-independent endocytic pathway and is required for seedling development. Plant Cell 24, 2105-2122.
[36]	Martiniere A, Lavagi I, Nageswaran G, Rolfe DJ, Maneta- Peyret L, Luu DT, Botchway SW, Webb SE, Mongrand S, Maurel C, Martin-Fernandez ML, Kleine-Vehn J, Friml J, Moreau P, Runions J (2012). Cell wall constrains lateral diffusion of plant plasma membrane proteins. Proc Natl Acad Sci USA 109, 12805-12810.
[37]	Michniewicz M, Brewer PB, Friml JI (2007). Polar auxin transport and asymmetric auxin distribution. Arabidopsis Book 5, e0108.
[38]	Mravec J, Skupa P, Bailly A, Hoyerova K, Krecek P, Bielach A, Petrasek J, Zhang J, Gaykova V, Stierhof YD, Dobrev PI, Schwarzerova K, Rolcik J, Seifertova D, Luschnig C, Benkova E, Zazimalova E, Geisler M, Friml J (2009). Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter. Nature 459, 1136-1140.
[39]	Naramoto S, Otegui MS, Kutsuna N, de Rycke R, Dainobu T, Karampelias M, Fujimoto M, Feraru E, Miki D, Fukuda H, Nakano A, Friml J (2014). Insights into the localization and function of the membrane trafficking re- gulator GNOM ARF-GEF at the golgi apparatus in Arabidopsis. Plant Cell 26, 3062-3076.
[40]	Perrot-Rechenmann C (2010). Cellular responses to auxin: division versus expansion. Cold Spring Harb Perspect Biol 2, a001446.
[41]	Petrasek J, Mravec J, Bouchard R, Blakeslee JJ, Abas M, Seifertova D, Wisniewska J, Tadele Z, Kubes M, Covanova M, Dhonukshe P, Skupa P, Benkova E, Perry L, Krecek P, Lee OR, Fink GR, Geisler M, Murphy AS, Luschnig C, Zazimalova E, Friml J (2006). PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312, 914-918. DOI PMID
[42]	Pierre-Jerome E, Moss BL, Nemhauser JL (2013). Tuning the auxin transcriptional response. J Exp Bot 64, 2557-2563. DOI PMID
[43]	Pinon V, Prasad K, Grigg SP, Sanchez-Perez GF, Scheres B (2013). Local auxin biosynthesis regulation by PLETHORA transcription factors controls phyllotaxis in Arabidopsis. Proc Natl Acad Sci USA 110, 1107-1112. DOI PMID
[44]	Prasad K, Grigg SP, Barkoulas M, Yadav RK, Sanchez- Perez GF, Pinon V, Blilou I, Hofhuis H, Dhonukshe P, Galinha C, Mahonen AP, Muller WH, Raman S, Verkleij AJ, Snel B, Reddy GV, Tsiantis M, Scheres B (2011). Arabidopsis PLETHORA transcription factors control phy- llotaxis. Curr Biol 21, 1123-1128.
[45]	Raven JA (1975). Transport of indoleacetic acid in plant cells in relation to pH and electrical potential gradients, and its significance for polar IAA transport. New Phytol 74, 163-172.
[46]	Rigo G, Ayaydin F, Tietz O, Zsigmond L, Kovacs H, Pay A, Salchert K, Darula Z, Medzihradszky KF, Szabados L, Palme K, Koncz C, Cseplo A (2013). Inactivation of plasma membrane-localized CDPK-RELATED KINASE5 decelerates PIN2 exocytosis and root gravitropic response in Arabidopsis. Plant Cell 25, 1592-1608.
[47]	Ritzenthaler C, Nebenfuhr A, Movafeghi A, Stussi- Garaud C, Behnia L, Pimpl P, Staehelin LA, Robinson DG (2002). Reevaluation of the effects of brefeldin A on plant cells using tobacco Bright Yellow 2 cells expressing Golgi-targeted green fluorescent protein and COPI antisera. Plant Cell 14, 237-261. DOI PMID
[48]	Rubery PH, Sheldrake AR (1974). Carrier-mediated auxin transport. Planta 118, 101-121. DOI PMID
[49]	Sauer M, Balla J, Luschnig C, Wisniewska J, Reinohl V, Friml J, Benkova E (2006). Canalization of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity. Genes Dev 20, 2902-2911.
[50]	Shevell DE, Leu WM, Gillmor CS, Xia G, Feldmann KA, Chua NH (1994). EMB30 is essential for normal cell division, cell expansion, and cell adhesion in Arabidopsis and encodes a protein that has similarity to Sec7. Cell 77, 1051-1062. DOI PMID
[51]	Spitzer C, Reyes FC, Buono R, Sliwinski MK, Haas TJ, Otegui MS (2009). The ESCRT-related CHMP1A and B proteins mediate multivesicular body sorting of auxin carriers in Arabidopsis and are required for plant development. Plant Cell 21, 749-766. DOI PMID
[52]	Steinmann T, Geldner N, Grebe M, Mangold S, Jackson CL, Paris S, Galweiler L, Palme K, Jurgens G (1999). Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science 286, 316-318. DOI PMID
[53]	Takano J, Tanaka M, Toyoda A, Miwa K, Kasai K, Fuji K, Onouchi H, Naito S, Fujiwara T (2010). Polar localization and degradation of Arabidopsis boron transporters through distinct trafficking pathways. Proc Natl Acad Sci USA 107, 5220-5225. DOI PMID
[54]	Tejos R, Sauer M, Vanneste S, Palacios-Gomez M, Li H, Heilmann M, van Wijk R, Vermeer JE, Heilmann I, Munnik T, Friml J (2014). Bipolar plasma membrane distribution of phosphoinositides and their requirement for auxin-mediated cell polarity and patterning in Arabidopsis. Plant Cell 26, 2114-2128.
[55]	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 J 57, 27-44.
[56]	Tromas A, Paque S, Stierle V, Quettier AL, Muller P, Lechner E, Genschik P, Perrot-Rechenmann C (2013). Auxin-binding protein 1 is a negative regulator of the SCF (TIR1/AFB) pathway. Nat Commun 4, 2496.
[57]	Viaene T, Delwiche CF, Rensing SA, Friml J (2013). Origin and evolution of PIN auxin transporters in the green lineage. Trends Plant Sci 18, 5-10. DOI PMID
[58]	Vieten A, Vanneste S, Wisniewska J, Benkova E, Benjamins R, Beeckman T, Luschnig C, Friml J (2005). Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression. De- velopment 132, 4521-4531.
[59]	Wang C, Yan X, Chen Q, Jiang N, Fu W, Ma B, Liu J, Li C, Bednarek SY, Pan J (2013). Clathrin light chains regulate clathrin-mediated trafficking, auxin signaling, and deve- lopment in Arabidopsis. Plant Cell 25, 499-516.
[60]	Wenzel CL, Schuetz M, Yu Q, Mattsson J (2007). Dynamics of MONOPTEROS and PIN-FORMED1 expression during leaf vein pattern formation in Arabidopsis thaliana. Plant J 49, 387-398. DOI PMID
[61]	Xu J, Hofhuis H, Heidstra R, Sauer M, Friml J, Scheres B (2006). A molecular framework for plant regeneration. Science 311, 385-388. DOI PMID
[62]	Zazimalova E, Krecek P, Skupa P, Hoyerova K, Petrasek J (2007). Polar transport of the plant hormone auxin—the role of PIN-FORMED (PIN) proteins. Cell Mol Life Sci 64, 1621-1637.
[63]	Zhang J, Nodzynski T, Pencik A, Rolcik J, Friml J (2010). PIN phosphorylation is sufficient to mediate PIN polarity and direct auxin transport. Proc Natl Acad Sci USA 107, 918-922. DOI PMID