- Protein family review
- Open Access
The PIN-FORMED (PIN) protein family of auxin transporters
- Pavel Křeček†1,
- Petr Skůpa†1,
- Jiří Libus1,
- Satoshi Naramoto2,
- Ricardo Tejos2,
- Jiří Friml2Email author and
- Eva Zažímalová1
© BioMed Central Ltd 2009
- Published: 29 December 2009
The PIN-FORMED (PIN) proteins are secondary transporters acting in the efflux of the plant signal molecule auxin from cells. They are asymmetrically localized within cells and their polarity determines the directionality of intercellular auxin flow. PIN genes are found exclusively in the genomes of multicellular plants and play an important role in regulating asymmetric auxin distribution in multiple developmental processes, including embryogenesis, organogenesis, tissue differentiation and tropic responses. All PIN proteins have a similar structure with amino- and carboxy-terminal hydrophobic, membrane-spanning domains separated by a central hydrophilic domain. The structure of the hydrophobic domains is well conserved. The hydrophilic domain is more divergent and it determines eight groups within the protein family. The activity of PIN proteins is regulated at multiple levels, including transcription, protein stability, subcellular localization and transport activity. Different endogenous and environmental signals can modulate PIN activity and thus modulate auxin-distribution-dependent development. A large group of PIN proteins, including the most ancient members known from mosses, localize to the endoplasmic reticulum and they regulate the subcellular compartmentalization of auxin and thus auxin metabolism. Further work is needed to establish the physiological importance of this unexpected mode of auxin homeostasis regulation. Furthermore, the evolution of PIN-based transport, PIN protein structure and more detailed biochemical characterization of the transport function are important topics for further studies.
- Auxin Transport
- Hydrophobic Domain
- Hydrophilic Domain
- Auxin Homeostasis
- Hydrophilic Loop
The first PIN family members identified and associated with auxin transport were described in the model plant Arabidopsis thaliana. The significance and function of AtPIN1 was discovered through the phenotype generated by the loss-of-function mutation in the gene: mutant plants fail to develop floral organs properly and generate naked, pin-like inflorescences, which gave the name PIN-FORMED (PIN) to the family [5, 6]. At the same time, several groups identified the homologous protein AtPIN2 under different names on the basis of a strong root agravitropic phenotype of the loss-of-function mutant. Independently identified mutant alleles of PIN2 were pin2, ethylene insensitive root1 (eir1), agravitropic1 (agr1), and wavy6 (wav6) [7–10]. Altogether, Arabidopsis has eight annotated PIN genes, of which six have been functionally characterized up to now: PIN1 , PIN2 [7–10], PIN3 , PIN4 , PIN5 , and PIN7 . PIN6 and PIN8 are still awaiting characterization.
With the possible exception of the PIN6-related proteins, the general function of all long PINs from seed plants is to transport auxin out of the cell. The groups differ in the regulation of their expression, localization and activity rather than in the auxin-transport function itself. It has been shown, for example, that AtPIN1 and AtPIN2, which are distinct representatives of the long PINs, can functionally replace each other in planta when expressed in the same cells and localized at the same side of the cell [16, 19].
The second major PIN gene subfamily encodes proteins with the central hydrophilic loop virtually absent ('short' PINs) and comprises AtPIN5 and AtPIN8. Sequence diversification within the subfamily of short PINs tends to be higher than between the long PINs. From this subfamily, only AtPIN5 has been characterized so far , and reveals a striking difference from the canonical long PINs in its subcellular localization and thus in its physiological function (see below). The short PINs appear to localize to a large extent to the endoplasmic reticulum, and although they presumably act as auxin transporters, they do not directly facilitate auxin transport between cells but mediate intracellular auxin compartmentalization and homeostasis .
The precise origin of PIN proteins in the evolutionary history of plants is not known. The basal split of the Viridiplantae - that is, the separation of the Streptophyta (the clade containing land plants (Embryophyta) and some green algae) from the Chlorophyta (representing the majority of green algae) - probably occurred some 725-1,200 million years ago  (Figure 1). All green algae with genomes sequenced so far (Chlamydomonas, Ostreococcus and Micromonas) belong to the clade Chlorophyta and none of these organisms contains a PIN gene. On the other hand, sequence data from the most primitive land plants available - the moss Physcomitrella patens and the club moss Selaginella moellendorffii - have revealed the presence of PIN genes of groups 1 and 2, both belonging to the long PIN subfamily. Nonetheless, to assess the evolutionary origin of PIN proteins more precisely, the genomic data from algae more closely related to land plants (that is, from the Streptophyta) and also from the liverworts, land plants even more ancient than the club mosses, is needed. Interestingly, the P. patens and S. oellendorffii PINs do not cluster with PINs of seed plants or with each other (Figure 3, groups 1 and 2), suggesting separate evolutionary establishment of PIN families in each of the lineages. The only exception is P. patens PpPIND (accession number XP_001765763), which is in the same group as AtPIN6. However, its intron sequences suggest the possibility of horizontal transfer of this gene from monocots .
The predicted structure of canonical long PIN proteins is similar to the structures of secondary transporters - that is, membrane transport proteins that use the electrochemical gradient across the membrane, rather than ATP hydrolysis, to power transport. The PIN proteins have two hydrophobic domains (each with five transmembrane helices) that are separated by a hydrophilic domain with a presumably cytoplasmic orientation. This predicted structure is based only on bioinformatic analyses of the sequen available and has not been verified experimentally. The hydrophobic domains of PIN proteins are highly conserved in sequence, mainly in the transmembrane helices, which tolerate no insertions or deletions; the loops between the transmembrane helices within the hydrophobic domains exhibit much greater variability both in size and sequence. The hydrophilic domains of PIN proteins from the same group (Figure 3) are very similar in sequence, but there is only limited sequence similarity between hydrophilic domains of PINs from different groups.
There is a substantial difference in the sequence variability of the hydrophobic domains between short and long PINs. The hydrophobic domains of long PINs contain positions that have the same amino acid in all available sequences - that is, they are invariant - but not all of these positions are invariant in the short PINs. However, there are no amino-acid positions that are invariant in short PINs but not in the long PINs (Figure 2). This indicates that the positions that are invariant only in long PINs must be crucial for some important function of long PINs that has not been retained in short PINs.
Two motifs important for intracellular trafficking of PIN proteins can be predicted. One comprises two diacidic motifs presumably important for trafficking of proteins from the endoplasmic reticulum that are located in the amino-terminal part of the hydrophilic domain of all long PINs. The other is a tyrosine-based internalization motif present in all PINs that is important for recruitment of the protein into clathrin-dependent vesicles. The importance of these residues for PIN action, however, remains to be demonstrated.
Tissue distribution and subcellular localization
PIN promoter activity can be flexibly regulated, which accounts for a compensatory type of functional redundancy. Several pin knockout mutants in Arabidopsis show ectopic activity of other PIN proteins compensating for the lost PIN activity . This phenomenon seems to account for the high degree of functional redundancy among PIN genes, masking most of the phenotypic manifestations expected to result from single, and some double, PIN gene inactivations [14, 23, 24].
Factors regulating the function of PIN proteins
The PIN proteins mediate asymmetric auxin distribution within tissues, and various endogenous and exogenous signals modulate auxin distribution and thus plant development by acting on PIN proteins. PIN protein activity can be regulated at many levels, including regulation of transcription, protein degradation, subcellular trafficking (endocytic recycling and polarized targeting) and transport activity [3, 4, 25]. For many of the Arabidopsis PIN genes, regulation by other hormonal pathways has been demonstrated. Auxin itself upregulates the transcription of many long PINs. In contrast, the 'short' AtPIN5 is downregulated by auxin . Other phytohormones and plant growth regulators also influence the activity of the PIN promoters to various degrees. The effects are organ- or even cell-type-specific and strongly depend on the particular part of the plant examined and growth regulator used (brassinosteroids [26–28], cytokinins [29–31], gibberellins , ethylene , flavonoids [34, 35]). PIN abundance is also regulated at the level of protein stability. Several PIN proteins, mainly AtPIN2, exhibit pronounced auxin-regulated turnover based on PIN trafficking to the vacuole and their degradation there [36–38].
The only genetically characterized member of the short PIN subfamily is AtPIN5. Its auxin-transport function (shown in yeast cells) together with its subcellular localization at the endoplasmic reticulum membrane implies the transport of auxin molecules from the cytosol into the lumen of endoplasmic reticulum. As a result of this translocation, auxin molecules are exposed to metabolic enzymes localized in the endoplasmic reticulum, leading to metabolic changes that decrease the availability of free active auxin molecules in the cytosol. In this way, AtPIN5 contributes to control of intracellular auxin homeostasis .
In contrast to the wealth of data on the developmental roles of PIN proteins, there is only limited knowledge on their structure, their structure-function relationships and the mechanism of transport. Earlier physiological experiments  established that auxin efflux requires a membrane H+ gradient. Moreover, no ATP-binding motifs suggesting ATP-dependent transport have been recognized in PIN protein sequences. These findings, together with PIN topology in the membrane, suggest that the PIN proteins are gradient-driven secondary transporters. In particular physiological situations, they can act cooperatively with the ATP-dependent auxin transporters of the ABCB (ATP-binding cassette B) family [53, 54].
Out of the eight PIN proteins in Arabidopsis, the canonical long PINs are already well characterized and their developmental roles in generating intercellular auxin distribution patterns have been demonstrated . On the other hand, the existence of auxin transport into the endoplasmic reticulum and its role in regulating auxin homeostasis is a novel and unexpected finding and there is still lot of work needed to elucidate the details and physiological importance of this activity. From the evolutionary point of view, it would be interesting to know which function of PINs is the older: the plasma-membrane-based intercellular auxin transport by long PINs or the endoplasmic-reticulum-based control of intracellular auxin homeostasis by short PINs? The most ancient PIN proteins currently known, from mosses, are localized to the endoplasmic reticulum, which suggests that intracellular function is evolutionarily ancestral, but this remains to be experimentally verified. The other obvious open questions relate to experimental information on PIN protein structure and membrane topology. This, as well as more detailed biochemical characterization of PIN-driven auxin transport is still largely lacking.
The authors acknowledge the support for their work from the Ministry of Education of the Czech Republic, project LC06034 (PK, PS, JL, EZ), from the Grant Agency of the ASCR, project KJB600380904 (JL), and IAA601630703 (JF).
- Lau S, Shao N, Bock R, Jürgens G, De Smet I: Auxin signaling in algal lineages: Fact or myth?. Trends Plant Sci. 2009, 14: 182-188. 10.1016/j.tplants.2009.01.004.PubMedView ArticleGoogle Scholar
- Johri MM: Hormonal regulation in green plant lineage families. Physiol Mol Biol Plants. 2008, 14: 23-38. 10.1007/s12298-008-0003-5.PubMedPubMed CentralView ArticleGoogle Scholar
- Vieten A, Sauer M, Brewer PB, Friml J: Molecular and cellular aspects of auxin-transport-mediated development. Trends Plant Sci. 2007, 12: 160-168. 10.1016/j.tplants.2007.03.006.PubMedView ArticleGoogle Scholar
- Petrášek J, Friml J: Auxin transport routes in plant development. Development. 2009, 136: 2675-2688. 10.1242/dev.030353.PubMedView ArticleGoogle Scholar
- Okada K, Ueda J, Komaki MK, Bell CJ, Shimura Y: Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell. 1991, 3: 677-684. 10.1105/tpc.3.7.677.PubMedPubMed CentralView ArticleGoogle Scholar
- Gälweiler L, Guan C, Müller A, Wisman E, Mendgen K, Yephremov A, Palme K: Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science. 1998, 282: 2226-2230. 10.1126/science.282.5397.2226.PubMedView ArticleGoogle Scholar
- Müller A, Guan C, Gälweiler L, Tänzler P, Huijser P, Marchant A, Parry G, Bennett M, Wisman E, Palme K: AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J. 1998, 17: 6903-6911. 10.1093/emboj/17.23.6903.PubMedPubMed CentralView ArticleGoogle Scholar
- Luschnig C, Gaxiola RA, Grisafi P, Fink GR: EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev. 1998, 12: 2175-2187. 10.1101/gad.12.14.2175.PubMedPubMed CentralView ArticleGoogle Scholar
- Chen R, Hilson P, Sedbrook J, Rosen E, Caspar T, Masson PH: The Arabidopsis thaliana AGRAVITROPIC 1 gene encodes a component of the polar-auxin-transport efflux carrier. Proc Natl Acad Sci USA. 1998, 95: 15112-15117. 10.1073/pnas.95.25.15112.PubMedPubMed CentralView ArticleGoogle Scholar
- Utsuno K, Shikanai T, Yamada Y, Hashimoto T: AGR, an agravitropic locus of Arabidopsis thaliana, encodes a novel membrane-protein family member. Plant Cell Physiol. 1998, 39: 1111-1118.PubMedView ArticleGoogle Scholar
- Friml J, Wiśniewska J, Benková E, Mendgen K, Palme K: Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature. 2002, 415: 806-809.PubMedView ArticleGoogle Scholar
- Friml J, Benková E, Blilou I, Wisniewska J, Hamann T, Ljung K, Woody S, Sandberg G, Scheres B, Jürgens G, Palme K: AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis. Cell. 2002, 108: 661-673. 10.1016/S0092-8674(02)00656-6.PubMedView ArticleGoogle Scholar
- Mravec J, Skůpa P, Bailly A, Hoyerová K, Křeček P, Bielach A, Petrášek J, Zhang J, Gaykova V, Stierhof Y-D, Dobrev PI, Schwarzerová K, Rolčík J, Seifertová D, Luschnig C, Benková E, Zažímalová E, Geisler M, Friml J: Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter. Nature. 2009, 459: 1136-1140. 10.1038/nature08066.PubMedView ArticleGoogle Scholar
- 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. 10.1038/nature02085.PubMedView ArticleGoogle Scholar
- Petrášek J, Mravec J, Bouchard R, Blakeslee JJ, Abas M, Seifertová D, Wisniewska J, Tadele Z, Kubeš M, Čovanová M, Dhonukshe P, Skůpa P, Benková E, Perry L, Křeček P, Lee OR, Fink GR, Geisler M, Murphy AS, Luschnig C, Zažímalová E, Friml J: PIN proteins perform a rate-limiting function in cellular auxin efflux. Science. 2006, 312: 914-918. 10.1126/science.1123542.PubMedView ArticleGoogle Scholar
- Wiśniewska J, Xu J, Seifertová D, Brewer PB, Růžička K, Blilou I, Rouquié D, Benková E, Scheres B, Friml J: Polar PIN localization directs auxin flow in plants. Science. 2006, 312: 883-10.1126/science.1121356.PubMedView ArticleGoogle Scholar
- Carraro N, Forestan C, Canova S, Traas J, Varotto S: ZmPIN1a and ZmPIN1b encode two novel putative candidates for polar auxin transport and plant architecture determination of maize. Plant Physiol. 2006, 142: 254-264. 10.1104/pp.106.080119.PubMedPubMed CentralView ArticleGoogle Scholar
- Xu M, Zhu L, Shou H, Wu P: A PIN1 family gene, OsPIN1, involved in auxin-dependent adventitious root emergence and tillering in rice. Plant Cell Physiol. 2005, 46: 1674-1681. 10.1093/pcp/pci183.PubMedView ArticleGoogle Scholar
- Zhang J, Nodzyñski T, Pìnčík A, Rolčík J, Friml J: PIN phosphorylation is sufficient to mediate PIN polarity and direct auxin transport. Proc Natl Acad Sci USA.Google Scholar
- Becker B, Marin B: Streptophyte algae and the origin of embryophytes. Ann Bot. 2009, 103: 999-1004. 10.1093/aob/mcp044.PubMedPubMed CentralView ArticleGoogle Scholar
- Scarpella E, Marcos D, Friml J, Berleth T: Control of leaf vascular patterning by polar auxin transport. Genes Dev. 2006, 20: 1015-1027. 10.1101/gad.1402406.PubMedPubMed CentralView ArticleGoogle Scholar
- 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. 10.1016/S0092-8674(03)00924-3.PubMedView ArticleGoogle Scholar
- Vieten A, Vanneste S, Wisniewska J, Benková E, Benjamins R, Beeckman T, Luschnig C, Friml J: Functional redundancy of PIN proteins is accompanied by auxin-dependent cross-regulation of PIN expression. Development. 2005, 132: 4521-4531. 10.1242/dev.02027.PubMedView ArticleGoogle Scholar
- Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B: The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature. 2005, 433: 39-44. 10.1038/nature03184.PubMedView ArticleGoogle Scholar
- Tanaka H, Dhonukshe P, Brewer PB, Friml J: Spatiotemporal asymmetric auxin distribution: a means to coordinate plant development. Cell Mol Life Sci. 2006, 63: 2738-2754. 10.1007/s00018-006-6116-5.PubMedView ArticleGoogle Scholar
- Nemhauser JL, Mockler TC, Chory J: Interdependency of brassinosteroid and auxin signaling in Arabidopsis. PLoS Biol. 2004, 2: E258-10.1371/journal.pbio.0020258.PubMedPubMed CentralView ArticleGoogle Scholar
- Goda H, Sawa S, Asami T, Fujioka S, Shimada Y, Yoshida S: Comprehensive comparison of auxin-regulated and brassinosteroid-regulated genes in Arabidopsis. Plant Physiol. 2004, 134: 1555-1573. 10.1104/pp.103.034736.PubMedPubMed CentralView ArticleGoogle Scholar
- Li L, Xu J, Xu Z, Xue H: Brassinosteroids stimulate plant tropisms through modulation of polar auxin transport in Brassica and Arabidopsis. Plant Cell. 2005, 17: 2738-2753. 10.1105/tpc.105.034397.PubMedPubMed CentralView ArticleGoogle Scholar
- Pernisová M, Klíma P, Horák J, Válková M, Malbeck J, Souček P, Reichman P, Hoyerová K, Dubová J, Friml J, Zažímalová E, Hejátko J: Cytokinins modulate auxin-induced organogenesis in plants via regulation of the auxin efflux. Proc Natl Acad Sci USA. 2009, 106: 3609-3614. 10.1073/pnas.0811539106.PubMedPubMed CentralView ArticleGoogle Scholar
- Růžička K, Šimášková M, Duclercq J, Petrášek J, Zažímalová E, Simon S, Friml J, Van Montagu M, Benková E: Cytokinin regulates root meristem activity via modulation of the polar auxin transport. Proc Natl Acad Sci USA. 2009, 106: 4284-4289. 10.1073/pnas.0900060106.PubMedPubMed CentralView ArticleGoogle Scholar
- Dello Ioio R, Nakamura K, Moubayidin L, Perilli S, Taniguchi M, Morita MT, Aoyama T, Costantino P, Sabatini S: A genetic framework for the control of cell division and differentiation in the root meristem. Science. 2008, 322: 1380-1384. 10.1126/science.1164147.PubMedView ArticleGoogle Scholar
- Ogawa M, Hanada A, Yamauchi Y, Kuwahara A, Kamiya Y, Yamaguchi S: Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell. 2003, 15: 1591-1604. 10.1105/tpc.011650.PubMedPubMed CentralView ArticleGoogle Scholar
- Růžička K, Ljung K, Vanneste S, Podhorska R, Beeckman T, Friml J, Benkova E: Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell. 2007, 19: 2197-2212. 10.1105/tpc.107.052126.PubMedPubMed CentralView ArticleGoogle Scholar
- Lazar G, Goodman HM: MAX1, a regulator of the flavonoid pathway, controls vegetative axillary bud outgrowth in Arabidopsis. Proc Natl Acad Sci USA. 2006, 103: 472-476. 10.1073/pnas.0509463102.PubMedPubMed CentralView ArticleGoogle Scholar
- Wang J, Hu H, Wang G, Li J, Chen J, Wu P: Expression of PIN genes in rice (Oryza sativa L.): Tissue specificity and regulation by hormones. Mol Plant. 2009, 2: 823-831. 10.1093/mp/ssp023.PubMedView ArticleGoogle Scholar
- Sieberer T, Seifert GJ, Hauser MT, Grisafi P, Fink GF, Luschnig C: Post-transcriptional control of the Arabidopsis auxin efflux carrier EIR1 requires AXR1. Curr Biol. 2000, 10: 1595-1598. 10.1016/S0960-9822(00)00861-7.PubMedView ArticleGoogle Scholar
- Abas L, Benjamins R, Malenica N, Paciorek T, Wisniewska J, Moulinier-Anzola JC, Sieberer T, Friml J, Luschnig C: Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat Cell Biol. 2006, 8: 249-256. 10.1038/ncb1369.PubMedView ArticleGoogle Scholar
- Kleine-Vehn J, Leitner J, Zwiewka M, Sauer M, Abas L, Luschnig C, Friml J: Differential degradation of PIN2 auxin efflux carrier by retromer-dependent vacuolar targeting. Proc Natl Acad Sci USA. 2008, 105: 17812-17817. 10.1073/pnas.0808073105.PubMedPubMed CentralView ArticleGoogle Scholar
- Kleine-Vehn J, Friml J: Polar targeting and endocytic recycling in auxin-dependent plant development. Annu Rev Cell Dev Biol. 2008, 24: 447-473. 10.1146/annurev.cellbio.24.110707.175254.PubMedView ArticleGoogle Scholar
- Dhonukshe P, Aniento F, Hwang I, Robinson DG, Mravec J, Stierhof Y-D, Friml J: Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr Biol. 2007, 17: 520-527. 10.1016/j.cub.2007.01.052.PubMedView ArticleGoogle Scholar
- Geldner N, Friml J, Stierhof Y-D, Jürgens G, Palme K: Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature. 2001, 413: 425-428. 10.1038/35096571.PubMedView ArticleGoogle Scholar
- Paciorek T, Zažímalová E, Ruthardt N, Petrášek J, Stierhof Y-D, Kleine-Vehn J, Morris DA, Emans N, Jürgens G, Geldner N, Friml J: Auxin inhibits endocytosis and promotes its own efflux from cells. Nature. 2005, 435: 1251-1256. 10.1038/nature03633.PubMedView ArticleGoogle Scholar
- Reinhardt D, Pesce ER, Stieger P, Mandel T, Baltensperger K, Bennett M, Traas J, Friml J, Kuhlemeier C: Regulation of phyllotaxis by polar auxin transport. Nature. 2003, 426: 255-260. 10.1038/nature02081.PubMedView ArticleGoogle Scholar
- Heisler MG, Ohno C, Das P, Sieber P, Reddy GV, Long JA, Meyerowitz EM: Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr Biol. 2005, 15: 1899-1911. 10.1016/j.cub.2005.09.052.PubMedView ArticleGoogle Scholar
- Kleine-Vehn J, Dhonukshe P, Sauer M, Brewer P, Wiśniewska J, Paciorek T, Benková E, Friml J: ARF GEF-dependent transcytosis and polar delivery of PIN auxin carriers in Arabidopsis. Curr Biol. 2008, 18: 526-531. 10.1016/j.cub.2008.03.021.PubMedView ArticleGoogle Scholar
- Michniewicz M, Zago MK, Abas L, Weijers D, Schweighofer A, Meskiene I, Heisler MG, Ohno C, Zhang J, Huang F, Schwab R, Weigel D, Meyerowitz EM, Luschnig C, Offringa R, Friml J: Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell. 2007, 130: 1044-1056. 10.1016/j.cell.2007.07.033.PubMedView ArticleGoogle Scholar
- 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: A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science. 2004, 306: 862-865. 10.1126/science.1100618.PubMedView ArticleGoogle Scholar
- Zourelidou M, Müller I, Willige BC, Nill C, Jikumaru Y, Li H, Schwechheimer C: The polarly localised D6 PROTEIN KINASE is required for efficient auxin transport in Arabidopsis thaliana. Development. 2009, 136: 627-636. 10.1242/dev.028365.PubMedView ArticleGoogle Scholar
- Peer WA, Murphy AS: Flavonoids and auxin transport: modulators or regulators?. Trends Plant Sci. 2007, 12: 556-563. 10.1016/j.tplants.2007.10.003.PubMedView ArticleGoogle Scholar
- Zažímalová E, Křeček P, Skůpa P, Hoyerová K, Petrášek J: Polar transport of plant hormone auxin - the role of PIN-FORMED (PIN) proteins. Cell Mol Life Sci. 2007, 64: 1621-1637. 10.1007/s00018-007-6566-4.PubMedView ArticleGoogle Scholar
- Dhonukshe P, Grigoriev I, Fischer R, Tominaga M, Robinson DG, Hašek J, Paciorek T, Petrášek J, Seifertová D, Tejos R, Meisel LA, Zažímalová E, Gadella TWJ, Stierhof Y-D, Ueda T, Oiwa K, Akhmanova A, Brock R, Spang A, Friml J: Auxin transport inhibitors impair vesicle motility and actin cytoskeleton dynamics in diverse eukaryotes. Proc Natl Acad Sci USA. 2008, 105: 4489-4494. 10.1073/pnas.0711414105.PubMedPubMed CentralView ArticleGoogle Scholar
- Lomax TL, Muday GK, Rubery PH: Auxin transport. Plant Hormones: Physiology, Biochemistry and Molecular Biology. Edited by: Davies PJ. 1995, Dordrecht, Boston, London: Kluwer Academic Publishers, 509-530. 2View ArticleGoogle Scholar
- Blakeslee JJ, Bandyopadhyay A, Lee OR, Mravec J, Titapiwatanakun B, Sauer M, Makam SN, Cheng Y, Bouchard R, Adamec J, Geisler M, Nagashima A, Sakai T, Martinoia E, Friml J, Peer WA, Murphy AS: Interactions among PIN-FORMED and P-glycoprotein auxin transporters in Arabidopsis. Plant Cell. 2007, 19: 131-147. 10.1105/tpc.106.040782.PubMedPubMed CentralView ArticleGoogle Scholar
- Yang H, Murphy AS: Functional expression and characterization of Arabidopsis ABCB, AUX 1 and PIN auxin transporters in Schizosaccharomyces pombe. Plant J. 2009, 59: 179-191. 10.1111/j.1365-313X.2009.03856.x.PubMedView ArticleGoogle Scholar
- Vanneste S, Friml J: Auxin: A trigger for change in plant development. Cell. 2009, 136: 1005-1016. 10.1016/j.cell.2009.03.001.PubMedView ArticleGoogle Scholar
- Benschop JJ, Mohammed S, O'Flaherty M, Heck AJR, Slijper M, Menke FLH: Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis. Mol Cell Proteomics. 2007, 6: 1198-1214. 10.1074/mcp.M600429-MCP200.PubMedView ArticleGoogle Scholar
- Reyes-Prieto A, Bhattacharya D: Phylogeny of nuclear-encoded plastid-targeted proteins supports an early divergence of glaucophytes within plantae. Mol Biol Evol. 2007, 24: 2358-2361. 10.1093/molbev/msm186.PubMedView ArticleGoogle Scholar
- Lemieux C, Otis C, Turmel M: A clade uniting the green algae Mesostigma viride and Chlorokybus atmophyticus represents the deepest branch of the streptophyta in chloroplast genome-based phylogenies. BMC Biol. 2007, 5: 2-10.1186/1741-7007-5-2.PubMedPubMed CentralView ArticleGoogle Scholar
- Qiu Y, Li L, Wang B, Chen Z, Knoop V, Groth-Malonek M, Dombrovska O, Lee J, Kent L, Rest J, Estabrook GF, Hendry TA, Taylor DW, Testa CM, Ambros M, Crandall-Stotler B, Duff RJ, Stech M, Frey W, Quandt D, Davis CC: The deepest divergences in land plants inferred from phylogenomic evidence. Proc Natl Acad Sci USA. 2006, 103: 15511-15516. 10.1073/pnas.0603335103.PubMedPubMed CentralView ArticleGoogle Scholar
- Smith SA, Beaulieu JM, Donoghue MJ: Mega-phylogeny approach for comparative biology: An alternative to supertree and supermatrix approaches. BMC Evol Biol. 2009, 9: 37-10.1186/1471-2148-9-37.PubMedPubMed CentralView ArticleGoogle Scholar
- Pryer KM, Schneider H, Smith AR, Cranfill R, Wolf PG, Hunt JS, Sipes SD: Horsetails and ferns are a monophyletic group and the closest living relatives to seed plants. Nature. 2001, 409: 618-621. 10.1038/35054555.PubMedView ArticleGoogle Scholar
- Phytozome. [http://www.phytozome.org]
- Katoh K, Toh H: Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform. 2008, 9: 286-298. 10.1093/bib/bbn013.PubMedView ArticleGoogle Scholar
- Ronquist F, Huelsenbeck JP: MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003, 19: 1572-1574. 10.1093/bioinformatics/btg180.PubMedView ArticleGoogle Scholar
- Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertle L, Widmayer P, Gruissem W, Zimmermann P: Genevestigator V3: A reference expression database for the meta-analysis of transcriptomes. Adv Bioinformatics. 2008, 420747-Google Scholar
- Cell Signaling and Endocytosis in Plants. [http://www.ens-lyon.fr/RDP/SiCE/english/photos-uk.html]