Advances in the Functions of Immunophilins in Plants

doi:10.11983/CBB16202

Abstract

Abstract: Immunophilins are receptors for immunosuppressive drugs that exist widely in bacteria, viruses, fungi, plants and animals. In plants, immunophilins have three subfamilies: FK506-binding proteins, cyclosporine A-binding proteins (cyclophilins) and parvulins. Many members of immunophilins are peptidyl-prolyl cis-trans isomerases that may act as molecular chaperones for protein folding. In this review, we summarize the research progress in the functions of plant immunophilins in hormone signaling, photosynthesis, stress response and gene expression etc., to provide valuable information for further study of immunophilin functions.

Key words: growth and development, gene expression, immunophilins, photosynthesis, stress response

Sun Wanmei, Wang Xiaozhu, Han Erqin, Han Li, Sun Liping, Peng Zaihui, Wang Bangjun. Advances in the Functions of Immunophilins in Plants[J]. Chinese Bulletin of Botany, 2017, 52(6): 808-819.

Add to citation manager EndNote|Ris|BibTeX

URL: https://www.chinbullbotany.com/EN/10.11983/CBB16202

https://www.chinbullbotany.com/EN/Y2017/V52/I6/808

Figures/Tables 2

Table 1 The localization and function of some immunophilins in plant cells

Figure 1 Immunophilins regulate downstream signaling by interacting with related proteins(A) TWD1 helps the correct secretion of ABCB transporters to the plasma membrane, thus regulating ABCB-mediated auxin transport; Brassinosteroid might affect this process (Geisler and Bailly, 2007; Wu et al., 2010); (B) TWD1 physically interacts with BRI1 and BAK1 in a BR-independent manner, which may facilitate the phosphorylation of BRI1 and BAK1, inhibit BIN2 activity,and affect BES1/BZR1 phosphorylation, eventually regulate the BR response gene expression (Zhao et al., 2016; Chaiwanon et al., 2016); (C) A conformational change of BZR1 mediated by AtCYP20-2 causes altered flowering time through the modulation of FLD expression (Zhang et al., 2013); (D) In the presence of auxin, OsIAA11 conformation was changed by interacting with LRT2, and then formed the OsTIR1-OsIAA11 complex. OsTIR1-OsIAA11 complex facilitated OsIAA11 binding to 26S proteasome and caused OsIAA11 degradation; Finally, ARFs became active and activated auxin-regulated genes (Jing et al., 2015).

References 81

[1]	于彦丽, 李艳娇, 庞凯元, 张发军, 孙琦, 李文才, 孟昭东 (2014). 植物FKBP基因家族的结构及生物学功能. 遗传 36, 536-546.
[2]	Ahn JC, Kim DW, You YN, Seok MS, Park JM, Hwang H, Kim BG, Luan S, Park HS, Cho HS (2010). Classification of rice ( Oryza sativa l. Japonica nipponbare) immunophi- lins (FKBPs, CYPs) and expression patterns under water stress. BMC Plant Biol 10, 253.
[3]	Arevalo-Rodriguez M, Wu XY, Hanes SD, Heitman J (2004). Prolyl isomerases in yeast.Front Biosci 9, 2420-2446. DOI URL PMID
[4]	Aviezer-Hagai K, Skovorodnikova J, Galigniana M, Farchi-Pisanty O, Maayan E, Bocovza S, Efrat Y, von Koskull-D?ring P, Ohad N, Breiman A (2007). Arabidopsis immunophilins ROF1 (AtFKBP62) and ROF2 (At- FKBP65) exhibit tissue specificity, are heat-stress induced, and bind HSP90.Plant Mol Biol 63, 237-255. DOI URL
[5]	Banasavadi-Siddegowda YK, Mai JB, Fan YF, Bhattacharya S, Giovannucci DR, Sanchez ER, Fischer G, Wang XD (2011). FKBP38 peptidylprolyl isomerase promotes the folding of cystic fibrosis transmembrane conductance regulator in the endoplasmic reticulum.J Biol Chem 286, 43071-43080. DOI URL PMID
[6]	Barik S (2006). Immunophilins: for the love of proteins.Cell Mol Life Sci 63, 2889-2900. DOI URL PMID
[7]	Bissoli G, Ni?oles R, Fresquet S, Palombieri S, Bueso E, Rubio L, García-Sánchez MJ, Fernández JA, Mulet JM, Serrano R (2012). Peptidyl-prolyl cis-trans isomerase RO- F2 modulates intracellular pH homeostasis in Arabidopsis. Plant J 70, 704-716.
[8]	Chaiwanon J, Garcia VJ, Cartwright H, Sun Y, Wang ZY (2016). Immunophilin-like FKBP42/TWISTED DWARF1 in- teracts with the receptor kinase BRI1 to regulate brassino- steroid signaling in Arabidopsis.Mol Plant 9, 593-600. DOI URL PMID
[9]	Dominguez-Solis JR, He ZY, Lima A, Ting JL, Buchanan BB, Luan S (2008). A cyclophilin links redox and light signals to cysteine biosynthesis and stress responses in chloroplasts.Proc Natl Acad Sci USA 105, 16386-16391. DOI URL
[10]	Dunyak BM, Gestwicki JE (2016). Peptidyl-proline isomerases (PPIases): targets for natural products and natural product-inspired compounds.J Med Chem 59, 9622-9644. DOI URL PMID
[11]	Earley K, Smith MR, Weber R, Gregory BD, Poethig RS (2010). An endogenous F-box protein regulates ARGONAUTE1 inArabidopsis thaliana. Silence 1, 15.
[12]	Fu AG, He ZY, Cho HS, Lima A, Buchanan BB, Luan S (2007). A chloroplast cyclophilin functions in the assembly and maintenance of photosystem II in Arabidopsis thali- ana. Proc Natl Acad Sci USA 104, 15947-15952. DOI URL PMID
[13]	Geisler M, Bailly A (2007). Tête-à-tête: the function of FKBPs in plant development.Trends Plant Sci 12, 465-473. DOI URL
[14]	Geisler M, Girin M, Brandt S, Vincenzetti V, Plaza S, Paris N, Kobae Y, Maeshima M, Billion K, Kolukisaoglu üH, Schulz B, Martinoia E (2004). Arabidopsis immunophilin-like TWD1 functionally interacts with vacuolar ABC transporters.Mol Biol Cell 15, 3393-3405. DOI URL PMID
[15]	Geisler M, Kolukisaoglu Hü, Bouchard R, Billion K, Berger J, Saal B, Frangne N, Koncz-Kálmán Z, Koncz C, Dudler R, Blakeslee JJ, Murphy AS, Martinoia E, Schulz B (2003). TWISTED DWARF1, a unique plasma membrane-anchored immunophilin-like protein, interacts with Arabidopsis multidrug resistance-like transporters AtPGP1 and AtPGP19.Mol Biol Cell 14, 4238-4249. DOI URL
[16]	Gollan PJ, Bhave M (2010). Genome-wide analysis of genes encoding FK506-binding proteins in rice.Plant Mol Biol 72, 1-16. DOI URL PMID
[17]	Gollan PJ, Ziemann M, Bhave M (2011). PPIase activities and interaction partners of FK506-binding proteins in the wheat thylakoid.Physiol Plant 143, 385-395. DOI URL PMID
[18]	Grebe M, Gadea J, Steinmann T, Kientz M, Rahfeld JU, Salchert K, Koncz C, Jürgens G (2000). A conserved domain of the Arabidopsis GNOM protein mediates subunit interaction and cyclophilin 5 binding.Plant Cell 12, 343-356. DOI URL PMID
[19]	Gupta R, Mould RM, He ZY, Luan S (2002). A chloroplast FKBP interacts with and affects the accumulation of Rieske subunit of cytochrome bf complex. Proc Natl Acad Sci USA 99, 15806-15811. DOI URL PMID
[20]	Harrar Y, Bellec Y, Bellini C, Faure JD (2003). Hormonal control of cell proliferation requires PASTICCINO genes. Plant Physiol 132, 1217-1227. DOI URL
[21]	He ZY, Li LG, Luan S (2004). Immunophilins and parvulins. Superfamily of peptidyl prolyl isomerases in Arabidopsis.Plant Physiol 134, 1248-1267. DOI URL PMID
[22]	Hennig L, Christner C, Kipping M, Schelbert B, Rücknagel KP, Grabley S, Küllertz G, Fischer G (1998). Selective inactivation of parvulin-like peptidyl-prolyl cis/trans isomerases by juglone. Biochemistry 37, 5953-5960. DOI URL PMID
[23]	Ingelsson B, Shapiguzov A, Kieselbach T, Vener AV (2009). Peptidyl-prolyl isomerase activity in chloroplast th- ylakoid lumen is a dispensable function of immunophilins in Arabidopsis thaliana. Plant Cell Physiol 50, 1801-1814.
[24]	Ivanchenko MG, Zhu JS, Wang BJ, Medvecká E, Du YL, Azzarello E, Mancuso S, Megraw M, Filichkin S, Dubrovsky JG, Friml J, Geisler M (2015). The cyclophilin A DIAGEOTROPICA gene affects auxin transport in both root and shoot to control lateral root formation.Development 142, 712-721. DOI URL PMID
[25]	Jackson K, S?ll D (1999). Mutations in a new Arabidopsis cyclophilin disrupt its interaction with protein phosphatase 2A.Mol Gen Genet 262, 830-838. DOI URL PMID
[26]	Jing HW, Yang XL, Zhang J, Liu XH, Zheng HK, Dong GJ, Nian JQ, Feng J, Xia B, Qian Q, Li JY, Zuo JR (2015). Peptidyl-prolyl isomerization targets rice Aux/IAAs for pro- teasomal degradation during auxin signaling.Nat Commun 6, 7395. DOI URL
[27]	Kamphausen T, Fangh?nel J, Neumann D, Schulz B, Rahfeld JU (2002). Characterization of Arabidopsis tha- liana AtFKBP42 that is membrane-bound and interacts with Hsp90. Plant J 32, 263-276.
[28]	Kang B, Zhang ZC, Wang LL, Zheng LB, Mao WH, Li MF, Wu YR, Wu P, Mo XR (2013). OsCYP2, a chaperone involved in degradation of auxin-responsive proteins, plays crucial roles in rice lateral root initiation.Plant J 74, 86-97. DOI URL
[29]	Karali D, Oxley D, Runions J, Ktistakis N, Farmaki T (2012). The Arabidopsis thaliana immunophilin ROF1 directly interacts with PI(3)P and PI(3, 5)P2 and affects germination under osmotic stress. PLoS One 7, e48241. DOI URL PMID
[30]	Kaur G, Singh S, Singh H, Chawla M, Dutta T, Kaur H, Bender K, Snedden WA, Kapoor S, Pareek A, Singh P (2015). Characterization of peptidyl-prolyl cis-trans isomerase-and calmodulin-binding activity of a cytosolic Arab- idopsis thaliana cyclophilin AtCyp19-3. PLoS One 10, e0136692.
[31]	Kong GH, Zhao Y, Jing MF, Huang J, Yang J, Xia YQ, Kong L, Ye WW, Xiong Q, Qiao YL, Dong SM, Ma WB, Wang YC (2015). The activation of Phytophthora effector Avr3b by plant cyclophilin is required for the nudix hydrolase activity of Avr3b. PLoS Pathog 11, e1005139. DOI URL PMID
[32]	Lee SS, Park HJ, Yoon DH, Kim BG, Ahn JC, Luan S, Cho HS (2015). Rice cyclophilin OsCYP18-2 is translocated to the nucleus by an interaction with SKIP and enhances drought tolerance in rice and Arabidopsis.Plant Cell Environ 38, 2071-2087. DOI URL PMID
[33]	Li BB, Xu WZ, Xu YY, Zhang YY, Wang T, Bai Y, Han CG, Zhang AM, Xu ZH, Chong K (2010). Integrative study on proteomics, molecular physiology, and genetics reveals an accumulation of cyclophilin-like protein, TaCYP20-2, lead- ing to an increase of Rht protein and dwarf in a novel GA- insensitive mutant ( gaid) in wheat. J Proteome Res 9, 4242-4253. DOI URL PMID
[34]	Li H, He ZY, Lu GH, Lee SC, Alonso J, Ecker JR, Luan S (2007). A WD40 domain cyclophilin interacts with histone H3 and functions in gene repression and organogenesis in Arabidopsis.Plant Cell 19, 2403-2416. DOI URL PMID
[35]	Li H, Luan S (2010). AtFKBP53 is a histone chaperone required for repression of ribosomal RNA gene expression in Arabidopsis.Cell Res 20, 357-366. DOI URL
[36]	Li H, Luan S (2011). The cyclophilin AtCYP71 interacts with CAF-1 and LHP1 and functions in multiple chromatin remodeling processes.Mol Plant 4, 748-758. DOI URL PMID
[37]	Li M, Ma XQ, Chiang YH, Yadeta KA, Ding PF, Dong LS, Zhao Y, Li XM, Yu YF, Zhang L, Shen QH, Xia B, Coaker G, Liu D, Zhou JM (2014). Proline isomerization of the immune receptor-interacting protein RIN4 by a cyclophilin inhibits effector-triggered immunity in Arabidopsis.Cell Host Microbe 16, 473-483. DOI URL PMID
[38]	Lighezan L, Meiri D, Breiman A, Neagu A (2013). Circular dichroism and the secondary structure of the ROF2 protein from Arabidopsis thaliana. J Biol Phys 39, 635-648.
[39]	Lima A, Lima S, Wong JH, Phillips RS, Buchanan BB, Luan S (2006). A redox-active FKBP-type immunophilin functions in accumulation of the photosystem II supercomplex in Arabidopsis thaliana. Proc Natl Acad Sci USA 103, 12631-12636. DOI URL PMID
[40]	Lu Y, Du JJ, Yu ZB, Peng JJ, Xu JN, Wang XY (2014). Identification of potential targets for thylakoid oxidoreductase AtVKOR/LTO1 in chloroplasts.Protein Pept Lett 22, 219-225. DOI URL PMID
[41]	Ma XQ, Song L, Yang YX, Liu D (2013). A gain-of-function mutation in the ROC1 gene alters plant architecture in Ara- bidopsis. New Phytol 197, 751-762.
[42]	Mainali HR, Chapman P, Dhaubhadel S (2014). Genome- wide analysis of Cyclophilin gene family in soybean(Glycine max). BMC Plant Biol 14, 282.
[43]	Maris C, Dominguez C, Allain FH (2005). The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression.FEBS J 272, 2118-2131. DOI URL PMID
[44]	Meiri D, Breiman A (2009). Arabidopsis ROF1 (FKBP62) modulates thermotolerance by interacting with HSP90.1 and affecting the accumulation of HsfA2-regulated sHSPs.Plant J 59, 387-399. DOI URL PMID
[45]	Mokriakova MV, Pogorelko GV, Bruskin SA, Piruzian ES, Abdeeva IA (2014). The role of peptidyl-prolyl cis/trans isomerase genes of Arabidopsis thaliana in plant defense during the course of Xanthomonas campestris infection. Genetika 50, 157-166.
[46]	Pai? AT, Fulgosi H (2016). Chloroplast immunophilins.Protoplasma 253, 249-258. DOI URL
[47]	Park HJ, Lee SS, You YN, Yoon DH, Kim BG, Ahn JC, Cho HS (2013a). A rice immunophilin gene, OsFKBP16-3, con- fers tolerance to environmental stress in Arabidopsis and rice. Int J Mol Sci 14, 5899-5919.
[48]	Park SW, Li W, Viehhauser A, He B, Kim S, Nilsson AK, Andersson MX, Kittle JD, Ambavaram MM, Luan S, Esker AR, Tholl D, Cimini D, Ellerstr?m M, Coaker G, Mitchell TK, Pereira A, Dietz KJ, Lawrence CB (2013b). Cyclophilin 20-3 relays a 12-oxo-phytodienoic acid signal during stress responsive regulation of cellular redox homeostasis.Proc Natl Acad Sci USA 110, 9559-9564. DOI URL
[49]	Peng LW, Fukao Y, Fujiwara M, Takami T, Shikanai T (2009). Efficient operation of NAD(P)H dehydrogenase re- quires supercomplex formation with photosystem I via minor LHCI in Arabidopsis.Plant Cell 21, 3623-3640. DOI URL PMID
[50]	Pogorelko GV, Mokryakova M, Fursova OV, Abdeeva I, Piruzian ES, Bruskin SA (2014). Characterization of three Arabidopsis thaliana immunophilin genes involved in the plant defense response against Pseudomonas syringae. Gene 538, 12-22.
[51]	Rahfeld JU, Schierhorn A, Mann K, Fischer G (1994). A novel peptidyl-prolyl cis/trans isomerase from Escherichia coli. FEBS Lett 343, 65-69.
[52]	Rokka A, Aro EM, Herrmann RG, Andersson B, Vener AV (2000). Dephosphorylation of photosystem II reaction cen- ter proteins in plant photosynthetic membranes as an immediate response to abrupt elevation of temperature.Plant Physiol 123, 1525-1536. DOI URL
[53]	Roudier F, Gissot L, Beaudoin F, Haslam R, Michaelson L, Marion J, Molino D, Lima A, Bach L, Morin H, Tellier F, Palauqui JC, Bellec Y, Renne C, Miquel M, DaCosta M, Vignard J, Rochat C, Markham JE, Moreau P, Napier J, Faure JD (2010). Very-long-chain fatty acids are involved in polar auxin transport and developmental patterning in Arabidopsis.Plant Cell 22, 364-375. DOI URL PMID
[54]	Ruan SL, Ma HS, Wang SH, Fu YP, Xin Y, Liu WZ, Wang F, Tong JX, Wang SZ, Chen HZ (2011). Proteomic identification of OsCYP2, a rice cyclophilin that confers salt tolerance in rice ( Oryza sativa L.) seedlings when overexpressed. BMC Plant Biol 11, 34. DOI URL PMID
[55]	Schiene-Fischer C (2015). Multidomain peptidyl prolyl cis/ trans isomerases. Biochim Biophys Acta 1850, 2005-2016. DOI URL PMID
[56]	Seok MS, You YN, Park HJ, Lee SS, Aigen F, Luan S, Ahn JC, Cho HS (2014). AtFKBP16-1, a chloroplast lumenal immunophilin, mediates response to photosynthetic stress by regulating PsaL stability.Plant Physiol 150, 620-631. DOI URL PMID
[57]	Sirpi? S, Holmstr?m M, Battchikova N, Aro EM (2009). AtCYP20-2 is an auxiliary protein of the chloroplast NAD(P)H dehydrogenase complex.FEBS Lett 583, 2355-2358. DOI URL PMID
[58]	Sirpi? S, Khrouchtchova A, Allahverdiyeva Y, Hansson M, Fristedt R, Vener AV, Scheller HV, Jensen PE, Haldrup A, Aro EM (2008). AtCYP38 ensures early biogenesis, correct assembly and sustenance of photosystem II.Plant J 55, 639-651. DOI URL PMID
[59]	Sivils JC, Storer CL, Galigniana MD, Cox MB (2011). Regulation of steroid hormone receptor function by the 52-kDa FK506-binding protein (FKBP52).Curr Opin Phar- macol 11, 314-319. DOI URL PMID
[60]	Smyczynski C, Roudier F, Gissot L, Vaillant E, Grandjean O, Morin H, Masson T, Bellec Y, Geelen D, Faure JD (2006). The C terminus of the immunophilin PASTICCI- NO1 is required for plant development and for interaction with a NAC-like transcription factor.J Biol Chem 281, 25475-25484. DOI URL PMID
[61]	Spiegelman Z, Ham BK, Zhang ZL, Toal TW, Brady SM, Zheng Y, Fei ZJ, Lucas WJ, Wolf S (2015). A tomato phloem-mobile protein regulates the shoot-to-root ratio by mediating the auxin response in distant organs.Plant J 83, 853-863. DOI URL PMID
[62]	Trivedi DK, Yadav S, Vaid N, Tuteja N (2012). Genome wide analysis of Cyclophilin gene family from rice and Ara- bidopsis and its comparison with yeast. Plant Signal Behav 7, 1653-1666.
[63]	Trupkin SA, Mora-García S, Casal JJ (2012). The cyclophilin ROC1 links phytochrome and cryptochrome to bras- sinosteroid sensitivity.Plant J 71, 712-723. DOI URL PMID
[64]	Vasudevan D, Fu AG, Luan S, Swaminathan K (2012). Crystal structure of Arabidopsis cyclophilin38 reveals a previously uncharacterized immunophilin fold and a possible autoinhibitory mechanism.Plant Cell 24, 2666-2674. DOI URL PMID
[65]	Vasudevan D, Gopalan G, Kumar A, Garcia VJ, Luan S, Swaminathan K (2015). Plant immunophilins: a review of their structure-function relationship.Biochim Biophys Acta 1850, 2145-2158. DOI URL PMID
[66]	Vespa L, Vachon G, Berger F, Perazza D, Faure JD, Herzog M (2004). The immunophilin-interacting protein AtFIP37 from Arabidopsis is essential for plant development and is involved in trichome endoreduplication.Plant Physiol 134, 1283-1292. DOI URL
[67]	Voinnet O (2009). Origin, biogenesis, and activity of plant microRNAs.Cell 136, 669-687. DOI URL PMID
[68]	Wang B, Bailly A, Zwiewka M, Henrichs S, Azzarello E, Mancuso S, Maeshima M, Friml J, Schulz A, Geisler M (2013). Arabidopsis TWISTED DWARF1 functionally inter- acts with auxin exporter ABCB1 on the root plasma membrane. Plant Cell 25, 202-214. DOI URL PMID
[69]	Wang P, Li XZ, Cui HR, Feng YG, Wang XY (2014). Identification and functional analysis of a novel parvulin-type peptidyl-prolyl isomerase from Gossypium hirsutum. Plant Physiol Biochem 76, 58-66. DOI URL PMID
[70]	Wang Y, Han R, Zhang W, Yuan Y, Zhang X, Long Y, Mi H (2008). Human CyP33 binds specifically to mRNA and binding stimulates PPIase activity of hCyP33.FEBS Lett 582, 835-839. DOI URL PMID
[71]	Wang Y, Liu C, Yang DW, Yu H, Liou YC (2010). Pin1At encoding a peptidyl-prolyl cis/trans isomerase regulates flowering time in Arabidopsis. Mol Cell 37, 112-122.
[72]	Wang YQ, Zeng LZ, Xing D (2015). ROS-mediated enhanced transcription of CYP38 promotes the plant tolerance to high light stress by suppressing GTPase activation of PsbO2.Front Plant Sci 6, 777. DOI URL PMID
[73]	Wu GS, Otegui MS, Spalding EP (2010). The ER-Localized TWD1 immunophilin is necessary for localization of multidrug resistance-like proteins required for polar auxin transport in Arabidopsis roots.Plant Cell 22, 3295-3304. DOI URL PMID
[74]	Xi WY, Gong XM, Yang QY, Yu H, Liou YC (2016). Pin1At regulates PIN1 polar localization and root gravitropism.Nat Commun 7, 10430. DOI URL PMID
[75]	Yoon DH, Lee SS, Park HJ, Lyu JI, Chong WS, Liu JR, Kim BG, Ahn JC, Cho HS (2016). Overexpression of OsCYP19-4 increases tolerance to cold stress and enhances grain yield in rice ( Oryza sativa). J Exp Bot 67, 69-82.
[76]	Yu YL, Li YZ, Huang GX, Meng ZD, Zhang D, Wei J, Yan K, Zheng CC, Zhang YL (2011). PwHAP5, a CCAAT-binding transcription factor, interacts with PwFKBP12 and plays a role in pollen tube growth orientation inPicea wilsonii. J Exp Bot 62, 4805-4817. DOI URL PMID
[77]	Zhang YY, Li BB, Xu YY, Li H, Li SS, Zhang DJ, Mao ZW, Guo SY, Yang CH, Weng YX, Chong K (2013). The cyclophilin CYP20-2 modulates the conformation of BRAS- SINAZOLE-RESISTANT1, which binds the promoter of FLOWERING LOCUS D to regulate flowering in Arabidopsis. Plant Cell 25, 2504-2521. DOI URL PMID
[78]	Zhao BL, Lv MH, Feng ZX, Campbell T, Liscum E, Li J (2016). TWISTED DWARF 1 associates with BRASSINOSTEROID-INSENSITIVE 1 to regulate early events of the brassinosteroid signaling pathway.Mol Plant 9, 582-592. DOI URL PMID
[79]	Zheng HK, Li SJ, Ren B, Zhang J, Ichii M, Taketa S, Tao YZ, Zuo JR, Wang H (2013). LATERAL ROOTLESS2, a cyclophilin protein, regulates lateral root initiation and au- xin signaling pathway in rice.Mol Plant 6, 1719-1721. DOI URL PMID
[80]	Zhu JS, Bailly A, Zwiewka M, Sovero V, Di Donato M, Ge P, Oehri J, Aryal B, Hao PC, Linnert M, Burgardt NI, Lücke C, Weiwad M, Michel M, Weiergr?ber OH, Pollmann S, Azzarello E, Mancuso S, Ferro N, Fukao Y, Hoffmann C, Wedlich-S?ldner R, Friml J, Thomas C, Geisler M (2016). TWISTED DWARF1 mediates the action of auxin transport inhibitors on actin cytoskeleton dynamics.Plant Cell 28, 930-948. DOI URL PMID
[81]	Zhu JS, Geisler M (2015). Keeping it all together: auxin-actin crosstalk in plant development.J Exp Bot 66, 4983-4998. DOI URL PMID