A transcriptome-wide identification of ATP-binding cassette (ABC) transporters revealed participation of ABCB subfamily in abiotic stress management of Glycyrrhiza glabra L.
Glycyrrhiza glabra
ATP-binding cassette transporter
Gene expression
N-1-naphthylphthalamic acid
Nucleotide binding domain
Phytohormones
Transmembrane binding domain
Journal
BMC genomics
ISSN: 1471-2164
Titre abrégé: BMC Genomics
Pays: England
ID NLM: 100965258
Informations de publication
Date de publication:
27 Mar 2024
27 Mar 2024
Historique:
received:
20
10
2023
accepted:
15
03
2024
medline:
27
3
2024
pubmed:
27
3
2024
entrez:
27
3
2024
Statut:
epublish
Résumé
Transcriptome-wide survey divulged a total of 181 ABC transporters in G. glabra which were phylogenetically classified into six subfamilies. Protein-Protein interactions revealed nine putative GgABCBs (-B6, -B14, -B15, -B25, -B26, -B31, -B40, -B42 &-B44) corresponding to five AtABCs orthologs (-B1, -B4, -B11, -B19, &-B21). Significant transcript accumulation of ABCB6 (31.8 folds), -B14 (147.5 folds), -B15 (17 folds), -B25 (19.7 folds), -B26 (18.31 folds), -B31 (61.89 folds), -B40 (1273 folds) and -B42 (51 folds) was observed under the influence of auxin. Auxin transport-specific inhibitor, N-1-naphthylphthalamic acid, showed its effectiveness only at higher (10 µM) concentration where it down regulated the expression of ABCBs, PINs (PIN FORMED) and TWD1 (TWISTED DWARF 1) genes in shoot tissues, while their expression was seen to enhance in the root tissues. Further, qRT-PCR analysis under various growth conditions (in-vitro, field and growth chamber), and subjected to abiotic stresses revealed differential expression implicating role of ABCBs in stress management. Seven of the nine genes were shown to be involved in the stress physiology of the plant. GgABCB6, 15, 25 and ABCB31 were induced in multiple stresses, while GgABCB26, 40 & 42 were exclusively triggered under drought stress. No study pertaining to the ABC transporters from G. glabra is available till date. The present investigation will give an insight to auxin transportation which has been found to be associated with plant growth architecture; the knowledge will help to understand the association between auxin transportation and plant responses under the influence of various conditions.
Identifiants
pubmed: 38532362
doi: 10.1186/s12864-024-10227-z
pii: 10.1186/s12864-024-10227-z
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
315Informations de copyright
© 2024. The Author(s).
Références
Do THT, Martinoia E, Lee Y, Hwang J-U. 2021 update on ATP-binding cassette (ABC) transporters: how they meet the needs of plants. Plant Physiol. 2021;187:1876–92.
doi: 10.1093/plphys/kiab193
Saha J, Sengupta A, Gupta K, Gupta B. Molecular phylogenetic study and expression analysis of ATP-binding cassette transporter gene family in Oryza sativa in response to salt stress. Comput Biol Chem. 2015;54:18–32.
doi: 10.1016/j.compbiolchem.2014.11.005
Dahuja A, Kumar RR, Sakhare A, Watts A, Singh B, Goswami S, Sachdev A, Praveen S. Role of ATP-binding cassette transporters in maintaining plant homeostasis under abiotic and biotic stresses. Physiol Plant. 2021;171:785–801.
doi: 10.1111/ppl.13302
Sanchez-Fernandez R, Davies TGE, Coleman JOD, Rea PA. The Arabidopsis thaliana ABC protein superfamily, a complete inventory. J Biol Chem. 2001;276:30231–44.
doi: 10.1074/jbc.M103104200
Wilkens S. Structure and mechanism of ABC transporters. F1000Prime Rep. 2015;7:14.
doi: 10.12703/P7-14
Campbell EJ, Schenk PM, Kazan K, Penninckx IAMA, Anderson JP, Maclean DJ. Pathogen-responsive expression of a putative ATP-binding cassette transporter gene conferring resistance to the diterpenoid sclareol is regulated by multiple defence signaling pathways in Arabidopsis. Plant Physiol. 2003;133(3):1272–84.
doi: 10.1104/pp.103.024182
Chen S, Sãnchez-Fernãndez R, Lyver ER, Dancis A, Rea PA. Functional characterization of AtATM1, AtATM2, and AtATM3, a subfamily of Arabidopsis half-molecule ATP-binding cassette transporters implicated in iron homeostasis. J Biol Chem. 2007;282(29):21561–71.
doi: 10.1074/jbc.M702383200
Frelet-Barrand A, Kolukisaoglu HU, Plaza S, Ruffer M, Azevedo L, Hortensteiner S. Comparative mutant analysis of arabidopsis ABCC-type ABC transporters: AtMRP2 contributes to detoxification, vacuolar organic anion transport and chlorophyll degradation. Plant Cell Physiol. 2008;49(4):557–69.
doi: 10.1093/pcp/pcn034
Borghi L, Kang J, de Brito FR. Filling the Gap: Functional Clustering of ABC Proteins for the Investigation of Hormonal Transport in planta. Front Plant Sci. 2019;10:422.
doi: 10.3389/fpls.2019.00422
An L, Ma Q, Du J, Yu M, Li F, Luan J, Jiang J, Li H. Preliminary Classification of the ABC Transporter Family in Betula halophila and Expression Patterns in Response to Exogenous Phytohormones and Abiotic Stresses. Forests. 2019;10:722.
doi: 10.3390/f10090722
Hall T, Biosciences I, Carlsbad C. BioEdit: an important software for molecular biology. GERF Bull Biosci. 2011;2:60–1.
Yoon BJ. Hidden Markov models and their applications in biological sequence analysis. Curr Genomics. 2009;10:402–15.
doi: 10.2174/138920209789177575
Gasteiger E, Gattiker A, Hoogland C, Ivanyi I, Appel RD, Bairoch A. ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res. 2003;31:3784–8.
doi: 10.1093/nar/gkg563
Horton P, Park K-J, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K. WoLF PSORT: protein localization predictor. Nucleic Acids Res. 2007;35:W585–7.
doi: 10.1093/nar/gkm259
Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 2009;37:W202–8.
doi: 10.1093/nar/gkp335
Lamesch P, Berardini TZ, Li D, Swarbreck D, Wilks C, Sasidharan R, Muller R, Dreher K, Alexander DL, Garcia-Hernandez M. The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res. 2012;40:D1202–10.
doi: 10.1093/nar/gkr1090
Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016;33:1870–4.
doi: 10.1093/molbev/msw054
Letunic I, Bork P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 2021;49:W293–6.
doi: 10.1093/nar/gkab301
Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, Simonovic M, Roth A, Santos A, Tsafou KP. STRING v10: protein–protein interaction networks, integrated over the tree of life. Nucleic Acids Res. 2015;43:D447–52.
doi: 10.1093/nar/gku1003
Gupta S, Pandotra P, Gupta AP, Verma MK, Ahuja A, Vishwakarma RA. Direct rhizogenesis, in vitro stolon proliferation and high-throughput regeneration of plantlets in Glycyrrhiza glabra. Acta Physiol Plant. 2013;35:2699–705.
doi: 10.1007/s11738-013-1302-1
Reuscher S, Akiyama M, Yasuda T, Makino H, Aoki K, Shibata D, Shiratake K. The sugar transporter inventory of tomato: genome-wide identification and expression analysis. Plant Cell Physiol. 2014;55:1123–41.
doi: 10.1093/pcp/pcu052
Peelman F, Labeur C, Vanloo B, Roosbeek S, Devaud C, Duverger N, Denefle P, Rosier M, Vandekerckhove Jl, Rosseneu M. Characterization of the ABCA transporter subfamily: identification of prokaryotic and eukaryotic members, phylogeny and topology. J Mol Biol. 2003;325:259–74.
doi: 10.1016/S0022-2836(02)01105-1
Kaminski WE, Piehler A, Wenzel JrJ. ABC A-subfamily transporters: structure, function and disease. Biochim Biophys Acta Mol Basis Dis. 2006;1762(5):510–24.
doi: 10.1016/j.bbadis.2006.01.011
Garcia O, Bouige P, Forestier C, Dassa E. Inventory and comparative analysis of rice and Arabidopsis ATP-binding cassette (ABC) systems. J Mol Biol. 2004;343:249–65.
doi: 10.1016/j.jmb.2004.07.093
Sugiyama A, Shitan N, Sato S, Nakamura Y, Tabata S, Yazaki K. Genome-wide analysis of ATP-binding cassette (ABC) proteins in a model legume plant, Lotus japonicus: comparison with Arabidopsis ABC protein family. DNA Res. 2006;13:205–28.
doi: 10.1093/dnares/dsl013
Cakir B, Kilickaya O. Whole-genome survey of the putative ATP-binding cassette transporter family genes in Vitis vinifera. PLoS ONE. 2013;8: e78860.
doi: 10.1371/journal.pone.0078860
Ofori PA, Mizuno A, Suzuki M, Martinoia E, Reuscher S, Aoki K, Shibata D, Otagaki S, Matsumoto S, Shiratake K. Genome-wide analysis of ATP binding cassette (ABC) transporters in tomato. PLoS ONE. 2018;13: e0200854.
doi: 10.1371/journal.pone.0200854
Yan C, Duan W, Lyu S, Li Y, Hou X. Genome-wide identification, evolution, and expression analysis of the ATP-binding cassette transporter gene family in Brassica rapa. Front Plant Sci. 2017;8:349.
doi: 10.3389/fpls.2017.00349
Yan L, Zhang J, Chen H, Luo H. Genome-wide analysis of ATP-binding cassette transporter provides insight to genes related to bioactive metabolite transportation in Salvia miltiorrhiza. BMC Genom. 2021;22:315.
doi: 10.1186/s12864-021-07623-0
Chen P, Li Y, Zhao L, Hou Z, Yan M, Hu B, Liu Y, Azam SM, Zhang Z, Rahman ZU. Genome-wide identification and expression profiling of ATP-binding cassette (ABC) transporter gene family in pineapple (Ananas comosus (L.) Merr.) reveal the role of AcABCG38 in pollen development. Front Plant Sci. 2017;8:2150.
doi: 10.3389/fpls.2017.02150
Ferro M, Brugiere S, Salvi D, Seigneurin-Berny D, Moyet L, Ramus C, Miras S, Mellal M, Le Gall S, Kieffer-Jaquinod S. AT_CHLORO, a comprehensive chloroplast proteome database with subplastidial localization and curated information on envelope proteins. Mol Cell Proteomics. 2010;9:1063–84.
doi: 10.1074/mcp.M900325-MCP200
Jaquinod M, Villiers F, Kieffer-Jaquinod S, Hugouvieux Vr, Bruley C, Garin Jrm, Bourguignon J. A proteomics dissection of Arabidopsis thaliana vacuoles isolated from cell culture. Mol Cell Proteomics. 2007;6(3):394–412.
doi: 10.1074/mcp.M600250-MCP200
Larsen PB, Cancel J, Rounds M, Ochoa V. Arabidopsis ALS1 encodes a root tip and stele localized half type ABC transporter required for root growth in an aluminum toxic environment. Planta. 2007;225:1447–58.
doi: 10.1007/s00425-006-0452-4
Geisler M, Blakeslee JJ, Bouchard R, Lee OR, Vincenzetti V, Bandyopadhyay A, Titapiwatanakun B, Peer WA, Bailly A, Richards EL. Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1. Plant J. 2005;44:179–94.
doi: 10.1111/j.1365-313X.2005.02519.x
Wu G, Cameron JN, Ljung K, Spalding EP. A role for ABCB19-mediated polar auxin transport in seedling photomorphogenesis mediated by cryptochrome 1 and phytochrome B. Plant J. 2010;62:179–91.
doi: 10.1111/j.1365-313X.2010.04137.x
Pang K, Li Y, Liu M, Meng Z, Yu Y. Inventory and general analysis of the ATP-binding cassette (ABC) gene superfamily in maize(Zea mays L.). Gene. 2013;526:411–28.
doi: 10.1016/j.gene.2013.05.051
Sheppard DN, Welsh MJ. Structure and function of the CFTR chloride channel. Physiol Rev. 1999;79:S23–45.
doi: 10.1152/physrev.1999.79.1.S23
Moreau C, Prost A-L, Derand R, Vivaudou M. SUR, ABC proteins targeted by KATP channel openers. J Mol Cell Cardiol. 2005;38:951–63.
doi: 10.1016/j.yjmcc.2004.11.030
Verrier PJ, Bird D, Burla B, Dassa E, Forestier C, Geisler M, Klein M, Kolukisaoglu U, Lee Y, Martinoia E. Plant ABC proteins- a unified nomenclature and updated inventory. Trends Plant Sci. 2008;13:151–9.
doi: 10.1016/j.tplants.2008.02.001
Nagy Rk, Grob H, Weder B, Green P, Klein M, Frelet-Barrand A, Schjoerring JK, Brearley C, Martinoia E. The Arabidopsis ATP-binding cassette protein AtMRP5/AtABCC5 is a high affinity inositol hexakisphosphate transporter involved in guard cell signaling and phytate storage. J Biol Chem. 2009;284:33614–22.
doi: 10.1074/jbc.M109.030247
Remy E, Duque P. Beyond cellular detoxification: a plethora of physiological roles for MDR transporter homologs in plants. Front Physiol. 2014;5:201.
doi: 10.3389/fphys.2014.00201
Murina V, Kasari M, Takada H, Hinnu M, Saha CK, Grimshaw JW, Seki T, Reith M, Putrina M, Tenson T. ABCF ATPases involved in protein synthesis, ribosome assembly and antibiotic resistance: structural and functional diversification across the tree of life. J Mol Biol. 2019;431(18):3568–90.
doi: 10.1016/j.jmb.2018.12.013
Huang J, Li X, Chen X, Guo Y, Liang W, Wang H. Genome-wide identification of soybean ABC transporters relate to aluminum toxicity. Int J Mol Sci. 2021;22:6556.
doi: 10.3390/ijms22126556
Tyzack JK, Wang X, Belsham GJ, Proud CG. ABC50 interacts with eukaryotic initiation factor 2 and associates with the ribosome in an ATP-dependent manner. J Biol Chem. 2000;275:34131–9.
doi: 10.1074/jbc.M002868200
Izquierdo Y, Kulasekaran S, Benito P, Lopez B, Marcos R, Cascon T, Hamberg M, Castresana C. Arabidopsis nonresponding to oxylipins locus NOXY7 encodes a yeast GCN1 homolog that mediates noncanonical translation regulation and stress adaptation. Plant Cell Environ. 2018;41:1438–52.
doi: 10.1111/pce.13182
Han T-T, Liu W-C, Lu Y-T. General control non-repressible 20 (GCN20) functions in root growth by modulating DNA damage repair in Arabidopsis. BMC Plant Biol. 2018;18:1–10.
doi: 10.1186/s12870-018-1444-9
Li S, Li D, Zhang P, Wang R, Sun L, Wan J, Xu J. ABCF3 regulates the expression of aquaporin genes and endoplasmic reticulum stress-related genes in Arabidopsis. Theor Exp Plant Physiol. 2018;30:215–22.
doi: 10.1007/s40626-018-0116-3
Kaundal A, Ramu VS, Oh S, Lee S, Pant B, Lee H-K, Rojas CM, Senthil-Kumar M, Mysore KS. GENERAL CONTROL NONREPRESSIBLE4 degrades 14-3-3 and the RIN4 complex to regulate stomatal aperture with implications on nonhost disease resistance and drought tolerance. Plant Cell. 2017;29:2233–48.
doi: 10.1105/tpc.17.00070
Bienert MD, Baijot A, Boutry M. ABCG transporters and their role in the biotic stress response. In: Geisler, M. (eds) Plant ABC Transporters. Signaling and Communication in Plants. 2014;22.
Borghi L, Kang J, Ko D, Lee Y, Martinoia E. The role of ABCG-type ABC transporters in phytohormone transport. Biochem Soc Trans. 2015;43:924–30.
doi: 10.1042/BST20150106
Le Hir R, Sorin C, Chakraborti D, Moritz T, Schaller H, Tellier F, Robert S, Morin H, Bako L, Bellini C. Plant J.ABCG 9, ABCG 11 and ABCG 14 ABC transporters are required for vascular development in Arabidopsis. Plant J. 2013;76(5):811–24.
doi: 10.1111/tpj.12334
Ko D, Kang J, Kiba T, Park J, Kojima M, Do J, Kim KY, Kwon M, Endler A, Song W-Y. Arabidopsis ABCG14 is essential for the root-to-shoot translocation of cytokinin. Proc Natl. 2014;111:7150–5.
doi: 10.1073/pnas.1321519111
Zhang K, Novak O, Wei Z, Gou M, Zhang X, Yu Y, Yang H, Cai Y, Strnad M, Liu C-J. Arabidopsis ABCG14 protein controls the acropetal translocation of root-synthesized cytokinins. Nat Commun. 2014;5:3274.
doi: 10.1038/ncomms4274
Wang S, Wang S, Sun Q, Yang L, Zhu Y, Yuan Y, Hua J. A role of cytokinin transporter in Arabidopsis immunity. Mol Plant Microbe Interact. 2017;30:325–33.
doi: 10.1094/MPMI-01-17-0011-R
Fedi F, O’Neill CM, Menard G, Trick M, Dechirico S, Corbineau F, Bailly C, Eastmond PJ, Penfield S. Awake1, an ABC-type transporter, reveals an essential role for suberin in the control of seed dormancy. Plant Physiol. 2017;174:276–83.
doi: 10.1104/pp.16.01556
Kuromori T, Sugimoto E, Ohiraki H, Yamaguchi-Shinozaki K, Shinozaki K. Functional relationship of AtABCG21 and AtABCG22 in stomatal regulation. Sci Rep. 2017;7:12501.
doi: 10.1038/s41598-017-12643-6
Yadav V, Molina I, Ranathunge K, Castillo IQ, Rothstein SJ, Reed JW. ABCG transporters are required for suberin and pollen wall extracellular barriers in Arabidopsis. Plant Cell. 2014;26:3569–88.
doi: 10.1105/tpc.114.129049
Xu XM, Moller SG. AtNAP7 is a plastidic SufC-like ATP-binding cassette/ATPase essential for Arabidopsis embryogenesis. Proc Natl Acad Sci. 2004;101:9143–8.
doi: 10.1073/pnas.0400799101
Rayapuram N, Hagenmuller Jrm, Grienenberger J-M, Giege P, Bonnard Gr. AtCCMA interacts with AtCcmB to form a novel mitochondrial ABC transporter involved in cytochrome c maturation in Arabidopsis. J Biol Chem. 2007;282(29):21015–23.
doi: 10.1074/jbc.M704091200
Yazaki K, Shitan N, Sugiyama A, Takanashi K. Cell and molecular biology of ATP-binding cassette proteins in plants. Int Rev Cell Mol Biol. 2009;276:263–99.
doi: 10.1016/S1937-6448(09)76006-X
Kang J, Park J, Choi H, Burla B, Kretzschmar T, Lee Y, Martinoia E. Plant ABC transporters. Arabidopsis Book9. 2011;e0153.
Voith von Voithenberg L, Park J, Stube R, Lux C, Lee Y, Philippar K. A novel prokaryote-type ECF/ABC transporter module in chloroplast metal homeostasis. Front Plant Sci. 2019;10:1264.
doi: 10.3389/fpls.2019.01264
Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P. Protein function. In Molecular Biology of the Cell. 4th ed. Garland Science. New York, NY, USA. 2002.
Okamoto K, Ueda H, Shimada T, Tamura K, Koumoto Y, Tasaka M, Morita MT, Hara-Nishimura I. An ABC transporter B family protein, ABCB19, is required for cytoplasmic streaming and gravitropism of the inflorescence stems. Plant Signal Behav. 2016;11: e1010947.
doi: 10.1080/15592324.2015.1010947
Marchant A, Kargul J, May ST, Muller P, Delbarre A, Perrot-Rechenmann C, Bennett MJ. AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues. EMBO J. 1999;8:2066–73.
doi: 10.1093/emboj/18.8.2066
O’Connor DL, Runions A, Sluis A, Bragg J, Vogel JP, Prusinkiewicz P, Hake S. A division in PIN-mediated auxin patterning during organ initiation in grasses. PLoS Comput Biol. 2014;10: e1003447.
doi: 10.1371/journal.pcbi.1003447
Shen C, Bai Y, Wang S, Zhang S, Wu Y, Chen M, Jiang D, Qi Y. Expression profile of PIN, AUX/LAX and PGP auxin transporter gene families in Sorghum bicolor under phytohormone and abiotic stress. FEBS J. 2010;277:2954–69.
doi: 10.1111/j.1742-4658.2010.07706.x
Chai C, Subudhi PK. Comprehensive analysis and expression profiling of the OsLAX and OsABCB auxin transporter gene families in rice (Oryza sativa) under phytohormone stimuli and abiotic stresses. Front Plant Sci. 2016;7:593.
doi: 10.3389/fpls.2016.00593
Nguyen VNT, Moon S, Jung K-H. Genome-wide expression analysis of rice ABC transporter family across spatio-temporal samples and in response to abiotic stresses. J Plant Physiol. 2014;171:1276–88.
doi: 10.1016/j.jplph.2014.05.006
Yue R, Tie S, Sun T, Zhang L, Yang Y, Qi J, Yan S, Han X, Wang H, Shen C. Genome-wide identification and expression profiling analysis of ZmPIN, ZmPILS, ZmLAX and ZmABCB auxin transporter gene families in maize (Zea mays L.) under various abiotic stresses. PLoS One. 2015;10(3):e0118751.
doi: 10.1371/journal.pone.0118751
Yu C, Dong W, Zhan Y, Huang Z-a, Li Z, Kim IS, Zhang C. Genome-wide identification and expression analysis of ClLAX, ClPIN and ClABCB genes families in Citrullus lanatus under various abiotic stresses and grafting. BMC Genet. 2017;18:1–15.
doi: 10.1186/s12863-017-0500-z
Kamimoto Y, Terasaka K, Hamamoto M, Takanashi K, Fukuda S, Shitan N, Sugiyama A, Suzuki H, Shibata D, Wang B. Arabidopsis ABCB21 is a facultative auxin importer/exporter regulated by cytoplasmic auxin concentration. Plant Cell Physiol. 2012;53:2090–100.
doi: 10.1093/pcp/pcs149
Kubeš M, Yang H, Richter GL, Cheng Y, Młodzińska E, Wang X, Blakeslee JJ, Carraro N, Petrášek J, Zažímalová E. The Arabidopsis concentration-dependent influx/efflux transporter ABCB4 regulates cellular auxin levels in the root epidermis. Plant J. 2012;69:640–54.
doi: 10.1111/j.1365-313X.2011.04818.x
Noh B, Murphy AS, Spalding EP. Multidrug resistance-like genes of Arabidopsis required for auxin transport and auxin-mediated development. Plant Cell. 2001;13(11):2441–54.
Xu Y, Zhang S, Guo H, Wang S, Xu L, Li C, Qian Q, Chen F, Geisler M, Qi Y, Jiang DA. OsABCB14 functions in auxin transport and iron homeostasis in rice (Oryza sativa L.). Plant J. 2014;79(1):106–17.
doi: 10.1111/tpj.12544
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;58:1601–14.
doi: 10.1093/pcp/pcx104
Butler JH, Hu S, Brady SR, Dixon MW, Muday GK. In vitro and in vivo evidence for actin association of the naphthylphthalamic acid-binding protein from zucchini hypocotyls. Plant J. 1998;13:291–301.
doi: 10.1046/j.1365-313X.1998.00017.x
Reed RC, Brady SR, Muday GK. Inhibition of auxin movement from the shoot into the root inhibits lateral root development in Arabidopsis. Plant Physiol. 1998;118:1369–78.
doi: 10.1104/pp.118.4.1369
Zhiyi N, Guijuan K, Yu L, Longjun D, Rizhong Z. Whole-transcriptome survey of the putative ATP-binding cassette (ABC) transporter family genes in the latex-producing laticifers of Hevea brasiliensis. PLoS ONE. 2015;10: e0116857.
doi: 10.1371/journal.pone.0116857
Nagashima A, Uehara Y, Sakai T. The ABC Subfamily B Auxin Transporter AtABCB19 is Involved in the Inhibitory Effects of N-1-Naphthyphthalamic Acid on the Phototropic and Gravitropic Responses of Arabidopsis Hypocotyls. Plant Cell Physiol. 2008;49:1250–5.
doi: 10.1093/pcp/pcn092
Shitan N, Dalmas F, Dan K, Kato N, Ueda K, Sato F, Forestier C, Yazaki K. Characterization of Coptis japonica CjABCB2, an ATP-binding cassette protein involved in alkaloid transport. Phytochemistry. 2013;91:109–16.
doi: 10.1016/j.phytochem.2012.02.012
Tamizhselvan P, Madhavan S, Constan-Aguilar C, Elrefaay ER, Liu J. PÄ›nÄÃk A, Novák Oe, CairÃ
doi: 10.3390/plants13010007
Lee M, Choi Y, Burla B, Kim YY, Jeon B, Maeshima M, Yoo JY, Martinoia E, Lee Y. The ABC transporter AtABCB14 is a malate importer and modulates stomatal response to CO
doi: 10.1038/ncb1782
Klein M, Geisler M, Suh SJ, Kolukisaoglu HÜ, Azevedo L, Plaza S, Curtis MD, Richter A, Weder B, Schulz B. Disruption of AtMRP4, a guard cell plasma membrane ABCC-type ABC transporter, leads to deregulation of stomatal opening and increased drought susceptibility. Plant J. 2004;39:219–36.
doi: 10.1111/j.1365-313X.2004.02125.x
Brunetti P, Zanella L, De Paolis A, Di Litta D, Cecchetti V, Falasca G, Barbieri M, Altamura MM, Costantino P, Cardarelli M. Cadmium-inducible expression of the ABC-type transporter AtABCC3 increases phytochelatin-mediated cadmium tolerance in Arabidopsis. J Exp Bot. 2015;66:3815–29.
doi: 10.1093/jxb/erv185
Lu Y-P, Li Z-S, Drozdowicz YM, Hörtensteiner S, Martinoia E, Rea PA. AtMRP2, an Arabidopsis ATP binding cassette transporter able to transport glutathione S-conjugates and chlorophyll catabolites: functional comparisons with AtMRP1. Plant Cell. 1998;10:267–82.
Park J, Song WY, Ko D, Eom Y, Hansen TH, Schiller M, Lee TG, Martinoia E, Lee Y. The phytochelatin transporters AtABCC1 and AtABCC2 mediate tolerance to cadmium and mercury. Plant J. 2012;69:278–88.
doi: 10.1111/j.1365-313X.2011.04789.x
Gaillard S, Jacquet H, Vavasseur A, Leonhardt N, Forestier C. AtMRP6/AtABCC6, an ATP-binding cassette transporter gene expressed during early steps of seedling development and up-regulated by cadmium in Arabidopsis thaliana. BMC Plant Biol. 2008;8:1–11.
doi: 10.1186/1471-2229-8-22
Takeuchi M, Kegasa T, Watanabe A, Tamura M, Tsutsumi Y. Expression analysis of transporter genes for screening candidate monolignol transporters using Arabidopsis thaliana cell suspensions during tracheary element differentiation. J Plant Res. 2018;131:297–305.
doi: 10.1007/s10265-017-0979-4
Xi J, Xu P, Xiang CB. Loss of AtPDR11, a plasma membrane-localized ABC transporter, confers paraquat tolerance in Arabidopsis thaliana. Plant J. 2012;69:782–91.
doi: 10.1111/j.1365-313X.2011.04830.x
Stein M, Dittgen J, Sanchez-Rodriguez C, Hou BH, Molina A, Schulze-Lefert P. Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell. 2006;18(3):731–46.
doi: 10.1105/tpc.105.038372
Kim DY, Bovet L, Maeshima M, Martinoia E, Lee Y. The ABC transporter AtPDR8 is a cadmium extrusion pump conferring heavy metal resistance. Plant J. 2007;50:207–18.
doi: 10.1111/j.1365-313X.2007.03044.x
Strader LC, Bartel B. The Arabidopsis PLEIOTROPIC DRUG RESISTANCE8/ABCG36 ATP binding cassette transporter modulates sensitivity to the auxin precursor indole-3-butyric acid. Plant Cell. 2009;21:1992–2007.
doi: 10.1105/tpc.109.065821
Kim DY, Jin JY, Alejandro S, Martinoia E, Lee Y. Overexpression of AtABCG36 improves drought and salt stress resistance in Arabidopsis. Physiol Plant. 2010;139:170–80.
doi: 10.1111/j.1399-3054.2010.01353.x
Choi H, Jin JY, Choi S, Hwang JU, Kim YY, Suh MC, Lee Y. An ABCG/WBC-type ABC transporter is essential for transport of sporopollenin precursors for exine formation in developing pollen. Plant J. 2011;65:181–93.
doi: 10.1111/j.1365-313X.2010.04412.x
Zhao G, Shi J, Liang W, Zhang D. ATP binding cassette G transporters and plant male reproduction. Plant Signal Behav. 2016;1: e1136764.
doi: 10.1080/15592324.2015.1136764
Kuromori T, Miyaji T, Yabuuchi H, Shimizu H, Sugimoto E, Kamiya A, Moriyama Y, Shinozaki K. ABC transporter AtABCG25 is involved in abscisic acid transport and responses. Proc Natl Acad Sci. 2010;107:2361–6.
doi: 10.1073/pnas.0912516107
Kang J, Yim S, Choi H, Kim A, Lee KP, Lopez-Molina L, Martinoia E, Lee Y. Abscisic acid transporters cooperate to control seed germination. Nat Commun. 2015;6:8113.
doi: 10.1038/ncomms9113
Shimadzu S, Seo M, Terashima I, Yamori W. Whole irradiated plant leaves showed faster photosynthetic induction than individually irradiated leaves via improved stomatal opening. Front Plant Sci. 2019;10:1512.
doi: 10.3389/fpls.2019.01512
Lee M, Lee K, Lee J, Noh EW, Lee Y. AtPDR12 contributes to lead resistance in Arabidopsis. Plant Physiol. 2005;138:827–36.
doi: 10.1104/pp.104.058107
Kang J, Hwang JU, Lee M, Kim YY, Assmann SM, Martinoia E. PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. Proc Natl Acad Sci. 2010;107(5):2355–60.
doi: 10.1073/pnas.0909222107
Panikashvili D, Shi JX, Bocobza S, Franke RB, Schreiber L, Aharoni A. The Arabidopsis DSO/ABCG11 transporter affects cutin metabolism in reproductive organs and suberin in roots. Mol Plant. 2010;3:563–75.
doi: 10.1093/mp/ssp103
Bessire M, Borel S, Fabre G, Carrac L, Efremova N, Yephremov A, Cao Y, Jetter R, Jacquat AC, Metraux JP, Nawratha C. A member of the PDR-family of ABC transporters is required for the formation of a functional cuticle in Arabidopsis. Plant Cell. 2011;23:1958–70.
Do THT, Choi H, Palmgren M, Martinoia E, Hwang J-U, Lee Y. Arabidopsis ABCG28 is required for the apical accumulation of reactive oxygen species in growing pollen tubes. Proc Natl Acad Sci. 2019;16:12540–9.
doi: 10.1073/pnas.1902010116
Alejandro S, Lee Y, Tohge T, Sudre D, Osorio S, Park J, Bovet L, Lee Y, Geldner N, Fernie AR, Martinoia E. AtABCG29 is a monolignol transporter involved in lignin biosynthesis. Curr Biol. 2012;22:1207–12.
doi: 10.1016/j.cub.2012.04.064
Khare D, Choi H, Huh SU, Bassin B, Kim J, Martinoia E, Sohn KH, Paek K-H, Lee Y. Arabidopsis ABCG34 contributes to defense against necrotrophic pathogens by mediating the secretion of camalexin. Proc Natl Acad Sci. 2017;114:E5712–20.
doi: 10.1073/pnas.1702259114
Pighin JA, Zheng HQ, Balakshin LJ, Goodman IP, Western TL, Jetter R. Plant cuticular lipid export requires an ABC transporter. Science. 2004;306(5696):702–4.
doi: 10.1126/science.1102331