ATP-binding cassette transporters in nonmodel plants.
ABC transporters
agriculture
chemodiversity
evolution
functional adaptation
nonmodel plants
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
02 2022
02 2022
Historique:
received:
22
06
2021
accepted:
21
09
2021
pubmed:
7
10
2021
medline:
25
3
2022
entrez:
6
10
2021
Statut:
ppublish
Résumé
Knowledge about plant ATP-binding cassette (ABC) proteins is of great value for sustainable agriculture, economic yield, and the generation of high-quality products, especially under unfavorable growth conditions. We have learned much about ABC proteins in model organisms, notably Arabidopsis thaliana; however, the importance of research dedicated to these transporters extends far beyond Arabidopsis biology. Recent progress in genomic and transcriptomic approaches for nonmodel and noncanonical model plants allows us to look at ABC transporters from a wider perspective and consider chemodiversity and functionally driven adaptation as distinctive mechanisms during their evolution. Here, by considering several representatives from agriculturally important families and recent progress in functional characterization of nonArabidopsis ABC proteins, we aim to bring attention to understanding the evolutionary background, distribution among lineages and possible mechanisms underlying the adaptation of this versatile transport system for plant needs. Increasing the knowledge of ABC proteins in nonmodel plants will facilitate breeding and development of new varieties based on, for example, genetic variations of endogenous genes and/or genome editing, representing an alternative to transgenic approaches.
Substances chimiques
ATP-Binding Cassette Transporters
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
1597-1612Informations de copyright
© 2021 Institute of Bioorganic Chemistry, Polish Academy of Sciences. New Phytologist © 2021 New Phytologist Foundation.
Références
Adebesin F, Widhalm JR, Boachon B, Lefèvre F, Pierman B, Lynch JH, Alam I, Junqueira B, Benke R, Ray S et al. 2017. Emission of volatile organic compounds from petunia flowers is facilitated by an ABC transporter. Science 356: 1386-1388.
Akiyama K, Hayashi H. 2006. Strigolactones: chemical signals for fungal symbionts and parasitic weeds in plant roots. Annals of Botany 97: 925-931.
Akiyama K, Matsuzaki K, Hayashi H. 2005. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435: 824-827.
Andolfo G, Ruocco M, Di Donato A, Frusciante L, Lorito M, Scala F, Ercolano MR. 2015. Genetic variability and evolutionary diversification of membrane ABC transporters in plants. BMC Plant Biology 15: 51.
Banasiak J, Biala W, Staszkow A, Swarcewicz B, Kepczynska E, Figlerowicz M, Jasinski M. 2013. A Medicago truncatula ABC transporter belonging to subfamily G modulates the level of isoflavonoids. Journal of Experimental Botany 64: 1005-1015.
Banasiak J, Borghi L, Stec N, Martinoia E, Jasinski M. 2020. The full-size ABCG transporter of Medicago truncatula is involved in strigolactone secretion, affecting arbuscular mycorrhiza. Frontiers in Plant Science 11: 18.
Basu U, Upadhyaya HD, Srivastava R, Daware A, Malik N, Sharma A, Bajaj D, Narnoliya L, Thakro V, Kujur A et al. 2019. ABC transporter-mediated transport of glutathione conjugates enhances seed yield and quality in chickpea. Plant Physiology 180: 253-275.
Bednarek P, Pislewska-Bednarek M, Svatos A, Schneider B, Doubsky J, Mansurova M, Humphry M, Consonni C, Panstruga R, Sanchez-Vallet A et al. 2009. A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science 323: 101-106.
Behrens CE, Smith KE, Iancu CV, Choe JY, Dean JV. 2019. Transport of anthocyanins and other flavonoids by the Arabidopsis ATP-binding cassette transporter AtABCC2. Scientific Reports 9: 437.
Bessire M, Borel S, Fabre G, Carraca L, Efremova N, Yephremov A, Cao Y, Jetter R, Jacquat AC, Metraux JP et al. 2011. A member of the pleiotropic drug resistance family of ATP binding cassette transporters is required for the formation of a functional cuticle in Arabidopsis. Plant Cell 23: 1958-1970.
Biala W, Banasiak J, Jarzyniak K, Pawela A, Jasinski M. 2017. Medicago truncatula ABCG10 is a transporter of 4-coumarate and liquiritigenin in the medicarpin biosynthetic pathway. Journal of Experimental Botany 68: 3231-3241.
Biala W, Jasinski M. 2018. The phenylpropanoid case - it is transport that matters. Frontiers in Plant Science 9: 1610.
Bird D, Beisson F, Brigham A, Shin J, Greer S, Jetter R, Kunst L, Wu XW, Yephremov A, Samuels L. 2007. Characterization of Arabidopsis ABCG11/WBC11, an ATP binding cassette (ABC) transporter that is required for cuticular lipid secretion. The Plant Journal 52: 485-498.
Borghi L, Kang J, de Brito FR. 2019. Filling the gap: functional clustering of ABC proteins for the investigation of hormonal transport in planta. Frontiers in Plant Science 10: 422.
Bowman JL, Kohchi T, Yamato KT, Jenkins J, Shu S, Ishizaki K, Yamaoka S, Nishihama R, Nakamura Y, Berger F et al. 2017. Insights into land plant evolution garnered from the Marchantia polymorpha genome. Cell 171: 287-304.
de Brito FR, Martinoia E. 2018. The vacuolar transportome of plant specialized metabolites. Plant and Cell Physiology 59: 1326-1336.
Chen GX, Komatsuda T, Ma JF, Nawrath C, Pourkheirandish M, Tagiri A, Hu YG, Sameri M, Li XR, Zhao X et al. 2011. An ATP-binding cassette subfamily G full transporter is essential for the retention of leaf water in both wild barley and rice. Proceedings of the National Academy of Sciences, USA 108: 12354-12359.
Chen P, Li YI, Zhao L, Hou Z, Yan M, Hu B, Liu Y, Azam SM, Zhang Z, Rahman ZU et al. 2017. 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. Frontiers in Plant Science 8: 2150.
Cheng SF, Melkonian M, Smith SA, Brockington S, Archibald JM, Delaux PM, Li FW, Melkonian B, Mavrodiev EV, Sun WJ et al. 2018. 10KP: a phylodiverse genome sequencing plan. GigaScience 7: giy013.
Cho CH, Jang S, Choi BY, Hong DW, Choi DS, Choi S, Kim H, Han SK, Kim S, Kim MS et al. 2020. Phylogenetic analysis of ABCG subfamily proteins in plants: functional clustering and coevolution with ABCGs of pathogens. Physiologia Plantarum 172: 1422-1438.
Clay NK, Adio AM, Denoux C, Jander G, Ausubel FM. 2009. Glucosinolate metabolites required for an Arabidopsis innate immune response. Science 323: 95-101.
Colombo F, Paolo D, Cominelli E, Sparvoli F, Nielsen E, Pilu R. 2020. MRP transporters and low phytic acid mutants in major crops: main pleiotropic effects and future perspectives. Frontiers in Plant Science 11: 1301.
Cosme M, Fernandez I, Van der Heijden MGA, Pieterse CMJ. 2018. Non-mycorrhizal plants: the exceptions that prove the rule. Trends in Plant Science 23: 577-587.
Cox DE, Dyer S, Weir R, Cheseto X, Sturrock M, Coyne D, Torto B, Maule AG, Dalzell JJ. 2019. ABC transporter genes ABC-C6 and ABC-G33 alter plant-microbe-parasite interactions in the rhizosphere. Scientific Reports 9: 19899.
Crouzet J, Roland J, Peeters E, Trombik T, Ducos E, Nader J, Boutry M. 2013. NtPDR1, a plasma membrane ABC transporter from Nicotiana tabacum, is involved in diterpene transport. Plant Molecular Biology 82: 181-192.
Dastmalchi M, Bernards MA, Dhaubhadel S. 2016. Twin anchors of the soybean isoflavonoid metabolon: evidence for tethering of the complex to the endoplasmic reticulum by IFS and C4H. The Plant Journal 85: 689-706.
Demessie Z, Woolfson KN, Yu F, Qu Y, De Luca V. 2017. The ATP binding cassette transporter, VmTPT2/VmABCG1, is involved in export of the monoterpenoid indole alkaloid, vincamine in Vinca minor leaves. Phytochemistry 140: 118-124.
Demurtas OC, Francisco R, Diretto G, Ferrante P, Frusciante S, Pietrella M, Aprea G, Borghi L, Feeney M, Frigerio L et al. 2019. ABCC transporters mediate the vacuolar accumulation of crocins in saffron stigmas. Plant Cell 31: 2789-2804.
Deppe JP, Rabbat R, Hortensteiner S, Keller B, Martinoia E, Lopez-Marques RL. 2018. The wheat ABC transporter Lr34 modifies the lipid environment at the plasma membrane. Journal of Biological Chemistry 293: 18667-18679.
Dixon RA, Achnine L, Kota P, Liu CJ, Reddy MS, Wang L. 2002. The phenylpropanoid pathway and plant defence-a genomics perspective. Molecular Plant Pathology 3: 371-390.
Do THT, Martinoia E, Lee Y. 2018. Functions of ABC transporters in plant growth and development. Current Opinion in Plant Biology 41: 32-38.
Do THT, Martinoia E, Lee Y, Hwang JU. 2021. 2021 update on ATP-binding cassette (ABC) transporters: how they meet the needs of plants. Plant Physiology. doi: 10.1093/plphys/kiab193.
Dong Q, Magwanga RO, Cai XY, Lu P, Kirungu JN, Zhou ZL, Wang XF, Wang XX, Xu YC, Hou YQ et al. 2019. RNA-sequencing, physiological and RNAi analyses provide insights into the response mechanism of the ABC-mediated resistance to Verticillium dahliae infection in cotton. Genes 10: 110.
Elejalde-Palmett C, Martinez San Segundo I, Garroum I, Charrier L, De Bellis D, Mucciolo A, Guerault A, Liu J, Zeisler-Diehl V, Aharoni A et al. 2021. ABCG transporters export cutin precursors for the formation of the plant cuticle. Current Biology 31: 2111-2123.
Fabre G, Garroum I, Mazurek S, Daraspe J, Mucciolo A, Sankar M, Humbel BM, Nawrath C. 2016. The ABCG transporter PEC1/ABCG32 is required for the formation of the developing leaf cuticle in Arabidopsis. New Phytologist 209: 192-201.
Feng Y, Sun QR, Zhang GF, Wu T, Zhang XZ, Xu XF, Han ZH, Wang Y. 2019. Genome-wide identification and characterization of ABC transporters in nine Rosaceae species identifying MdABCG28 as a possible cytokinin transporter linked to dwarfing. International Journal of Molecular Sciences 20: 5783.
Fernandez I, Cosme M, Stringlis IA, Yu K, de Jong R, van Wees SCM, Pozo MJ, Pieterse CMJ, van der Heijden MGA. 2019. Molecular dialogue between arbuscular mycorrhizal fungi and the nonhost plant Arabidopsis thaliana switches from initial detection to antagonism. New Phytologist 223: 867-881.
Francisco RM, Regalado A, Ageorges A, Burla BJ, Bassin B, Eisenach C, Zarrouk O, Vialet S, Marlin T, Chaves MM et al. 2013. ABCC1, an ATP binding cassette protein from grape berry, transports anthocyanidin 3-O-glucosides. Plant Cell 25: 1840-1854.
Frugier F, Kosuta S, Murray JD, Crespi M, Szczyglowski K. 2008. Cytokinin: secret agent of symbiosis. Trends in Plant Science 13: 115-120.
Fu XQ, Shi P, He Q, Shen Q, Tang YL, Pan QF, Ma YA, Yan TX, Chen MH, Hao XL et al. 2017. AaPDR3, a PDR transporter 3, is involved in sesquiterpene β-caryophyllene transport in Artemisia annua. Frontiers in Plant Science 8: 723.
Geisler M, Aryal B, di Donato M, Hao PC. 2017. A critical view on ABC transporters and their interacting partners in auxin transport. Plant and Cell Physiology 58: 1601-1614.
Geisler M, Blakeslee JJ, Bouchard R, Lee OR, Vincenzetti V, Bandyopadhyay A, Titapiwatanakun B, Peer WA, Bailly A, Richards EL et al. 2005. Cellular efflux of auxin catalyzed by the Arabidopsis MDR/PGP transporter AtPGP1. The Plant Journal 44: 179-194.
Goodman CD, Casati P, Walbot V. 2004. A multidrug resistance-associated protein involved in anthocyanin transport in Zea mays. Plant Cell 16: 1812-1826.
Gutjahr C, Radovanovic D, Geoffroy J, Zhang Q, Siegler H, Chiapello M, Casieri L, An K, An G, Guiderdoni E et al. 2012. The half-size ABC transporters STR1 and STR2 are indispensable for mycorrhizal arbuscule formation in rice. The Plant Journal 69: 906-920.
Halkier BA, Gershenzon J. 2006. Biology and biochemistry of glucosinolates. Annual Review of Plant Biology 57: 303-333.
Han TT, Liu WC, Lu YT. 2018. General control non-repressible 20 (GCN20) functions in root growth by modulating DNA damage repair in Arabidopsis. BMC Plant Biology 18: 274.
Hanada K, Zou C, Lehti-Shiu MD, Shinozaki K, Shiu SH. 2008. Importance of lineage-specific expansion of plant tandem duplicates in the adaptive response to environmental stimuli. Plant Physiology 148: 993-1003.
Hartmann K, Peiter E, Koch K, Schubert S, Schreiber L. 2002. Chemical composition and ultrastructure of broad bean (Vicia faba L.) nodule endodermis in comparison to the root endodermis. Planta 215: 14-25.
He YX, Xu J, Wang XY, He XM, Wang YXY, Zhou JG, Zhang SQ, Meng XZ. 2019. The Arabidopsis pleiotropic drug resistance transporters PEN3 and PDR12 mediate camalexin secretion for resistance to Botrytis cinerea. Plant Cell 31: 2206-2222.
Hinrichs M, Fleck AT, Biedermann E, Ngo NS, Schreiber L, Schenk MK. 2017. An ABC transporter is involved in the silicon-induced formation of casparian bands in the exodermis of rice. Frontiers in Plant Science 8: 671.
Huang CF, Yamaji N, Mitani N, Yano M, Nagamura Y, Ma JF. 2009. A bacterial-type ABC transporter is involved in aluminum tolerance in rice. Plant Cell 21: 655-667.
Hwang J-U, Song W-Y, Hong D, Ko D, Yamaoka Y, Jang S, Yim S, Lee E, Khare D, Kim K et al. 2016. Plant ABC transporters enable many unique aspects of a terrestrial plant's lifestyle. Molecular Plant 9: 338-355.
Induri BR, Ellis DR, Slavov GT, Yin TM, Zhang XY, Muchero W, Tuskan GA, DiFazio SP. 2012. Identification of quantitative trait loci and candidate genes for cadmium tolerance in Populus. Tree Physiology 32: 626-638.
Izquierdo Y, Kulasekaran S, Benito P, Lopez B, Marcos R, Cascon T, Hamberg M, Castresana C. 2018. Arabidopsis nonresponding to oxylipins locus NOXY7 encodes a yeast GCN1 homolog that mediates noncanonical translation regulation and stress adaptation. Plant, Cell & Environment 41: 1438-1452.
Jaganathan D, Ramasamy K, Sellamuthu G, Jayabalan S, Venkataraman G. 2018. CRISPR for crop improvement: an update review. Frontiers in Plant Science 9: 985.
Jardinaud MF, Boivin S, Rodde N, Catrice O, Kisiala A, Lepage A, Moreau S, Roux B, Cottret L, Sallet E et al. 2016. A laser dissection-RNAseq analysis highlights the activation of cytokinin pathways by nod factors in the Medicago truncatula root epidermis. Plant Physiology 171: 2256-2276.
Jarzyniak K, Banasiak J, Jamruszka T, Pawela A, Di Donato M, Novak O, Geisler M, Jasinski M. 2021. Early stages of legume-rhizobia symbiosis are controlled by ABCG-mediated transport of active cytokinins. Nature Plants 7: 428-436.
Jasinski M, Stukkens Y, Degand H, Purnelle B, Marchand-Brynaert J, Boutry M. 2001. A plant plasma membrane ATP binding cassette-type transporter is involved in antifungal terpenoid secretion. Plant Cell 13: 1095-1107.
Jones JDG, Dangl JL. 2006. The plant immune system. Nature 444: 323-329.
Juliao MHM, Silva SR, Ferro JA, Varani AM. 2020. A genomic and transcriptomic overview of MATE, ABC, and MFS transporters in Citrus sinensis interaction with Xanthomonas citri subsp. citri. Plants 9: 794.
Kang J, Hwang JU, Lee M, Kim YY, Assmann SM, Martinoia E, Lee Y. 2010. PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. Proceedings of the National Academy of Sciences, USA 107: 2355-2360.
Kang J, Yim S, Choi H, Kim A, Lee KP, Lopez-Molina L, Martinoia E, Lee Y. 2015. Abscisic acid transporters cooperate to control seed germination. Nature Communications 6: 8113.
Kaundal A, Ramu VS, Oh S, Lee S, Pant B, Lee HK, Rojas CM, Senthil-Kumar M, Mysore KS. 2017. 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 29: 2233-2248.
Khan N, You FM, Datla R, Ravichandran S, Jia BS, Cloutier S. 2020. Genome-wide identification of ATP binding cassette (ABC) transporter and heavy metal associated (HMA) gene families in flax (Linum usitatissimum L.). BMC Genomics 21: 722.
Khare D, Choi H, Huh SU, Bassin B, Kim J, Martinoia E, Sohn KH, Paek KH, Lee Y. 2017. Arabidopsis ABCG34 contributes to defense against necrotrophic pathogens by mediating the secretion of camalexin. Proceedings of the National Academy of Sciences, USA 114: E5712-E5720.
Khush GS. 2001. Green revolution: the way forward. Nature Reviews Genetics 2: 815-822.
Kim A, Chen J, Khare D, Jin JY, Yamaoka Y, Maeshima M, Zhao Y, Martinoia E, Hwang JU, Lee Y. 2020. Non-intrinsic ATP-binding cassette proteins ABCI19, ABCI20 and ABCI21 modulate cytokinin response at the endoplasmic reticulum in Arabidopsis thaliana. Plant Cell Reports 39: 473-487.
Ko D, Kang J, Kiba T, Park J, Kojima M, Do J, Kim KY, Kwon M, Endler A, Song WY et al. 2014. Arabidopsis ABCG14 is essential for the root-to-shoot translocation of cytokinin. Proceedings of the National Academy of Sciences, USA 111: 7150-7155.
Kobae Y, Sekino T, Yoshioka H, Nakagawa T, Martinoia E, Maeshima M. 2006. Loss of AtPDR8, a plasma membrane ABC transporter of Arabidopsis thaliana, causes hypersensitive cell death upon pathogen infection. Plant and Cell Physiology 47: 309-318.
Kolmer JA, Singh RP, Garvin DF, Viccars L, William HM, Huerta-Espino J, Ogbonnaya FC, Raman H, Orford S, Bariana HS et al. 2008. Analysis of the Lr34/Yr18 rust resistance region in wheat germplasm. Crop Science 48: 1841-1852.
Kong LY, Liu YN, Zhi PF, Wang XY, Xu B, Gong ZZ, Chang C. 2020. Origins and evolution of cuticle biosynthetic machinery in land plants. Plant Physiology 184: 1998-2010.
Krattinger SG, Jordan DR, Mace ES, Raghavan C, Luo MC, Keller B, Lagudah ES. 2013. Recent emergence of the wheat Lr34 multi-pathogen resistance: insights from haplotype analysis in wheat, rice, sorghum and Aegilops tauschii. Theoretical and Applied Genetics 126: 663-672.
Krattinger SG, Kang J, Braunlich S, Boni R, Chauhan H, Setter LL, Robinson MD, Schmid MW, Wiederhold E, Hensel G et al. 2019. Abscisic acid is a substrate of the ABC transporter encoded by the durable wheat disease resistance gene Lr34. New Phytologist 223: 853-866.
Krattinger SG, Lagudah ES, Spielmeyer W, Singh RP, Huerta-Espino J, McFadden H, Bossolini E, Selter LL, Keller B. 2009. A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323: 1360-1363.
Krattinger SG, Sucher J, Selter LL, Chauhan H, Zhou B, Tang MZ, Upadhyaya NM, Mieulet D, Guiderdoni E, Weidenbach D et al. 2016. The wheat durable, multipathogen resistance gene Lr34 confers partial blast resistance in rice. Plant Biotechnology Journal 14: 1261-1268.
Kretzschmar T, Kohlen W, Sasse J, Borghi L, Schlegel M, Bachelier JB, Reinhardt D, Bours R, Bouwmeester HJ, Martinoia E. 2012. A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching. Nature 483: 341-344.
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. 2018. MegaX: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35: 1547-1549.
Landgraf R, Smolka U, Altmann S, Eschen-Lippold L, Senning M, Sonnewald S, Weigel B, Frolova N, Strehmel N, Hause G et al. 2014. The ABC transporter ABCG1 is required for suberin formation in potato tuber periderm. Plant Cell 26: 3403-3415.
Lane TS, Rempe CS, Davitt J, Staton ME, Peng Y, Soltis DE, Melkonian M, Deyholos M, Leebens-Mack JH, Chase M et al. 2016. Diversity of ABC transporter genes across the plant kingdom and their potential utility in biotechnology. BMC Biotechnology 16: 47.
Lee M, Choi Y, Burla B, Kim YY, Jeon B, Maeshima M, Yoo JY, Martinoia E, Lee Y. 2008. The ABC transporter AtABCB14 is a malate importer and modulates stomatal response to CO2. Nature Cell Biology 10: 1217-1223.
Lefevre F, Boutry M. 2018. Towards identification of the substrates of ATP-binding cassette transporters. Plant Physiology 178: 18-39.
Li N, Shang J, Wang J, Zhou D, Li N, Ma S. 2018. Fine mapping and discovery of candidate genes for seed size in watermelon by genome survey sequencing. Scientific Reports 8: 17843.
Liu CW, Murray JD. 2016. The role of flavonoids in nodulation host-range specificity: an update. Plants 5: 33.
Lopez-Ortiz C, Dutta SK, Natarajan P, Pena-Garcia Y, Abburi V, Saminathan T, Nimmakayala P, Reddy UK. 2019. Genome-wide identification and gene expression pattern of ABC transporter gene family in Capsicum spp. PLoS ONE 14: e0215901.
Lu X, Dittgen J, Piślewska-Bednarek M, Molina A, Schneider B, Svatoš A, Doubský J, Schneeberger K, Weigel D, Bednarek P et al. 2015. Mutant allele-specific uncoupling of PENETRATION3 functions reveals engagement of the ATP-binding cassette transporter in distinct tryptophan metabolic pathways. Plant Physiology 168: 814-827.
Matern A, Böttcher C, Eschen-Lippold L, Westermann B, Smolka U, Döll S, Trempel F, Aryal B, Scheel D, Geisler M et al. 2019. A substrate of the ABC transporter PEN3 stimulates bacterial flagellin (flg22)-induced callose deposition in Arabidopsis thaliana. Journal of Biological Chemistry 294: 6857-6870.
McFarlane HE, Shin JJH, Bird DA, Samuels AL. 2010. Arabidopsis ABCG transporters, which are required for export of diverse cuticular lipids, dimerize in different combinations. Plant Cell 22: 3066-3075.
Mendiondo GM, Medhurst A, van Roermund CW, Zhang X, Devonshire J, Scholefield D, Fernández J, Axcell B, Ramsay L, Waterham HR et al. 2014. Barley has two peroxisomal ABC transporters with multiple functions in β-oxidation. Journal of Experimental Botany 65: 4833-4847.
Meng D, Gu Z, Li W, Wang A, Yuan H, Yang Q, Li T. 2014. Apple MdABCF assists in the transportation of S-RNase into pollen tubes. The Plant Journal 78: 990-1002.
Mishra AK, Choi J, Rabbee MF, Baek KH. 2019. In silico genome-wide analysis of the ATP-binding cassette transporter gene family in soybean (Glycine max L.) and their expression profiling. BioMed Research International 2019: 8150523.
Multani DS, Briggs SP, Chamberlin MA, Blakeslee JJ, Murphy AS, Johal GS. 2003. Loss of an MDR transporter in compact stalks of maize br2 and sorghum dw3 mutants. Science 302: 81-84.
Naoumkina M, Farag MA, Sumner LW, Tang YH, Liu CJ, Dixon RA. 2007. Different mechanisms for phytoalexin induction by pathogen and wound signals in Medicago truncatula. Proceedings of the National Academy of Sciences, USA 104: 17909-17915.
Navarro-Quiles C, Mateo-Bonmati E, Micol JL. 2018. ABCE proteins: from molecules to development. Frontiers in Plant Science 9: 1125.
Ofori PA, Mizuno A, Suzuki M, Martinoia E, Reuscher S, Aoki K, Shibata D, Otagaki S, Matsumoto S, Shiratake K. 2018. Genome-wide analysis of ATP binding cassette (ABC) transporters in tomato. PLoS ONE 13: e0200854.
Orsi CH, Tanksley SD. 2009. Natural variation in an ABC transporter gene associated with seed size evolution in tomato species. PLoS Genetics 5: e1000347.
Pan L, Yu Q, Wang J, Han H, Mao L, Nyporko A, Maguza A, Fan L, Bai L, Powles S. 2021. An ABCC-type transporter endowing glyphosate resistance in plants. Proceedings of the National Academy of Sciences, USA 118: e2100136118.
Pan XW, Li YC, Liu WQ, Liu SX, Min J, Xiong HB, Dong Z, Duan YH, Yu YY, Li XX. 2020. QTL mapping and candidate gene analysis of cadmium accumulation in polished rice by genome-wide association study. Scientific Reports 10: 11791.
Pang KY, Li YJ, Liu MH, Meng ZD, Yu YL. 2013. Inventory and general analysis of the ATP-binding cassette (ABC) gene superfamily in maize (Zea mays L.). Gene 526: 411-428.
Panikashvili D, Shi JX, Bocobza S, Franke RB, Schreiber L, Aharoni A. 2010. The Arabidopsis DSO/ABCG11 transporter affects cutin metabolism in reproductive organs and suberin in roots. Molecular Plant 3: 563-575.
Panikashvili D, Shi JX, Schreiber L, Aharoni A. 2011. The Arabidopsis ABCG13 transporter is required for flower cuticle secretion and patterning of the petal epidermis. New Phytologist 190: 113-124.
Pawela A, Banasiak J, Biala W, Martinoia E, Jasinski M. 2019. MtABCG20 is an ABA exporter influencing root morphology and seed germination of Medicago truncatula. The Plant Journal 98: 511-523.
Pierman B, Toussaint F, Bertin A, Levy D, Smargiasso N, De Pauw E, Boutry M. 2017. Activity of the purified plant ABC transporter NtPDR1 is stimulated by diterpenes and sesquiterpenes involved in constitutive and induced defenses. Journal of Biological Chemistry 292: 19491-19502.
Pighin JA, Zheng HQ, Balakshin LJ, Goodman IP, Western TL, Jetter R, Kunst L, Samuels AL. 2004. Plant cuticular lipid export requires an ABC transporter. Science 306: 702-704.
Quinby JR, Karper RE. 1954. Inheritance of height in sorghum. Agronomy Journal 46: 211-216.
Radhakrishnan GV, Keller J, Rich MK, Vernié T, Mbadinga Mbadinga DL, Vigneron N, Cottret L, Clemente HS, Libourel C, Cheema J et al. 2020. An ancestral signalling pathway is conserved in intracellular symbioses-forming plant lineages. Nature Plants 6: 280-289.
Rajagopalan N, Lu Y, Burton IW, Monteil-Rivera F, Halasz A, Reimer E, Tweidt R, Brûlé-Babel A, Kutcher HR, You FM et al. 2020. A phenylpropanoid diglyceride associates with the leaf rust resistance Lr34res gene in wheat. Phytochemistry 178: 112456.
Rayapuram N, Hagenmuller J, Grienenberger JM, Giege P, Bonnard G. 2007. AtCCMA interacts with AtCcmB to form a novel mitochondrial ABC transporter involved in cytochrome c maturation in Arabidopsis. Journal of Biological Chemistry 282: 21015-21023.
Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, Shapiro H, Nishiyama T, Perroud PF, Lindquist EA, Kamisugi Y et al. 2008. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319: 64-69.
Rin S, Mizuno Y, Shibata Y, Fushimi M, Katou S, Sato I, Chiba S, Kawakita K, Takemoto D. 2017. EIN2-mediated signaling is involved in pre-invasion defense in Nicotiana benthamiana against potato late blight pathogen, Phytophthora infestans. Plant Signaling & Behavior 12: e1300733.
Risk JM, Selter LL, Chauhan H, Krattinger SG, Kumlehn J, Hensel G, Viccars LA, Richardson TM, Buesing G, Troller A et al. 2013. The wheat Lr34 gene provides resistance against multiple fungal pathogens in barley. Plant Biotechnology Journal 11: 847-854.
Risk JM, Selter LL, Krattinger SG, Viccars LA, Richardson TM, Buesing G, Herren G, Lagudah ES, Keller B. 2012. Functional variability of the Lr34 durable resistance gene in transgenic wheat. Plant Biotechnology Journal 10: 477-487.
Saitou N, Nei M. 1987. The neighbor-joining method - a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4: 406-425.
Samelak-Czajka A, Marszalek-Zenczak M, Marcinkowska-Swojak M, Kozlowski P, Figlerowicz M, Zmienko A. 2017. MLPA-based analysis of copy number variation in plant populations. Frontiers in Plant Science 8: 222.
Sanchez-Vallet A, Ramos B, Bednarek P, Lopez G, Pislewska-Bednarek M, Schulze-Lefert P, Molina A. 2010. Tryptophan-derived secondary metabolites in Arabidopsis thaliana confer non-host resistance to necrotrophic Plectosphaerella cucumerina fungi. The Plant Journal 63: 115-127.
Sasse J, Schlegel M, Borghi L, Ullrich F, Lee M, Liu GW, Giner JL, Kayser O, Bigler L, Martinoia E et al. 2016. Petunia hybrida PDR2 is involved in herbivore defense by controlling steroidal contents in trichomes. Plant, Cell & Environment 39: 2725-2739.
Sasse J, Simon S, Gubeli C, Liu GW, Cheng X, Friml J, Bouwmeester H, Martinoia E, Borghi L. 2015. Asymmetric localizations of the ABC transporter PaPDR1 trace paths of directional strigolactone transport. Current Biology 25: 647-655.
Schnippenkoetter W, Lo C, Liu G, Dibley K, Chan WL, White J, Milne R, Zwart A, Kwong E, Keller B et al. 2017. The wheat Lr34 multipathogen resistance gene confers resistance to anthracnose and rust in sorghum. Plant Biotechnology Journal 15: 1387-1396.
Shen CJ, Yue RQ, Bai YH, Feng R, Sun T, Wang XF, Yang YJ, Tie SG, Wang HZ. 2015. Identification and analysis of Medicago truncatula auxin transporter gene families uncover their roles in responses to Sinorhizobium meliloti Infection. Plant and Cell Physiology 56: 1930-1943.
Shibata Y, Ojika M, Sugiyama A, Yazaki K, Jones DA, Kawakita K, Takemoto D. 2016. The full-size ABCG transporters Nb-ABCG1 and Nb-ABCG2 function in pre- and postinvasion defense against Phytophthora infestans in Nicotiana benthamiana. Plant Cell 28: 1163-1181.
Shim D, Kim S, Choi YI, Song WY, Park J, Youk ES, Jeong SC, Martinoia E, Noh EW, Lee Y. 2013. Transgenic poplar trees expressing yeast cadmium factor 1 exhibit the characteristics necessary for the phytoremediation of mine tailing soil. Chemosphere 90: 1478-1486.
Shimada N, Aoki T, Sato S, Nakamura Y, Tabata S, Ayabe S. 2003. A cluster of genes encodes the two types of chalcone isomerase involved in the biosynthesis of general flavonoids and legume-specific 5-deoxy(iso)flavonoids in Lotus japonicus. Plant Physiology 131: 941-951.
Shiono K, Ando M, Nishiuchi S, Takahashi H, Watanabe K, Nakamura M, Matsuo Y, Yasuno N, Yamanouchi U, Fujimoto M et al. 2014. RCN1/OsABCG5, an ATP-binding cassette (ABC) transporter, is required for hypodermal suberization of roots in rice (Oryza sativa). The Plant Journal 80: 40-51.
Shitan N, Bazin I, Dan K, Obata K, Kigawa K, Ueda K, Sato F, Forestier C, Yazaki K. 2003. Involvement of CjMDR1, a plant multidrug-resistance-type ATP-binding cassette protein, in alkaloid transport in Coptis japonica. Proceedings of the National Academy of Sciences, USA 100: 751-756.
Shitan N, Dalmas F, Dan K, Kato N, Ueda K, Sato F, Forestier C, Yazaki K. 2013. Characterization of Coptis japonica CjABCB2, an ATP-binding cassette protein involved in alkaloid transport. Phytochemistry 91: 109-116.
Stein M, Dittgen J, Sanchez-Rodriguez C, Hou BH, Molina A, Schulze-Lefert P, Lipka V, Somerville S. 2006. Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell 18: 731-746.
Strader LC, Bartel B. 2009. The Arabidopsis pleiotropic drug resistance 8/ABCG36 ATP binding cassette transporter modulates sensitivity to the auxin precursor indole-3-butyric acid. Plant Cell 21: 1992-2007.
Sucher J, Boni R, Yang P, Rogowsky P, Buchner H, Kastner C, Kumlehn J, Krattinger SG, Keller B. 2017. The durable wheat disease resistance gene Lr34 confers common rust and northern corn leaf blight resistance in maize. Plant Biotechnology Journal 15: 489-496.
Sugiyama A, Shitan N, Sato S, Nakamura Y, Tabata S, Yazaki K. 2006. Genome-wide analysis of ATP-binding cassette (ABC) proteins in a model legume plant, Lotus japonicus: comparison with Arabidopsis ABC protein family. DNA Research 13: 205-228.
Sugiyama A, Shitan N, Yazaki K. 2007. Involvement of a soybean ATP-binding cassette - type transporter in the secretion of genistein, a signal flavonoid in legume-rhizobium symbiosis. Plant Physiology 144: 2000-2008.
Sun DY, Zhang XG, Li SH, Jiang CZ, Zhang YL, Niu LX. 2016. LrABCF1, a GCN-type ATP-binding cassette transporter from Lilium regale, is involved in defense responses against viral and fungal pathogens. Planta 244: 1185-1199.
Takanashi K, Sugiyama A, Sato S, Tabata S, Yazaki K. 2012. LjABCB1, an ATP-binding cassette protein specifically induced in uninfected cells of Lotus japonicus nodules. Journal of Plant Physiology 169: 322-326.
One Thousand Plant Transcriptomes. 2019. One thousand plant transcriptomes and the phylogenomics of green plants. Nature 574: 679-685.
Unamba CIN, Nag A, Sharma RK. 2015. Next generation sequencing technologies: the doorway to the unexplored genomics of non-model plants. Frontiers in Plant Science 6: 1074.
Veitch NC. 2013. Isoflavonoids of the Leguminosae. Natural Product Reports 30: 988-1027.
Verrier PJ, Bird D, Burla BO, Dassa E, Forestier C, Geisler M, Klein M, Kolukisaoglu Ü, Lee Y, Martinoia E et al. 2008. Plant ABC proteins - a unified nomenclature and updated inventory. Trends in Plant Science 13: 151-159.
von Voithenberg LV, Park J, Stube R, Lux C, Lee Y, Philippar K. 2019. A novel prokaryote-type ECF/ABC transporter module in chloroplast metal homeostasis. Frontiers in Plant Science 10: 1264.
Walter S, Brennan JM, Arunachalam C, Ansari KI, Hu X, Khan MR, Trognitz F, Trognitz B, Leonard G, Egan D et al. 2008. Components of the gene network associated with genotype-dependent response of wheat to the Fusarium mycotoxin deoxynivalenol. Functional & Integrative Genomics 8: 421-427.
Walter S, Kahla A, Arunachalam C, Perochon A, Khan MR, Scofield SR, Doohan FM. 2015. A wheat ABC transporter contributes to both grain formation and mycotoxin tolerance. Journal of Experimental Botany 66: 2583-2593.
Wang S, Li L, Li H, Sahu SK, Wang H, Xu Y, Xian W, Song BO, Liang H, Cheng S et al. 2020. Genomes of early-diverging streptophyte algae shed light on plant terrestrialization. Nature Plants 6: 95-106.
Wang XW, Wang HZ, Wang J, Sun RF, Wu J, Liu SY, Bai YQ, Mun JH, Bancroft I, Cheng F et al. 2011. The genome of the mesopolyploid crop species Brassica rapa. Nature Genetics 43: 1035-1039.
Wei L, Zhang X, Zhang ZH, Liu HH, Lin ZW. 2018. A new allele of the Brachytic2 gene in maize can efficiently modify plant architecture. Heredity 121: 75-86.
Xing A, Gao Y, Ye L, Zhang W, Cai L, Ching A, Llaca V, Johnson B, Liu L, Yang X et al. 2015. A rare SNP mutation in brachytic2 moderately reduces plant height and increases yield potential in maize. Journal of Experimental Botany 66: 3791-3802.
Yan C, Duan WK, Lyu SW, Li Y, Hou XL. 2017. Genome-wide identification, evolution, and expression analysis of the ATP-binding cassette transporter gene family in Brassica rapa. Frontiers in Plant Science 8: 349.
Yan L, Zhang J, Chen H, Luo H. 2021. Genome-wide analysis of ATP-binding cassette transporter provides insight to genes related to bioactive metabolite transportation in Salvia miltiorrhiza. BMC Genomics 22: 315.
Yasuno N, Takamure I, Kidou SI, Tokuji Y, Ureshi AN, Funabiki A, Ashikaga K, Yamanouchi U, Yano M, Kato K. 2009. Rice shoot branching requires an ATP-binding cassette subfamily G protein. New Phytologist 182: 91-101.
Yu F, De Luca V. 2013. ATP-binding cassette transporter controls leaf surface secretion of anticancer drug components in Catharanthus roseus. Proceedings of the National Academy of Sciences, USA 110: 15830-15835.
Zhang Q, Blaylock LA, Harrison MJ. 2010. Two Medicago truncatula half-ABC transporters are essential for arbuscule development in arbuscular mycorrhizal symbiosis. Plant Cell 22: 1483-1497.
Zhang X, Hou X, Liu Y, Zheng L, Yi Q, Zhang H, Huang X, Zhang J, Hu Y, Yu G et al. 2019. Maize brachytic2 (br2) suppresses the elongation of lower internodes for excessive auxin accumulation in the intercalary meristem region. BMC Plant Biology 19: 589.
Zhang XD, Zhao KX, Yang ZM. 2018. Identification of genomic ATP binding cassette (ABC) transporter genes and Cd-responsive ABCs in Brassica napus. Gene 664: 139-151.
Zhang ZL, Tong T, Fang YX, Zheng JJ, Zhang X, Niu CY, Li J, Zhang XQ, Xue DW. 2020. Genome-wide identification of barley ABC genes and their expression in response to abiotic stress treatment. Plants 9: 1281.
Zhu B, Li H, Xia X, Meng Y, Wang NA, Li LuLu, Shi J, Pei Y, Lin M, Niu L et al. 2020. ATP-binding cassette G transporters SGE1 and MtABCG13 control stigma exsertion. Plant Physiology 184: 223-235.
Zhu H, Zhang M, Sun S, Yang S, Li J, Li H, Yang H, Zhang K, Hu J, Liu D et al. 2019. A single nucleotide deletion in an ABC transporter gene leads to a dwarf phenotype in watermelon. Frontiers in Plant Science 10: 1399.
Zmienko A, Marszalek-Zenczak M, Wojciechowski P, Samelak-Czajka A, Luczak M, Kozlowski P, Karlowski WM, Figlerowicz M. 2020. AthCNV: a map of DNA copy number variations in the Arabidopsis genome. Plant Cell 32: 1797-1819.
Zolman BK, Silva ID, Bartel B. 2001. The Arabidopsis pxa1 mutant is defective in an ATP-binding cassette transporter-like protein required for peroxisomal fatty acid β-oxidation. Plant Physiology 127: 1266-1278.