Skip to main content
SpringerLink
Log in

PrMATE1 Is Differentially Expressed in Radiata Pine Exposed to Inclination and the Deduced Protein Displays High Affinity to Proanthocyanidin Substrates by a Computational Approach

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

The response to inclination in plants is an attractive and extensively studied biological process. The most commonly held theory proposes a differential growth in stem tissue due to unequal auxin redistribution. Further evidence proposed that flavonoids act as molecular regulators of auxin distribution or flux. It is well known that flavonoids affect auxin distribution, but how intracellular concentration is controlled during the gravitropic response in woody species is still unknown. The MATE family has been widely studied, however the molecular basis of flavonoids transport is still poorly understood. Here, we identified and characterized a full-length cDNA from radiate pine encoding a putative MATE protein. Transcript abundance analysis showed that PrMATE1 is expressed in a spatial and temporal manner in inclined stems. Additionally, PrMATE1 fused to GFP is mainly localized in the vacuolar membrane. A 3D protein model showed 12 transmembrane helices and an open cavity. The protein–ligand interaction was evaluated; favourable binding affinity energies were obtained and suggested epicatechin 3′-O-glucoside as the best putative ligand. In silico mutagenesis analysis was used to identify five residues as important to protein–ligand interaction. The data provide a dynamic view of interaction between PrMATE1 and their putative ligands at the molecular scale.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abramson J, Smirnova I, Kasho V, Verner G, Kaback HR, Iwata S (2003) Structure and mechanism of the lactose permease of Escherichia coli. Science 301:610–615

    Article  CAS  PubMed  Google Scholar 

  • Andersson-Gunnerås S, Hellgren JM, Björklund S, Regan S, Moritz T, Sundberg B (2003) Asymmetric expression of poplar ACC oxidase controls ethylene production during gravitational induction of tension wood. Plant J 34:339–349

    Article  PubMed  Google Scholar 

  • Besseau S, Hoffmann L, Geoffroy P, Lapierre C, Pollet B, Legrand M (2007) Flavonoid accumulation in Arabidopsis repressed in lignin synthesis affects auxin transport and plant growth. Plant Cell 19:148–162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bolte S, Talbot C, Boutte Y, Catrice O, Read ND, Satiat-Jeunemaitre B (2004) FM-dyes as experimental probes for dissecting vesicle trafficking in living plant cells. J Microsc 214:159–173

    Article  CAS  PubMed  Google Scholar 

  • Brown MH, Paulsen IT, Skurray RA (1999) The multidrug efflux protein NorM is a prototype of a new family of transporters. Mol Microbiol 31:394–395

    Article  CAS  PubMed  Google Scholar 

  • Burko Y, Geva Y, Refael-Cohen A, Shleizer-Burko S, Shani E, Berger Y, Halon E, Chuck G, Moshelion M, Ori N (2011) From organelle to organ: ZRIZI MATE-type transporter is an organelle transporter that enhances organ initiation. Plant Cell Physiol 52:518–527

    Article  CAS  PubMed  Google Scholar 

  • Debeaujon I, Peeters AJ, Leon-Kloosterziel KM, Koornneef M (2001) The TRANSPARENT TESTA12 gene of Arabidopsis encodes a multidrug secondary transporter-like protein required for flavonoid sequestration in vacuoles of the seed coat endothelium. Plant Cell 13:853–871

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Espinoza A, Contreras R, Zúñiga GE, Herrera R, Moya-León MA, Norambuena L, Handford M (2016) FcLDP1, a gene encoding a late embryogenesis abundant (LEA) domain protein, responds to brassinosteroids and abscisic acid during the development of fruits in Fragaria chiloensis. Front Plant Sci 7:788

    Article  PubMed  PubMed Central  Google Scholar 

  • Falcone Ferreyra ML, Rius SP, Casati P (2012) Flavonoids: Biosynthesis, biological functions, and biotechnological applications. Front Plant Sci 3:222

    CAS  PubMed  PubMed Central  Google Scholar 

  • Frank S, Keck M, Sagasser M, Niehaus K, Weisshaar B, Stracke R (2011) Two differentially expressed MATE factor genes from apple complement the Arabidopsis transparent testa12 mutant. Plant Biol 13:42–50

    Article  CAS  PubMed  Google Scholar 

  • Friesner RA, Banks JL, Murphy RB, Halgren TA, Klicic JJ, Mainz DT, Repasky MP, Knoll EH, Shelley M, Perry JK, Shaw DE, Francis P, Shenkin PS (2004) Glide: A New Approach for Rapid, Accurate Docking and Scoring. 1. Method and Assessment of Docking Accuracy. J Med Chem 47:1739–1749

    Article  CAS  PubMed  Google Scholar 

  • Gagne S, Saucier C, Geny L (2006) Composition and cellular localization of tannins in cabernet sauvignon skins during growth. J Agric Food Chem 54:9465–9471

    Article  CAS  PubMed  Google Scholar 

  • Geisler G, Wang B, Zhu J (2014) Auxin transport during root gravitropism: transporters and techniques. Plant Biol 16:50–57

    Article  PubMed  Google Scholar 

  • Gomez C, Terrier N, Torregrosa L, Vialet S, Fournier-Level A, Verriès C, Souquet JM, Mazauric JP, Klein M, Cheynier V, Ageorges A (2009) Grapevine MATE-type proteins act as vacuolar H+-dependent acylated anthocyanin transporters. Plant Physiol 150:402–415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gomez R, Gonzalez J, Herrera R, Ramos P (2017) MYB Transcription Factors and a Putative Flavonoid Transporter ABCC-Like are Differentially Expressed in Radiata Pine Seedlings Exposed to Inclination. J Plant Growth Regul 1–12

  • Hadacek F (2002) Secondary metabolites as plant traits: current assessment and future perspectives. Crit Rev Plant Sci 21:273–322

    Article  CAS  Google Scholar 

  • He X, Szewczyk P, Karyakin A, Evin M, Hong WX, Zhang Q, Chang G (2010) Structure of a cation-bound multidrug and toxic compound extrusion transporter. Nature 467:991–994

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hellgren J, Olofsson K, Sundberg B (2004) Patterns of auxin distribution during gravitational induction of reaction wood in poplar and pine. Plant Physiol 125:212–220

    Article  Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Higo H (1998) PLACE: a database of plant cis-acting regulatory DNA elements. NAR 26:358–359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K (2007) WoLF PSORT: protein localization predictor. NAR 35:585–587

    Article  Google Scholar 

  • Huang YF, Lemieux MJ, Song JM, Auer M, Wang DN (2003) Structure and mechanism of the glycerol-3-phosphate transporter from Escherichia coli. Science 301:616–620

    Article  CAS  PubMed  Google Scholar 

  • Jorgensen WL, Chandresekhar J, Madura JD, Impey RW, Klein ML (1983) Comparison of simple potential functions for simulating liquid water. J Chem Phys 79:926–935

    Article  CAS  Google Scholar 

  • Jorgensen WL, Maxwell DS, Tirado-Rives J (1996) Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids. J Am Chem Soc 118:11225–11236

    Article  CAS  Google Scholar 

  • Laskowski RA, MacArthur MW, Moss DS, Thornton JM (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Cryst 26:283–291

    Article  CAS  Google Scholar 

  • Le Provost G, Herrera R, Paiva JA, Chaumeil P, Salin F, Plomion C (2007) A micromethod for high throughput RNA extraction in forest trees. Biol Res 40:291–297

    Article  PubMed  Google Scholar 

  • Li L, He Z, Pandey GK, Tsuchiya T, Luan S (2002) Functional cloning and characterization of a plant efflux carrier for multidrug and heavy metal detoxification. J Biol Chem 277:5360–5368

    Article  CAS  PubMed  Google Scholar 

  • Li J, Abel R, Zhu K, Cao Y, Zhao S, Friesner RA (2011) The VSGB 2.0 model: a next generation energy model for high resolution protein structure modeling. Proteins 79:2794–2812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Love L, Björklund S, Vahala J, Hertzberg M, Kangasjärvi J, Sundberg B (2009) Ethylene is an endogenous stimulator of cell division in the cambial meristem of Populus. Proc Natl Acad Sci USA 106:5984–5989

    Article  PubMed  PubMed Central  Google Scholar 

  • Magalhaes JV, Liu J, Guimarães CT, Lana UG, Alves VM, Wang YH, Schaffert RE, Hoekenga OA, Piñeros MA, Shaff JE, Klein PE, Carneiro NP, Coelho CM, Trick HN, Kochian LV (2007) A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nat Genet 39:1156–1161

    Article  CAS  PubMed  Google Scholar 

  • Marinova K, Pourcel L, Weder B, Schwarz M, Barron D, Routaboul JM, Debeaujon I, Klein M (2007) The Arabidopsis MATE transporter TT12 acts as a vacuolar flavonoid/H+-antiporter active in proanthocyanidin-accumulating cells of the seed coat. Plant Cell 19:2023–2038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marrs KA, Alfenito MR, Lloyd AM, Walbot VA (1995) Glutathione S-transferase involved in vacuolar transfer encoded by the maize gene Bronze-2. Nature 375:397–400

    Article  CAS  PubMed  Google Scholar 

  • Mathews H, Clendennen SK, Caldwell CG, Liu XL, Connors K, Matheis N, Schuster DK, Menasco DJ, Wagoner W, Lightener J, Wagner DR (2003) Activation tagging in tomato identifies a transcriptional regulator of anthocyanin biosynthesis, modification, and transport. Plant Cell 15:1689–1703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mellerowicz E, Baucher M, Sundberg B, Boerjan W (2001) Unravelling cell wall formation in woody dicot stem. Plant Mol Biol 47:239–274

    Article  CAS  PubMed  Google Scholar 

  • Méndez-Yañez A, Beltrán D, Campano-Romero C, Molinett S, Herrera R, Moya-León MA, Morales-Quintana L (2017) Glycosylation is important for FcXTH1 activity as judged by its structural and biochemical characterization. Plant Physiol Biochem 119:200–210

    Article  CAS  PubMed  Google Scholar 

  • Morales-Quintana L, Fuentes L, Gaete-Eastman C, Herrera R, Moya-León MA (2011) Structural characterization and substrate specificity of VpAAT1 protein related to ester biosynthesis in mountain papaya fruit. J Mol Graph Model 29:635–642

    Article  CAS  PubMed  Google Scholar 

  • Morrison KL, Weiss GA (2001) Combinatorial alanine-scanning. Curr Opin Chem Biol 5:302–307

    Article  CAS  PubMed  Google Scholar 

  • Muday GK (2001) Auxins and tropisms. J Plant Growth Regul 20:226–243

    Article  CAS  PubMed  Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. NAR 8:4321–4326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nawrath C, Heck S, Parinthawong N, Métraux JP (2002) EDS5, an essential component of salicylic acid-dependent signaling for disease resistance in Arabidopsis, is a member of the MATE transporter family. Plant Cell 14:275–286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Omote H, Hiasa M, Matsumoto T, Otsuka M, Moriyama Y (2006) The MATE proteins as fundamental transporters of metabolic and xenobiotic organic cations. Trends Pharmacol Sci 27:587–593

    Article  CAS  PubMed  Google Scholar 

  • Peer WA, Murphy AS (2007) Flavonoids and auxin transport: modulators or regulators? Trends Plant Sci 12:556–563

    Article  CAS  PubMed  Google Scholar 

  • Pérez-Díaz R, Ryngajllo M, Pérez-Díaz J, Peña-Cortés H, Casaretto JA, González-Villanueva E, Ruiz-Lara S (2014) VvMATE1 and VvMATE2 encode putative proanthocyanidin transporters expressed during berry development in Vitis vinifera L. Plant Cell Rep 33:1147–1159

    Article  CAS  PubMed  Google Scholar 

  • Petrussa E, Braidot E, Zancani M, Peresson C, Bertolini A, Patui S, Vianello A (2013) Plant flavonoids—biosynthesis, transport and involvement in stress responses. Int J Mol Sci 14:14950–14973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E, Chipot C, Skeel RD, Kale L, Schulten K (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26:1781–1802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pineau C, Loubet S, Lefoulon C, Chalies C, Fizames C, Lacombe B, Ferrand M, Loudet O, Berthomieu P, Richard O (2012) Natural variation at the FRD3 MATE transporter locus reveals cross-talk between Fe homeostasis and Zn tolerance in Arabidopsis thaliana. PLoS Genet 8:e1003120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Plomion C, Pionneau C, Brach J, Costa P, Bailleres H (2000) Compression wood-responsive proteins in developing xylem of maritime pine (Pinus pinaster Ait.). Plant Physiol 123:959–969

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramos P, Herrera R (2013) Anatomical changes of xylem cells in stem of Pinus radiata seedlings exposed to inclination and ethylene. Biol Plant 57:523–530

    Article  CAS  Google Scholar 

  • Ramos P, Le Provost G, Plomion C, Gantz C, Herrera R (2012a) Transcriptional analysis of differential expressed genes in response to stem inclination in young seedlings of pine. Plant Biol 14:923–933

    Article  CAS  PubMed  Google Scholar 

  • Ramos P, Valenzuela C, Provost G, Plomion C, Gantz C, Moya-León M, Herrera R (2012b) ACC oxidase and ACC synthase expression profiles after leaning of young radiata (Pinus radiata D. Don) and maritime pine (Pinus pinaster Ait.) seedlings. J Plant Growth Regul 31:382–391

    Article  CAS  Google Scholar 

  • Ramos P, Guajardo J, Moya-Leon MA, Herrera R (2016) A differential distribution of auxin and flavonols in radiata pine stem seedlings exposed to inclination. Tree Genet Genomes 12:1–13

    Article  Google Scholar 

  • Rogers EE, Wu X, Stacey G, Nguyen HT (2009) Two MATE proteins play a role in iron efficiency in soybean. J Plant Physiol 166:1453–1459

    Article  CAS  PubMed  Google Scholar 

  • Rombauts S, Dehais P, Van Montagu M, Rouze P (1999) PlantCARE a plant cis-acting regulatory element database. NAR 27:295–296

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Savidge RA, Mutumba GMC, Heald JK, Wareing JK (1983) Gas chromatography-mass spectroscopy identification of 1-aminocyclopropane-1-carboxylic acid in compression wood vascular cambium of Pinus contorta Dougl. Plant Physiol 71:434–436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schrödinger (2015) Schrödinger Release 2015-1: LigPrep. Schrödinger, LLC, New York

    Google Scholar 

  • Shelley JC, Cholleti A, Frye LL, Greenwood JR, Timlin MR, Uchimaya M (2007) Epik: a software program for pKa prediction and protonation state generation for drug-like molecules. J Comput Aided Mol Des 21:681–691

    Article  CAS  PubMed  Google Scholar 

  • Shen J, Zeng Y, Zhuang X, Sun L, Yao X, Piml P, Jiang L (2013) Organelle pH in the Arabidopsis endomembrane system. Mol Plant 5:1419–1437

    Article  CAS  Google Scholar 

  • Shitan N, Yazaki K (2013) New insights into the transport mechanisms in plant vacuoles. Int Rev Cell Mol Biol 305:383–433

    Article  CAS  PubMed  Google Scholar 

  • Shitan N, Minami S, Morita M, Hayashida M, Ito S, Takanashi K, Omote H, Moriyama Y, Sugiyama A, Goossens A, Moriyasu M, Yazaki K (2014) Involvement of the leaf-specific multidrug and toxic compound extrusion (MATE) transporter Nt-JAT2 in vacuolar sequestration of nicotine in Nicotiana tabacum. PLoS ONE 9:e108789

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smart OS, Neduvelil JG, Wang X, Wallace BA, Sansom MS (1996) HOLE: a program for the analysis of the pore dimensions of ion channel structural models. J Mol Graph 14:354–360

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Tasaka M, Kato T, Fukaki H (1999) The endodermis and shoot gravitropism. Trends Plants Sci 4:103–107

    Article  CAS  Google Scholar 

  • Taylor LP, Grotewold E (2005) Flavonoids as developmental regulators. Curr Opin Plant Biol 8:317–323

    Article  CAS  PubMed  Google Scholar 

  • Telewski F (2006) A unified hypothesis of mechanoperception in plants. Am J Bot 93:1466–1476

    Article  PubMed  Google Scholar 

  • Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of realtime quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:1–11

    Article  Google Scholar 

  • Voss NR, Gerstein M, Steitz TA, Moore PB (2006) The geometry of the ribosomal polypeptide exit tunnel. J Mol Biol 360:893–906

    Article  CAS  PubMed  Google Scholar 

  • Went FW (1974) Reflections and speculations. Annu Rev Plant Phys 25:1–26

    Article  CAS  Google Scholar 

  • Williams CA, Grayer RJ (2004) Anthocyanins and other flavonoids. Nat Prod Rep 21:539–573

    Article  CAS  PubMed  Google Scholar 

  • Winkel-Shirley B (2001) Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol 126:485–493

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yazaki K (2005) Transporters of secondary metabolites. Curr Opin Plant Biol 8:301–307

    Article  CAS  PubMed  Google Scholar 

  • Yin Y, He X, Szewczyk P, Nguyen T, Chang G (2006) Structure of the multidrug transporter EmrD from Escherichia coli. Science 312:741–744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yin R, Han K, Heller W, Albert A, Dobrev PI, Zažímalová E, Schäffner AR (2014) Kaempferol 3-O-rhamnoside-7-O-rhamnoside is an endogenous flavonol inhibitor of polar auxin transport in Arabidopsis shoots. New Phytol 201:466–475

    Article  CAS  PubMed  Google Scholar 

  • Zhao J (2015) Flavonoid transport mechanisms: how to go, and with whom. Trends Plant Sci 20:576–585

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, Dixon RA (2009) MATE transporters facilitate vacuolar uptake of epicatechin 3′-O-glucoside for proanthocyanidin biosynthesis in Medicago truncatula and Arabidopsis. Plant Cell 21:2323–2340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao J, Dixon RA (2010) The ‘ins’ and ‘outs’ of flavonoid transport. Trends Plant Sci 15:72–80

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, Huhman D, Shadle G, He XZ, Sumner LW, Tang Y, Dixon RA (2011) MATE2 mediates vacuolar sequestration of flavonoid glycosides and glycoside malonates in Medicago truncatula. Plant Cell 23:1536–1555

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work has been supported by PAI/Academia Nº 79140027, FONDECYT N° 11121170, and FONDECYT N° 1150964. PR acknowledges ‘Núcleo Científico Multidisciplinario’ from Universidad de Talca. Authors would like to thank the reviewers for their highly valuable comments.

Author information

Author notes

    Authors and Affiliations

    1. Instituto de Ciencias Biológicas, Universidad de Talca, 2 Norte 685, Talca, Chile

      Luis Morales-Quintana, Jaime González, Daniela C. Urbina, Raúl Herrera & Patricio Ramos

    2. Multidiscipliary Agroindustry Reseach Laboratory, Instituto Ciencias Biomedicas, Universidad Autónoma de Chile, Talca, Chile

      Luis Morales-Quintana

    3. Center for Bioinformatics and Molecular Simulations, Facultad de Ingeniería, Universidad De Talca, 2 Norte 685, Talca, Chile

      Daniel Bustos

    Authors
    1. Luis Morales-Quintana
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Daniel Bustos
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Jaime González
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Daniela C. Urbina
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Raúl Herrera
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Patricio Ramos
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Patricio Ramos.

    Ethics declarations

    Conflict of interest

    The authors declares that they have no conflict of interest.

    Additional information

    Luis Morales-Quintana and Daniel Bustos have contributed equally to this work.

    Electronic Supplementary Material

    Below is the link to the electronic supplementary material.

    Supplementary material 1 (PDF 3117 KB)

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Morales-Quintana, L., Bustos, D., González, J. et al. PrMATE1 Is Differentially Expressed in Radiata Pine Exposed to Inclination and the Deduced Protein Displays High Affinity to Proanthocyanidin Substrates by a Computational Approach. J Plant Growth Regul 38, 14–29 (2019). https://doi.org/10.1007/s00344-018-9801-3

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s00344-018-9801-3

    Keywords

    Search

    Navigation