Advertisement

Plant Molecular Biology

, Volume 91, Issue 3, pp 341–354 | Cite as

Transferring an optimized TAP-toolbox for the isolation of protein complexes to a portfolio of rice tissues

  • Maarten DedeckerEmail author
  • Jelle Van Leene
  • Nancy De Winne
  • Dominique Eeckhout
  • Geert Persiau
  • Eveline Van De Slijke
  • Bernard Cannoot
  • Leen Vercruysse
  • Lies Dumoulin
  • Nathalie Wojsznis
  • Kris Gevaert
  • Steven Vandenabeele
  • Geert De JaegerEmail author
Article

Abstract

Proteins are the cell’s functional entities. Rather than operating independently, they interact with other proteins. Capturing in vivo protein complexes is therefore crucial to gain understanding of the function of a protein in a cellular context. Affinity purification coupled to mass spectrometry has proven to yield a wealth of information about protein complex constitutions for a broad range of organisms. For Oryza sativa, the technique has been initiated in callus and shoots, but has not been optimized ever since. We translated an optimized tandem affinity purification (TAP) approach from Arabidopsis thaliana toward Oryza sativa, and demonstrate its applicability in a variety of rice tissues. A list of non-specific and false positive interactors is presented, based on re-occurrence over more than 170 independent experiments, to filter bona fide interactors. We demonstrate the sensitivity of our approach by isolating the complexes for the rice ANAPHASE PROMOTING COMPLEX SUBUNIT 10 (APC10) and CYCLIN-DEPENDENT KINASE D (CDKD) proteins from the proliferation zone of the emerging fourth leaf. Next to APC10 and CDKD, we tested several additional baits in the different rice tissues and reproducibly retrieved at least one interactor for 81.4 % of the baits screened for in callus tissue and T1 seedlings. By transferring an optimized TAP tag combined with state-of-the-art mass spectrometry, our TAP protocol enables the discovery of interactors for low abundance proteins in rice and opens the possibility to capture complex dynamics by comparing tissues at different stages of a developing rice organ.

Keywords

Anaphase promoting complex CYCLIN-DEPENDENT KINASE D Oryza sativa (rice) Protein–protein interactions Tandem affinity purification coupled to mass spectrometry (TAP–MS) 

Abbreviations

AP–MS

Affinity purification coupled to mass spectrometry

TAP

Tandem affinity purification

APC10

ANAPHASE PROMOTING COMPLEX SUBUNIT 10

CDKD

CYCLIN-DEPENDENT KINASE D

PPI

Protein–protein interaction

Y2H

Yeast two-hybrid

ORF

Open reading frame

PCA

Protein complementation analysis

RING

REALLY INTERESTING NEW GENE

CCS52A

CELL CYCLE SWITCH PROTEIN 52 A

CAK

CDK-activating kinase

CYCH

CYCLIN H

MAT1

MENAGE A TROIS

TFIIH

General transcription factor II H

XPB

XERODERMA PIGMENTOSUM B

XPD

XERODERMA PIGMENTOSUM D

SBP

Streptavidin-binding peptide

MS

Mass spectrometry

TEV

Tobacco etch virus

IgG

Immunoglobulin G

RAP

Rice annotation project

MSU

Michigan State University

CBP

Calmodulin-binding peptide

EGTA

Ethylene glycol tetra-acetic acid

Notes

Acknowledgments

Maarten Dedecker is supported by a predoctoral fellowship from the Agency for Innovation by Science and Technology and CropDesign N.V. (‘Baekeland’ funding, IWT 100222). The authors thank Annick Bleys for help in preparing the manuscript.

Author contributions

M.D., S.V. and G.D.J. designed the research. N.D.W., G.P., E.V.D.S, B.C., L.V., L.D. and N.W. performed experiments. M.D., D.E. and G.D.J. analyzed the data. K.G. provided protocols for LC–MS/MS analysis. J.V.L. and K.G. commented on the manuscript. M.D. and G.D.J. wrote the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11103_2016_471_MOESM1_ESM.docx (1.9 mb)
Supplementary material 1 (DOCX 1966 kb)

References

  1. Abe M, Fujiwara M, Kurotani K-I, Yokoi S, Shimamoto K (2008) Identification of dynamin as an interactor of rice GIGANTEA by tandem affinity purification (TAP). Plant Cell Physiol 49:420–432. doi: 10.1093/pcp/pcn019 CrossRefPubMedGoogle Scholar
  2. Boruc J, Van den Daele H, Hollunder J, Rombauts S, Mylle E, Hilson P, Inzé D, De Veylder L, Russinova E (2010) Functional modules in the Arabidopsis core cell cycle binary protein-protein interaction network. Plant Cell 22:1264–1280. doi: 10.1105/tpc.109.073635 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Boudolf V, Rombauts S, Naudts M, Inzé D, De Veylder L (2001) Identification of novel cyclin-dependent kinases interacting with the CKS1 protein of Arabidopsis. J Exp Bot 52:1381–1382CrossRefPubMedGoogle Scholar
  4. Braun P, Carvunis AR, Charloteaux B, Dreze M, Ecker JR, Hill DE, Roth FP, Vidal M, Galli M, Balumuri P, Bautista V, Chesnut JD, Kim RC, de los Reyes C, Gilles P, Kim CJ, Matrubutham U, Mirchandani J, Olivares E, Patnaik S, Quan R, Ramaswamy G, Shinn P, Sw VM (2011) Evidence for network evolution in an Arabidopsis interactome map. Science 333:601–607. doi: 10.1126/science.1203877 CrossRefGoogle Scholar
  5. Bürckstümmer T, Bennett KL, Preradovic A, Schütze G, Hantschel O, Superti-Furga G, Bauch A (2006) An efficient tandem affinity purification procedure for interaction proteomics in mammalian cells. Nat Methods 3:1013–1019. doi: 10.1038/nmeth968 CrossRefPubMedGoogle Scholar
  6. Capron A, Serralbo O, Fülöp K, Frugier F, Parmentier Y, Dong A, Lecureuil A, Guerche P, Kondorosi E, Scheres B, Genschik P (2003) The Arabidopsis anaphase-promoting complex or cyclosome: molecular and genetic characterization of the APC2 subunit. Plant Cell 15:2370–2382. doi: 10.1105/tpc.013847 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Carbon S, Ireland A, Mungall CJ, Shu S, Marshall B, Lewis S (2009) AmiGO: online access to ontology and annotation data. Bioinformatics 25:288–289. doi: 10.1093/bioinformatics/btn615 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Chang WH, Kornberg RD (2000) Electron crystal structure of the transcription factor and DNA repair complex, core TFIIH. Cell 102:609–613CrossRefPubMedGoogle Scholar
  9. Chang L, Zhang Z, Yang J, McLaughlin SH, Barford D (2014) Molecular architecture and mechanism of the anaphase-promoting complex. Nature 513:388–393. doi: 10.1038/nature13543 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Christensen AH, Sharrock RA, Quail PH (1992) Maize polyubiquitin genes: structure, thermal perturbation of expression and transcript splicing, and promoter activity following transfer to protoplasts by electroporation. Plant Mol Biol 18:675–689CrossRefPubMedGoogle Scholar
  11. De Veylder L, Beeckman T, Beemster GT, Krols L, Terras F, Landrieu I, van der Schueren E, Maes S, Naudts M, Inzé D (2001) Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. Plant Cell 13:1653–1668CrossRefPubMedPubMedCentralGoogle Scholar
  12. Dedecker M, Van Leene J, De Jaeger G (2015) Unravelling plant molecular machineries through affinity purification coupled to mass spectrometry. Curr Opin Plant Biol 24:1–9. doi: 10.1016/j.pbi.2015.01.001 CrossRefPubMedGoogle Scholar
  13. Ding X, Richter T, Chen M, Fujii H, Seo YS, Xie M, Zheng X, Kanrar S, Stevenson RA, Dardick C, Li Y, Jiang H, Zhang Y, Yu F, Bartley LE, Chern M, Bart R, Chen X, Zhu L, Farmerie WG, Gribskov M, Zhu J-K, Fromm ME, Ronald PC, Song W-Y (2009) A rice kinase-protein interaction map. Plant Physiol 149:1478–1492. doi: 10.1104/pp.108.128298 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Dong H, Fei G-L, Wu C-Y, Wu F-Q, Sun Y-Y, Chen M-J, Ren Y-L, Zhou K-N, Cheng Z-J, Wang J-L, Jiang L, Zhang X, Guo X-P, Lei C-L, Su N, Wang H, Wan J-M (2013) A rice virescent-yellow leaf mutant reveals new insights into the role and assembly of plastid caseinolytic protease in higher plants. Plant Physiol 162:1867–1880. doi: 10.1104/pp.113.217604 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Eloy NB, Coppens F, Beemster GTS, Hemerly AS, Ferreira PCG (2006) The Arabidopsis anaphase promoting complex (APC): regulation through subunit availability in plant tissues. Cell Cycle 5:1957–1965CrossRefPubMedGoogle Scholar
  16. Eloy NB, Gonzalez N, Van Leene J, Maleux K, Vanhaeren H, De Milde L, Dhondt S, Vercruysse L, Witters E, Mercier R, Cromer L, Beemster GTS, Remaut H, Van Montagu MCE, De Jaeger G, Ferreira PCG, Inzé D (2012) SAMBA, a plant-specific anaphase-promoting complex/cyclosome regulator is involved in early development and A-type cyclin stabilization. Proc Natl Acad Sci USA 109:13853–13858. doi: 10.1073/pnas.1211418109 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Fabian-Marwedel T, Umeda M, Sauter M (2002) The rice cyclin-dependent kinase-activating kinase R2 regulates S-phase progression. Plant Cell 14:197–210. doi: 10.1105/tpc.010386 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Gadeyne A, Sánchez-Rodríguez C, Vanneste S, Di Rubbo S, Zauber H, Vanneste K, Van Leene J, De Winne N, Eeckhout D, Persiau G, Van De Slijke E, Cannoot B, Vercruysse L, Mayers JR, Adamowski M, Kania U, Ehrlich M, Schweighofer A, Ketelaar T, Maere S, Bednarek SY, Friml J, Gevaert K, Witters E, Russinova E, Persson S, De Jaeger G, Van Damme D (2014) The TPLATE adaptor complex drives clathrin-mediated endocytosis in plants. Cell 156:691–704. doi: 10.1016/j.cell.2014.01.039 CrossRefPubMedGoogle Scholar
  19. Gibbons BJ, Brignole EJ, Azubel M, Murakami K, Voss NR, Bushnell DA, Asturias FJ, Kornberg RD (2012) Subunit architecture of general transcription factor TFIIH. Proc Natl Acad Sci USA 109:1949–1954. doi: 10.1073/pnas.1105266109 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Gibson TJ, Seiler M, Veitia RA (2013) The transience of transient overexpression. Nat Methods 10:715–721. doi: 10.1038/nmeth.2534 CrossRefPubMedGoogle Scholar
  21. Heyman J, De Veylder L (2012) The anaphase-promoting complex/cyclosome in control of plant development. Mol Plant 5:1182–1194. doi: 10.1093/mp/sss094 CrossRefPubMedGoogle Scholar
  22. Jacqmard A, De Veylder L, Segers G, de Almeida EJ, Bernier G, Van Montagu M, Inze D (1999) Expression of CKS1At in Arabidopsis thaliana indicates a role for the protein in both the mitotic and the endoreduplication cycle. Planta 207:496–504CrossRefPubMedGoogle Scholar
  23. Kawahara Y, de la Bastide M, Hamilton JP, Kanamori H, McCombie WR, Ouyang S, Schwartz DC, Tanaka T, Wu J, Zhou S, Childs KL, Davidson RM, Lin H, Quesada-Ocampo L, Vaillancourt B, Sakai H, Lee SS, Kim J, Numa H, Itoh T, Buell CR, Matsumoto T (2013) Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data. Rice (NY) 6:4. doi: 10.1186/1939-8433-6-4 CrossRefGoogle Scholar
  24. Keilhauer EC, Hein MY, Mann M (2015) Accurate protein complex retrieval by affinity enrichment mass spectrometry (AE-MS) rather than affinity purification mass spectrometry (AP–MS). Mol Cell Proteomics 14:120–135. doi: 10.1074/mcp.M114.041012 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Lima MDF, Eloy NB, Pegoraro C, Sagit R, Rojas C, Bretz T, Vargas L, Elofsson A, de Oliveira AC, Hemerly AS, Ferreira PC (2010) Genomic evolution and complexity of the anaphase-promoting complex (APC) in land plants. BMC Plant Biol 10:254. doi: 10.1186/1471-2229-10-254 CrossRefPubMedCentralGoogle Scholar
  26. Lin Q, Wang D, Dong H, Gu S, Cheng Z, Gong J, Qin R, Jiang L, Li G, Wang JL, Wu F, Guo X, Zhang X, Lei C, Wang H, Wan J (2012) Rice APC/C(TE) controls tillering by mediating the degradation of MONOCULM 1. Nat Commun 3:752. doi: 10.1038/ncomms1716 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Lumba S, Toh S, Handfield L-F, Swan M, Liu R, Youn J-Y, Cutler SR, Subramaniam R, Provart N, Moses A, Desveaux D, McCourt P (2014) A mesoscale abscisic acid hormone interactome reveals a dynamic signaling landscape in Arabidopsis. Dev Cell 29:360–372. doi: 10.1016/j.devcel.2014.04.004 CrossRefPubMedGoogle Scholar
  28. Nallamilli BRR, Zhang J, Mujahid H, Malone BM, Bridges SM, Peng Z (2013) Polycomb group gene OsFIE2 regulates rice (Oryza sativa) seed development and grain filling via a mechanism distinct from Arabidopsis. PLoS Genet 9:e1003322. doi: 10.1371/journal.pgen.1003322 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Rohila JS, Chen M, Chen S, Chen J, Cerny R, Dardick C, Canlas P, Xu X, Gribskov M, Kanrar S, Zhu J-K, Ronald P, Fromm ME (2006) Protein–protein interactions of tandem affinity purification-tagged protein kinases in rice. Plant J 46:1–13. doi: 10.1111/j.1365-313X.2006.02671.x CrossRefPubMedGoogle Scholar
  30. Rohila JS, Chen M, Chen S, Chen J, Cerny RL, Dardick C, Canlas P, Fujii H, Gribskov M, Kanrar S, Knoflicek L, Stevenson B, Xie M, Xu X, Zheng X, Zhu J-K, Ronald P, Fromm ME (2009) Protein–protein interactions of tandem affinity purified protein kinases from rice. PLoS ONE 4:e6685. doi: 10.1371/journal.pone.0006685 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Sakai H, Lee SS, Tanaka T, Numa H, Kim J, Kawahara Y, Wakimoto H, Yang C, Iwamoto M, Abe T, Yamada Y, Muto A, Inokuchi H, Ikemura T, Matsumoto T, Sasaki T, Itoh T (2013) Rice Annotation Project Database (RAP-DB): an integrative and interactive database for rice genomics. Plant Cell Physiol 54:e6. doi: 10.1093/pcp/pcs183 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Schultz P, Fribourg S, Poterszman A, Mallouh V, Moras D, Egly JM (2000) Molecular structure of human TFIIH. Cell 102:599–607CrossRefPubMedGoogle Scholar
  33. Seo Y-S, Chern M, Bartley LE, Han M, Jung K-H, Lee I, Walia H, Richter T, Xu X, Cao P, Bai W, Ramanan R, Amonpant F, Arul L, Canlas PE, Ruan R, Park C-J, Chen X, Hwang S, Jeon J-S, Ronald PC (2011) Towards establishment of a rice stress response interactome. PLoS Genet 7:e1002020. doi: 10.1371/journal.pgen.1002020 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Shimotohno A, Umeda-Hara C, Bisova K, Uchimiya H, Umeda M (2004) The plant-specific kinase CDKF;1 is involved in activating phosphorylation of cyclin-dependent kinase-activating kinases in Arabidopsis. Plant Cell 16:2954–2966. doi: 10.1105/tpc.104.025601 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Smaczniak C, Immink RGH, Muiño JM, Blanvillain R, Busscher M, Busscher-Lange J, Dinh QDP, Liu S, Westphal AH, Boeren S, Parcy F, Xu L, Carles CC, Angenent GC, Kaufmann K (2012) Characterization of MADS-domain transcription factor complexes in Arabidopsis flower development. Proc Natl Acad Sci USA 109:1560–1565. doi: 10.1073/pnas.1112871109 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Van Bel M, Proost S, Wischnitzki E, Movahedi S, Scheerlinck C, Van de Peer Y, Vandepoele K (2012) Dissecting plant genomes with the PLAZA comparative genomics platform. Plant Physiol 158:590–600. doi: 10.1104/pp.111.189514 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Van Leene J, Stals H, Eeckhout D, Persiau G, Van De Slijke E, Van Isterdael G, De Clercq A, Bonnet E, Laukens K, Remmerie N, Henderickx K, De Vijlder T, Abdelkrim A, Pharazyn A, Van Onckelen H, Inzé D, Witters E, De Jaeger G (2007) A tandem affinity purification-based technology platform to study the cell cycle interactome in Arabidopsis thaliana. Mol Cell Proteomics 6:1226–1238. doi: 10.1074/mcp.M700078-MCP200 CrossRefPubMedGoogle Scholar
  38. Van Leene J, Witters E, Inzé D, De Jaeger G (2008) Boosting tandem affinity purification of plant protein complexes. Trends Plant Sci 13:517–520. doi: 10.1016/j.tplants.2008.08.002 CrossRefPubMedGoogle Scholar
  39. Van Leene J, Hollunder J, Eeckhout D, Persiau G, Van De Slijke E, Stals H, Van Isterdael G, Verkest A, Neirynck S, Buffel Y, De Bodt S, Maere S, Laukens K, Pharazyn A, Ferreira PCG, Eloy N, Renne C, Meyer C, Faure J-D, Steinbrenner J, Beynon J, Larkin JC, Van de Peer Y, Hilson P, Kuiper M, De Veylder L, Van Onckelen H, Inzé D, Witters E, De Jaeger G (2010) Targeted interactomics reveals a complex core cell cycle machinery in Arabidopsis thaliana. Mol Syst Biol 6:397. doi: 10.1038/msb.2010.53 PubMedPubMedCentralGoogle Scholar
  40. Van Leene J, Eeckhout D, Cannoot B, De Winne N, Persiau G, Van De Slijke E, Vercruysse L, Dedecker M, Verkest A, Vandepoele K, Martens L, Witters E, Gevaert K, De Jaeger G (2015) An improved toolbox to unravel the plant cellular machinery by tandem affinity purification of Arabidopsis protein complexes. Nat Protoc 10:169–187. doi: 10.1038/nprot.2014.199 CrossRefPubMedGoogle Scholar
  41. Vanstraelen M, Baloban M, Da O, Cultrone A, Lammens T, Brown SC, De VL, Mergaert P, Kondorosi E (2009) APC/C CCS52A complexes control meristem maintenance in the Arabidopsis root. Proc Natl Acad Sci USA 106(28):11806–11811. doi: 10.1073/pnas.0901193106 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Vercruyssen L, Verkest A, Gonzalez N, Heyndrickx KS, Eeckhout D, Han S-K, Jégu T, Archacki R, Van Leene J, Andriankaja M, De Bodt S, Abeel T, Coppens F, Dhondt S, De Milde L, Vermeersch M, Maleux K, Gevaert K, Jerzmanowski A, Benhamed M, Wagner D, Vandepoele K, De Jaeger G, Inzé D (2014) ANGUSTIFOLIA3 binds to SWI/SNF chromatin remodeling complexes to regulate transcription during Arabidopsis leaf development. Plant Cell 26:210–229. doi: 10.1105/tpc.113.115907 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Xu C, Wang Y, Yu Y, Duan J, Liao Z, Xiong G, Meng X, Liu G, Qian Q, Li J (2012) Degradation of MONOCULM 1 by APC/C(TAD1) regulates rice tillering. Nat Commun 3:750. doi: 10.1038/ncomms1743 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Yamaguchi M, Umeda M, Uchimiya H (1998) A rice homolog of Cdk7/MO15 phosphorylates both cyclin-dependent protein kinases and the carboxy-terminal domain of RNA polymerase II. Plant J 16:613–619CrossRefPubMedGoogle Scholar
  45. Zhong J, Haynes PA, Zhang S, Yang X, Andon NL, Eckert D, Yates JR, Wang X, Budworth P (2003) Development of a system for the study of protein–protein interactions in planta: characterization of a TATA-box binding protein complex in Oryza sativa. J Proteome Res 2:514–522Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Maarten Dedecker
    • 1
    • 2
    • 3
    Email author
  • Jelle Van Leene
    • 1
    • 2
  • Nancy De Winne
    • 1
    • 2
  • Dominique Eeckhout
    • 1
    • 2
  • Geert Persiau
    • 1
    • 2
  • Eveline Van De Slijke
    • 1
    • 2
  • Bernard Cannoot
    • 1
    • 2
  • Leen Vercruysse
    • 1
    • 2
  • Lies Dumoulin
    • 3
  • Nathalie Wojsznis
    • 3
  • Kris Gevaert
    • 4
    • 5
  • Steven Vandenabeele
    • 3
  • Geert De Jaeger
    • 1
    • 2
    Email author
  1. 1.Department of Plant Systems BiologyVIBGhentBelgium
  2. 2.Department of Plant Biotechnology and BioinformaticsGhent UniversityGhentBelgium
  3. 3.CropDesign N.V.GhentBelgium
  4. 4.Department of Medical Protein Research and BiochemistryVIBGhentBelgium
  5. 5.Department of BiochemistryGhent UniversityGhentBelgium

Personalised recommendations