Location, location, location: surveying the intracellular real estate through proteomics in plants
A. Harvey MillarPlant Molecular Biology Group, School of Biomedical and Chemical Sciences, The University of Western Australia, Crawley, WA 6009, Australia. Corresponding author; email: hmillar@cyllene.uwa.edu.au
Functional Plant Biology 31(6) 563-582 https://doi.org/10.1071/FP04034
Submitted: 4 February 2004 Accepted: 16 March 2004 Published: 23 June 2004
Abstract
Knowledge of cellular compartmentation is critical to an understanding of many aspects of biological function in plant cells but it remains an under-emphasised concept in the use of and investment in plant functional genomic tools. The emerging effort in plant subcellular proteomics is discussed, and the current datasets that are available for a series of organelles and cellular membranes isolated from a range of plant species are noted. The benefit of knowing subcellular location in determining the role of proteins of unknown function is considered alongside the challenges faced in this endeavour. These include clear problems in dealing with contamination during the isolation of subcellular compartments, the meaningful integration of these datasets once completed to assemble a jigsaw of the cellular proteome as a whole, and the use of the wider literature in supplementing this proteomic discovery effort.
Keywords: mass spectrometry, membranes, organelles, plants, proteomics, subcellular fractionation.
Acknowledgments
AHM is an Australian Research Council QEII Research Fellow and also thanks the Australian Research Council for grants through the Discovery Program to fund this research.
Andon NL,
Hollingworth S,
Koller A,
Greenland AJ,
Yates JR, Haynes PA
(2002) Proteomic characterisation of wheat amyloplasts using identification of proteins by tandem mass spectrometry. Proteomics 2, 1156–1168.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bae MS,
Cho EJ,
Choi EY, Park OK
(2003) Analysis of the Arabidopsis nuclear proteome and its response to cold stress. The Plant Journal 36, 652–663.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bardel J,
Louwagie M,
Jaquinod M,
Jourdain A,
Luche S,
Rabilloud T,
Macherel D,
Garin J, Bourguignon J
(2002) A survey of the plant mitochondrial proteome in relation to development. Proteomics 2, 880–898.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bardy N,
Carrasco A,
Galaud JP,
Pont-Lezica R, Canut H
(1998) Free-flow electrophoresis for fractionation of Arabidopsis thaliana membranes. Electrophoresis 19, 1145–1153.
| PubMed |
Borner GH,
Lilley KS,
Stevens TJ, Dupree P
(2003) Identification of glycosylphosphatidylinositol-anchored proteins in Arabidopsis. A proteomic and genomic analysis. Plant Physiology 132, 568–577.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Burgess RR, Thompson NE
(2002) Advances in gentle immunoaffinity chromatography. Current Opinion in Biotechnology 13, 304–308.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Calikowski TT,
Meulia T, Meier I
(2003) A proteomic study of the Arabidopsis nuclear matrix. Journal of Cellular Biochemistry 90, 361–378.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Chew O,
Whelan J, Millar AH
(2003) Molecular definition of the ascorbate–glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. Journal of Biological Chemistry 278, 46 869–46 877.
| Crossref | GoogleScholarGoogle Scholar |
Chew O,
Lister R,
Qbadou S,
Heazlewood JL,
Soll J,
Schleiff E,
Millar AH, Whelan J
(2004) A plant outer mitochondrial membrane protein with high amino acid sequence identity to a chloroplast protein import receptor. FEBS Letters 557, 109–114.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Chivasa S,
Ndimba BK,
Simon WJ,
Robertson D,
Yu XL,
Knox JP,
Bolwell P, Slabas AR
(2002) Proteomic analysis of the Arabidopsis thaliana cell wall. Electrophoresis 23, 1754–1765.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Cutler SR,
Ehrhardt DW,
Griffitts JS, Somerville CR
(2000) Random GFP::cDNA fusions enable visualisation of subcellular structures in cells of Arabidopsis at a high frequency. Proceedings of the National Academy of Sciences USA 97, 3718–3723.
| Crossref | GoogleScholarGoogle Scholar |
Dreger M
(2003) Subcellular proteomics. Mass Spectrometry Reviews 22, 27–56.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Elortza F,
Nuhse TS,
Foster LJ,
Stensballe A,
Peck SC, Jensen ON
(2003) Proteomic analysis of glycosylphosphatidylinositol–anchored membrane proteins. Molecular and Cellular Proteomics 2, 1261–1270.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Emanuelsson O
(2002) Predicting protein subcellular localisation from amino acid sequence information. Briefing in Bioinformatics 3, 361–376.
Emanuelsson O, von Heijne G
(2001) Prediction of organellar targeting signals. Biochimica et Biophysica Acta 1541, 114–119.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Escobar NM,
Haupt S,
Thow G,
Boevink P,
Chapman S, Oparka K
(2003) High-throughput viral expression of cDNA-green fluorescent protein fusions reveals novel subcellular addresses and identifies unique proteins that interact with plasmodesmata. The Plant Cell 15, 1507–1523.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Eubel H,
Jansch L, Braun HP
(2003) New insights into the respiratory chain of plant mitochondria. supercomplexes and a unique composition of complex II. Plant Physiology 133, 274–286.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Faraday CD,
Spanswick RM, Bisson MA
(1996) Plasma membrane isolation from freshwater and salt-tolerant species of Chara: antibody cross-reactions and phosphohydrolase activities. Journal of Experimental Botany 47, 589–594.
| PubMed |
Fecht-Christoffers MM,
Braun HP,
Lemaitre-Guillier C,
VanDorsselaer A, Horst WJ
(2003) Effect of manganese toxicity on the proteome of the leaf apoplast in cowpea. Plant Physiology 133, 1935–1946.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ferro M,
Salvi D,
Brugiere S,
Miras S,
Kowalski S,
Louwagie M,
Garin J,
Joyard J, Rolland N
(2003) Proteomics of the chloroplast envelope membranes from Arabidopsis thaliana. Molecular and Cellular Proteomics 2, 325–345.
| PubMed |
Friso G,
Ytterberg AJ,
Giacomelli L,
Peltier JB,
Rudella A,
Sun Q, van Wijk KJ
(2004) In-depth analysis of the thylakoid membrane proteome of Arabidopsis thaliana chloroplasts; new proteins, functions and a plastid proteome database. The Plant Cell 16, 478–499.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Froehlich JE,
Wilkerson CG,
Ray K,
McAndrew RS,
Osteryoung KW,
Gage DA, Phinney BS
(2003) Proteomic study of the Arabidopsis thaliana chloroplastic envelope membrane utilising alternatives to traditional two-dimensional electrophoresis. Journal of Proteome Research 2, 413–425.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Fukao Y,
Hayashi M, Nishimura M
(2002) Proteomic analysis of leaf peroxisomal proteins in greening cotyledons of Arabidopsis thaliana. Plant and Cell Physiology 43, 689–696.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Fukao Y,
Hayashi M,
Hara-Nishimura I, Nishimura M
(2003) Novel glyoxysomal protein kinase, GPK1, identified by proteomic analysis of glyoxysomes in etiolated cotyledons of Arabidopsis thaliana. Plant and Cell Physiology 44, 1002–1012.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Goff SA,
Ricke D,
Lan T-H,
Presting G, Wang R, ,
et al
.
(2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296, 92–100.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Guo T,
Hua S,
Ji X, Sun Z
(2004) DBSubLoc: database of protein subcellular localisation. Nucleic Acids Research 32, D122–D124.
| Crossref | GoogleScholarGoogle Scholar |
Hamdan M, Righetti PG
(2002) Modern strategies for protein quantification in proteome analysis: advantages and limitations. Mass Spectrometry Reviews 21, 287–302.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Haslam RP,
Downie AL,
Raveton M,
Gallardo K,
Job D,
Pallett KE,
John P,
Parry MAJ, Coleman JOD
(2003) The assessment of enriched apoplastic extracts using proteomic approaches. The Annals of Applied Biology 143, 81–91.
Heazlewood JL, Millar AH
(2003) Integrated plant proteomics: putting the green genomes to work. Functional Plant Biology 30, 471–482.
| Crossref | GoogleScholarGoogle Scholar |
Heazlewood JL,
Howell KA, Millar AH
(2003a) Mitochondrial complex I form Arabidopsis and rice: orthologs of mammalian and funal components coupled with plant-specific subunits. Biochimica et Biophysica Acta 1604, 159–169.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Heazlewood JL,
Howell KA,
Whelan J, Millar AH
(2003b) Towards an analysis of the rice mitochondrial proteome. Plant Physiology 132, 230–242.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Heazlewood JL,
Whelan J, Millar AH
(2003c) The products of the mitochondrial orf25 and orfB genes are FO components in the plant F1FO ATP synthase. FEBS Letters 540, 201–205.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Heazlewood JL,
Tonti-Filippini JS,
Gout AM,
Day DA,
Whelan J, Millar AH
(2004) Experimental analysis of the Arabidopsis mitochondrial proteome highlights signalling and regulatory components, provides assessment of targeting prediction programs and points to plant specific mitochondrial proteins. The Plant Cell 16, 241–256.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Herald VL,
Heazlewood JL,
Day DA, Millar AH
(2003) Proteomic identification of divalent metal cation binding proteins in plant mitochondria. FEBS Letters 537, 96–100.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hochholdinger F,
Guo L, Schnable PS
(2004) Cytoplasmic regulation of the accumulation of nuclear-encoded proteins in the mitochondrial proteome of maize. The Plant Journal 37, 199–208.
| PubMed |
Hoffmann-Benning S,
McIntosh DA,
Gage L,
Kende H, Zeevaart JAD
(2002) Comparison of peptides in the phloem sap of flowering and non-flowering Perilla and lupine plants using microbore HPLC followed by matrix-assisted laser desorption / ionisation time-of-flight mass spectrometry. Planta 216, 140–147.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Huber LA,
Pfaller K, Vietor I
(2003) Organelle proteomics: implications for subcellular fractionation in proteomics. Circulation Research 92, 962–968.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Huh WK,
Falvo JV,
Gerke LC,
Carroll AS,
Howson RW,
Weissman JS, O’Shea EK
(2003) Global analysis of protein localisation in budding yeast. Nature 425, 686–691.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Jonsson AP
(2001) Mass spectrometry for protein and peptide characterisation. Cellular and Molecular Life Sciences 58, 868–884.
| PubMed |
Jung E,
Heller M,
Sanchez JC, Hochstrasser DF
(2000) Proteomics meets cell biology: the establishment of subcellular proteomes. Electrophoresis 21, 3369–3377.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Komatsu S,
Kojima K,
Suzuki K,
Ozaki K, Higo K
(2004) Rice proteome database based on two-dimensional polyacrylamide gel electrophoresis: its status in 2003. Nucleic Acids Research 32, D388–D392.
| Crossref | GoogleScholarGoogle Scholar |
Kruft V,
Eubel H,
Jansch L,
Werhahn W, Braun HP
(2001) Proteomic approach to identify novel mitochondrial proteins in Arabidopsis. Plant Physiology 127, 1694–1710.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Maltman DJ,
Simon WJ,
Wheeler CH,
Dunn MJ,
Wait R, Slabas AR
(2002) Proteomic analysis of the endoplasmic reticulum from developing and germinating seed of castor (Ricinus communis). Electrophoresis 23, 626–639.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Millar AH, Heazlewood JL
(2003) Genomic and proteomic analysis of mitochondrial carrier proteins in Arabidopsis. Plant Physiology 131, 443–453.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Millar AH,
Sweetlove LJ,
Giege P, Leaver CJ
(2001) Analysis of the Arabidopsis mitochondrial proteome. Plant Physiology 127, 1711–1727.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Mithoefer A,
Mueller B,
Wanner G, Eichacker LA
(2002) Identification of defence-related cell wall proteins in Phytophthora
sojae-infected soybean roots by ESI–MS / MS. Molecular Plant Pathology 3, 163–166.
| Crossref | GoogleScholarGoogle Scholar |
Nuhse TS,
Stensballe A,
Jensen ON, Peck SC
(2003) Large-scale analysis of in vivo phosphorylated membrane proteins by immobilised metal ion affinity chromatography and mass spectrometry. Molecular and Cellular Proteomics 2, 1234–1243.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Peeters N, Small I
(2001) Dual targeting to mitochondria and chloroplasts. Biochimica et Biophysica Acta 1541, 54–63.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Peltier JB,
Friso G,
Kalume DE,
Roepstorff P,
Nilsson F,
Adamska I, van Wijk KJ
(2000) Proteomics of the chloroplast: systematic identification and targeting analysis of lumenal and peripheral thylakoid proteins. The Plant Cell 12, 319–341.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Peltier J-B,
Emanuelsson O,
Kalume DE,
Ytterberg J, Friso G ,
et al
.
(2002) Central functions of the lumenal and peripheral thylakoid proteome of Arabidopsis determined by experimentation and genome-wide prediction. The Plant Cell 14, 211–236.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Prime TA,
Sherrier DJ,
Mahon P,
Packman LC, Dupree P
(2000) A proteomic analysis of organelles from Arabidopsis thaliana. Electrophoresis 21, 3488–3499.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Rial DV,
Lombardo VA,
Ceccarelli EA, Ottado J
(2002) The import of ferredoxin-NADP+ reductase precursor into chloroplasts is modulated by the region between the transit peptide and the mature core of the protein. European Journal of Biochemistry 269, 5431–5439.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Richly E,
Chinnery PF, Leister D
(2003) Evolutionary diversification of mitochondrial proteomes: implications for human disease. Trends in Genetics 19, 356–362.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Rochester CP,
Kjellbom P,
Andersson B, Larsson C
(1987) Lipid composition of plasma membranes isolated from light-grown barley (Hordeum vulgare) leaves: identification of cerebroside as a major component. Archives of Biochemistry and Biophysics 255, 385–391.
| PubMed |
Saalbach G,
Erik P, Wienkoop S
(2002) Characterisation by proteomics of peribacteroid space and peribacteroid membrane preparations from pea (Pisum sativum) symbiosomes. Proteomics 2, 325–337.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Santoni V,
Doumas P,
Rouquie D,
Mansion M,
Rabilloud T, Rossignol M
(1999) Large scale characterisation of plant plasma membrane proteins. Biochimie 81, 655–661.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Santoni V,
Vinh J,
Pflieger D,
Sommerer N, Maurel C
(2003) A proteomic study reveals novel insights into the diversity of aquaporin forms expressed in the plasma membrane of plant roots. The Biochemical Journal 373, 289–296.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Schubert M,
Petersson UA,
Haas BJ,
Funk C,
Schroder WP, Kieselbach T
(2002) Proteome map of the chloroplast lumen of Arabidopsis thaliana. Journal of Biological Chemistry 277, 8354–8365.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sickmann A,
Reinders J,
Wagner Y,
Joppich C, Zahedi R ,
et al
.
(2003) The proteome of Saccharomyces cerevisiae mitochondria. Proceedings of the National Academy of Sciences USA 100, 13207–13212.
| Crossref | GoogleScholarGoogle Scholar |
Simpson JC, Pepperkok R
(2003) Localising the proteome. Genome Biology 4, 240.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sweetlove LJ,
Heazlewood JL,
Herald V,
Holtzapffel R,
Day DA,
Leaver CJ, Millar AH
(2002) The impact of oxidative stress on Arabidopsis mitochondria. The Plant Journal 32, 891–904.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tanaka N,
Fujita M,
Handa H,
Murayama S, Uemura M ,
et al
.
(2004) Proteomics of the rice cell: systematic identification of the protein population in subcellular compartments. Molecular Genetics and Genomics In press ,
| Crossref | GoogleScholarGoogle Scholar |
The Arabidopsis genome initiative
(2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796–815.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Werhahn W, Braun HP
(2002) Biochemical dissection of the mitochondrial proteome from Arabidopsis thaliana by three-dimensional gel electrophoresis. Electrophoresis 23, 640–646.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wienkoop S, Saalbach G
(2003) Proteome analysis. Novel proteins identified at the peribacteroid membrane from Lotus japonicus root nodules. Plant Physiology 131, 1080–1090.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Zhou J, Weiner H
(2001) The N-terminal portion of mature aldehyde dehydrogenase affects protein folding and assembly. Protein Science 10, 1490–1497.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
