Single-cell-type Proteomics: Toward a Holistic Understanding of Plant Function

Multicellular organisms such as plants contain different types of cells with specialized functions. Analyzing the protein characteristics of each type of cell will not only reveal specific cell functions, but also enhance understanding of how an organism works. Most plant proteomics studies have focused on using tissues and organs containing a mixture of different cells. Recent single-cell-type proteomics efforts on pollen grains, guard cells, mesophyll cells, root hairs, and trichomes have shown utility. We expect that high resolution proteomic analyses will reveal novel functions in single cells. This review provides an overview of recent developments in plant single-cell-type proteomics. We discuss application of the approach for understanding important cell functions, and we consider the technical challenges of extending the approach to all plant cell types. Finally, we consider the integration of single-cell-type proteomics with transcriptomics and metabolomics with the goal of providing a holistic understanding of plant function. Multicellular organisms such as plants contain different types of cells with specialized functions. Analyzing the protein characteristics of each type of cell will not only reveal specific cell functions, but also enhance understanding of how an organism works. Most plant proteomics studies have focused on using tissues and organs containing a mixture of different cells. Recent single-cell-type proteomics efforts on pollen grains, guard cells, mesophyll cells, root hairs, and trichomes have shown utility. We expect that high resolution proteomic analyses will reveal novel functions in single cells. This review provides an overview of recent developments in plant single-cell-type proteomics. We discuss application of the approach for understanding important cell functions, and we consider the technical challenges of extending the approach to all plant cell types. Finally, we consider the integration of single-cell-type proteomics with transcriptomics and metabolomics with the goal of providing a holistic understanding of plant function. Plant organs and tissues are composed of various differentiated cells. Each cell type has specific functions in plant growth, development, and interaction with the environment. The analysis of different types of highly specialized cells is essential for understanding the sophisticated molecular networks of regulatory and metabolic pathways underlying plant functions. Most of the functional genomics studies have used entire plant organs or tissues (e.g. leaves, roots, flowers, and seeds) as experimental materials. For instance, proteomics of plant tissues/organs has revealed thousands of proteins in different plant species under different environmental conditions (1Baerenfaller K. Grossmann J. Grobei M.A. Hull R. Hirsch-Hoffmann M. Yalovsky S. Zimmermann P. Grossniklaus U. Gruissem W. Baginsky S. Genome-scale proteomics reveals Arabidopsis thaliana gene models and proteome dynamics.Science. 2008; 320: 938-941Crossref PubMed Scopus (415) Google Scholar). In Arabidopsis and rice, 13,029 and 2528 proteins have been identified, respectively, in various tissues (1Baerenfaller K. Grossmann J. Grobei M.A. Hull R. Hirsch-Hoffmann M. Yalovsky S. Zimmermann P. Grossniklaus U. Gruissem W. Baginsky S. Genome-scale proteomics reveals Arabidopsis thaliana gene models and proteome dynamics.Science. 2008; 320: 938-941Crossref PubMed Scopus (415) Google Scholar, 2Koller A. Washburn M.P. Lange B.M. Andon N.L. Deciu C. Haynes P.A. Hays L. Schieltz D. Ulaszek R. Wei J. Wolters D. Yates III, J.R. Proteomic survey of metabolic pathways in rice.Proc. Natl. Acad. Sci. U.S.A. 2002; 99: 11969-11974Crossref PubMed Scopus (345) Google Scholar). These results are useful in deriving tissue- and organ-specific functions. However, they lack the resolution and selectivity necessary for understanding specific proteins and their functions in different cell types because the information at the cellular level has been diluted and averaged. Therefore, single-cell-type studies are important for unraveling molecular processes underlying the functions of various differentiated cells. State-of-the-art proteomics technologies have enabled high throughput and sensitive analysis of signaling and metabolic processes in single cells. To date, most reports of single-cell-type proteomic studies are on bacteria, yeast, cultured mammalian cell lines, and red blood cells (3Ishii N. Nakahigashi K. Baba T. Robert M. Soga T. Kanai A. Hirasawa T. Naba M. Hirai K. Hoque A. Ho P.Y. Kakazu Y. Sugawara K. 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Proteomics. 2008; 7: 1317-1330Abstract Full Text Full Text PDF PubMed Scopus (50) Google Scholar) because of the ease of material acquisition. In contrast, there are only a limited number of plant single-cell-type proteomics studies. This situation can be partly attributed to the technical challenges of isolating an adequate quantity and quality of cells from plant tissues. Clearly, dedifferentiated plant cell cultures have advantages, as they contain all the genetic information and are not limited in quantity. Using cell suspension cultures of Arabidopsis, rice (Oryza sativa), tobacco (Nicotiana tabacum), Medicago, and chickpea (Cicer arietinum), a total of 1107, 1528, 360, 1708, and 724 proteins have been identified, respectively (7Böhmer M. Schroeder J.I. 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Proteomics identification of differentially expressed proteins associated with pollen germination and tube growth reveals characteristics of germinated Oryza sativa pollen.Mol. Cell. Proteomics. 2007; 6: 207-230Abstract Full Text Full Text PDF PubMed Scopus (139) Google Scholar, 25Han B. Chen S. Dai S. Yang N. Wang T. Isobaric tags for relative and absolute quantification-based comparative proteomics reveals the features of plasma membrane-associated proteomes of pollen grains and pollen tubes from Lilium davidii.J. Integr. Plant Biol. 2010; 52: 1043-1058Crossref PubMed Scopus (33) Google Scholar, 26Pertl H. Schulze W.X. Obermeyer G. The pollen organelle membrane proteome reveals highly spatial-temporal dynamics during germination and tube growth of lily pollen.J. Proteome Res. 2009; 8: 5142-5152Crossref PubMed Scopus (46) Google Scholar, 27Petersen A. Dresselhaus T. Grobe K. Becker W.M. Proteome analysis of maize pollen for allergy-relevant components.Proteomics. 2006; 6: 6317-6325Crossref PubMed Scopus (52) Google Scholar, 28Fernando D.D. Characterization of pollen tube development in Pinus strobus (Eastern white pine) through proteomic analysis of differentially expressed proteins.Proteomics. 2005; 5: 4917-4926Crossref PubMed Scopus (55) Google Scholar, 29Wu X. Chen T. Zheng M. Chen Y. Teng N. Samaj J. Baluska F. Lin J. Integrative proteomic and cytological analysis of the effects of extracellular Ca2+ influx on Pinus bungeana pollen tube development.J. Proteome Res. 2008; 7: 4299-4312Crossref PubMed Scopus (33) Google Scholar, 30Chen T. Wu X. Chen Y. Li X. Huang M. Zheng M. Baluska F. Samaj J. Lin J. Combined proteomic and cytological analysis of Ca2+-calmodulin regulation in Picea meyeri pollen tube growth.Plant Physiol. 2009; 149: 1111-1126Crossref PubMed Scopus (58) Google Scholar, 31Chen Y. Chen T. Shen S. Zheng M. Guo Y. Lin J. Baluska F. Samaj J. Differential display proteomic analysis of Picea meyeri pollen germination and pollen-tube growth after inhibition of actin polymerization by latrunculin B.Plant J. 2006; 47: 174-195Crossref PubMed Scopus (60) Google Scholar, 32Okamoto T. Higuchi K. Shinkawa T. Isobe T. Lörz H. Koshiba T. Kranz E. Identification of major proteins in maize egg cells.Plant Cell Physiol. 2004; 45: 1406-1412Crossref PubMed Scopus (62) Google Scholar), specialized leaf epidermal cells (guard cells and trichomes) (33Zhao Z. Zhang W. Stanley B.A. Assmann S.M. Functional proteomics of Arabidopsis thaliana guard cells uncovers new stomatal signaling pathways.Plant Cell. 2008; 20: 3210-3226Crossref PubMed Scopus (223) Google Scholar, 34Zhao Z. Stanley B.A. Zhang W. Assmann S.M. ABA-regulated G protein signaling in Arabidopsis guard cells: a proteomic perspective.J. Proteome Res. 2010; 9: 1637-1647Crossref PubMed Scopus (65) Google Scholar, 35Zhu M. Dai S. McClung S. Yan X. Chen S. Functional differentiation of Brassica napus guard cells and mesophyll cells revealed by comparative proteomics.Mol. Cell. Proteomics. 2009; 8: 752-766Abstract Full Text Full Text PDF PubMed Scopus (105) Google Scholar, 36Zhu M. Simons B. Zhu N. Oppenheimer D.G. Chen S. Analysis of abscisic acid responsive proteins in Brassica napus guard cells by multiplexed isobaric tagging.J. Proteomics. 2010; 73: 790-805Crossref PubMed Scopus (61) Google Scholar, 37Zhu M. Dai S. Zhu N. Booy A. Chen S. Methyl jasmonate responsive proteins in Brassica napus guard cells revealed by iTRAQ-based quantitative proteomics.J. Proteome Res. 2012; 11: 3728-3742Crossref PubMed Scopus (39) Google Scholar, 38Wienkoop S. Zoeller D. Ebert B. Simon-Rosin U. Fisahn J. Glinski M. Weckwerth W. Cell-specific protein profiling in Arabidopsis thaliana trichomes: identification of trichome-located proteins involved in sulfur metabolism and detoxification.Phytochem. 2004; 65: 1641-1649Crossref PubMed Scopus (80) Google Scholar, 39Van Cutsem E. Simonart G. Degand H. Faber A.M. Morsomme P. Boutry M. Gel-based and gel-free proteomic analysis of Nicotiana tabacum trichomes identifies proteins involved in secondary metabolism and in the (a) biotic stress response.Proteomics. 2011; 11: 440-454Crossref PubMed Scopus (51) Google Scholar, 40Amme S. Rutten T. Melzer M. Sonsmann G. Vissers J.P. Schlesier B. Mock H.P. A proteome approach defines protective functions of tobacco leaf trichomes.Proteomics. 2005; 5: 2508-2518Crossref PubMed Scopus (73) Google Scholar, 41Xie Z. Kapteyn J. Gang D.R. A systems biology investigation of the MEP/terpenoid and shikimate/phenylpropanoid pathways points to multiple levels of metabolic control in sweet basil glandular trichomes.Plant J. 2008; 54: 349-361Crossref PubMed Scopus (113) Google Scholar, 42Schilmiller A.L. Miner D.P. Larson M. McDowell E. Gang D.R. Wilkerson C. Last R.L. Studies of a biochemical factory: tomato trichome deep expressed sequence tag sequencing and proteomics.Plant Physiol. 2010; 153: 1212-1223Crossref PubMed Scopus (106) Google Scholar), mesophyll cells (35Zhu M. Dai S. McClung S. Yan X. Chen S. Functional differentiation of Brassica napus guard cells and mesophyll cells revealed by comparative proteomics.Mol. Cell. Proteomics. 2009; 8: 752-766Abstract Full Text Full Text PDF PubMed Scopus (105) Google Scholar), and root hair cells (43Wan J. Torres M. Ganapathy A. Thelen J. DaGue B.B. Mooney B. Xu D. Stacey G. Proteomic analysis of soybean root hairs after infection by Bradyrhizobium japonicum.Mol. 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Proteomics. 2007; 6: 207-230Abstract Full Text Full Text PDF PubMed Scopus (139) Google Scholar, 25Han B. Chen S. Dai S. Yang N. Wang T. Isobaric tags for relative and absolute quantification-based comparative proteomics reveals the features of plasma membrane-associated proteomes of pollen grains and pollen tubes from Lilium davidii.J. Integr. Plant Biol. 2010; 52: 1043-1058Crossref PubMed Scopus (33) Google Scholar, 26Pertl H. Schulze W.X. Obermeyer G. The pollen organelle membrane proteome reveals highly spatial-temporal dynamics during germination and tube growth of lily pollen.J. Proteome Res. 2009; 8: 5142-5152Crossref PubMed Scopus (46) Google Scholar, 29Wu X. Chen T. Zheng M. Chen Y. Teng N. Samaj J. Baluska F. Lin J. Integrative proteomic and cytological analysis of the effects of extracellular Ca2+ influx on Pinus bungeana pollen tube development.J. Proteome Res. 2008; 7: 4299-4312Crossref PubMed Scopus (33) Google Scholar, 30Chen T. Wu X. Chen Y. Li X. Huang M. Zheng M. Baluska F. Samaj J. Lin J. Combined proteomic and cytological analysis of Ca2+-calmodulin regulation in Picea meyeri pollen tube growth.Plant Physiol. 2009; 149: 1111-1126Crossref PubMed Scopus (58) Google Scholar, 31Chen Y. Chen T. Shen S. Zheng M. Guo Y. Lin J. Baluska F. Samaj J. Differential display proteomic analysis of Picea meyeri pollen germination and pollen-tube growth after inhibition of actin polymerization by latrunculin B.Plant J. 2006; 47: 174-195Crossref PubMed Scopus (60) Google Scholar, 34Zhao Z. Stanley B.A. Zhang W. Assmann S.M. ABA-regulated G protein signaling in Arabidopsis guard cells: a proteomic perspective.J. Proteome Res. 2010; 9: 1637-1647Crossref PubMed Scopus (65) Google Scholar, 36Zhu M. Simons B. Zhu N. Oppenheimer D.G. Chen S. Analysis of abscisic acid responsive proteins in Brassica napus guard cells by multiplexed isobaric tagging.J. Proteomics. 2010; 73: 790-805Crossref PubMed Scopus (61) Google Scholar, 37Zhu M. Dai S. Zhu N. Booy A. Chen S. Methyl jasmonate responsive proteins in Brassica napus guard cells revealed by iTRAQ-based quantitative proteomics.J. Proteome Res. 2012; 11: 3728-3742Crossref PubMed Scopus (39) Google Scholar, 43Wan J. Torres M. Ganapathy A. Thelen J. DaGue B.B. Mooney B. Xu D. Stacey G. Proteomic analysis of soybean root hairs after infection by Bradyrhizobium japonicum.Mol. Plant Microbe Interact. 2005; 18: 458-467Crossref PubMed Scopus (114) Google Scholar). The knowledge obtained has enhanced our understanding of specific proteins and cellular events and provided novel insights into the molecular networks and dynamics underlying the functions of specific types of plant cells. In this review, we focus on reviewing the current status and recent development in differentiated single-cell-type plant proteomics. We discuss technical challenges and perspectives in its integration with other large-scale "omics" results with the goal of providing a holistic understanding of plant function.Table ISummary of current publications on plant single-cell-type proteomicsCell typeSpeciesSample/treatmentApproachesProtein identitiesUnique proteinsReferencePollenArabidopsis thalianaMature pollen1DE, ICAT, LC-MS/MS3500387618Grobei M.A. Qeli E. Brunner E. Rehrauer H. Zhang R. Roschitzki B. Basler K. Ahrens C.H. Grossniklaus U. Deterministic protein inference for shotgun proteomics data provides new insights into Arabidopsis pollen development and function.Genome Res. 2009; 19: 1786-1800Crossref PubMed Scopus (149) Google ScholarMature and germinated pollen2-DE, MALDI-TOF/TOF MS18919Zou J. Song L. Zhang W. Wang Y. Ruan S. Wu W.H. Comparative proteomic analysis of Arabidopsis mature pollen and germinated pollen.J. Integr. Plant Biol. 2009; 51: 438-455Crossref PubMed Scopus (64) Google ScholarMature pollen2-DE, LC-MS/MS13520Holmes-Davis R. Tanaka C.K. Vensel W.H. Hurkman W.J. McCormick S. Proteome mapping of mature pollen of Arabidopsis thaliana.Proteomics. 2005; 5: 4864-4884Crossref PubMed Scopus (211) Google ScholarMature pollen2-DE, MALDI-TOF MS, LC-MS/MS12121Noir S. Bräutigam A. Colby T. Schmidt J. Panstruga R. A reference map of the Arabidopsis thaliana mature pollen proteome.Biochem. Biophys. Res. Commun. 2005; 337: 1257-1266Crossref PubMed Scopus (125) Google ScholarLycopersicon esculentumMature pollen2-DE, MALDI-TOF MS15815822Sheoran I.S. Ross A.R. Olson D.J. Sawhney V.K. Proteomic analysis of tomato (Lycopersicon esculentum) pollen.J. Exp. Bot. 2007; 58: 3525-3535Crossref PubMed Scopus (97) Google ScholarOryza sativaMature pollen and coat2-DE, MALDI-TOF MS, LC-MS/MS32240123Dai S. Li L. Chen T. Chong K. Xue Y. Wang T. Proteomic analyses of Oryza sativa mature pollen reveal novel proteins associated with pollen germination and tube growth.Proteomics. 2006; 6: 2504-2529Crossref PubMed Scopus (161) Google ScholarMature and germinated pollen2-DE, MALDI-TOF MS, LC-MS/MS16024Dai S. Chen T. Chong K. Xue Y. Liu S. Wang T. Proteomics identification of differentially expressed proteins associated with pollen germination and tube growth reveals characteristics of germinated Oryza sativa pollen.Mol. Cell. Proteomics. 2007; 6: 207-230Abstract Full Text Full Text PDF PubMed Scopus (139) Google ScholarLilium davidiiPM from mature and germinated polleniTRAQ, LC-MS/MS22322325Han B. Chen S. Dai S. Yang N. Wang T. Isobaric tags for relative and absolute quantification-based comparative proteomics reveals the features of plasma membrane-associated proteomes of pollen grains and pollen tubes from Lilium davidii.J. Integr. Plant Biol. 2010; 52: 1043-1058Crossref PubMed Scopus (33) Google ScholarLilium longiflorumMembrane/organelle from pollen tube1-DE, LC-MS/MS27027026Pertl H. Schulze W.X. Obermeyer G. The pollen organelle membrane proteome reveals highly spatial-temporal dynamics during germination and tube growth of lily pollen.J. Proteome Res. 2009; 8: 5142-5152Crossref PubMed Scopus (46) Google ScholarZea maysPollen coat2-DE, immunoblot4427Petersen A. Dresselhaus T. Grobe K. Becker W.M. Proteome analysis of maize pollen for allergy-relevant components.Proteomics. 2006; 6: 6317-6325Crossref PubMed Scopus (52) Google ScholarPinus strobusPollen tube2-DE, MALDI-TOF MS383828Fernando D.D. Characterization of pollen tube development in Pinus strobus (Eastern white pine) through proteomic analysis of differentially expressed proteins.Proteomics. 2005; 5: 4917-4926Crossref PubMed Scopus (55) Google ScholarPinus bungeanaPollen tube treated with nifedipine2-DE, LC-MS/MS343429Wu X. Chen T. Zheng M. Chen Y. Teng N. Samaj J. Baluska F. Lin J. Integrative proteomic and cytological analysis of the effects of extracellular Ca2+ influx on Pinus bungeana pollen tube development.J. Proteome Res. 2008; 7: 4299-4312Crossref PubMed Scopus (33) Google ScholarPicea meyeriPollen tube treated with trifluoperazine2-DE, LC-MS/MS9311630Chen T. Wu X. Chen Y. Li X. Huang M. Zheng M. Baluska F. Samaj J. Lin J. Combined proteomic and cytological analysis of Ca2+-calmodulin regulation in Picea meyeri pollen tube growth.Plant Physiol. 2009; 149: 1111-1126Crossref PubMed Scopus (58) Google ScholarPollen tube treated with latrunculin B2-DE, LC-MS/MS5331Chen Y. Chen T. Shen S. Zheng M. Guo Y. Lin J. Baluska F. Samaj J. Differential display proteomic analysis of Picea meyeri pollen germination and pollen-tube growth after inhibition of actin polymerization by latrunculin B.Plant J. 2006; 47: 174-195Crossref PubMed Scopus (60) Google ScholarEgg cellZ. maysEgg cell1-DE, 2-DE, LC-MS/MS6632Okamoto T. Higuchi K. 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Proteomics. 2009; 8: 752-766Abstract Full Text Full Text PDF PubMed Scopus (105) Google ScholarABA treatmentiTRAQ, LC-MS/MS43136Zhu M. Simons B. Zhu N. Oppenheimer D.G. Chen S. Analysis of abscisic acid responsive proteins in Brassica napus guard cells by multiplexed isobaric tagging.J. Proteomics. 2010; 73: 790-805Crossref PubMed Scopus (61) Google ScholarMeJA treatmentiTRAQ, LC-MS/MS122037Zhu M. Dai S. Zhu N. Booy A. Chen S. Methyl jasmonate responsive proteins in Brassica napus guard cells revealed by iTRAQ-based quantitative proteomics.J. Proteome Res. 2012; 11: 3728-3742Crossref PubMed Scopus (39) Google ScholarTrichomeA. thalianaNon-glandularLC/MS/MS636338Wienkoop S. Zoeller D. Ebert B. Simon-Rosin U. Fisahn J. Glinski M. Weckwerth W. 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