Advances in plant cell type-specific genome-wide studies of gene expression

Abstract

Cell is the functional unit of life. To study the complex interactions of systems of biological molecules, it is crucial to dissect these molecules at the cell level. In recent years, major progresses have been made by plant biologists to profile gene expression in specific cell types at the genome-wide level. Approaches based on the isolation of cells, polysomes or nuclei have been developed and successfully used for studying the cell types from distinct organs of several plant species. These cell-level data sets revealed previously unrecognized cellular properties, such as cell-specific gene expression modules and hormone response centers, and should serve as essential resources for functional genomic analyses. Newly developed technologies are more affordable to many laboratories and should help to provide new insights at the cellular resolution in the near future.

Key words： transcriptome; cell type; plant

Acknowledgments

We thank EM Meyerowitz for his continuous support. We apologize to those authors for not being able to directly cite their work due to space constraints. YJ is supported in part by the State Key Laboratory of Plant Genomics, and by the ‘100 Talents Project’ of Chinese Academy of Sciences.

References

1 Birnbaum K, Shasha D E, Wang J Y, Jung J W, Lambert G M, Galbraith D W, Benfey P N (2003). A gene expression map of the Arabidopsis root. Science, 302(5652): 1956–1960

PMID

2 Brady S M, Orlando D A, Lee J Y, Wang J Y, Koch J, Dinneny J R, Mace D, Ohler U, Benfey P N (2007). A high-resolution root spatiotemporal map reveals dominant expression patterns. Science, 318(5851): 801–806

PMID

3 Brooks L 3rd, Strable J, Zhang X, Ohtsu K, Zhou R, Sarkar A, Hargreaves S, Elshire R J, Eudy D, Pawlowska T, Ware D, Janick-Buckner D, Buckner B, Timmermans M C, Schnable P S, Nettleton D, Scanlon M J (2009). Microdissection of shoot meristem functional domains. PLoS Genet, 5(5): e1000476

PMID

4 Cai S, Lashbrook C C (2008). Stamen abscission zone transcriptome profiling reveals new candidates for abscission control: enhanced retention of floral organs in transgenic plants overexpressing Arabidopsis ZINC FINGER PROTEIN2. Plant Physiol, 146(3): 1305–1321

PMID

5 Casson S, Spencer M, Walker K, Lindsey K (2005). Laser capture microdissection for the analysis of gene expression during embryogenesis of Arabidopsis. Plant J, 42(1): 111–123

PMID

6 Cho Y, Fernandes J, Kim SH, Walbot V (2002). Gene-expression profile comparisons distinguish seven organs of maize. Genome Biol, 3: research0045.1-0045.16

7 Deal R B, Henikoff S (2010). A simple method for gene expression and chromatin profiling of individual cell types within a tissue. Dev Cell, 18(6): 1030–1040

PMID

8 Dembinsky D, Woll K, Saleem M, Liu Y, Fu Y, Borsuk L A, Lamkemeyer T, Fladerer C, Madlung J, Barbazuk B, Nordheim A, Nettleton D, Schnable P S, Hochholdinger F (2007). Transcriptomic and proteomic analyses of pericycle cells of the maize primary root. Plant Physiol, 145(3): 575–588

PMID

9 Demura T, Tashiro G, Horiguchi G, Kishimoto N, Kubo M, Matsuoka N, Minami A, Nagata-Hiwatashi M, Nakamura K, Okamura Y, Sassa N, Suzuki S, Yazaki J, Kikuchi S, Fukuda H (2002). Visualization by comprehensive microarray analysis of gene expression programs during transdifferentiation of mesophyll cells into xylem cells. Proc Natl Acad Sci USA, 99(24): 15794–15799

PMID

10 Dinneny J R, Long T A, Wang J Y, Jung J W, Mace D, Pointer S, Barron C, Brady S M, Schiefelbein J, Benfey P N (2008). Cell identity mediates the response of Arabidopsis roots to abiotic stress. Science, 320(5878): 942–945

PMID

11 Edwards D, Murray J A, Smith A G (1998). Multiple genes encoding the conserved CCAAT-box transcription factor complex are expressed in Arabidopsis. Plant Physiol, 117(3): 1015–1022

PMID

12 Emrich S J, Barbazuk W B, Li L, Schnable P S (2007). Gene discovery and annotation using LCM-454 transcriptome sequencing. Genome Res, 17(1): 69–73

PMID

13 Engel M L, Chaboud A, Dumas C, McCormick S (2003). Sperm cells of Zea mays have a complex complement of mRNAs. Plant J, 34(5): 697–707

PMID

14 Galbraith D W, Birnbaum K (2006). Global studies of cell type-specific gene expression in plants. Annu Rev Plant Biol, 57(1): 451–475

PMID

15 Honys D, Twell D (2004). Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol, 5(11): R85

PMID

16 Ideker T, Galitski T, Hood L (2001). A new approach to decoding life: systems biology. Annu Rev Genomics Hum Genet, 2(1): 343–372

PMID

17 Jiao Y, Lau O S, Deng X W (2007). Light-regulated transcriptional networks in higher plants. Nat Rev Genet, 8(3): 217–230

PMID

18 Jiao Y, Meyerowitz E M (2010). Cell-type specific analysis of translating RNAs in developing flowers reveals new levels of control. Mol Syst Biol, 6: 419

PMID

19 Jiao Y, Tausta S L, Gandotra N, Sun N, Liu T, Clay N K, Ceserani T, Chen M, Ma L, Holford M, Zhang H Y, Zhao H, Deng X W, Nelson T (2009). A transcriptome atlas of rice cell types uncovers cellular, functional and developmental hierarchies. Nat Genet, 41(2): 258–263

PMID

20 Lee J Y, Colinas J, Wang J Y, Mace D, Ohler U, Benfey P N (2006). Transcriptional and posttranscriptional regulation of transcription factor expression in Arabidopsis roots. Proc Natl Acad Sci USA, 103(15): 6055–6060

PMID

21 Lee J Y, Levesque M, Benfey P N (2005). High-throughput RNA isolation technologies. New tools for high-resolution gene expression profiling in plant systems. Plant Physiol, 138(2): 585–590

PMID

22 Leonhardt N, Kwak J M, Robert N, Waner D, Leonhardt G, Schroeder J I (2004). Microarray expression analyses of Arabidopsis guard cells and isolation of a recessive abscisic acid hypersensitive protein phosphatase 2C mutant. Plant Cell, 16(3): 596–615

PMID

23 Levesque M P, Vernoux T, Busch W, Cui H, Wang J Y, Blilou I, Hassan H, Nakajima K, Matsumoto N, Lohmann J U, Scheres B, Benfey P N (2006). Whole-genome analysis of the SHORT-ROOT developmental pathway in Arabidopsis. PLoS Biol, 4(5): e143

PMID

24 Li P, Ponnala L, Gandotra N, Wang L, Si Y, Tausta S L, Kebrom T H, Provart N, Patel R, Myers C R, Reidel E J, Turgeon R, Liu P, Sun Q, Nelson T, Brutnell T P (2010). The developmental dynamics of the maize leaf transcriptome. Nat Genet, 42(12): 1060–1067

PMID

25 Long T A, Brady S M, Benfey P N (2008). Systems approaches to identifying gene regulatory networks in plants. Annu Rev Cell Dev Biol, 24(1): 81–103

PMID

26 Ma L, Sun N, Liu X, Jiao Y, Zhao H, Deng X W (2005). Organ-specific expression of Arabidopsis genome during development. Plant Physiol, 138(1): 80–91

PMID

27 Motose H, Sugiyama M, Fukuda H (2004). A proteoglycan mediates inductive interaction during plant vascular development. Nature, 429(6994): 873–878

PMID

28 Mustroph A, Zanetti M E, Jang C J, Holtan H E, Repetti P P, Galbraith D W, Girke T, Bailey-Serres J (2009). Profiling translatomes of discrete cell populations resolves altered cellular priorities during hypoxia in Arabidopsis. Proc Natl Acad Sci USA, 106(44): 18843–18848

PMID

29 Nakazono M, Qiu F, Borsuk L A, Schnable P S (2003). Laser-capture microdissection, a tool for the global analysis of gene expression in specific plant cell types: identification of genes expressed differentially in epidermal cells or vascular tissues of maize. Plant Cell, 15(3): 583–596

PMID

30 Nawy T, Lee J Y, Colinas J, Wang J Y, Thongrod S C, Malamy J E, Birnbaum K, Benfey P N (2005). Transcriptional profile of the Arabidopsis root quiescent center. Plant Cell, 17(7): 1908–1925

PMID

31 Nelson T, Gandotra N, Tausta S L (2008). Plant cell types: reporting and sampling with new technologies. Curr Opin Plant Biol, 11(5): 567–573

PMID

32 Nelson T, Tausta S L, Gandotra N, Liu T (2006). Laser microdissection of plant tissue: what you see is what you get. Annu Rev Plant Biol, 57(1): 181–201

PMID

33 Pina C, Pinto F, Feijó J A, Becker J D (2005). Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control, and gene expression regulation. Plant Physiol, 138(2): 744–756

PMID

34 Schmid M, Davison T S, Henz S R, Pape U J, Demar M, Vingron M, Schölkopf B, Weigel D, Lohmann J U (2005). A gene expression map of Arabidopsis thaliana development. Nat Genet, 37(5): 501–506

PMID

35 Spencer M W, Casson S A, Lindsey K (2007). Transcriptional profiling of the Arabidopsis embryo. Plant Physiol, 143(2): 924–940

PMID

36 Tang F, Barbacioru C, Wang Y, Nordman E, Lee C, Xu N, Wang X, Bodeau J, Tuch B B, Siddiqui A, Lao K, Surani M A (2009). mRNA-Seq whole-transcriptome analysis of a single cell. Nat Methods, 6(5): 377–382

PMID

37 Van Gelder R N, von Zastrow M E, Yool A, Dement W C, Barchas J D, Eberwine J H (1990). Amplified RNA synthesized from limited quantities of heterogeneous cDNA. Proc Natl Acad Sci USA, 87(5): 1663–1667

PMID

38 Wienkoop S, Zoeller D, Ebert B, Simon-Rosin U, Fisahn J, Glinski M, Weckwerth W (2004). Cell-specific protein profiling in Arabidopsis thaliana trichomes: identification of trichome-located proteins involved in sulfur metabolism and detoxification. Phytochemistry, 65(11): 1641–1649

PMID

39 Wuest S E, Vijverberg K, Schmidt A, Weiss M, Gheyselinck J, Lohr M, Wellmer F, Rahnenführer J, von Mering C, Grossniklaus U (2010). Arabidopsis female gametophyte gene expression map reveals similarities between plant and animal gametes. Curr Biol, 20(6): 506–512

PMID

40 Yadav R K, Girke T, Pasala S, Xie M, Reddy G V (2009). Gene expression map of the Arabidopsis shoot apical meristem stem cell niche. Proc Natl Acad Sci USA, 106(12): 4941–4946

PMID

41 Zanetti M E, Chang I F, Gong F, Galbraith D W, Bailey-Serres J (2005). Immunopurification of polyribosomal complexes of Arabidopsis for global analysis of gene expression. Plant Physiol, 138(2): 624–635

PMID

42 Zhang C, Barthelson R A, Lambert G M, Galbraith D W (2008). Global characterization of cell-specific gene expression through fluorescence-activated sorting of nuclei. Plant Physiol, 147(1): 30–40

PMID