Functional genomics of root growth and development in Arabidopsis

Current Opinion in Plant Biology

Volumn 12, Issue 2, 2009, Pages 165-171

  Iyer Pascuzzi, Anjali ^a   Simpson, June ^b   Herrera Estrella, Luis ^b   Benfey, Philip N ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b DEPARTAMENTO DE FÍSICA   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; GENETICS; GENOMICS; GROWTH, DEVELOPMENT AND AGING; MAIZE; METABOLOMICS; PLANT ROOT; REVIEW; RICE;

ARABIDOPSIS; GENOMICS; METABOLOMICS; ORYZA SATIVA; PLANT ROOTS; ZEA MAYS;

ARABIDOPSIS;

EID: 62349137506     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2008.11.002     Document Type: Review

References (56)

1. Iyer-Pascuzzi A, Benfey P.: Transcriptional networks in root cell fate specification. BBA Gene Reg Mech, doi:10.1016/j.bbagrm.2008.09.006. A thorough review covering Arabidopsis root patterning.
2. Birnbaum K., Shasha D.E., Wang J.Y., Jung J.W., Lambert G.M., Galbraith D.W., and Benfey P.N. A gene expression map of the Arabidopsis root. Science 302 (2003) 1956-1960
3. Brady S.M., Orlando D.A., Lee J.Y., Wang J.Y., Koch J., Dinneny J.R., Mace D., Ohler U., and Benfey P.N. A high-resolution root spatiotemporal map reveals dominant expression patterns. Science 318 (2007) 801-806. In this elegant work, the authors created a spatiotemporal transcriptional map of the Arabidopsis root by profiling nearly all cell types and 12 developmental stages, creating the most comprehensive transcriptional view of any organ to date. They identified dominant transcription patterns and used coexpressed genes to find transcriptional modules.
4. Schmid M., Davison T.S., Henz S.R., Pape U.J., Demar M., Vingron M., Scholkopf B., Weigel D., and Lohmann J.U. A gene expression map of Arabidopsis thaliana development. Nat Genet 37 (2005) 501-506
5. Kilian J., Whitehead D., Horak J., Wanke D., Weinl S., Batistic O., D'Angelo C., Bornberg-Bauer E., Kudla J., and Harter K. The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J 50 (2007) 347-363
6. Goda H., Sasaki E., Akiyama K., Maruyama-Nakashita A., Nakabayashi K., Li W., Ogawa M., Yamauchi Y., Preston J., Aoki K., et al. The AtGenExpress hormone and chemical treatment data set: experimental design, data evaluation, model data analysis and data access. Plant J 55 (2008) 526-542
7. Baerenfaller K., Grossmann J., Grobei M.A., Hull R., Hirsch-Hoffmann M., Yalovsky S., Zimmermann P., Grossniklaus U., Gruissem W., and Baginsky S. Genome-scale proteomics reveals Arabidopsis thaliana gene models and proteome dynamics. Science 320 (2008) 938-941. The first proteomic map of Arabidopsis, this paper gives the first large-scale view into the root proteome.
8. Rowe H.C., Hansen B.G., Halkier B.A., and Kliebenstein D.J. Biochemical networks and epistasis shape the Arabidopsis thaliana metabolome. Plant Cell 20 (2008) 1199-1216
9. Keurentjes J.J.B., Fu J.Y., de Vos C.H.R., Lommen A., Hall R.D., Bino R.J., van der Plas L.H.W., Jansen R.C., Vreugdenhil D., and Koornneef M. The genetics of plant metabolism. Nat Genet 38 (2006) 842-849
10. Nikiforova V.J., Kopka J., Tolstikov V., Fiehn O., Hopkins L., Hawkesford M.J., Hesse H., and Hoefgen R. Systems rebalancing of metabolism in response to sulfur deprivation, as revealed by metabolome analysis of Arabidopsis plants. Plant Physiol 138 (2005) 304-318
11. Cook D., Fowler S., Fiehn O., and Thomashow M.F. A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis. Proc Natl Acad Sci U S A 101 (2004) 15243-15248
12. Hirai M.Y., Yano M., Goodenowe D.B., Kanaya S., Kimura T., Awazuhara M., Arita M., Fujiwara T., and Saito K. Integration of transcriptomics and metabolomics for understanding of global responses to nutritional stresses in Arabidopsis thaliana. Proc Natl Acad Sci U S A 101 (2004) 10205-10210
13. Jiao Y, Tausta LS, Gandotra N, Sun N, Liu T, Clay NK, Ceserani T, Chen M, Ma L, Holford M, et al.: A transcriptome atlas of rice cell types reveals cellular, functional, and developmental hierarchies. Nat Genet 2008, in press. The authors used LCM and microarray analysis to profile 40 cell types in rice, including 13 cell types and 3 developmental stages in the root. They identify interesting differences between the rice and Arabidopsis roots that will be an exciting area for future research.
14. Poroyko V., Hejlek L.G., Spollen W.G., Springer G.K., Nguyen H.T., Sharp R.E., and Bohnert H.J. The maize root transcriptome by serial analysis of gene expression. Plant Physiol 138 (2005) 1700-1710
15. Dembinsky D., Woll K., Saleem M., Liu Y., Fu Y., Borsuk L.A., Lamkemeyer T., Fladerer C., Madlung J., Barbazuk B., et al. Transcriptomic and proteomic analyses of pericycle cells of the maize primary root. Plant Physiol 145 (2007) 575-588
16. Zhu J., Alvarez S., Marsh E.L., LeNoble M.E., Cho I.-J., Sivaguru M., Chen S., Nguyen H.T., Wu Y., Schachtman D.P., et al. Cell wall proteome in the maize primary root elongation zone. II. Region-specific changes in water soluble and lightly ionically bound proteins under water deficit. Plant Physiol 145 (2007) 1533-1548
17. Zhu J.M., Chen S.X., Alvarez S., Asirvatham V.S., Schachtman D.P., Wu Y.J., and Sharp R.E. Cell wall proteome in the maize primary root elongation zone. I. Extraction and identification of water-soluble and lightly ionically bound proteins. Plant Physiol 140 (2006) 311-325
18. Jiang K., Zhang S.B., Lee S., Tsai G., Kim K., Huang H.Y., Chilcott C., Zhu T., and Feldman L.J. Transcription profile analyses identify genes and pathways central to root cap functions in maize. Plant Mol Biol 60 (2006) 343-363
19. Sauer M., Jakob A., Nordheim A., and Hochholdinger F. Proteomic analysis of shoot-borne root initiation in maize (Zea mays L.). Proteomics 6 (2006) 2530-2541
20. Liu Y., Lamkemeyer T., Jakob A., Mi G.H., Zhang F.S., Nordheim A., and Hochholdinger F. Comparative proteome analyses of maize (Zea mays L.) primary roots prior to lateral root initiation reveal differential protein expression in the lateral root initiation mutant rum1. Proteomics 6 (2006) 4300-4308
21. Woll K., Borsuk L.A., Stransky H., Nettleton D., Schnable P.S., and Hochholdinger F. Isolation, characterization, and pericycle-specific transcriptome analyses of the novel maize lateral and seminal root initiation mutant rum1. Plant Physiol 139 (2005) 1255-1267
22. Yuan J.S., Galbraith D.W., Dai S.Y., Griffin P., and Stewart C.N. Plant systems biology comes of age. Trend Plant Sci 13 (2008) 165-171
23. Aoki K., Ogata Y., and Shibata D. Approaches for extracting practical information from gene co-expression networks in plant biology. Plant Cell Physiol 48 (2007) 381-390
24. Rhee S.Y., Dickerson J., and Xu D. Bioinformatics and its applications in plant biology. Annu Rev Plant Bio 57 (2006) 335-360
25. Saito K., Hirai M.Y., and Yonekura-Sakakibara K. Decoding genes with coexpression networks and metabolomics - 'majority report by precogs'. Trend Plant Sci 13 (2008) 36-43. A good review covering coexpression analyses and large datasets.
26. Levesque M.P., Vernoux T., Busch W., Cui H.C., Wang J.Y., Blilou I., Hassan H., Nakajima K., Matsumoto N., Lohmann J.U., et al. Whole-genome analysis of the SHORT-ROOT developmental pathway in Arabidopsis. PLoS Biol 4 (2006) e143. This is a good example of how meta-analysis can lead to the identification of downstream targets, network architecture, and new functions for well-studied genes.
27. Hannah M.A., Heyer A.G., and Hincha D.K. A global survey of gene regulation during cold acclimation in Arabidopsis thaliana. PLoS Genet 1 (2005) 179-196
28. Ma S.S., and Bohnert H.J. Integration of Arabidopsis thaliana stress-related transcript profiles, promoter structures, and cell-specific expression. Genome Biol 8 (2007) R49
29. Walther D., Brunnemann R., and Selbig J. The regulatory code for transcriptional response diversity and its relation to genome structural properties in A-thaliana. PLoS Genet 3 (2007) 216-229
30. Helariutta Y., Fukaki H., Wysocka-Diller J., Nakajima K., Jung J., Sena G., Hauser M.T., and Benfey P.N. The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101 (2000) 555-567
31. Nakajima K., Sena G., Nawy T., and Benfey P.N. Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413 (2001) 307-311
32. Hirai M.Y., Sugiyama K., Sawada Y., Tohge T., Obayashi T., Suzuki A., Araki R., Sakurai N., Suzuki H., Aoki K., et al. Omics-based identification of Arabidopsis Myb transcription factors regulating aliphatic glucosinolate biosynthesis. Proc Natl Acad Sci U S A 104 (2007) 6478-6483. A good example of coexpression and data integration analyses combined with reverse genetics to identify gene function and gene-to-metabolite networks.
33. Sønderby I.E., Hansen B.G., Bjarnholt N., Ticconi C., Halkier B.A., and Kliebenstein D.J. A systems biology approach identifies a R2R3 MYB gene subfamily with distinct and overlapping functions in regulation of aliphatic glucosinolates. PLoS ONE 2 (2007) e1322
34. Persson S., Wei H.R., Milne J., Page G.P., and Somerville C.R. Identification of genes required for cellulose synthesis by regression analysis of public microarray data sets. Proc Natl Acad Sci U S A 102 (2005) 8633-8638
35. Yonekura-Sakakibara K., Tohge T., Matsuda F., Nakabayashi R., Takayama H., Niida R., Watanabe-Takahashi A., Inoue E., and Saito K. Comprehensive flavonol profiling and transcriptome coexpression analysis leading to decoding gene-metabolite correlations in Arabidopsis. Plant Cell 20 (2008) 2160-2176
36. Gutierez R.A., Stokes T.L., Thum K., Xu X., Obertello M., Katari M.S., Tanurdzic M., Dean A., Nero D.C., McClung C.R., et al. Systems approach identifies an organic nitrogen-responsive gene network that is regulated by the master clock control gene CCA1. Proc Natl Acad Sci U S A 105 (2008) 4939-4944
37. Desnos T. Root branching responses to phosphate and nitrate. Curr Opin Plant Biol 11 (2008) 82-87
38. Misson J., Raghothama K.G., Jain A., Jouhet J., Block M.A., Bligny R., Ortet P., Creff A., Somerville S., Rolland N., et al. A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc Natl Acad Sci U S A 102 (2005) 11934-11939
39. Morcuende R., Bari R., Gibon Y., Zheng W.M., Pant B.D., Blasing O., Usadel B., Czechowski T., Udvardi M.K., Stitt M., et al. Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant Cell Environ 30 (2007) 85-112
40. Calderon-Vazquez C., Ibarra-Laclette E., Caballero-Perez J., and Herrera-Estrella L. Transcript profiling of Zea mays roots reveals gene responses to phosphate deficiency at the plant- and species-specific levels. J Exp Bot 59 (2008) 2479-2497
41. Cruz-Ramirez A., Oropeza-Aburto A., Razo-Hernandez F., Ramirez-Chavez E., and Herrera-Estrella L. Phospholipase DZ2 plays an important role in extraplastidic galactolipid biosynthesis and phosphate recycling in Arabidopsis roots. Proc Natl Acad Sci U S A 103 (2006) 6765-6770
42. Li M.Y., Qin C.B., Welti R., and Wang X.M. Double knockouts of phospholipases D zeta 1 and D zeta 2 in Arabidopsis affect root elongation during phosphate-limited growth but do not affect root hair patterning. Plant Physiol 140 (2006) 761-770
43. Devaiah B.N., Nagarajan V.K., and Raghothama K.G. Phosphate homeostasis and root development in Arabidopsis are synchronized by the zinc finger transcription factor ZAT6. Plant Physiol 145 (2007) 147-159
44. Chen Z.H., Nimmo G.A., Jenkins G.I., and Nimmo H.G. BHLH32 modulates several biochemical and morphological processes that respond to P-i starvation in Arabidopsis. Biochem J 405 (2007) 191-198
45. Devaiah B.N., Karthikeyan A.S., and Raghothama K.G. WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol 143 (2007) 1789-1801
46. Yi K.K., Wu Z.C., Zhou J., Du L.M., Guo L.B., Wu Y.R., and Wu P. OsPTF1, a novel transcription factor involved in tolerance to phosphate starvation in rice. Plant Physiol 138 (2005) 2087-2096. This manuscript describes the identification of a phosphorous-responsive transcription factor that when overexpressed in transgenic rice plants leads to an increase in productivity under phosphate limiting conditions.
47. Li K.P., Xu C.Z., Li Z.X., Zhang K.W., Yang A.F., and Zhang J.R. Comparative proteome analyses of phosphorus responses in maize (Zea mays L.) roots of wild-type and a low-P-tolerant mutant reveal root characteristics associated with phosphorus efficiency. Plant J 55 (2008) 927-939
48. Lin S.I., Chiang S.F., Lin W.Y., Chen J.W., Tseng C.Y., Wu P.C., and Chiou T.J. Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiol 147 (2008) 732-746
49. Pant B.D., Buhtz A., Kehr J., and Scheible W.R. MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J 53 (2008) 731-738. In conjunction with the manuscript by Lin et al. [48], these papers describe the role of microRNAs as systemic signals that participate in the regulation of phosphorus homeostasis in plants by targeting the UBC24 ubiquitin conjugase mRNA.
50. Shin R., and Schachtman D.P. Hydrogen peroxide mediates plant root cell response to nutrient deprivation. Proc Natl Acad Sci U S A 101 (2004) 8827-8832
51. Shin R., Burch A.Y., Huppert K.A., Tiwari S.B., Murphy A.S., Guilfoyle T.J., and Schachtman D.P. The Arabidopsis transcription factor MYB77 modulates auxin signal transduction. Plant Cell 19 (2007) 2440-2453. This work shows for the first time that nutrient availability impinges into root development by altering the sensitivity of Arabidopsis roots to auxin.
52. Liu J.X., Han L.L., Chen F.J., Bao J., Zhang F.S., and Mi G.H. Microarray analysis reveals early responsive genes possibly involved in localized nitrate stimulation of lateral root development in maize (Zea mays L.). Plant Sci 175 (2008) 272-282
53. Scheible W.R., Morcuende R., Czechowski T., Fritz C., Osuna D., Palacios-Rojas N., Schindelasch D., Thimm O., Udvardi M.K., and Stitt M. Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiol 136 (2004) 2483-2499
54. Ruffel S., Freixes S., Balzergue S., Tillard P., Jeudy C., Martin-Magniette M.L., van der Merwe M.J., Kakar K., Gouzy J., Fernie A.R., et al. Systemic signaling of the plant nitrogen status triggers specific transcriptome responses depending on the nitrogen source in Medicago truncatula. Plant Physiol 146 (2008) 2020-2035
55. Dinneny J.R., Long T.A., Wang J.Y., Jung J.W., Mace D., Pointer S., Barron C., Brady S.M., Schiefelbein J., and Benfey P.N. Cell identity mediates the response of Arabidopsis roots to abiotic stress. Science 320 (2008) 942-945. The authors examined the effect of two environmental stresses on cellular responses in the root, using three datasets covering five cell types, four developmental zones, and a whole root time course. This is one of the first reports to examine the effect of stress at this level of resolution.
56. Gifford M.L., Dean A., Gutierrez R.A., Coruzzi G.M., and Birnbaum K.D. Cell-specific nitrogen responses mediate developmental plasticity. Proc Natl Acad Sci U S A 105 (2008) 803-808. Using a similar approach to Dinneny and Long, the authors examine the response to nitrate by different cell types within the root. Using this dataset, they identified a nitrogen-regulated transcriptional module controlling lateral root development.