#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

A Gene Regulatory Network for Root Epidermis Cell Differentiation in Arabidopsis


The root epidermis of Arabidopsis provides an exceptional model for studying the molecular basis of cell fate and differentiation. To obtain a systems-level view of root epidermal cell differentiation, we used a genome-wide transcriptome approach to define and organize a large set of genes into a transcriptional regulatory network. Using cell fate mutants that produce only one of the two epidermal cell types, together with fluorescence-activated cell-sorting to preferentially analyze the root epidermis transcriptome, we identified 1,582 genes differentially expressed in the root-hair or non-hair cell types, including a set of 208 “core” root epidermal genes. The organization of the core genes into a network was accomplished by using 17 distinct root epidermis mutants and 2 hormone treatments to perturb the system and assess the effects on each gene's transcript accumulation. In addition, temporal gene expression information from a developmental time series dataset and predicted gene associations derived from a Bayesian modeling approach were used to aid the positioning of genes within the network. Further, a detailed functional analysis of likely bHLH regulatory genes within the network, including MYC1, bHLH54, bHLH66, and bHLH82, showed that three distinct subfamilies of bHLH proteins participate in root epidermis development in a stage-specific manner. The integration of genetic, genomic, and computational analyses provides a new view of the composition, architecture, and logic of the root epidermal transcriptional network, and it demonstrates the utility of a comprehensive systems approach for dissecting a complex regulatory network.


Vyšlo v časopise: A Gene Regulatory Network for Root Epidermis Cell Differentiation in Arabidopsis. PLoS Genet 8(1): e32767. doi:10.1371/journal.pgen.1002446
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002446

Souhrn

The root epidermis of Arabidopsis provides an exceptional model for studying the molecular basis of cell fate and differentiation. To obtain a systems-level view of root epidermal cell differentiation, we used a genome-wide transcriptome approach to define and organize a large set of genes into a transcriptional regulatory network. Using cell fate mutants that produce only one of the two epidermal cell types, together with fluorescence-activated cell-sorting to preferentially analyze the root epidermis transcriptome, we identified 1,582 genes differentially expressed in the root-hair or non-hair cell types, including a set of 208 “core” root epidermal genes. The organization of the core genes into a network was accomplished by using 17 distinct root epidermis mutants and 2 hormone treatments to perturb the system and assess the effects on each gene's transcript accumulation. In addition, temporal gene expression information from a developmental time series dataset and predicted gene associations derived from a Bayesian modeling approach were used to aid the positioning of genes within the network. Further, a detailed functional analysis of likely bHLH regulatory genes within the network, including MYC1, bHLH54, bHLH66, and bHLH82, showed that three distinct subfamilies of bHLH proteins participate in root epidermis development in a stage-specific manner. The integration of genetic, genomic, and computational analyses provides a new view of the composition, architecture, and logic of the root epidermal transcriptional network, and it demonstrates the utility of a comprehensive systems approach for dissecting a complex regulatory network.


Zdroje

1. VanderpoeleKQuimbayaMCasneufTDeVeylderLVan de PeerY 2009 Unraveling transcriptional control in Arabidopsis using cis-regulatory elements and coexpression networks. Plant Physiol 150 535 546

2. DavidsonEH 2010 Emerging properties of animal gene regulatory networks. Nature 468 911 920

3. SchellmannSHulskampMUhrigJ 2007 Epidermal pattern formation in the root and shoot of Arabidopsis. Biochem Soc Trans 35 146 148

4. GriersonCSchiefelbeinJ 2002 Root hairs. SomervilleCMeyerowitzEM The Arabidopsis Book: American Society of Plant Biologists http://www.aspb.org/publications/arabidopsis/

5. Tominaga-WadaRIshidaTWadaT 2011 New insights into the mechanism of development of Arabidopsis root hairs and trichomes. Int Rev Cell Mol Biol 286 67 106

6. DolanLJanmaatKWillemsenVLinsteadPPoethigS 1993 Cellular organisation of the Arabidopsis thaliana root. Development 119 71 84

7. DolanLDuckettCGriersonCLinsteadPSchneiderK 1994 Clonal relations and patterning in the root epidermis of Arabidopsis. Development 120 2465 2474

8. ScheresBWolkenfeltHWillemsenVTerlouwMLawsonE 1994 Embryonic origin of the Arabidopsis primary root and root meristem initials. Development 120 2475 2487

9. DolanLDuckettCGriersonCLinsteadPSchneiderK 1994 Clonal relations and patterning in the root epidermis of Arabidopsis. Development 120 2465 2474

10. GalwayMEMasucciJDLloydAMWalbotVDavisRW 1994 The TTG gene is required to specify epidermal cell fate and cell patterning in the Arabidopsis root. Dev Biol 166 740 754

11. BergerFHaseloffJSchiefelbeinJDolanL 1998 Positional information in root epidermis is defined during embryogenesis and acts in domains with strict boundaries. Curr Biol 8 421 430

12. MasucciJDRerieWGForemanDRZhangMGalwayME 1996 The homeobox gene GLABRA2 is required for position-dependent cell differentiation in the root epidermis of Arabidopsis thaliana. Development 122 1253 1260

13. FreshourGClayRPFullerMSAlbersheimPDarvillAG 1996 Developmental and tissue-specific structural alterations of the cell-wall polysaccharides of Arabidopsis thaliana roots. Plant Physiol 110 1413 1429

14. CostaSShawP 2005 Chromatin organization and cell fate switch respond to positional information in Arabidopsis. Nature

15. GriersonCSSchiefelbeinJ 2008 Genetics of Root Hair Formation. Root Hairs Heidelberg Springer-Verlag

16. BernhardtCLeeMMGonzalezAZhangFLloydA 2003 The bHLH genes GLABRA3 (GL3) and ENHANCER OF GLABRA3 (EGL3) specify epidermal cell fate in the Arabidopsis root. Development 130 6431 6439

17. LeeMMSchiefelbeinJ 1999 WEREWOLF, a MYB-related protein in Arabidopsis, is a position-dependent regulator of epidermal cell patterning. Cell 99 473 483

18. KangYHKirikVHulskampMNamKHHagelyK 2009 The MYB23 gene provides a positive feedback loop for cell fate specification in the Arabidopsis root epidermis. Plant Cell 21 1080 1094

19. WadaTTachibanaTShimuraYOkadaK 1997 Epidermal cell differentiation in Arabidopsis determined by a Myb homolog, CPC. Science 277 1113 1116

20. KirikVSimonMHuelskampMSchiefelbeinJ 2004 The ENHANCER OF TRY AND CPC1 gene acts redundantly with TRIPTYCHON and CAPRICE in trichome and root hair cell patterning in Arabidopsis. Dev Biol in press

21. SchellmannSSchnittgerAKirikVWadaTOkadaK 2002 TRIPTYCHON and CAPRICE mediate lateral inhibition during trichome and root hair patterning in Arabidopsis. Embo J 21 5036 5046

22. WalkerARDavisonPABolognesi-WinfieldACJamesCMSrinivasanN 1999 The TRANSPARENT TESTA GLABRA1 locus, which regulates trichome differentiation and anthocyanin biosynthesis in Arabidopsis, encodes a WD40 repeat protein. Plant Cell 11 1337 1350

23. BernhardtCLeeMMGonzalezAZhangFLloydA 2003 The bHLH genes GLABRA3 (GL3) and ENHANCER OF GLABRA3 (EGL3) specify epidermal cell fate in the Arabidopsis root. Development 130 6431 6439

24. BernhardtCZhaoMGonzalezALloydASchiefelbeinJ 2005 The bHLH genes GL3 and EGL3 participate in an intercellular regulatory circuit that controls cell patterning in the Arabidopsis root epidermis. Development 132 291 298

25. ZhangFGonzalezAZhaoMPayneCTLloydA 2003 A network of redundant bHLH proteins functions in all TTG1-dependent pathways of Arabidopsis. Development 130 4859 4869

26. WangSHubbardLChangYGuoJSchiefelbeinJ 2008 Comprehensive analysis of single-repeat R3 MYB proteins in epidermal cell patterning and their transcriptional regulation in Arabidopsis. BMC Plant Biol 8 81

27. WadaTKurataTTominagaRKoshino-KimuraYTachibanaT 2002 Role of a positive regulator of root hair development, CAPRICE, in Arabidopsis root epidermal cell differentiation. Development 129 5409 5419

28. KurataTIshidaTKawabata-AwaiCNoguchiMHattoriS 2005 Cell-to-cell movement of the CAPRICE protein in Arabidopsis root epidermal cell differentiation. Development 132 5387 5398

29. RyuKHKangYHParkYHHwangISchiefelbeinJ 2005 The WEREWOLF MYB protein directly regulates CAPRICE transcription during cell fate specification in the Arabidopsis root epidermis. Development 132 4765 4775

30. Koshino-KimuraYWadaTTachibanaTTsugekiRIshiguroS 2005 Regulation of CAPRICE transcription by MYB proteins for root epidermis differentiation in Arabidopsis. Plant Cell Physiol 46 817 826

31. TominagaRIwataMOkadaKWadaT 2007 Functional analysis of the epidermal-specific MYB genes CAPRICE and WEREWOLF in Arabidopsis. Plant Cell 19 2264 2277

32. EschJJChenMSandersMHillestadMNdkiumS 2003 A contradictory GLABRA3 allele helps define gene interactions controlling trichome development in Arabidopsis. Development 130 5885 5894

33. WangSBarronCSchiefelbeinJChenJG 2010 Distinct relationships between GLABRA2 and single-repeat R3 MYB transcription factors in the regulation of trichome and root hair patterning in Arabidopsis. New Phytol 185 387 400

34. KwakSHSchiefelbeinJ 2007 The role of the SCRAMBLED receptor-like kinase in patterning the Arabidopsis root epidermis. Dev Biol 302 118 131

35. KwakSHShenRSchiefelbeinJ 2005 Positional signaling mediated by a receptor-like kinase in Arabidopsis. Science 307 1111 1113

36. KwakSHSchiefelbeinJ 2008 A feedback mechanism controlling SCRAMBLED receptor accumulation and cell-type pattern in Arabidopsis. Current Biology 18 1949 1954

37. RerieWGFeldmannKAMarksMD 1994 The GLABRA2 gene encodes a homeo domain protein required for normal trichome development in Arabidopsis. Genes Dev 8 1388 1399

38. Di CristinaMSessaGDolanLLinsteadPBaimaS 1996 The Arabidopsis Athb-10 (GLABRA2) is an HD-Zip protein required for regulation of root hair development. Plant J 10 393 402

39. MasucciJDSchiefelbeinJW 1994 The rhd6 Mutation of Arabidopsis thaliana Alters Root-Hair Initiation through an Auxin- and Ethylene-Associated Process. Plant Physiol 106 1335 1346

40. MasucciJDSchiefelbeinJW 1996 Hormones act downstream of TTG and GL2 to promote root hair outgrowth during epidermis development in the Arabidopsis root. Plant Cell 8 1505 1517

41. MenandBYiKJouannicSHoffmannLRyanE 2007 An ancient mechanism controls the development of cells with a rooting function in land plants. Science 316 1477 1480

42. PittsRJCernacAEstelleM 1998 Auxin and ethylene promote root hair elongation in Arabidopsis. Plant J 16 553 560

43. RahmanAHosokawaSOonoYAmakawaTGotoN 2002 Auxin and ethylene response interactions during Arabidopsis root hair development dissected by auxin influx modulators. Plant Physiol 130 1908 1917

44. BirnbaumKShashaDEWangJYJungJWLambertGM 2003 A gene expression map of the Arabidopsis root. Science 302 1956 1960

45. BirnbaumKJungJWWangJYLambertGMHirstJA 2005 Cell type-specific expression profiling in plants via cell sorting of protoplasts from fluorescent reporter lines. Nat Methods 2 615 619

46. HungCYLinYZhangMPollockSMarksMD 1998 A common position-dependent mechanism controls cell-type patterning and GLABRA2 regulation in the root and hypocotyl epidermis of Arabidopsis. Plant Physiol 117 73 84

47. SimonMLeeMMLinYGishLSchiefelbeinJ 2007 Distinct and overlapping roles of single-repeat MYB genes in root epidermal patterning. Dev Biol 311 566 578

48. KirikVSimonMHuelskampMSchiefelbeinJ 2004 The ENHANCER OF TRY AND CPC1 gene acts redundantly with TRIPTYCHON and CAPRICE in trichome and root hair cell patterning in Arabidopsis. Dev Biol 268 506 513

49. BernhardtCTierneyML 2000 Expression of AtPRP3, a proline-rich structural cell wall protein from Arabidopsis, is regulated by cell-type-specific developmental pathways involved in root hair formation. Plant Physiol 122 705 714

50. IshidaTHattoriSSanoRInoueKShiranoY 2007 Arabidopsis TRANSPARENT TESTA GLABRA2 is directly regulated by R2R3 MYB transcription factors and is involved in regulation of GLABRA2 transcription in epidermal differentiation. Plant Cell 19 2531 2543

51. ChoHTCosgroveDJ 2002 Regulation of root hair initiation and expansin gene expression in Arabidopsis. Plant Cell 14 3237 3253

52. WonSKLeeYJLeeHYHeoYKChoM 2009 Cis-element- and transcriptome-based screening of root hair-specific genes and their functional characterization in Arabidopsis. Plant Physiol 150 1459 1473

53. HeimMAJakobyMWerberMMartinCWeisshaarB 2003 The basic helix-loop-helix transcription factor family in plants: A genome-wide study of protein structure and functional diversity. Mol Biol Evol 20 735 747

54. BaumbergerNRingliCKellerB 2001 The chimeric leucine-rich repeat/extensin cell wall protein LRX1 is required for root hair morphogenesis in Arabidopsis thaliana. Genes Dev 15 1128 1139

55. ForemanJDemidchikVBothwellJHMylonaPMiedemaH 2003 Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422 442 446

56. SchiefelbeinJWSomervilleC 1990 Genetic Control of Root Hair Development in Arabidopsis thaliana. Plant Cell 2 235 243

57. FaveryBRyanEForemanJLinsteadPBoudonckK 2001 KOJAK encodes a cellulose synthase-like protein required for root hair cell morphogenesis in Arabidopsis. Genes Dev 15 79 89

58. GalwayMEEngRCSchiefelbeinJWWasteneysGO 2011 Root hair-specific disruption of cellulose and xyloglucan in AtCSLD3 mutants, and factors affecting the post-rupture resumption of mutant root hair growth. Planta 233 985 999

59. FischerUIkedaYGrebeM 2007 Planar polarity of root hair positioning in Arabidopsis. Biochem Soc Trans 35 149 151

60. ZhangYJLynchJPBrownKM 2003 Ethylene and phosphorus availability have interacting yet distinct effects on root hair development. J Exp Bot 54 2351 2361

61. NeapolitanRE 2003 Learning Bayesian Networks Harlow Prentice Hall

62. HonkelaAGirardotCGustafsonEHLiuYHFurlongEE 2010 Model-based method for transcription factor target identification with limited data. Proc Natl Acad Sci U S A 107 7793 7798

63. SaitoKFujimura-KamadaKFurutaNKatoUUmedaM 2004 Cdc50p, a protein required for polarized growth, associates with the Drs2p P-type ATPase implicated in phospholipid translocation in Saccharomyces cerevisiae. Mol Biol Cell 15 3418 3432

64. BradySMOrlandoDALeeJYWangJYKochJ 2007 A high-resolution root spatiotemporal map reveals dominant expression patterns. Science 318 801 806

65. IshidaTKurataTOkadaKWadaT 2008 A genetic regulatory network in the development of trichomes and root hairs. Annu Rev Plant Biol 59 365 386

66. YiKMenandBBellEDolanL 2010 A basic helix-loop-helix transcription factor controls cell growth and size in root hairs. Nat Genet 42 264 267

67. JonesMARaymondMJSmirnoffN 2006 Analysis of the root-hair morphogenesis transcriptome reveals the molecular identity of six genes with roles in root-hair development in Arabidopsis. Plant J 45 83 100

68. DealRBHenikoffS 2010 A simple method for gene expression and chromatin profiling of individual cell types within a tissue. Dev Cell 18 1030 1040

69. LeeMMSchiefelbeinJ 2002 Cell pattern in the Arabidopsis root epidermis determined by lateral inhibition with feedback. Plant Cell 14 611 618

70. StepanovaANAlonsoJM 2009 Ethylene signaling and response: where different regulatory modules meet. Curr Opin Plant Biol 12 548 555

71. ZimmermannIMHeimMAWeisshaarBUhrigJF 2004 Comprehensive identification of Arabidopsis thaliana MYB transcription factors interacting with R/B-like BHLH proteins. Plant J 40 22 34

72. SavageNSWalkerTWieckowskiYSchiefelbeinJDolanL 2008 A mutual support mechanism through intercellular movement of CAPRICE and GLABRA3 can pattern the Arabidopsis root epidermis. PLoS Biol 6 e235 doi:10.1371/journal.pbio.0060235

73. MorohashiKGrotewoldE 2009 A systems approach reveals regulatory circuitry for Arabidopsis trichome initiation by the GL3 and GL1 selectors. PLoS Genet 5 e1000396 doi:10.1371/journal.pgen.1000396

74. KarasBAmyotLJohansenCSatoSTabataS 2009 Conservation of lotus and Arabidopsis basic helix-loop-helix proteins reveals new players in root hair development. Plant Physiol 151 1175 1185

75. DongJBergmannDC 2010 Stomatal patterning and development. Curr Top Dev Biol 91 267 297

76. FarnhamPJ 2009 Insights from genomic profiling of transcription factors. Nat Rev Genet 10 605 616

77. FerrierTMatusJTJinJRiechmannJL 2011 Arabidopsis paves the way: genomic and network analyses in crops. Curr Opin Biotech 22 260 270

78. HeimMAJakobyMWerberMMartinCWeisshaarB 2003 The basic helix-loop-helix transcription factor family in plants: a genome-wide study of protein structure and functional diversity. Mol Biol Evol 20 735 747

79. HaseloffJSiemeringKRPrasherDCHodgeS 1997 Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. Proc Natl Acad Sci U S A 94 2122 2127

80. CloughSJBentAF 1998 Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16 735 743

81. XiangCHanPLutzigerIWangKOliverDJ 1999 A mini binary vector series for plant transformation. Plant Mol Biol 40 711 717

82. BargmannBOBirnbaumKD 2010 Fluorescence activated cell sorting of plant protoplasts. J Vis Exp

83. IrizarryRABolstadBMCollinFCopeLMHobbsB 2003 Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Research 31 e15

84. DaiMWangPBoydADKostovGAtheyB 2005 Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data. Nucleic Acids Res 33 e175

85. TusherVGTibshiraniRChuG 2001 Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98 5116 5121

86. BenjaminiYHochbergY 1995 Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc 57 289 300

87. ReichMLiefeldTGouldJLernerJTamayoP 2006 GenePattern 2.0. Nat Genet 38 500 501

88. de HoonMJImotoSNolanJMiyanoS 2004 Open source clustering software. Bioinformatics 20 1453 1454

89. ShahAWoolfP 2009 Python Environment for Bayesian Learning: Inferring the Structure of Bayesian Networks from Knowledge and Data. J Mach Learn Res 10 159 162

90. ShahATenzenTMcMahonAPWoolfPJ 2009 Using mechanistic Bayesian networks to identify downstream targets of the sonic hedgehog pathway. BMC Bioinformatics 10 433

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2012 Číslo 1
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#