#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

A Central Regulatory System Largely Controls Transcriptional Activation and Repression Responses to Phosphate Starvation in Arabidopsis


Plants respond to different stresses by inducing or repressing transcription of partially overlapping sets of genes. In Arabidopsis, the PHR1 transcription factor (TF) has an important role in the control of phosphate (Pi) starvation stress responses. Using transcriptomic analysis of Pi starvation in phr1, and phr1 phr1-like (phl1) mutants and in wild type plants, we show that PHR1 in conjunction with PHL1 controls most transcriptional activation and repression responses to phosphate starvation, regardless of the Pi starvation specificity of these responses. Induced genes are enriched in PHR1 binding sequences (P1BS) in their promoters, whereas repressed genes do not show such enrichment, suggesting that PHR1(-like) control of transcriptional repression responses is indirect. In agreement with this, transcriptomic analysis of a transgenic plant expressing PHR1 fused to the hormone ligand domain of the glucocorticoid receptor showed that PHR1 direct targets (i.e., displaying altered expression after GR:PHR1 activation by dexamethasone in the presence of cycloheximide) corresponded largely to Pi starvation-induced genes that are highly enriched in P1BS. A minimal promoter containing a multimerised P1BS recapitulates Pi starvation-specific responsiveness. Likewise, mutation of P1BS in the promoter of two Pi starvation-responsive genes impaired their responsiveness to Pi starvation, but not to other stress types. Phylogenetic footprinting confirmed the importance of P1BS and PHR1 in Pi starvation responsiveness and indicated that P1BS acts in concert with other cis motifs. All together, our data show that PHR1 and PHL1 are partially redundant TF acting as central integrators of Pi starvation responses, both specific and generic. In addition, they indicate that transcriptional repression responses are an integral part of adaptive responses to stress.


Vyšlo v časopise: A Central Regulatory System Largely Controls Transcriptional Activation and Repression Responses to Phosphate Starvation in Arabidopsis. PLoS Genet 6(9): e32767. doi:10.1371/journal.pgen.1001102
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1001102

Souhrn

Plants respond to different stresses by inducing or repressing transcription of partially overlapping sets of genes. In Arabidopsis, the PHR1 transcription factor (TF) has an important role in the control of phosphate (Pi) starvation stress responses. Using transcriptomic analysis of Pi starvation in phr1, and phr1 phr1-like (phl1) mutants and in wild type plants, we show that PHR1 in conjunction with PHL1 controls most transcriptional activation and repression responses to phosphate starvation, regardless of the Pi starvation specificity of these responses. Induced genes are enriched in PHR1 binding sequences (P1BS) in their promoters, whereas repressed genes do not show such enrichment, suggesting that PHR1(-like) control of transcriptional repression responses is indirect. In agreement with this, transcriptomic analysis of a transgenic plant expressing PHR1 fused to the hormone ligand domain of the glucocorticoid receptor showed that PHR1 direct targets (i.e., displaying altered expression after GR:PHR1 activation by dexamethasone in the presence of cycloheximide) corresponded largely to Pi starvation-induced genes that are highly enriched in P1BS. A minimal promoter containing a multimerised P1BS recapitulates Pi starvation-specific responsiveness. Likewise, mutation of P1BS in the promoter of two Pi starvation-responsive genes impaired their responsiveness to Pi starvation, but not to other stress types. Phylogenetic footprinting confirmed the importance of P1BS and PHR1 in Pi starvation responsiveness and indicated that P1BS acts in concert with other cis motifs. All together, our data show that PHR1 and PHL1 are partially redundant TF acting as central integrators of Pi starvation responses, both specific and generic. In addition, they indicate that transcriptional repression responses are an integral part of adaptive responses to stress.


Zdroje

1. DixonRA

PaivaNL

1995 Stress-Induced Phenylpropanoid Metabolism. Plant Cell 7 1085 1097

2. MolJ

JenkinsG

SchäferE

WeissD

1996 Signal perception, transduction, and gene expression involved in anthocyanin. Crit Rev Plant Sci 15 525 557

3. LimPO

KimHJ

NamHG

2007 Leaf senescence. Annu Rev Plant Biol 58 115 136

4. MaS

BohnertHJ

2007 Integration of Arabidopsis thaliana stress-related transcript profiles, promoter structures, and cell-specific expression. Genome Biol 8 R49

5. WalleyJW

CoughlanS

HudsonME

CovingtonMF

KaspiR

2007 Mechanical stress induces biotic and abiotic stress responses via a novel cis-element. PLoS Genet 3 1800 1812

6. HammondJP

BennettMJ

BowenHC

BroadleyMR

EastwoodDC

2003 Changes in gene expression in Arabidopsis shoots during phosphate starvation and the potential for developing smart plants. Plant Physiol 132 578 596

7. WasakiJ

YonetaniR

KurodaS

2003 Transcriptomic analysis of metabolic changes by phosphorus stress in rice plant roots. Plant Cell Environ 26 1515 1523

8. WuP

MaL

HouX

WangM

WuY

2003 Phosphate starvation triggers distinct alterations of genome expression in Arabidopsis roots and leaves. Plant Physiol 132 1260 1271

9. MissonJ

RaghothamaKG

JainA

JouhetJ

BlockMA

2005 A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc Natl Acad Sci USA 102 11934 11939

10. MorcuendeR

BariR

GibonY

ZhengW

PantBD

2007 Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant Cell Environ 30 85 112

11. MullerR

MorantM

JarmerH

NilssonL

NielsenTH

2007 Genome-wide analysis of the Arabidopsis leaf transcriptome reveals interaction of phosphate and sugar metabolism. Plant Physiol 143 156 171

12. RubioV

LinharesF

SolanoR

MartinAC

IglesiasJ

2001 A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev 15 2122 2133

13. YiK

WuZ

ZhouJ

DuL

GuoL

2005 OsPTF1, a novel transcription factor involved in tolerance to phosphate starvation in rice. Plant Physiol 138 2087 2096

14. ChenZH

NimmoGA

JenkinsGI

NimmoHG

2007 BHLH32 modulates several biochemical and morphological processes that respond to Pi starvation in Arabidopsis. Biochem J 405 191 198

15. DevaiahBN

KarthikeyanAS

RaghothamaKG

2007 WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol 143 1789 1801

16. DevaiahBN

NagarajanVK

RaghothamaKG

2007 Phosphate homeostasis and root development in Arabidopsis are synchronized by the zinc finger transcription factor ZAT6. Plant Physiol 145 147 159

17. DevaiahB

MadhuvanthiR

KarthikeyanAS

RaghothamaKG

2009 Phosphate starvation responses and gibberellic acid biosynthesis are regulated by the MYB62 transcription factor in Arabidopsis. Molec Plant 2 43 58

18. MiuraK

RusA

SharkhuuA

YokoiS

KarthikeyanAS

2005 The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proc Natl Acad Sci USA 102 7760 7765

19. AungK

LinSI

WuCC

HuangYT

SuCL

2006 pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiol 141 1000 1011

20. BariR

Datt PantB

StittM

ScheibleWR

2006 PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141 988 999

21. LinSI

ChiangSF

LinWY

ChenJW

TsengCY

2008 Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiol 147 732 746

22. GonzalezE

SolanoR

RubioV

LeyvaA

Paz-AresJ

2005 PHOSPHATE TRANSPORTER TRAFFIC FACILITATOR1 is a plant-specific SEC12-related protein that enables the endoplasmic reticulum exit of a high-affinity phosphate transporter in Arabidopsis. Plant Cell 17 3500 3512

23. FujiiH

ChiouTJ

LinSI

AungK

ZhuJK

2005 A miRNA involved in phosphate-starvation response in Arabidopsis. Curr Biol 15 2038 2043

24. ChiouTJ

AungK

LinSI

WuCC

ChiangSF

2006 Regulation of phosphate homeostasis by MicroRNA in Arabidopsis. Plant Cell 18 412 421

25. Franco-ZorrillaJM

ValliA

TodescoM

MateosI

PugaMI

2007 Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 39 1033 1037

26. HsiehLC

LinSI

ShihAC

ChenJW

LinWY

2009 Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiol 151 2120 32

27. PantBD

Musialak-LangeM

NucP

MayP

BuhtzA

2009 Identification of nutrient-responsive Arabidopsis and rapeseed microRNAs by comprehensive real-time polymerase chain reaction profiling and small RNA sequencing. Plant Physiol 150 1541 1555

28. DuanK

YiK

DangL

HuangH

WuW

2008 Characterization of a sub-family of Arabidopsis genes with the SPX domain reveals their diverse functions in plant tolerance to phosphorus starvation. Plant J 54 965 975

29. WangC

YingS

HuangH

LiK

WuP

2009 Involvement of OsSPX1 in phosphate homeostasis in rice. Plant J 57 895 904

30. ZimmermannP

Hirsch-HoffmannM

HennigL

GruissemW

2004 GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136 2621 2632

31. AoyamaT

ChuaNH

1997 A glucocorticoid-mediated transcriptional induction system in transgenic plants. Plant J 11 605 612

32. NilssonL

MullerR

NielsenTH

2007 Increased expression of the MYB-related transcription factor, PHR1, leads to enhanced phosphate uptake in Arabidopsis thaliana. Plant Cell Environ 30 1499 1512

33. ZhouJ

JiaoF

WuZ

LiY

WangX

2008 OsPHR2 is involved in phosphate-starvation signaling and excessive phosphate accumulation in shoots of plants. Plant Physiol 146 4 1673 1686

34. HopeIA

StruhlK

1987 GCN4, a eukaryotic transcriptional activator protein, binds as a dimer to target DNA. EMBO J 6 9 2781 2784

35. ThimmO

BläsingO

GibonY

NagelA

MeyerS

2004 MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37 914 939

36. YuB

XuC

BenningC

2002 Arabidopsis disrupted in SQD2 encoding sulfolipid synthase is impaired in phosphate-limited growth. Proc Natl Acad Sci USA 99 5732 5737

37. JouhetJ

MaréchalE

BaldanB

BlignyR

JoyardJ

2004 Phosphate deprivation induces transfer of DGDG galactolipid from chloroplast to mitochondria. J Cell Biol 167 863 874

38. BenningC

OthaH

2005 Three enzyme systems for galactoglycerolipid biosynthesis are coordinately regulated in plants. J Biol Chem 280 2397 2400

39. RubioV

BustosR

IrigoyenML

Cardona-LopezX

Rojas-TrianaM

2009 Plant hormones and nutrient signaling. Plant Mol Biol 69 361 373

40. GalaktionovK

ChenX

BeachD

1996 Cdc25 cell-cycle phosphatase as a target of c-myc. Nature 382 511 517

41. SablowskiRW

MeyerowitzEM

1998 A homolog of NO APICAL MERISTEM is an immediate target of the floral homeotic genes APETALA3/PISTILLATA. Cell 92 93 103

42. MartinAC

del PozoJC

IglesiasJ

RubioV

SolanoR

2000 Influence of cytokinins on the expression of phosphate starvation responsive genes in Arabidopsis. Plant J 24 559 567

43. LeBrasseurND

MacIntoshGC

Perez-AmadorMA

SaitohM

GreenPJ

2002 Local and systemic wound-induction of RNase and nuclease activities in Arabidopsis: RNS1 as a marker for a JA-independent systemic signaling pathway. Plant J 29 393 403

44. JeffersonRA

KavanaughTA

BevanMW

1987 GUS fusions: beta-glucuronidase as a sensitive and versatile gene RT fusion marker in higher plants. EMBO J 6 3901 3907

45. UlmasovT

LiuZB

HagenG

GuilfoyleTJ

1995 Composite Structure of Auxin Response Elements. Plant Cell 7 1611 1623

46. Franco-ZorrillaJM

MartínAC

LeyvaA

Paz-AresJ

2005 Interaction between phosphate-starvation, sugar, and cytokinin signaling in Arabidopsis and the roles of cytokinin receptors CRE1/AHK4 and AHK3. Plant Physiol 138 847 857

47. KarthikeyanAS

VaradarajanDK

JainA

HeldMA

CarpitaNC

2007 Phosphate starvation responses are mediated by sugar signaling in Arabidopsis. Planta 225 907 918

48. HammondJP

WhitePJ

2008 Sucrose transport in the phloem: integrating root responses to phosphorus starvation. J Exp Bot 59 93 109

49. CatarechaP

SeguraMD

Franco-ZorrillaJM

Garcia-PonceB

LanzaM

2007 A mutant of the Arabidopsis phosphate transporter PHT1;1 displays enhanced arsenic accumulation. Plant Cell 19 1123 1133

50. LiuTY

ChangCY

ChiouTJ

2009 The long-distance signaling of mineral macronutrients. Curr Opin Plant Biol 12 312 319

51. BatesTR

LynchJP

1996 Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Cell Environ 19 529 538

52. Baena-GonzalezE

RollandF

TheveleinJM

SheenJ

2007 A central integrator of transcription networks in plant stress and energy signalling. Nature 448 938 942

53. SchünmannPH

RichardsonAE

VickersCE

DelhaizeE

2004 Promoter analysis of the barley Pht1;1 phosphate transporter gene identifies regions controlling root expression and responsiveness to phosphate deprivation. Plant Physiology1 36 4205 4214

54. SessionsA

BurkeE

PrestingG

AuxG

McElverJ

2002 A high-throughput Arabidopsis reverse genetics system. Plant Cell 14 2985 2994

55. JohnsonCM

StoutPR

BroyerTC

CarltonAB

1957 Comparative chlorine requirements of different plants species. Plant Soil 8 337 353

56. SwainTR

HillisWE

1959 Phenolic constituents of Prunus domestica. I. Quantitative analysis of phenolic constituents. J Sci Food Agr 10 63 68

57. AmesBN

1966 Assay of inorganic phosphate, total phosphate and phosphatases. Methods Enzymol 8 115 118

58. BechtoldN

EllisJ

PelletierG

1993 In planta Agrobacterium mediated gene transfer by infiltration of adult Arabidopsis thaliana plants. C R Acad Sci Paris Life Sci 316 15 18

59. SambrookJ

FritschEF

ManiatisT

1989 Molecular Cloning: A Laboratory Manual, 2nd ed. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press)

60. MiesfeldR

RusconiS

GodowskiPJ

MalerBA

OkretS

1986 Genetic complementation of a glucocorticoid receptor deficiency by expression of cloned receptor cDNA. Cell 46 369 399

61. Aguilar-MartínezJA

Poza-CarriónC

CubasP

2007 Arabidopsis BRANCHED1 acts as an integrator of branching signals within axillary buds. Plant Cell 19 458 72

62. RomeroI

FuertesA

BenitoMJ

MalpicaJM

LeyvaA

1998 More than 80R2R3-MYB regulatory genes in the genome of Arabidopsis thaliana. Plant J 14 273 284

63. SolanoR

NietoC

Paz-AresJ

1995 MYB.Ph3 transcription factor from Petunia hybrida induces similar DNA-bending/distortions on its two types of binding site. Plant J 8 673 682

64. ChiniA

FonsecaS

FernándezG

AdieB

ChicoJM

2007 The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448 666 671

65. WettenhallJM

SimpsonKM

SatterleyK

SmythGK

2006 affylmGUI: a graphical user interface for linear modeling of single channel microarray data. Bioinformatics 22 897 899

66. IrizarryRA

HobbsB

CollinF

Beazer-BarclayYD

AntonellisKJ

2003 Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4 249 264

67. ReinerA

YekutieliD

BenjaminiY

2003 Identifying differentially expressed genes using false discovery rate controlling procedures. Bioinformatics 19 368 375

68. IidaK

SekiM

SakuraiT

SatouM

AkiyamaK

2005 RARTF: Database and Tools for Complete Sets of Arabidopsis Transcription Factors. DNA Res 12 247 256

69. MorgensternB

DressA

WernerT

1996 Multiple DNA and protein sequence alignment based on segment-to-segment comparison. Proc Natl Acad Sci USA 93 12098 12103

70. DereeperA

GuignonV

BlancG

AudicS

BuffetS

2008 Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36 W465 W469

71. BonkeM

ThitamadeeS

MahonenAP

HauserMT

HelariuttaY

2003 APL regulates vascular tissue identity in Arabidopsis. Nature 426 181 186

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2010 Číslo 9
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

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#