Home LiteratureArticle Details
PMID: 19897606 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

Histone H2A.Z regulates the expression of several classes of phosphate starvation response genes but not as a transcriptional activator.

Plant physiology ·Vol. 152 ·No. 1 ·2010-01-00 ·Pages 217-25

Smith AP, Jain A, Deal RB, Nagarajan VK, Poling MD, Raghothama KG, Meagher RB

Abstract

Phosphate (Pi) availability is a major constraint to plant growth. Consequently, plants have evolved complex adaptations to tolerate low Pi conditions. Numerous genes implicated in these adaptations have been identified, but their chromatin-level regulation has not been investigated. The nuclear actin-related protein ARP6 is conserved among all eukaryotes and is an essential component of the SWR1 chromatin remodeling complex, which regulates transcription via deposition of the H2A.Z histone variant into chromatin. Here, we demonstrate that ARP6 is required for proper H2A.Z deposition at a number of Pi starvation response (PSR) genes in Arabidopsis (Arabidopsis thaliana). The loss of H2A.Z at these target loci results in their derepression in arp6 mutants and correlates with the presence of multiple Pi-starvation-related phenotypes, including shortened primary roots and increases in the number and length of root hairs, as well as increased starch accumulation and phosphatase activity in shoots. Our data suggest a model for chromatin-level control of Pi starvation responses in which ARP6-dependent H2A.Z deposition modulates the transcription of a suite of PSR genes.

MeSH Terms
Arabidopsis/genetics,metabolism Arabidopsis Proteins/genetics,metabolism Gene Expression Regulation, Plant/physiology Histones/genetics,metabolism Illicium Microfilament Proteins/genetics,metabolism Mutation Phosphates Phosphoric Monoester Hydrolases/metabolism Plant Roots/growth & development,metabolism Plant Shoots/growth & development,metabolism Seedlings
Chemicals
ARP6 protein, Arabidopsis Arabidopsis Proteins Histones Microfilament Proteins Phosphates Phosphoric Monoester Hydrolases
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Smith Aaron P
Department of Genetics, University of Georgia, Fred C. Davison Life Sciences Complex, Athens, Georgia 30602, USA.
Jain Ajay
Deal Roger B
Nagarajan Vinay K
Poling Michael D
Raghothama Kashchandra G
Meagher Richard B
References (45)
45 references, click to expand
  1. Preferential occupancy of histone variant H2AZ at inactive promoters influences local histone modifications and chromatin remodeling.
    Proc Natl Acad Sci U S A. 2005 Dec 20;102(51):18385-90 PMID: 16344463
  2. OsPTF1, a novel transcription factor involved in tolerance to phosphate starvation in rice.
    Plant Physiol. 2005 Aug;138(4):2087-96 PMID: 16006597
  3. Redundancy of chromatin remodeling pathways for the induction of the yeast PHO5 promoter in vivo.
    J Biol Chem. 2007 Sep 21;282(38):27610-21 PMID: 17631505
  4. Loss of At4 function impacts phosphate distribution between the roots and the shoots during phosphate starvation.
    Plant J. 2006 Mar;45(5):712-26 PMID: 16460506
  5. SUPPRESSOR OF FRIGIDA3 encodes a nuclear ACTIN-RELATED PROTEIN6 required for floral repression in Arabidopsis.
    Plant Cell. 2005 Oct;17(10):2647-60 PMID: 16155178
  6. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method.
    Methods. 2001 Dec;25(4):402-8 PMID: 11846609
  7. Repression of flowering in Arabidopsis requires activation of FLOWERING LOCUS C expression by the histone variant H2A.Z.
    Plant Cell. 2007 Jan;19(1):74-83 PMID: 17220196
  8. A type 5 acid phosphatase gene from Arabidopsis thaliana is induced by phosphate starvation and by some other types of phosphate mobilising/oxidative stress conditions.
    Plant J. 1999 Sep;19(5):579-89 PMID: 10504579
  9. Profiling histone modification patterns in plants using genomic tiling microarrays.
    Nat Methods. 2005 Mar;2(3):213-8 PMID: 16163802
  10. Differential effects of sucrose and auxin on localized phosphate deficiency-induced modulation of different traits of root system architecture in Arabidopsis.
    Plant Physiol. 2007 May;144(1):232-47 PMID: 17369438
  11. A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation.
    Proc Natl Acad Sci U S A. 2005 Aug 16;102(33):11934-9 PMID: 16085708
  12. Changes in gene expression in Arabidopsis shoots during phosphate starvation and the potential for developing smart plants.
    Plant Physiol. 2003 Jun;132(2):578-96 PMID: 12805589
  13. The phosphatase system in Saccharomyces cerevisiae.
    Genes Genet Syst. 1997 Dec;72(6):323-34 PMID: 9544531
  14. Nutrient-regulated antisense and intragenic RNAs modulate a signal transduction pathway in yeast.
    PLoS Biol. 2008 Dec 23;6(12):2817-30 PMID: 19108609
  15. WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis.
    Plant Physiol. 2007 Apr;143(4):1789-801 PMID: 17322336
  16. Purple acid phosphatases of Arabidopsis thaliana. Comparative analysis and differential regulation by phosphate deprivation.
    J Biol Chem. 2002 Aug 2;277(31):27772-81 PMID: 12021284
  17. Histone H2A.Z regulats transcription and is partially redundant with nucleosome remodeling complexes.
    Cell. 2000 Oct 27;103(3):411-22 PMID: 11081628
  18. Isw1 functions in parallel with the NuA4 and Swr1 complexes in stress-induced gene repression.
    Mol Cell Biol. 2006 Aug;26(16):6117-29 PMID: 16880522
  19. Characterization of a sub-family of Arabidopsis genes with the SPX domain reveals their diverse functions in plant tolerance to phosphorus starvation.
    Plant J. 2008 Jun;54(6):965-75 PMID: 18315545
  20. The Arabidopsis plastidic glucose 6-phosphate/phosphate translocator GPT1 is essential for pollen maturation and embryo sac development.
    Plant Cell. 2005 Mar;17(3):760-75 PMID: 15722468
  21. Negative regulation in the expression of a sugar-inducible gene in Arabidopsis thaliana. A recessive mutation causing enhanced expression of a gene for beta-amylase.
    Plant Physiol. 1997 Jun;114(2):575-82 PMID: 9193090
  22. Arabidopsis homologs of components of the SWR1 complex regulate flowering and plant development.
    Development. 2007 May;134(10):1931-41 PMID: 17470967
  23. Reuniting the contrasting functions of H2A.Z.
    Biochem Cell Biol. 2006 Aug;84(4):528-35 PMID: 16936825
  24. The beauty of being a variant: H2A.Z and the SWR1 complex in plants.
    Mol Plant. 2009 Jul;2(4):565-577 PMID: 19825639
  25. Differential cofactor requirements for histone eviction from two nucleosomes at the yeast PHO84 promoter are determined by intrinsic nucleosome stability.
    Mol Cell Biol. 2009 Jun;29(11):2960-81 PMID: 19307305
  26. BHLH32 modulates several biochemical and morphological processes that respond to Pi starvation in Arabidopsis.
    Biochem J. 2007 Jul 1;405(1):191-8 PMID: 17376028
  27. Extracellular secretion of Aspergillus phytase from Arabidopsis roots enables plants to obtain phosphorus from phytate.
    Plant J. 2001 Mar;25(6):641-9 PMID: 11319031
  28. Phosphate starvation induces a determinate developmental program in the roots of Arabidopsis thaliana.
    Plant Cell Physiol. 2005 Jan;46(1):174-84 PMID: 15659445
  29. Regulation of phosphate acquisition in Saccharomyces cerevisiae.
    Curr Genet. 2003 Jul;43(4):225-44 PMID: 12740714
  30. SEF, a new protein required for flowering repression in Arabidopsis, interacts with PIE1 and ARP6.
    Plant Physiol. 2007 Feb;143(2):893-901 PMID: 17142478
  31. Effectors of lysine 4 methylation of histone H3 in Saccharomyces cerevisiae are negative regulators of PHO5 and GAL1-10.
    J Biol Chem. 2004 Aug 6;279(32):33057-62 PMID: 15180994
  32. PHOSPHATE ACQUISITION.
    Annu Rev Plant Physiol Plant Mol Biol. 1999 Jun;50:665-693 PMID: 15012223
  33. Conserved histone variant H2A.Z protects euchromatin from the ectopic spread of silent heterochromatin.
    Cell. 2003 Mar 7;112(5):725-36 PMID: 12628191
  34. Phosphate homeostasis and root development in Arabidopsis are synchronized by the zinc finger transcription factor ZAT6.
    Plant Physiol. 2007 Sep;145(1):147-59 PMID: 17631527
  35. Histone H2A.Z and DNA methylation are mutually antagonistic chromatin marks.
    Nature. 2008 Nov 6;456(7218):125-9 PMID: 18815594
  36. The transcriptional control of plant responses to phosphate limitation.
    J Exp Bot. 2004 Feb;55(396):285-93 PMID: 14718495
  37. Whole-genome expression analysis of snf/swi mutants of Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3364-9 PMID: 10725359
  38. Genetic responses to phosphorus deficiency.
    Ann Bot. 2004 Sep;94(3):323-32 PMID: 15292042
  39. PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants.
    Plant Physiol. 2006 Jul;141(3):988-99 PMID: 16679424
  40. A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae.
    Genes Dev. 2001 Aug 15;15(16):2122-33 PMID: 11511543
  41. Psr1, a nuclear localized protein that regulates phosphorus metabolism in Chlamydomonas.
    Proc Natl Acad Sci U S A. 1999 Dec 21;96(26):15336-41 PMID: 10611385
  42. Histone H2A.Z and homologues of components of the SWR1 complex are required to control immunity in Arabidopsis.
    Plant J. 2008 Feb;53(3):475-87 PMID: 17988222
  43. Variant histone H2A.Z is globally localized to the promoters of inactive yeast genes and regulates nucleosome positioning.
    PLoS Biol. 2005 Dec;3(12):e384 PMID: 16248679
  44. The nuclear actin-related protein ARP6 is a pleiotropic developmental regulator required for the maintenance of FLOWERING LOCUS C expression and repression of flowering in Arabidopsis.
    Plant Cell. 2005 Oct;17(10):2633-46 PMID: 16141450
  45. Histone variant H2A.Z marks the 5' ends of both active and inactive genes in euchromatin.
    Cell. 2005 Oct 21;123(2):233-48 PMID: 16239142
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
1532-2548
Published
2010-01-00
Epub
2009-00-06
Pages
217-25
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC2799358
Subset
IM
Grants
NIGMS NIH HHS · GM 36397-22 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com