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Protein Phosphatase 2A Controls Ethylene Biosynthesis by Differentially Regulating the Turnover of ACC Synthase Isoforms


The gaseous hormone ethylene is one of the master regulators of development and physiology throughout the plant life cycle. Ethylene biosynthesis is stringently regulated to permit maintenance of low levels during most phases of vegetative growth but to allow for rapid peaks of high production at developmental transitions and under stress conditions. In most tissues ethylene is a negative regulator of cell expansion, thus low basal levels of ethylene biosynthesis in dark-grown seedlings are critical for optimal cell expansion during early seedling development. The committed steps in ethylene biosynthesis are performed by the enzymes 1-aminocyclopropane 1-carboxylate synthase (ACS) and 1-aminocyclopropane 1-carboxylate oxidase (ACO). The abundance of different ACS enzymes is tightly regulated both by transcriptional control and by post-translational modifications and proteasome-mediated degradation. Here we show that specific ACS isozymes are targets for regulation by protein phosphatase 2A (PP2A) during Arabidopsis thaliana seedling growth and that reduced PP2A function causes increased ACS activity in the roots curl in 1-N-naphthylphthalamic acid 1 (rcn1) mutant. Genetic analysis reveals that ethylene overproduction in PP2A-deficient plants requires ACS2 and ACS6, genes that encode ACS proteins known to be stabilized by phosphorylation, and proteolytic turnover of the ACS6 protein is retarded when PP2A activity is reduced. We find that PP2A and ACS6 proteins associate in seedlings and that RCN1-containing PP2A complexes specifically dephosphorylate a C-terminal ACS6 phosphopeptide. These results suggest that PP2A-dependent destabilization requires RCN1-dependent dephosphorylation of the ACS6 C-terminus. Surprisingly, rcn1 plants exhibit decreased accumulation of the ACS5 protein, suggesting that a regulatory phosphorylation event leads to ACS5 destabilization. Our data provide new insight into the circuitry that ensures dynamic control of ethylene synthesis during plant development, showing that PP2A mediates a finely tuned regulation of overall ethylene production by differentially affecting the stability of specific classes of ACS enzymes.


Vyšlo v časopise: Protein Phosphatase 2A Controls Ethylene Biosynthesis by Differentially Regulating the Turnover of ACC Synthase Isoforms. PLoS Genet 7(4): e32767. doi:10.1371/journal.pgen.1001370
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1001370

Souhrn

The gaseous hormone ethylene is one of the master regulators of development and physiology throughout the plant life cycle. Ethylene biosynthesis is stringently regulated to permit maintenance of low levels during most phases of vegetative growth but to allow for rapid peaks of high production at developmental transitions and under stress conditions. In most tissues ethylene is a negative regulator of cell expansion, thus low basal levels of ethylene biosynthesis in dark-grown seedlings are critical for optimal cell expansion during early seedling development. The committed steps in ethylene biosynthesis are performed by the enzymes 1-aminocyclopropane 1-carboxylate synthase (ACS) and 1-aminocyclopropane 1-carboxylate oxidase (ACO). The abundance of different ACS enzymes is tightly regulated both by transcriptional control and by post-translational modifications and proteasome-mediated degradation. Here we show that specific ACS isozymes are targets for regulation by protein phosphatase 2A (PP2A) during Arabidopsis thaliana seedling growth and that reduced PP2A function causes increased ACS activity in the roots curl in 1-N-naphthylphthalamic acid 1 (rcn1) mutant. Genetic analysis reveals that ethylene overproduction in PP2A-deficient plants requires ACS2 and ACS6, genes that encode ACS proteins known to be stabilized by phosphorylation, and proteolytic turnover of the ACS6 protein is retarded when PP2A activity is reduced. We find that PP2A and ACS6 proteins associate in seedlings and that RCN1-containing PP2A complexes specifically dephosphorylate a C-terminal ACS6 phosphopeptide. These results suggest that PP2A-dependent destabilization requires RCN1-dependent dephosphorylation of the ACS6 C-terminus. Surprisingly, rcn1 plants exhibit decreased accumulation of the ACS5 protein, suggesting that a regulatory phosphorylation event leads to ACS5 destabilization. Our data provide new insight into the circuitry that ensures dynamic control of ethylene synthesis during plant development, showing that PP2A mediates a finely tuned regulation of overall ethylene production by differentially affecting the stability of specific classes of ACS enzymes.


Zdroje

1. AbelesFB

MorganPW

SaltveitMEJ

1992

Ethylene in Plant Biology

San Diego, CA

Aademic Press Inc

2. ChaeHS

KieberJJ

2005

Eto Brute? Role of ACS turnover in regulating ethylene biosynthesis.

Trends Plant Sci

10

291

296

3. De PaepeA

Van der StraetenD

2005

Ethylene biosynthesis and signaling: an overview.

Vitam Horm

72

399

430

4. WangKL

LiH

EckerJR

2002

Ethylene biosynthesis and signaling networks.

Plant Cell

14

S131

S151

5. KendeH

1993

Ethylene biosynthesis.

Annu Rev Plant Physiol Plant Mol Biol

44

283

307

6. YangSF

HoffmanNE

1984

Ethylene biosynthesis and its regulation in higher plants.

Annu Rev Plant Physiol

35

155

189

7. ZarembinskiTI

TheologisA

1994

Ethylene biosynthesis and action: a case of conservation.

Plant Mol Biol

26

1579

1597

8. ChaeHS

FaureF

KieberJJ

2003

The eto1, eto2, and eto3 mutations and cytokinin treatment increase ethylene biosynthesis in Arabidopsis by increasing the stability of ACS protein.

Plant Cell

15

545

559

9. ChristiansMJ

GingerichDJ

HansenM

BinderBM

KieberJJ

2009

The BTB ubiquitin ligases ETO1, EOL1 and EOL2 act collectively to regulate ethylene biosynthesis in Arabidopsis by controlling type-2 ACC synthase levels.

Plant J

57

332

345

10. JooS

LiuY

LuethA

ZhangS

2008

MAPK phosphorylation-induced stabilization of ACS6 protein is mediated by the non-catalytic C-terminal domain, which also contains the cis-determinant for rapid degradation by the 26S proteasome pathway.

Plant J

54

129

140

11. Hernández SebastiàC

HardinSC

ClouseSD

KieberJJ

HuberSC

2004

Identification of a new motif for CDPK phosphorylation in vitro that suggests ACC synthase may be a CDPK substrate.

Arch Biochem Biophys

428

81

91

12. KamiyoshiharaY

IwataM

FukayaT

TatsukiM

MoriH

2010

Turnover of LeACS2, a wound-inducible 1-aminocyclopropane-1-carboxylic acid synthase in tomato, is regulated by phosphorylation/dephosphorylation.

Plant J

64

140

150

13. LiuY

ZhangS

2004

Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis.

Plant Cell

16

3386

3399

14. HanL

LiGJ

YangKY

MaoG

WangR

2010

Mitogen-activated protein kinase 3 and 6 regulate Botrytis cinerea-induced ethylene production in Arabidopsis.

Plant J

64

114

127

15. TatsukiM

MoriH

2001

Phosphorylation of tomato 1-aminocyclopropane-1-carboxylic acid synthase, LE-ACS2, at the C-terminal region.

J Biol Chem

276

28051

28057

16. WangKL

YoshidaH

LurinC

EckerJR

2004

Regulation of ethylene gas biosynthesis by the Arabidopsis ETO1 protein.

Nature

428

945

950

17. YoshidaH

NagataM

SaitoK

WangKL

EckerJR

2005

Arabidopsis ETO1 specifically interacts with and negatively regulates type 2 1-aminocyclopropane-1-carboxylate synthases.

BMC Plant Biol

5

14

18. YoshidaH

WangKL

ChangCM

MoriK

UchidaE

2006

The ACC synthase TOE sequence is required for interaction with ETO1 family proteins and destabilization of target proteins.

Plant Mol Biol

62

427

437

19. SchweighoferA

KazanaviciuteV

ScheiklE

TeigeM

DocziR

2007

The PP2C-type phosphatase AP2C1, which negatively regulates MPK4 and MPK6, modulates innate immunity, jasmonic acid, and ethylene levels in Arabidopsis.

Plant Cell

19

2213

2224

20. LarsenPB

ChangC

2001

The Arabidopsis eer1 mutant has enhanced ethylene responses in the hypocotyl and stem.

Plant Physiol

125

1061

1073

21. BlakesleeJJ

ZhouHW

HeathJT

SkottkeKR

BarriosJA

2008

Specificity of RCN1-mediated protein phosphatase 2A regulation in meristem organization and stress response in roots.

Plant Physiol

53

539

553

22. MudayGK

BradySR

ArguesoC

DeruèreJ

KieberJJ

2006

RCN1-regulated phosphatase activity and EIN2 modulate hypocotyl gravitropism by a mechanism that does not require ethylene signaling.

Plant Physiol

141

1617

1629

23. DeruèreJ

JacksonK

GarbersC

SöllD

DeLongA

1999

The RCN1-encoded A subunit of protein phosphatase 2A increases phosphatase activity in vivo.

Plant J

20

389

399

24. GarbersC

DeLongA

DeruèreJ

BernasconiP

SöllD

1996

A mutation in protein phosphatase 2A regulatory subunit A affects auxin transport in Arabidopsis.

EMBO J

15

2115

2124

25. LarsenPB

CancelJD

2003

Enhanced ethylene responsiveness in the Arabidopsis eer1 mutant results from a loss-of-function mutation in the protein phosphatase 2A A regulatory subunit, RCN1.

Plant J

34

709

718

26. ZhouHW

NussbaumerC

ChaoY

DeLongA

2004

Disparate roles for the regulatory A subunit isoforms in Arabidopsis protein phosphatase 2A.

Plant Cell

16

709

722

27. TangW

YuanM

WangR

YangY

WangC

2011

PP2A activates brassinosteroid-responsive gene expression and plant growth by dephosphorylating BZR1.

Nature Cell Biology

13

124

131

28. TsuchisakaA

TheologisA

2004

Unique and overlapping expression patterns among the Arabidopsis 1-amino-cyclopropane-1-carboxylate synthase gene family members.

Plant Physiol

136

2982

3000

29. GuoH

EckerJR

2004

The ethylene signaling pathway: new insights.

Curr Opin Plant Biol

7

40

49

30. VogelJP

WoesteKE

TheologisA

KieberJJ

1998

Recessive and dominant mutations in the ethylene biosynthetic gene ACS5 of Arabidopsis confer cytokinin insensitivity and ethylene overproduction, respectively.

Proc Natl Acad Sci U S A

95

4766

4771

31. ChangIF

CurranA

WoolseyR

QuiliciD

CushmanJC

2009

Proteomic profiling of tandem affinity purified 14-3-3 protein complexes in Arabidopsis thaliana.

Proteomics

9

2967

2985

32. TsuchisakaA

YuG

JinH

AlonsoJM

EckerJR

2009

A combinatorial interplay among the 1-aminocyclopropane-1-carboxylate isoforms regulates ethylene biosynthesis in Arabidopsis thaliana.

Genetics

183

979

1003

33. KimJH

KimWT

KangBG

YangSF

1997

Induction of 1-aminocyclopropane-1-carboxylate oxidase mRNA by ethylene in mung bean hypocotyls: involvement of both protein phosphorylation and dephosphorylation in ethylene signaling.

Plant J

11

399

405

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


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