#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Dual-Level Regulation of ACC Synthase Activity by MPK3/MPK6 Cascade and Its Downstream WRKY Transcription Factor during Ethylene Induction in Arabidopsis


Plants under pathogen attack produce high levels of ethylene, which plays important roles in plant immunity. Previously, we reported the involvement of ACS2 and ACS6, two Type I ACS isoforms, in Botrytis cinerea–induced ethylene biosynthesis and their regulation at the protein stability level by MPK3 and MPK6, two Arabidopsis pathogen-responsive mitogen-activated protein kinases (MAPKs). The residual ethylene induction in the acs2/acs6 double mutant suggests the involvement of additional ACS isoforms. It is also known that a subset of ACS genes, including ACS6, is transcriptionally induced in plants under stress or pathogen attack. However, the importance of ACS gene activation and the regulatory mechanism(s) are not clear. In this report, we demonstrate using genetic analysis that ACS7 and ACS11, two Type III ACS isoforms, and ACS8, a Type II ACS isoform, also contribute to the B. cinerea–induced ethylene production. In addition to post-translational regulation, transcriptional activation of the ACS genes also plays a critical role in sustaining high levels of ethylene induction. Interestingly, MPK3 and MPK6 not only control the stability of ACS2 and ACS6 proteins via direct protein phosphorylation but also regulate the expression of ACS2 and ACS6 genes. WRKY33, another MPK3/MPK6 substrate, is involved in the MPK3/MPK6-induced ACS2/ACS6 gene expression based on genetic analyses. Furthermore, chromatin-immunoprecipitation assay reveals the direct binding of WRKY33 to the W-boxes in the promoters of ACS2 and ACS6 genes in vivo, suggesting that WRKY33 is directly involved in the activation of ACS2 and ACS6 expression downstream of MPK3/MPK6 cascade in response to pathogen invasion. Regulation of ACS activity by MPK3/MPK6 at both transcriptional and protein stability levels plays a key role in determining the kinetics and magnitude of ethylene induction.


Vyšlo v časopise: Dual-Level Regulation of ACC Synthase Activity by MPK3/MPK6 Cascade and Its Downstream WRKY Transcription Factor during Ethylene Induction in Arabidopsis. PLoS Genet 8(6): e32767. doi:10.1371/journal.pgen.1002767
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002767

Souhrn

Plants under pathogen attack produce high levels of ethylene, which plays important roles in plant immunity. Previously, we reported the involvement of ACS2 and ACS6, two Type I ACS isoforms, in Botrytis cinerea–induced ethylene biosynthesis and their regulation at the protein stability level by MPK3 and MPK6, two Arabidopsis pathogen-responsive mitogen-activated protein kinases (MAPKs). The residual ethylene induction in the acs2/acs6 double mutant suggests the involvement of additional ACS isoforms. It is also known that a subset of ACS genes, including ACS6, is transcriptionally induced in plants under stress or pathogen attack. However, the importance of ACS gene activation and the regulatory mechanism(s) are not clear. In this report, we demonstrate using genetic analysis that ACS7 and ACS11, two Type III ACS isoforms, and ACS8, a Type II ACS isoform, also contribute to the B. cinerea–induced ethylene production. In addition to post-translational regulation, transcriptional activation of the ACS genes also plays a critical role in sustaining high levels of ethylene induction. Interestingly, MPK3 and MPK6 not only control the stability of ACS2 and ACS6 proteins via direct protein phosphorylation but also regulate the expression of ACS2 and ACS6 genes. WRKY33, another MPK3/MPK6 substrate, is involved in the MPK3/MPK6-induced ACS2/ACS6 gene expression based on genetic analyses. Furthermore, chromatin-immunoprecipitation assay reveals the direct binding of WRKY33 to the W-boxes in the promoters of ACS2 and ACS6 genes in vivo, suggesting that WRKY33 is directly involved in the activation of ACS2 and ACS6 expression downstream of MPK3/MPK6 cascade in response to pathogen invasion. Regulation of ACS activity by MPK3/MPK6 at both transcriptional and protein stability levels plays a key role in determining the kinetics and magnitude of ethylene induction.


Zdroje

1. WangKL-CLiHEckerJR 2002 Ethylene biosynthesis and signaling networks. Plant Cell 14 S131 S151

2. SchallerGEKieberJJ 2002 Ethylene. SomervilleCRMeyerowitzEM The Arabidopsis Book Rockville, MD American Society of Plant Biologists 1 19 doi/10.1199/tab.0071, http://www.aspb.org.publications/arabidopsis/

3. KleeHJ 2004 Ethylene Signal Transduction. Moving beyond Arabidopsis. Plant Physiol 135 660 667

4. ZarembinskiTITheologisA 1994 Ethylene biosynthesis and action: a case of conservation. Plant Mol Biol 26 1579 1597

5. KendrickMDChangC 2008 Ethylene signaling: new levels of complexity and regulation. Curr Opin Plant Biol 11 479 485

6. BroekaertWFDelaureSLDe BolleMFCCammueBPA 2006 The role of ethylene in host-pathogen interactions. Ann Rev Phytopathol 44 393 416

7. van LoonLCGeraatsBPJLinthorstHJM 2006 Ethylene as a modulator of disease resistance in plants. Trends Plant Sci 11 184 191

8. ChangCBleeckerAB 2004 Ethylene Biology. More Than a Gas. Plant Physiol 136 2895 2899

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

10. KendeH 2001 Hormone response mutants: a plethora of surprises. Plant Physiol 125 81 84

11. AbelesFBMorganPWSaltveitMEJ 1992 Ethylene in plant biology San Diego Academic Press

12. YangSFHoffmanNE 1984 Ethylene biosynthesis and its regulation in higher plants. Ann Rev Plant Biol 35 155 189

13. SatoTTheologisA 1989 Cloning the mRNA encoding 1-aminocyclopropane-1-carboxylate synthase, the key enzyme of ethylene synthesis in plants. Proc Natl Acad Sci USA 86 6621 6624

14. ChaeHSKieberJJ 2005 Eto Brute? Role of ACS turnover in regulating ethylene biosynthesis. Trends Plant Sci 10 291 296

15. YoshidaHNagataMSaitoKWangKEckerJ 2005 Arabidopsis ETO1 specifically interacts with and negatively regulates type 2 1-aminocyclopropane-1-carboxylate synthases. BMC Plant Biol 5 14

16. LiuYZhangS 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

17. KamiyoshiharaYIwataMFukayaTTatsukiMMoriH 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

18. YamagamiTTsuchisakaAYamadaKHaddonWFHardenLA 2003 Biochemical diversity among the 1-amino-cyclopropane-1-carboxylate synthase isozymes encoded by the Arabidopsis gene family. J Biol Chem 278 49102 49112

19. TsuchisakaATheologisA 2004 Heterodimeric interactions among the 1-amino-cyclopropane-1-carboxylate synthase polypeptides encoded by the Arabidopsis gene family. Proc Natl Acad Sci USA 101 2275 2280

20. TsuchisakaATheologisA 2004 Unique and overlapping expression patterns among the Arabidopsis 1-amino-cyclopropane-1-carboxylate synthase gene family members. Plant Physiol 136 2982 3000

21. IchimuraKShinozakiKTenaGSheenJHenryY 2002 Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci 7 301 308

22. WidmannCGibsonSJarpeMBJohnsonGL 1999 Mitogen-activated protein kinase: Conservation of a three-kinase module from yeast to human. Physiol Rev 79 143 180

23. TenaGAsaiTChiuW-LSheenJ 2001 Plant mitogen-activated protein kinase signaling cascades. Curr Opin Plant Biol 4 392 400

24. ZhangSKlessigDF 2001 MAPK cascades in plant defense signaling. Trends Plant Sci 6 520 527

25. JonakCÖkrészLBögreLHirtH 2002 Complexity, crosstalk and integration of plant MAP kinase signalling. Curr Opin Plant Biol 5 415 424

26. RodriguezMCSPetersenMMundyJ 2010 Mitogen-activated protein kinase signaling in plants. Ann Rev Plant Biol 61 621 649

27. KimCYLiuYThorneETYangHFukushigH 2003 Activation of a stress-responsive mitogen-activated protein kinase cascade induces the biosynthesis of ethylene in plants. Plant Cell 15 2707 2718

28. HanLLiGJYangKYMaoGWangR 2010 Mitogen-activated protein kinase 3 and 6 regulate Botrytis cinerea-induced ethylene production in Arabidopsis. Plant J 64 114 127

29. JooSLiuYLuethAZhangS 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

30. SkottkeKRYoonGMKieberJJDeLongA 2011 Protein phosphatase 2A controls ethylene biosynthesis by differentially regulating the turnover of ACC Ssynthase isoforms. PLoS Genet 7 e1001370 doi:10.1371/journal.pgen.1001370

31. YoshidaHWangKLCChangC-MMoriKUchidaE 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

32. ChaeHSFaureFKieberJJ 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

33. WangKL-CYoshidaHLurinCEckerJR 2004 Regulation of ethylene gas biosynthesis by the Arabidopsis ETO1 protein. Nature 428 945 950

34. MaoGMengXLiuYZhengZChenZ 2011 Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. Plant Cell 23 1639 1653

35. TsuchisakaAYuGJinHAlonsoJMEckerJR 2009 A combinatorial interplay among the 1-aminocyclopropane-1-carboxylate isoforms regulates ethylene biosynthesis in Arabidopsis thaliana. Genetics 183 979 1003

36. ArtecaJMArtecaRN 1999 A multi-responsive gene encoding 1-aminocyclopropane-1-carboxylate synthase (ACS6) in mature Arabidopsis leaves. Plant Mol Biol 39 209 219

37. PengH-PLinT-YWangN-NShihM-C 2005 Differential expression of genes encoding 1-aminocyclopropane-1-carboxylate synthase in Arabidopsis during hypoxia. Plant Mol Biol 58 15 25

38. RenDLiuYYangK-YHanLMaoG 2008 A fungal-responsive MAPK cascade regulates phytoalexin biosynthesis in Arabidopsis. Proc Natl Acad Sci USA 105 5638 5643

39. WangHNgwenyamaNLiuYWalkerJCZhangS 2007 Stomatal development and patterning are regulated by environmentally responsive MAP kinases in Arabidopsis. Plant Cell 19 63 73

40. DongJChenCChenZ 2003 Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant Mol Biol 51 21 37

41. EulgemTSomssichIE 2007 Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10 366 371

42. VahalaJSchlagnhauferCDPellEJ 1998 Induction of an ACC synthase cDNA by ozone in light-grown Arabidopsis thaliana leaves. Physiol Plant 103 45 50

43. CampbellADLabavitchJM 1991 Induction and regulation of ethylene biosynthesis by pectic oligomers in cultured pear cells. Plant Physiol 97 699 705

44. SpanuPGrosskopfDGFelixGBollerT 1994 The apparent turnover of 1-aminocyclopropane-1-carboxylate synthase in tomato cells is regulated by protein phosphorylation and dephosphorylation. Plant Physiol 106 529 535

45. FelixGGrosskopfDGRegenassMBollerT 1991 Rapid changes of protein phosphorylation are involved in transduction of the elicitor signal in plant cells. Proc Natl Acad Sci USA 88 8831 8834

46. WuJHettenhausenCMeldauSBaldwinIT 2007 Herbivory rapidly activates MAPK signaling in attacked and unattacked leaf regions but not between leaves of Nicotiana attenuata. Plant Cell 19 1096 1122

47. ZhangSKlessigDF 1998 The tobacco wounding-activated MAP kinase is encoded by SIPK. Proc Natl Acad Sci USA 95 7225 7230

48. KimCYZhangS 2004 Activation of a mitogen-activated protein kinase cascade induces WRKY family of transcription factors and defense genes in tobacco. Plant J 38 142 151

49. YangK-YLiuYZhangS 2001 Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco. Proc Natl Acad Sci USA 98 741 746

50. BethkeGUnthanTUhrigJFPoschlYGustAA 2009 Flg22 regulates the release of an ethylene response factor substrate from MAP kinase 6 in Arabidopsis thaliana via ethylene signaling. Proc Natl Acad Sci USA 106 8067 8072

51. QiuJ-LFiilBKPetersenKNielsenHBBotangaCJ 2008 Arabidopsis MAP kinase 4 regulates gene expression through transcription factor release in the nucleus. EMBO J 27 2214 2221

52. BlumeBNürnbergerTNassNScheelD 2000 Receptor-mediated increase in cytoplasmic free calcium required for activation of pathogen defense in parsley. Plant Cell 12 1425 1440

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

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

55. KaufmannKMuinoJMOsterasMFarinelliLKrajewskiP 2010 Chromatin immunoprecipitation (ChIP) of plant transcription factors followed by sequencing (ChIP-SEQ) or hybridization to whole genome arrays (ChIP-CHIP). Nat Protocols 5 457 472

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2012 Číslo 6
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#