Plant Vascular Cell Division Is Maintained by an Interaction between PXY and Ethylene Signalling

English version České info

The procambium and cambium are meristematic tissues from which vascular tissue is derived. Vascular initials differentiate into phloem towards the outside of the stem and xylem towards the inside. A small peptide derived from CLV-3/ESR1-LIKE 41 (CLE41) is thought to promote cell divisions in vascular meristems by signalling through the PHLOEM INTERCALLATED WITH XYLEM (PXY) receptor kinase. pxy mutants, however, display only small reductions in vascular cell number, suggesting a mechanism exists that allows plants to compensate for the absence of PXY. Consistent with this idea, we identify a large number of genes specifically upregulated in pxy mutants, including several AP2/ERF transcription factors. These transcription factors are required for normal cell division in the cambium and procambium. These same transcription factors are also upregulated by ethylene and in ethylene-overproducing eto1 mutants. eto1 mutants also exhibit an increase in vascular cell division that is dependent upon the function of at least 2 of these ERF genes. Furthermore, blocking ethylene signalling using a variety of ethylene insensitive mutants such as ein2 enhances the cell division defect of pxy. Our results suggest that these factors define a novel pathway that acts in parallel to PXY/CLE41 to regulate cell division in developing vascular tissue. We propose a model whereby vascular cell division is regulated both by PXY signalling and ethylene/ERF signalling. Under normal circumstances, however, PXY signalling acts to repress the ethylene/ERF pathway.

Vyšlo v časopise: Plant Vascular Cell Division Is Maintained by an Interaction between PXY and Ethylene Signalling. PLoS Genet 8(11): e32767. doi:10.1371/journal.pgen.1002997
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002997

Souhrn

Zdroje

1. ChaffeyN, CholewaE, ReganS, SundbergB (2002) Secondary xylem development in Arabidopsis: a model for wood formation. Physiologia Plantarum 114: 594–600.

2. FisherK, TurnerS (2007) PXY, a receptor-like kinase essential for maintaining polarity during plant vascular-tissue development. Current Biology 17: 1061–1066.

3. HirakawaY, ShinoharaH, KondoY, InoueA, NakanomyoI, et al. (2008) Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system. Proceedings of the National Academy of Sciences, USA 105: 15208–15213.

4. ItoY, NakanomyoI, MotoseH, IwamotoK, SawaS, et al. (2006) Dodeca-CLE peptides as suppressors of plant stem cell differentiation. Science 313: 842–845.

5. OelkersK, GoffardN, WeillerG, GresshoffP, MathesiusU, et al. (2008) Bioinformatic analysis of the CLE signaling peptide family. BMC Plant Biology 8: 1.

6. StrabalaTJ, O'DonnellPJ, SmitAM, Ampomah-DwamenaC, MartinEJ, et al. (2006) Gain-of-function phenotypes of many CLAVATA3/ESR genes, including four new family members, correlate with tandem variations in the conserved CLAVATA3/ESR domain. Plant Physiology 140: 1331–1344.

7. EtchellsJP, TurnerSR (2010) The PXY-CLE41 receptor ligand pair defines a multifunctional pathway that controls the rate and orientation of vascular cell division. Development 137: 767–774.

8. WhitfordR, FernandezA, De GroodtR, OrtegaE, HilsonP (2008) Plant CLE peptides from two distinct functional classes synergistically induce division of vascular cells. Proceedings of the National Academy of Sciences USA 105: 18625–18630.

9. HirakawaY, KondoY, FukudaH (2010) TDIF Peptide Signaling Regulates Vascular Stem Cell Proliferation via the WOX4 Homeobox Gene in Arabidopsis. Plant Cell 22: 2618–2629.

10. SuerS, AgustiJ, SanchezP, SchwarzM, GrebT (2011) WOX4 Imparts Auxin Responsiveness to Cambium Cells in Arabidopsis. The Plant Cell 23: 3247–3259.

11. JiJ, StrableJ, ShimizuR, KoenigD, SinhaN, et al. (2010) WOX4 Promotes Procambial Development. Plant Physiology 152: 1346–1356.

12. BrownKM, LeopoldAC (1973) Ethylene and the Regulation of Growth in Pine. Canadian Journal of Forest Research 3: 142–145.

13. LeopoldAC, BrownKM, EmersonFH (1972) Ethylene in the Wood of Stressed Trees. Horticultural Science 7: 175.

14. SavidgeRA (1988) Auxin and ethylene regulation of diameter growth in trees. Tree Physiology 4: 401–414.

15. LoveJ, BjörklundS, VahalaJ, HertzbergM, KangasjärviJ, et al. (2009) Ethylene is an endogenous stimulator of cell division in the cambial meristem of Populus. Proceedings of the National Academy of Sciences, USA 106: 5984–5989.

16. NakanoT, SuzukiK, FujimuraT, ShinshiH (2006) Genome-Wide Analysis of the ERF Gene Family in Arabidopsis and Rice. Plant Physiology 140: 411–432.

17. KhandelwalA, ElvitigalaT, GhoshB, QuatranoRS (2008) Arabidopsis Transcriptome Reveals Control Circuits Regulating Redox Homeostasis and the Role of an AP2 Transcription Factor. Plant Physiology 148: 2050–2058.

18. PauwelsL, MorreelK, De WitteE, LammertynF, Van MontaguM, et al. (2008) Mapping methyl jasmonate-mediated transcriptional reprogramming of metabolism and cell cycle progression in cultured Arabidopsis cells. Proceedings of the National Academy of Sciences USA 105: 1380–1385.

19. SiboutR, PlantegenetS, HardtkeCS (2008) Flowering as a Condition for Xylem Expansion in Arabidopsis Hypocotyl and Root. Current Biology 18: 458–463.

20. RagniL, NieminenK, Pacheco-VillalobosD, SiboutR, SchwechheimerC, et al. (2011) Mobile Gibberellin Directly Stimulates Arabidopsis Hypocotyl Xylem Expansion. The Plant Cell Online 23: 1322–1336.

21. OyamaT, ShimuraY, OkadaK (1997) The Arabidopsis HY5 gene encodes a bZIP protein that regulates stimulus-induced development of root and hypocotyl. Genes & Development 11: 2983–2995.

22. FujimotoSY, OhtaM, UsuiA, ShinshiH, Ohme-TakagiM (2000) Arabidopsis Ethylene-Responsive Element Binding Factors Act as Transcriptional Activators or Repressors of GCC Box-Mediated Gene Expression. The Plant Cell 12: 393–404.

23. SolanoR, StepanovaA, ChaoQ, EckerJR (1998) Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. Genes & Development 12: 3703–3714.

24. AlonsoJM, StepanovaAN, LeisseTJ, KimCJ, ChenH, et al. (2003) Genome-Wide Insertional Mutagenesis of Arabidopsis thaliana. Science 301: 653–657.

25. NemhauserJL, HongF, ChoryJ (2006) Different Plant Hormones Regulate Similar Processes through Largely Nonoverlapping Transcriptional Responses. Cell 126: 467–475.

26. GuzmanP, EckerJR (1990) Exploiting the Triple Response of Arabidopsis To Identify Ethylene-Related Mutants. The Plant Cell 2: 513–523.

27. AlonsoJM, HirayamaT, RomanG, NourizadehS, EckerJR (1999) EIN2, a Bifunctional Transducer of Ethylene and Stress Responses in Arabidopsis. Science 284: 2148–2152.

28. KieberJJ, RothenbergM, RomanG, FeldmannKA, EckerJR (1993) CTR1, a negative regulator of the ethylene response pathway in arabidopsis, encodes a member of the Raf family of protein kinases. Cell 72: 427–441.

29. BleeckerAB, EstelleMA, SomervilleC, KendeH (1988) Insensitivity to Ethylene Conferred by a Dominant Mutation in Arabidopsis thaliana. Science 241: 1086–1089.

30. PotuschakT, VansiriA, BinderBM, LechnerE, VierstraRD, et al. (2006) The Exoribonuclease XRN4 Is a Component of the Ethylene Response Pathway in Arabidopsis. Plant Cell 18: 3047–3057.

31. OlmedoG, GuoH, GregoryBD, NourizadehSD, Aguilar-HenoninL, et al. (2006) ETHYLENE-INSENSITIVE5 encodes a 5′→3′ exoribonuclease required for regulation of the EIN3-targeting F-box proteins EBF1/2. Proceedings of the National Academy of Sciences, USA 103: 13286–13293.

32. EckerJR (1995) The ethylene signal transduction pathway in plants. Science 268: 667–675.

33. VogelJP, WoesteKE, TheologisA, KieberJJ (1998) Recessive and dominant mutations in the ethylene biosynthetic gene ACS5 of Arabidopsis confer cytokinin insensitivity and ethylene overproduction, respectively. Proceedings of the National Academy of Sciences USA 95: 4766–4771.

34. 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. The Plant Cell 15: 545–559.

35. YangSF, HoffmanNE (1984) Ethylene biosynthesis and its regulation in higher plants. Annu Rev Plant Physiol Plant Mol Biol 35: 155–189.

36. Ortega-MartínezO, PernasM, CarolRJ, DolanL (2007) Ethylene Modulates Stem Cell Division in the Arabidopsis thaliana Root. Science 317: 507–510.

37. DietzK-J, VogelM, ViehhauserA (2010) AP2/EREBP transcription factors are part of gene regulatory networks and integrate metabolic, hormonal and environmental signals in stress acclimation and retrograde signalling. Protoplasma 245: 3–14.

38. GuttersonN, ReuberTL (2004) Regulation of disease resistance pathways by AP2/ERF transcription factors. Current Opinion in Plant Biology 7: 465–471.

39. SehrEM, AgustiJ, LehnerR, FarmerEE, SchwarzM, et al. (2010) Analysis of secondary growth in the Arabidopsis shoot reveals a positive role of jasmonate signalling in cambium formation. The Plant Journal 63: 811–822.

40. LorenzoO, PiquerasR, Sanchez-SerranoJJ, SolanoR (2003) ETHYLENE RESPONSE FACTOR1 Integrates Signals from Ethylene and Jasmonate Pathways in Plant Defense. The Plant Cell 15: 165–178.

41. PauwelsL, InzéD, GoossensA (2009) Jasmonate-inducible gene: what does it mean? Trends in Plant Science 14: 87–91.

42. PandeySP, RoccaroM, SchönM, LogemannE, SomssichIE (2010) Transcriptional reprogramming regulated by WRKY18 and WRKY40 facilitates powdery mildew infection of Arabidopsis. The Plant Journal 64: 912–923.

43. KerchevPI, PellnyTK, VivancosPD, KiddleG, HeddenP, et al. (2011) The Transcription Factor ABI4 Is Required for the Ascorbic Acid–Dependent Regulation of Growth and Regulation of Jasmonate-Dependent Defense Signaling Pathways in Arabidopsis. The Plant Cell Online 23: 3319–3334.

44. Cano-DelgadoA, YinYH, YuC, VafeadosD, Mora-GarciaS, et al. (2004) BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development 131: 5341–5351.

45. PineauP, FreydierA, RanochaP, JauneauA, TurnerS, et al. (2005) hca: an Arabidopsis mutant exhibiting unusual cambial activity and altered vascular patterning. Plant Journal 44: 271–289.

46. MahonenAP, BishoppA, HiguchiM, NieminenKM, KinoshitaK, et al. (2006) Cytokinin Signaling and Its Inhibitor AHP6 Regulate Cell Fate During Vascular Development. Science 311: 94–98.

47. HejatkoJ, RyuH, KimG-T, DobesovaR, ChoiS, et al. (2009) The Histidine Kinases CYTOKININ-INDEPENDENT1 and ARABIDOPSIS HISTIDINE KINASE2 and 3 Regulate Vascular Tissue Development in Arabidopsis Shoots. The Plant Cell 21: 2008–2021.

48. AgustiJ, HeroldS, SchwarzM, SanchezP, LjungK, et al. (2011) Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants. Proceedings of the National Academy of Sciences

49. MattssonJ, SungZR, BerlethT (1999) Responses of plant vascular systems to auxin transport inhibition. Development 126: 2979–2991.

50. GälweilerL, GuanC, MüllerA, WismanE, MendgenK, et al. (1998) Regulation of Polar Auxin Transport by AtPIN1 in Arabidopsis Vascular Tissue. Science 282: 2226–2230.

51. SanchezP, NehlinL, GrebT (2012) From thin to thick: major transitions during stem development. Trends in plant science 17: 113–121.

52. FletcherLC, BrandU, RunningMP, SimonR, MeyerowitzEM (1999) Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283: 1911–1914.

53. ClarkSE, WilliamsRW, MeyerowitzEM (1997) The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89: 575–585.

54. KondoT, SawaS, KinoshitaA, MizunoS, KakimotoT, et al. (2006) A plant peptide encoded by CLV3 identified by in situ MALDI-TOF MS analysis. Science 313: 845–848.

55. OgawaM, ShinoharaH, SakagamiY, MatsubayashiY (2008) Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319: 294–294.

56. BrandU, FletcherJC, HobeM, MeyerowitzEM, SimonR (2000) Dependence of stem cell fate in Arabidopsis an a feedback loop regulated by CLV3 activity. Science 289: 617–619.

57. SchoofH, LenhardM, HaeckerA, MayerKFX, JurgensG, et al. (2000) The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100: 635–644.

58. GordonSP, ChickarmaneVS, OhnoC, MeyerowitzEM (2009) Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem. Proceedings of the National Academy of Sciences, USA 106: 16529–16534.

59. SwarbreckD, WilksC, LameschP, BerardiniTZ, Garcia-HernandezM, et al. (2008) The Arabidopsis Information Resource (TAIR): gene structure and function annotation. Nucl Acids Res 36: D1009–1014.

60. TsangDL, EdmondC, HarringtonJL, NühseTS (2011) Cell Wall Integrity Controls Root Elongation via a General 1-Aminocyclopropane-1-Carboxylic Acid-Dependent, Ethylene-Independent Pathway. Plant Physiology 156: 596–604.

61. LiC, WongWH (2001) Model-based analysis of oligonucleotide arrays: Expression index computation and outlier detection. Proceedings of the National Academy of Sciences, USA 98: 31–36.

62. BolstadBM, IrizarryRA, AstrandM, SpeedTP (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19: 185–193.

63. SmythGK (2004) Linear Models and Empirical Bayes Methods for Assessing Differential Expression in Microarray Experiments. Statistical Applications in Genetics and Molecular Biology 3: Article 3.

64. HardstedtM, FinneganCP, KirchhofN, HylandKA, WijkstromM, et al. (2005) Post-transplant upregulation of chemokine messenger RNA in non-human primate recipients of intraportal pig islet xenografts. Xenotransplantation 12: 293–302.

65. LongJA, MoanEI, MedfordJI, BartonMK (1996) A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379: 66–69.

66. PinonV, EtchellsJP, RossignolP, CollierSA, ArroyoJM, et al. (2008) Three PIGGYBACK genes that specifically influence leaf patterning encode ribosomal proteins. Development 135: 1315–1324.