The emerging role of reactive oxygen species signaling during lateral root development

Plant Physiology

Volumn 165, Issue 3, 2014, Pages 1105-1119

  Manzano, Concepción ^a   Pallero Baena, Mercedes ^a,b   Casimiro, Ilda ^a,b   De Rybel, Bert ^c,d   Orman Ligeza, Beata ^c,e   Van Isterdael, Gert ^c,d   Beeckman, Tom ^c,d   Draye, Xavier ^e   Casero, Pedro ^c   del Pozo, Juan C ^a  

^a ETSI MontesTechnical University of Madrid   (Spain)

^b UNIVERSITY OF EXTREMADURA   (Spain)

^c DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^d GHENT UNIVERSITY   (Belgium)

^e UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84903639076     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.114.238873     Document Type: Article

References (49)

1. Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115: 591-602
2. Bestwick CS, Brown IR, BennettMH, Mansfield JW (1997) Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv phaseolicola. Plant Cell 9: 209-221
3. Bolstad BM, Irizarry RA, Astrand M, Speed TP (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19: 185-193
4. Brady SM, Orlando DA, Lee JY, Wang JY, Koch J, Dinneny JR, Mace D, Ohler U, Benfey PN (2007) A high-resolution root spatiotemporal map reveals dominant expression patterns. Science 318: 801-806
5. Casamitjana-Martínez E, Hofhuis HF, Xu J, Liu CM, Heidstra R, Scheres B (2003) Root-specific CLE19 overexpression and the sol1/2 suppressors implicate a CLV-like pathway in the control of Arabidopsis root meristem maintenance. Curr Biol 13: 1435-1441
6. Casimiro I, Beeckman T, Graham N, Bhalerao R, Zhang H, Casero P, Sandberg G, Bennett MJ (2003) Dissecting Arabidopsis lateral root development. Trends Plant Sci 8: 165-171
7. Castelain M, Le Hir R, Bellini C (2012) The non-DNA-binding bHLH transcription factor PRE3/bHLH135/ATBS1/TMO7 is involved in the regulation of light signaling pathway in Arabidopsis. Physiologia Plantarum 145: 450-460
8. Cosio C, Vuillemin L, De Meyer M, Kevers C, Penel C, Dunand C (2009) An anionic class III peroxidase from zucchini may regulate hypocotyl elongation through its auxin oxidase activity. Planta 229: 823-836
9. del Pozo JC, Diaz-Trivino S, Cisneros N, Gutierrez C (2006) The balance between cell division and endoreplication depends on E2FC-DPB, transcription factors regulated by the ubiquitin-SCFSKP2A pathway in Arabidopsis. Plant Cell 18: 2224-2235
10. De Rybel B, Audenaert D, Xuan W, Overvoorde P, Strader LC, Kepinski S, Hoye R, Brisbois R, Parizot B, Vanneste S, et al (2012) A role for the root cap in root branching revealed by the non-auxin probe naxillin. Nat Chem Biol 8: 798-805
11. De Rybel B, Vassileva V, Parizot B, Demeulenaere M, Grunewald W, Audenaert D, Van Campenhout J, Overvoorde P, Jansen L, Vanneste S, et al (2010) A novel aux/IAA28 signaling cascade activates GATA23-dependent specification of lateral root founder cell identity. Curr Biol 20: 1697-1706
12. De Smet I, Tetsumura T, De Rybel B, Frei dit Frey N, Laplaze L, Casimiro I, Swarup R, Naudts M, Vanneste S, Audenaert D, et al (2007) Auxindependent regulation of lateral root positioning in the basal meristem of Arabidopsis. Development 134: 681-690
13. De Smet I, Vassileva V, De Rybel B, Levesque MP, Grunewald W, Van Damme D, Van Noorden G, Naudts M, Van Isterdael G, De Clercq R, et al (2008) Receptor-like kinase ACR4 restricts formative cell divisions in the Arabidopsis root. Science 322: 594-597
14. Dolan L, Janmaat K, Willemsen V, Linstead P, Poethig S, Roberts K, Scheres B (1993) Cellular organisation of the Arabidopsis thaliana root. Development 119: 71-84
15. Dubrovsky JG, Sauer M, Napsucialy-Mendivil S, Ivanchenko MG, Friml J, Shishkova S, Celenza J, Benková E (2008) Auxin acts as a local morphogenetic trigger to specify lateral root founder cells. Proc Natl Acad Sci USA 105: 8790-8794
16. Edgar R, Domrachev M, Lash AE (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30: 207-210
17. Fukaki H, Tameda S, Masuda H, Tasaka M (2002) Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. Plant J 29: 153-168
18. Fukaki H, Tasaka M (2009) Hormone interactions during lateral root formation. Plant Mol Biol 69: 437-449
19. Gazaryan IG, Lagrimini LM, Ashby GA, Thorneley RN (1996) Mechanism of indole-3-acetic acid oxidation by plant peroxidases: anaerobic stopped-flow spectrophotometric studies on horseradish and tobacco peroxidases. Biochem J 313: 841-847
20. Himanen K, Boucheron E, Vanneste S, de Almeida Engler J, Inzé D, Beeckman T (2002) Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell 14: 2339-2351
21. Himanen K, Vuylsteke M, Vanneste S, Vercruysse S, Boucheron E, Alard P, Chriqui D, Van Montagu M, Inzé D, Beeckman T (2004) Transcript profiling of early lateral root initiation. Proc Natl Acad Sci USA 101: 5146-5151
22. Hiraga S, Sasaki K, Ito H, Ohashi Y, Matsui H (2001) A large family of class III plant peroxidases. Plant Cell Physiol 42: 462-468
23. Iiyama K, Lam T, Stone BA (1994) Covalent cross-links in the cell wall. Plant Physiol 104: 315-320
24. Jiang K, Feldman LJ (2005) Regulation of root apical meristem development. Annu Rev Cell Dev Biol 21: 485-509
25. Kurup S, Runions J, Köhler U, Laplaze L, Hodge S, Haseloff J (2005) Marking cell lineages in living tissues. Plant J 42: 444-453
26. Lagrimini LM, Joly RJ, Dunlap JR, Liu TT (1997) The consequence of peroxidase overexpression in transgenic plants on root growth and development. Plant Mol Biol 33: 887-895
27. Lavenus J, Goh T, Roberts I, Guyomarc'h S, Lucas M, De Smet I, Fukaki H, Beeckman T, Bennett M, Laplaze L (2013) Lateral root development in Arabidopsis: fifty shades of auxin. Trends Plant Sci 18: 450-458
28. Lucas M, Swarup R, Paponov IA, Swarup K, Casimiro I, Lake D, Péret B, Zappala S, Mairhofer S, Whitworth M, et al (2011) Short-Root regulates primary, lateral, and adventitious root development in Arabidopsis. Plant Physiol 155: 384-398
29. Ma F, Wang L, Li J, Samma MK, Xie Y, Wang R, Wang J, Zhang J, Shen W (2014) Interaction between HY1 and H2O2 in auxin-induced lateral root formation in Arabidopsis. Plant Mol Biol 85: 49-61
30. Malamy JE, Benfey PN (1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124: 33-44
31. Manzano C, Ramirez-Parra E, Casimiro I, Otero S, Desvoyes B, De Rybel B, Beeckman T, Casero P, Gutierrez C, Del Pozo JC (2012) Auxin and epigenetic regulation of SKP2B, an F-box that represses lateral root formation. Plant Physiol 160: 749-762
32. Moreno-Risueño MA, Van Norman JM, Moreno A, Zhang J, Ahnert SE, Benfey PN (2010) Oscillating gene expression determines competence for periodic Arabidopsis root branching. Science 329: 1306-1311
33. Nakagawa T, Kurose T, Hino T, Tanaka K, Kawamukai M, Niwa Y, Toyooka K, Matsuoka K, Jinbo T, Kimura T (2007) Development of series of Gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J Biosci Bioeng 104: 34-41
34. Papdi C, Abrahám E, Joseph MP, Popescu C, Koncz C, Szabados L (2008) Functional identification of Arabidopsis stress regulatory genes using the controlled cDNA overexpression system. Plant Physiol 147: 528-542
35. Parizot B, De Rybel B, Beeckman T (2010) VisuaLRTC: a new view on lateral root initiation by combining specific transcriptome data sets. Plant Physiol 153: 34-40
36. Passaia G, Queval G, Bai J, Margis-Pinheiro M, Foyer CH (2014) The effects of redox controls mediated by glutathione peroxidases on root architecture in Arabidopsis thaliana. J Exp Bot 65: 1403-1413
37. Passardi F, Cosio C, Penel C, Dunand C (2005) Peroxidases have more functions than a Swiss army knife. Plant Cell Rep 24: 255-265
38. Péret B, Li G, Zhao J, Band LR, Voß U, Postaire O, Luu DT, Da Ines O, Casimiro I, Lucas M, et al (2012) Auxin regulates aquaporin function to facilitate lateral root emergence. Nat Cell Biol 14: 991-998
39. Redman JC, Haas BJ, Tanimoto G, Town CD (2004) Development and evaluation of an Arabidopsis whole genome Affymetrix probe array. Plant J 38: 545-561
40. Ren H, Santner A, del Pozo JC, Murray JA, Estelle M (2008) Degradation of the cyclin-dependent kinase inhibitor KRP1 is regulated by two different ubiquitin E3 ligases. Plant J 53: 705-716
41. Ros Barceló A (1997) Lignification in plant cell walls. Int Rev Cytol 176: 87-132
42. Schlereth A, Möller B, LiuW, Kientz M, Flipse J, Rademacher EH, SchmidM, Jürgens G, Weijers D (2010) MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 464: 913-916
43. Swarup K, Benková E, Swarup R, Casimiro I, Péret B, Yang Y, Parry G, Nielsen E, De Smet I, Vanneste S, et al (2008) The auxin influx carrier LAX3 promotes lateral root emergence. Nat Cell Biol 10: 946-954
44. Tognolli M, Penel C, Greppin H, Simon P (2002) Analysis and expression of the class III peroxidase large gene family in Arabidopsis thaliana. Gene 288: 129-138
45. Tsukagoshi H, Busch W, Benfey PN (2010) Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143: 606-616
46. Ubeda-Tomás S, Beemster GT, Bennett MJ (2012) Hormonal regulation of root growth: integrating local activities into global behaviour. Trends Plant Sci 17: 326-331
47. Vanneste S, De Rybel B, Beemster GT, Ljung K, De Smet I, Van Isterdael G, Naudts M, Iida R, Gruissem W, Tasaka M, et al (2005) Cell cycle progression in the pericycle is not sufficient for SOLITARY ROOT/IAA14-mediated lateral root initiation in Arabidopsis thaliana. Plant Cell 17: 3035-3050
48. Willemsen V, Bauch M, Bennett T, Campilho A, Wolkenfelt H, Xu J, Haseloff J, Scheres B (2008) The NAC domain transcription factors FEZ and SOMBRERO control the orientation of cell division plane in Arabidopsis root stem cells. Dev Cell 15: 913-922
49. Zuo J, NiuQW, ChuaNH(2000) An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. Plant J 24: 265-273