Transcription factor WRKY23 assists auxin distribution patterns during Arabidopsis root development through local control on flavonol biosynthesis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 5, 2012, Pages 1554-1559

  Grunewald, Wim ^a,b   De Smet, Ive ^a,b,c   Lewis, Daniel R ^d   Löfke, Christian ^e   Jansen, Leentje ^a,b   Goeminne, Geert ^a,b   Vanden Bossche, Robin ^a,b   Karimi, Mansour ^a,b   De Rybel, Bert ^a,b,f   Vanholme, Bartel ^a,b   Teichmann, Thomas ^e   Boerjan, Wout ^a,b   Van Montagu, Marc C E ^b   Gheysen, Godelieve ^b   Muday, Gloria K ^d   Friml, Jiří ^a,b   Beeckman, Tom ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^d WAKE FOREST UNIVERSITY   (United States)

^e UNIVERSITY OF GÖTTINGEN   (Germany)

^f WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Flavonoid; Lateral root; WRKY

Indexed keywords

AUXIN; FLAVONOL; FLAVONOL DERIVATIVE; PHYTOHORMONE; TRANSCRIPTION FACTOR;

ARABIDOPSIS; ARTICLE; AUXIN TRANSPORT; BIOSYNTHESIS; CELL TRANSPORT; FEEDBACK SYSTEM; NONHUMAN; PLANT GROWTH; PLANT ROOT; PRIORITY JOURNAL; ROOT DEVELOPMENT; ROOT GROWTH;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; FLAVONOLS; GENE EXPRESSION REGULATION, PLANT; INDOLEACETIC ACIDS; PLANT ROOTS; REAL-TIME POLYMERASE CHAIN REACTION; TRANSCRIPTION FACTORS;

ARABIDOPSIS;

EID: 84857131337     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1121134109     Document Type: Article

References (52)

1. Sabatini S, et al. (1999) An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99:463-472.
2. Dubrovsky JG, et al. (2008) Auxin acts as a local morphogenetic trigger to specify lateral root founder cells. Proc Natl Acad Sci USA 105:8790-8794. (Pubitemid 351987758)
3. Friml J, et al. (2002) AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis. Cell 108:661-673. (Pubitemid 34241427)
4. Ljung K, et al. (2005) Sites and regulation of auxin biosynthesis in Arabidopsis roots. Plant Cell 17:1090-1104. (Pubitemid 43142128)
5. Petersson SV, et al. (2009) An auxin gradient and maximum in the Arabidopsis root apex shown by high-resolution cell-specific analysis of IAA distribution and synthesis. Plant Cell 21:1659-1668.
6. Vieten A, Sauer M, Brewer PB, Friml J (2007) Molecular and cellular aspects of auxintransport-mediated development. Trends Plant Sci 12:160-168. (Pubitemid 46546474)
7. Bennett MJ, et al. (1996) Arabidopsis AUX1 gene: A permease-like regulator of root gravitropism. Science 273:948-950. (Pubitemid 26275169)
8. Geisler M, Murphy AS (2006) The ABC of auxin transport: The role of p-glycoproteins in plant development. FEBS Lett 580:1094-1102. (Pubitemid 43185289)
9. Grunewald W, Friml J (2010) The march of the PINs: Developmental plasticity by dynamic polar targeting in plant cells. EMBO J 29:2700-2714.
10. Swarup R, et al. (2001) Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. Genes Dev 15:2648-2653. (Pubitemid 32988875)
11. Jacobs M, Rubery PH (1988) Naturally occurring auxin transport regulators. Science 241:346-349.
12. Bailly A, et al. (2008) Modulation of P-glycoproteins by auxin transport inhibitors is mediated by interaction with immunophilins. J Biol Chem 283:21817-21826.
13. Brown DE, et al. (2001) Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis. Plant Physiol 126:524-535. (Pubitemid 32566609)
14. Buer CS, Djordjevic MA (2009) Architectural phenotypes in the transparent testa mutants of Arabidopsis thaliana. J Exp Bot 60:751-763.
15. Buer CS, Muday GK (2004) The transparent testa4 mutation prevents flavonoid synthesis and alters auxin transport and the response of Arabidopsis roots to gravity and light. Plant Cell 16:1191-1205. (Pubitemid 38641514)
16. Lewis DR, et al. (2011) Auxin and ethylene induce flavonol accumulation through distinct transcriptional networks. Plant Physiol 156:144-164.
17. Murphy A, Peer WA, Taiz L (2000) Regulation of auxin transport by aminopeptidases and endogenous flavonoids. Planta 211:315-324.
18. Peer WA, et al. (2004) Variation in expression and protein localization of the PIN family of auxin efflux facilitator proteins in flavonoid mutants with altered auxin transport in Arabidopsis thaliana. Plant Cell 16:1898-1911. (Pubitemid 38908783)
19. Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15:247-258.
20. Grunewald W, et al. (2008) A role for AtWRKY23 in feeding site establishment of plant-parasitic nematodes. Plant Physiol 148:358-368. (Pubitemid 352847612)
21. Brady SM, et al. (2007) A high-resolution root spatiotemporal map reveals dominant expression patterns. Science 318:801-806. (Pubitemid 351411772)
22. Okushima Y, et al. (2005) Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: Unique and overlapping functions of ARF7 and ARF19. Plant Cell 17:444-463. (Pubitemid 41672967)
23. Vanneste S, 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.
24. Hiratsu K, Matsui K, Koyama T, Ohme-Takagi M (2003) Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis. Plant J 34:733-739. (Pubitemid 36720206)
25. De Sutter V, et al. (2005) Exploration of jasmonate signalling via automated and standardized transient expression assays in tobacco cells. Plant J 44:1065-1076. (Pubitemid 43906733)
26. Benfey PN, Chua N-H (1990) The cauliflower mosaic virus 35S promoter: Combinatorial regulation of transcription in plants. Science 250:959-966. (Pubitemid 120031796)
27. Weijers D, et al. (2001) An Arabidopsis Minute-like phenotype caused by a semidominant mutation in a RIBOSOMAL PROTEIN S5 gene. Development 128:4289-4299. (Pubitemid 33077039)
28. van den Berg C, Willemsen V, Hendriks G, Weisbeek P, Scheres B (1997) Short-range control of cell differentiation in the Arabidopsis root meristem. Nature 390:287-289. (Pubitemid 27513310)
29. De Smet I, et al. (2008) Receptor-like kinase ACR4 restricts formative cell divisions in the Arabidopsis root. Science 322:594-597.
30. Sarkar AK, et al. (2007) Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446:811-814. (Pubitemid 46582034)
31. Stahl Y, Wink RH, Ingram GC, Simon R (2009) A signaling module controlling the stem cell niche in Arabidopsis root meristems. Curr Biol 19:909-914.
32. Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963-1971. (Pubitemid 28174069)
33. Benková E, et al. (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591-602. (Pubitemid 37506047)
34. Levée V, et al. (2009) Expression profiling and functional analysis of Populus WRKY23 reveals a regulatory role in defense. New Phytol 184:48-70.
35. Jones JT, Furlanetto C, Phillips MS (2007) The role of flavonoids produced in response to cyst nematode infection of Arabidopsis thaliana. Nematology 9:671-677. (Pubitemid 47480550)
36. Okushima Y, Fukaki H, Onoda M, Theologis A, Tasaka M (2007) ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant Cell 19:118-130. (Pubitemid 46852706)
37. Lau S, Jürgens G, De Smet I (2008) The evolving complexity of the auxin pathway. Plant Cell 20:1738-1746. (Pubitemid 352844529)
38. Dong JX, Chen CH, Chen ZX (2003) Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant Mol Biol 51:21-37. (Pubitemid 36189133)
39. Goda H, et al. (2004) Comprehensive comparison of auxin-regulated and brassinosteroid- regulated genes in Arabidopsis. Plant Physiol 134:1555-1573. (Pubitemid 38527365)
40. Lee DJ, et al. (2007) Genome-wide expression profiling of ARABIDOPSIS RESPONSE REGULATOR 7(ARR7) overexpression in cytokinin response. Mol Genet Genomics 277: 115-137. (Pubitemid 46208346)
41. Morant M, et al. (2010) Metabolomic, transcriptional, hormonal, and signaling crosstalk in superroot2. Mol Plant 3:192-211.
42. Hachez C, Ohashi-Ito K, Dong J, Bergmann DC (2011) Differentiation of Arabidopsis guard cells: Analysis of the networks incorporating the basic helix-loop-helix transcription factor, FAMA. Plant Physiol 155:1458-1472.
43. Johnson CS, Kolevski B, Smyth DR (2002) TRANSPARENT TESTA GLABRA2, a trichome and seed coat development gene of Arabidopsis, encodes a WRKY transcription factor. Plant Cell 14:1359-1375. (Pubitemid 34780437)
44. Luo M, Dennis ES, Berger F, Peacock WJ, Chaudhury A (2005) MINISEED3 (MINI3), a WRKY family gene, and HAIKU2 (IKU2), a leucine-rich repeat (LRR) KINASE gene, are regulators of seed size in Arabidopsis. Proc Natl Acad Sci USA 102:17531-17536. (Pubitemid 41740900)
45. Ueda M, Zhang Z, Laux T (2011) Transcriptional activation of Arabidopsis axis patterning genes WOX8/9 links zygote polarity to embryo development. Dev Cell 20: 264-270.
46. Blilou I, et al. (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39-44.
47. Stracke R, et al. (2007) Differential regulation of closely related R2R3-MYB transcription factors controls flavonol accumulation in different parts of the Arabidopsis thaliana seedling. Plant J 50:660-677. (Pubitemid 46733755)
48. Grunewald W, et al. (2009) Manipulation of auxin transport in plant roots during Rhizobium symbiosis and nematode parasitism. Plant Cell 21:2553-2562.
49. Grunewald W, Cannoot B, Friml J, Gheysen G (2009) Parasitic nematodes modulate PIN-mediated auxin transport to facilitate infection. PLoS Pathog 5:e1000266.
50. Hejátko J, et al. (2006) In situ hybridization technique for mRNA detection in whole mount Arabidopsis samples. Nat Protoc 1:1939-1946. (Pubitemid 46773315)
51. Kitakura S, et al. (2011) Clathrin mediates endocytosis and polar distribution of PIN auxin transporters in Arabidopsis. Plant Cell 23:1920-1931.
52. Grunewald W, et al. (2009) Expression of the Arabidopsis jasmonate signalling repressor JAZ1/TIFY10A is stimulated by auxin. EMBO Rep 10:923-928.