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Plant Molecular Biology

, Volume 78, Issue 6, pp 545–559 | Cite as

The Arabidopsis thaliana transcriptional activator STYLISH1 regulates genes affecting stamen development, cell expansion and timing of flowering

  • Veronika Ståldal
  • Izabela Cierlik
  • Song Chen
  • Katarina Landberg
  • Tammy Baylis
  • Mattias Myrenås
  • Jens F. Sundström
  • D. Magnus Eklund
  • Karin Ljung
  • Eva SundbergEmail author
Article

Abstract

SHORT-INTERNODES/STYLISH (SHI/STY)-family proteins redundantly regulate development of lateral organs in Arabidopsis thaliana. We have previously shown that STY1 interacts with the promoter of the auxin biosynthesis gene YUCCA (YUC)4 and activates transcription of the genes YUC4, YUC8 and OCTADECANOID-RESPONSIVE ARABIDOPSIS AP2/ERF (ORA)59 independently of protein translation. STY1 also affects auxin levels and auxin biosynthesis rates. Here we show that STY1 induces the transcription of 16 additional genes independently of protein translation. Several of these genes are tightly co-expressed with SHI/STY-family genes and/or down-regulated in SHI/STY-family multiple mutant lines, suggesting them to be regulated by SHI/STY proteins during plant development. The majority of the identified genes encode transcription factors or cell expansion-related enzymes and functional studies suggest their involvement in stamen and leaf development or flowering time regulation.

Keywords

SHI STY Gene regulation Stamen development Cell expansion Flowering 

Notes

Acknowledgments

We thank Yunde Zhao, Cristina Ferrandiz, Johan Memelink and Elin Övernäs for providing seeds, and John Chandler for critical reading of the manuscript. This work was supported by grants from the Swedish Research Council Formas to Eva Sundberg, the Nilsson-Ehle-donations and the Royal Swedish Academy of Science to Veronika Ståldal.

Supplementary material

11103_2012_9888_MOESM1_ESM.doc (231 kb)
Supplementary material 1 (DOC 231 kb)

References

  1. Alvarez JP, Goldshmidt A, Efroni I, Bowman JL, Eshed Y (2009) The NGATHA distal organ development genes are essential for style specification in Arabidopsis. Plant Cell 21:1373–1393PubMedCrossRefGoogle Scholar
  2. Anastasiou E, Kenz S, Gerstung M, MacLean D, Timmer J, Fleck C, Lenhard M (2007) Control of plant organ size by KLUH/CYP78A5-dependent intercellular signaling. Dev Cell 13(6):843–856PubMedCrossRefGoogle Scholar
  3. Andersen SU, Buechel S, Zhao Z, Ljung K, Novák O, Busch W, Schuster C, Lohmann JU (2008) Requirement of B2-type cyclin-dependent kinases for meristem integrity in Arabidopsis thaliana. Plant Cell 20(1):88–100PubMedCrossRefGoogle Scholar
  4. Barbehenn RV, Jaros A, Yip L, Tran L, Kanellis AK, Constabel CP (2008) Evaluating ascorbate oxidase as a plant defense against leaf-chewing insects using transgenic poplar. J Chem Ecol 34(10):1331–1340PubMedCrossRefGoogle Scholar
  5. Becker A, Bey M, Bürglin TR, Saedler H, Theissen G (2002) Ancestry and diversity of BEL1-like homeobox genes revealed by gymnosperm (Gnetum gnemon) homologs. Dev Genes Evol 212(9):452–457PubMedCrossRefGoogle Scholar
  6. Cecchetti V, Altamura MM, Falasca G, Costantino P, Cardarelli M (2008) Auxin regulates Arabidopsis anther dehiscence, pollen maturation, and filament elongation. Plant Cell 20(7):1760–1774PubMedCrossRefGoogle Scholar
  7. Chandler JW, Jacobs B, Cole M, Comelli P, Werr W (2011) DORNRÖSCHEN-LIKE expression marks Arabidopsis floral organ founder cells and precedes auxin response maxima. Plant Mol Biol 76(1–2):171–185PubMedCrossRefGoogle Scholar
  8. Cheng Y, Dai X, Zhao Y (2006) Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. Gene Dev 20(13):1790–1799PubMedCrossRefGoogle Scholar
  9. Coen ES (1992) Flower development. Curr Opin Cell Biol 4(6):929–933PubMedCrossRefGoogle Scholar
  10. Cona A, Rea G, Angelini R, Federico R, Tavladoraki P (2006) Functions of amine oxidases in plant development and defence. Trends Plant Sci 11(2):80–88PubMedCrossRefGoogle Scholar
  11. Cosgrove DJ (2000) Loosening of plant cell walls by expansions. Nature 407(6802):321–326PubMedCrossRefGoogle Scholar
  12. Edlund A, Eklof S, Sundberg B, Moritz T, Sandberg G (1995) A microscale technique for gas chromatography-mass spectrometry measurements of picogram amounts of indole-3-acetic acid in plant tissues. Plant Physiol 108(3):1043–1047PubMedGoogle Scholar
  13. Eklund DM, Ståldal V, Valsecchi I, Cierlik I, Eriksson C, Hiratsu K, Ohme-Takagi M, Sundström JF, Thelander M, Ezcurra I, Sundberg E (2010) The Arabidopsis thaliana STYLISH1 protein acts as a transcriptional activator regulating auxin biosynthesis. Plant Cell 22(2):349–363PubMedCrossRefGoogle Scholar
  14. Eklund DM, Cierlik I, Ståldal V, Claes A, Vestman D, Chandler J, Sundberg E (2011) Expression of Arabidopsis SHORT INTERNODES/STYLISH family genes in auxin biosynthesis zones of aerial organs is dependent on a GCC-box-like regulatory element. Plant Physiol 157(4):2069–2080PubMedCrossRefGoogle Scholar
  15. Eriksson S, Stransfeld L, Adamski NM, Breuninger H, Lenhard M (2010) KLUH/CYP78A5-dependent growth signaling coordinates floral organ growth in Arabidopsis. Curr Biol 20(6):527–532PubMedCrossRefGoogle Scholar
  16. Franco-Zorrilla JM, Cubas P, Jarillo JA, Fernández-Calvín B, Salinas J, Martínez-Zapater JM (2002) AtREM1, a member of a new family of B3 domain-containing genes, is preferentially expressed in reproductive meristems. Plant Physiol 128(2):418–427PubMedCrossRefGoogle Scholar
  17. Heisler MG, Ohno C, Das P, Sieber P, Reddy GV, Long JA, Meyerowitz EM (2005) Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr Biol 15(21):1899–1911PubMedCrossRefGoogle Scholar
  18. Hentrich M (2010) Molekulare Mechanismen der Octadecanoid-regulierten indol-3-essigsäure-biosynthese. PhD thesis. Ruhr-Universität Bochum, BochumGoogle Scholar
  19. 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 34:733–739PubMedCrossRefGoogle Scholar
  20. Ito T, Meyerowitz EM (2000) Overexpression of a gene encoding a cytochrome P450, CYP78A9, induces large and seedless fruit in Arabidopsis. Plant Cell 12(9):1541–1550PubMedCrossRefGoogle Scholar
  21. Jefferson RA (1987) Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol Biol Rep 5(4):387–405CrossRefGoogle Scholar
  22. Kaufmann K, Muiño JM, Jauregui R, Airoldi CA, Smaczniak C, Krajewski P, Angenent GC (2009) Target genes of the MADS transcription factor SEPALLATA3: integration of developmental and hormonal pathways in the Arabidopsis flower. PLoS Biol 7(4):e1000090PubMedCrossRefGoogle Scholar
  23. Kedzierska S (2006) Structure, function and mechanisms of action of ATPases from the AAA superfamily of proteins. Postepy Biochem 52(3):330–338PubMedGoogle Scholar
  24. Kim J, Shiu S, Thoma S, Li W, Patterson SE (2006) Patterns of expansion and expression divergence in the plant polygalacturonase gene family. Genome Biol 7(9):R87PubMedCrossRefGoogle Scholar
  25. Kuusk S, Sohlberg JJ, Long JA, Fridborg I, Sundberg E (2002) STY1 and STY2 promote the formation of apical tissues during Arabidopsis gynoecium development. Development 129(20):4707–4717PubMedGoogle Scholar
  26. Kuusk S, Sohlberg JJ, Eklund DM, Sundberg E (2006) Functionally redundant SHI family genes regulate Arabidopsis gynoecium development in a dose-dependent manner. Plant J 47(1):99–111PubMedCrossRefGoogle Scholar
  27. Levy YY, Mesnage S, Mylne JS, Gendall AR, Dean C (2002) Multiple roles of Arabidopsis VRN1 in vernalization and flowering time control. Science 297(5579):243–246PubMedCrossRefGoogle Scholar
  28. Mashiguchi K, Tanaka K, Sakai T, Sugawara S, Kawaide H, Natsume M, Hanada A, Yaeno T, Shirasu K, Yao H, McSteen P, Zhao Y, Hayashi K-I, Kamiya Y, Kasahara H (2011) The main auxin biosynthesis pathway in Arabidopsis. Proc Natl Acad Sci 108(45):18512–18517PubMedCrossRefGoogle Scholar
  29. Matias-Hernandez L, Battaglia R, Galbiati F, Rubes M, Eichenberger C, Grossniklaus U, Kater MM, Colombo L (2010) VERDANDI is a direct target of the MADS domain ovule identity complex and affects embryo sac differentiation in Arabidopsis. Plant Cell 22(6):1702–1715PubMedCrossRefGoogle Scholar
  30. Miska KB, Fetterer RH, Lillehoj HS, Jenkins MC, Allen PC, Harper SB (2007) Characterisation of macrophage migration inhibitory factor from Eimeria species infectious to chickens. Mol Biochem Parasit 151(2):173–183CrossRefGoogle Scholar
  31. Nagpal P, Ellis CM, Weber H, Ploense SE, Barkawi LS, Guilfoyle TJ, Hagen G, Alonso JM, Cohen JD, Farmer EE, Ecker JR, Reed JW (2005) Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation. Development 132(18):4107–4118PubMedCrossRefGoogle Scholar
  32. Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140(2):411–432PubMedCrossRefGoogle Scholar
  33. Nakayama N, Kuhlemeier C (2009) Leaf development: Untangling the spirals. Curr Biol 19(2):R71–R74PubMedCrossRefGoogle Scholar
  34. Nemhauser JL, Feldman LJ, Zambryski PC (2000) Auxin and ETTIN in Arabidopsis gynoecium morphogenesis. Development 127(18):3877–3888PubMedGoogle Scholar
  35. Ogawa M, Kay P, Wilson S, Swain SM (2009) ARABIDOPSIS DEHISCENCE ZONE POLYGALACTURONASE1 (ADPG1), ADPG2, and QUARTET2 are Polygalacturonases required for cell separation during reproductive development in Arabidopsis. Plant Cell 21(1):216–233PubMedCrossRefGoogle Scholar
  36. Ogura T, Wilkinson AJ (2001) AAA + superfamily ATPases: common structure-diverse function. Genes Cells 6(7):575–597PubMedCrossRefGoogle Scholar
  37. Ouyang J, Shao X, Li J (2000) Indole-3-glycerol phosphate, a branch point of indole-3-acetic acid biosynthesis from the tryptophan biosynthetic pathway in Arabidopsis thaliana. Plant J 24(3):327–333PubMedCrossRefGoogle Scholar
  38. Övernäs E (2010) Characterisation of members of the HD-Zip I and DREB/ERF transcription factor families and their functions in plant stress responses. PhD thesis. Uppsala University, UppsalaGoogle Scholar
  39. Phillips KA, Skirpan AL, Liu X, Christensen A, Slewinski TL, Hudson C, Barazesh S, Cohen JD, Malcomber S, McSteen P (2011) Vanishing tassel 2 encodes a grass-specific tryptophan aminotransferase required for vegetative and reproductive development in maize. Plant Cell 23:550–566PubMedCrossRefGoogle Scholar
  40. Pré M, Atallah M, Champion A, De Vos M, Pieterse CMJ, Memelink J (2008) The AP2/ERF domain transcription factor ORA59 integrates jasmonic acid and ethylene signals in plant defense. Plant Physiol 147(3):1347–1357PubMedCrossRefGoogle Scholar
  41. Rawat R, Schwartz J, Jones MA, Sairanen I, Cheng Y, Andersson CR, Zhao Y, Ljung K, Harmer SL (2009) REVEILLE1, a Myb-like transcription factor, integrates the circadian clock and auxin pathways. Proc Natl Acad Sci USA 106(39):16883–16888PubMedCrossRefGoogle Scholar
  42. Reiser L, Modrusan Z, Margossian L, Samach A, Ohad N, Haughn GW, Fischer RL (1995) The BELL1 gene encodes a homeodomain protein involved in pattern formation in the Arabidopsis ovule primordium. Cell 83(5):735–742PubMedCrossRefGoogle Scholar
  43. Romanel EAC, Schrago CG, Couñago RM, Russo CAM, Alves-Ferreira M (2009) Evolution of the B3 DNA binding superfamily: new insights into REM family gene diversification. PLoS ONE 4(6):e5791PubMedCrossRefGoogle Scholar
  44. Ru P, Xu L, Ma H, Huang H (2006) Plant fertility defects induced by the enhanced expression of microRNA 167. Cell Res 16(5):457–465PubMedCrossRefGoogle Scholar
  45. Rutjens B, Bao D, van Eck-Stouten E, Brand M, Smeekens S, Proveniers M (2009) Shoot apical meristem function in Arabidopsis requires the combined activities of three BEL1-like homeodomain proteins. Plant J 58(4):641–654PubMedCrossRefGoogle Scholar
  46. Shimizu R, Ji J, Kelsey E, Ohtsu K, Schnable PS, Scanlon MJ (2009) Tissue specificity and evolution of meristematic WOX3 function. Plant Physiol 149(2):841–850PubMedCrossRefGoogle Scholar
  47. Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2(8):755–767PubMedCrossRefGoogle Scholar
  48. Sohlberg JJ, Myrenås M, Kuusk S, Lagercrantz U, Kowalczyk M, Sandberg G, Sundberg E (2006) STY1 regulates auxin homeostasis and affects apical-basal patterning of the Arabidopsis gynoecium. Plant J 47(1):112–123PubMedCrossRefGoogle Scholar
  49. Ståldal V, Sohlberg JJ, Eklund DM, Ljung K, Sundberg E (2008) Auxin can act independently of CRC, LUG, SEU, SPT and STY1 in style development but not apical-basal patterning of the Arabidopsis gynoecium. New Phytol 180(4):798–808PubMedCrossRefGoogle Scholar
  50. Stepanova AN, Yun J, Robles LM, Novak O, He W, Guo H, Ljung K, Alonso JM (2011) The Arabidopsis YUCCA1 flavin monooxygenase functions in the indole-3-pyruvic acid branch of auxin biosynthesis. Plant Cell 23:1–13CrossRefGoogle Scholar
  51. Strader LC, Bartel B (2008) A new path to auxin. Nat Chem Biol 4(6):337–339PubMedCrossRefGoogle Scholar
  52. Tao Y, Ferrer JL, Ljung K, Pojer F, Hong F, Long JA, Li L, Moreno JE, Bowman ME, Ivans LJ, Cheng Y, Lim J, Zhao Y, Ballaré CL, Sandberg G, Noel JP, Chory J (2008) Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 133(1):164–176PubMedCrossRefGoogle Scholar
  53. Tobeña-Santamaria R, Bliek M, Ljung K, Sandberg G, Mol JNM, Souer E, Koes R (2002) FLOOZY of petunia is a flavin mono-oxygenase-like protein required for the specification of leaf and flower architecture. Gene Dev 16(6):753–763PubMedCrossRefGoogle Scholar
  54. Trigueros M, Navarrete-Gómez M, Sato S, Christensen SK, Pelaz S, Weigel D, Yanofsky MF, Ferrándiz C (2009) The NGATHA genes direct style development in the Arabidopsis gynoecium. Plant Cell 21(5):1394–1409PubMedCrossRefGoogle Scholar
  55. Vom Endt D, Soarese Silva M, Kijne JW, Pasquali G, Memelink J (2007) Identification of a bipartite jasmonate-responsive promoter element in the Catharanthus roseus ORCA3 transcription factor gene that interacts specifically with AT-Hook DNA-binding proteins. Plant Physiol 144(3):1680–1689PubMedCrossRefGoogle Scholar
  56. Wang J, Schwab R, Czech B, Mica E, Weigel D (2008) Dual Effects of miR156-Targeted SPL Genes and CYP78A5/KLUH on plastochron length and organ size in Arabidopsis thaliana. Plant Cell 20(5):1231–1243PubMedCrossRefGoogle Scholar
  57. Weigel D, Meyerowitz EM (1994) The ABCs of floral homeotic genes. Cell 78(2):203–209PubMedCrossRefGoogle Scholar
  58. Won C, Shen X, Mashiguchi K, Zheng Z, Dai X, Cheng Y, Kasahara H, Kamiya Y, Chory J, Zhao Y (2011) Conversion of tryptophan to indole-3-acetic acid by TRYPTOPHAN AMINOTRANSFERASES OF ARABIDOPSIS and YUCCAs in Arabidopsis. Proc Natl Acad Sci www.pnas.org/cgi/doi/10.1073/pnas.1108436108
  59. Wu M, Tian Q, Reed JW (2006) Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 133(21):4211–4218PubMedCrossRefGoogle Scholar
  60. Zhao Y, Christensen SK, Fankhauser C, Cashman JR, Cohen JD, Weigel D, Chory J (2001) A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science 291(5502):306–309PubMedCrossRefGoogle Scholar
  61. Zondlo SC, Irish VF (1999) CYP78A5 encodes a cytochrome P450 that marks the shoot apical meristem boundary in Arabidopsis. Plant J 19(3):259–268PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Veronika Ståldal
    • 1
  • Izabela Cierlik
    • 1
  • Song Chen
    • 1
    • 4
  • Katarina Landberg
    • 1
  • Tammy Baylis
    • 2
  • Mattias Myrenås
    • 1
  • Jens F. Sundström
    • 1
  • D. Magnus Eklund
    • 1
    • 5
  • Karin Ljung
    • 3
  • Eva Sundberg
    • 1
    Email author
  1. 1.Department of Plant Biology and Forest Genetics, Uppsala BioCenter, Linnean Centre of Plant Biology in UppsalaSwedish University of Agricultural SciencesUppsalaSweden
  2. 2.Department of Biological SciencesSimon Fraser UniversityBurnabyCanada
  3. 3.Department of Forest Genetics and Plant Physiology, Umeå Plant Science CenterSwedish University of Agricultural SciencesUmeåSweden
  4. 4.Cologne Biocenter, Botanical InstituteUniversity of CologneKölnGermany
  5. 5.School of Biological SciencesMonash UniversityMelbourneAustralia

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