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Plant Molecular Biology

, Volume 82, Issue 1–2, pp 71–83 | Cite as

A gain-of-function mutation in IAA8 alters Arabidopsis floral organ development by change of jasmonic acid level

  • Jing Wang
  • Da-Wei Yan
  • Ting-Ting Yuan
  • Xiang Gao
  • Ying-Tang LuEmail author
Article

Abstract

Auxin regulates a variety of physiological processes via its downstream factors included Aux/IAAs. In this study, one of these Aux/IAAs, IAA8 is shown to play its role in Arabidopsis development with transgenic plants expressing GFP-mIAA8 under the control of IAA8 promoter, in which IAA8 protein was mutated by changing Pro170 to Leu170 in its conserved domain II. These transgenic dwarfed plants had more lateral branches, short primary inflorescence stems, decreased shoot apical dominance, curled leaves and abnormal flower organs (short petal and stamen, and bent stigmas). Further experiments revealed that IAA8::GFP-mIAA8 plants functioned as gain-of-function mutation to increase GFP-mIAA8 amount probably by stabilizing IAA8 protein against proteasome-mediated protein degradation with IAA8::GFP-IAA8 plants as control. The searching for its downstream factors indicated its interaction with both ARF6 and ARF8, suggesting that IAA8 may involve in flower organ development. This was further evidenced by analyzing the expression of jasmonic acid (JA) biosynthetic genes and JA levels because ARF6 and ARF8 are required for normal JA production. These results indicated that in IAA8::GFP-mIAA8 plants, JA biosynthetic genes including DAD1 (AT2G44810), AOS (AT5G42650) and ORP3 (AT2G06050) were dramatically down-regulated and JA level in the flowers was reduced to 70 % of that in wild-type. Furthermore, exogenous JA application can partially rescue short petal and stamen observed IAA8::GFP-mIAA8 plants. Thus, IAA8 plays its role in floral organ development by changes in JA levels probably via its interaction with ARF6/8 proteins.

Keywords

Arabidopsis thaliana Aux/IAAs Auxin response factors Floral organ development IAA8 Jasmonic acid 

Notes

Acknowledgments

We thank Tom Beeckman for providing the plasmids including five pGBKT7-based vectors for ARF3, ARF7, ARF13, ARF17 and ARF23. This work was supported by Major State Basic Research Program (2013CB126901) and National Natural Science Foundation of China (Grant# 90917001) to YT Lu.

Supplementary material

11103_2013_39_MOESM1_ESM.doc (806 kb)
Supplementary material 1 (DOC 805 kb)

References

  1. Abel S, Theologis A (1996) Early genes and auxin action. Plant Physiol 111:9–17PubMedCrossRefGoogle Scholar
  2. Abel S, Oeller PW, Theologis A (1994) Early auxin-induced genes encode short-lived nuclear proteins. Proc Natl Acad Sci USA 91:326–330PubMedCrossRefGoogle Scholar
  3. Arase F, Nishitani H, Egusa M, Nishimoto N, Sakurai S, Sakamoto N, Kaminaka H (2012) IAA8 involved in lateral root formation interacts with the TIR1 auxin receptor and ARF transcription factors in Arabidopsis. PLoS ONE 7(8):e43414PubMedCrossRefGoogle Scholar
  4. Chapman EJ, Estelle M (2009) Mechanism of auxin-regulated gene expression in plants. Annu Rev Genet 43:265–285PubMedCrossRefGoogle Scholar
  5. Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139:5–17PubMedCrossRefGoogle Scholar
  6. De Rybel B, Vassileva V, Parizot B, Demeulenaere M, Grunewald W, Audenaert D, Van Campenhout J, Overvoorde P, Jansen L, Vanneste S, Moller B, Wilson M, Holman T, Van Isterdael G, Brunoud G, Vuylsteke M, Vernoux T, De Veylder L, Inze D, Weijers D, Bennett MJ, Beeckman T (2010) A novel Aux/IAA28 signaling cascade activates GATA23-dependent specification of lateral root founder cell identity. Curr Biol 20:1697–1706PubMedCrossRefGoogle Scholar
  7. Dharmasiri N, Dharmasiri S, Weijers D, Lechner E, Yamada M, Hobbie L, Ehrismann JS, Jurgens G, Estelle M (2005) Plant development is regulated by a family of auxin receptor F box proteins. Dev Cell 9:109–119PubMedCrossRefGoogle Scholar
  8. Fukaki H, Taniguchi N, Tasaka M (2006) PICKLE is required for SOLITARY-ROOT/IAA14-mediated repression of ARF7 and ARF19 activity during Arabidopsis lateral root initiation. Plant J 48:380–389PubMedCrossRefGoogle Scholar
  9. Gray WM, Kepinski S, Rouse D, Leyser O, Estelle M (2001) Auxin regulates SCF(TIR1)-dependent degradation of AUX/IAA proteins. Nature 414:271–276PubMedCrossRefGoogle Scholar
  10. Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10:453–460PubMedCrossRefGoogle Scholar
  11. Hamann T, Benkova E, Baurle I, Kientz M, Jurgens G (2002) The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. Genes Dev 16:1610–1615PubMedCrossRefGoogle Scholar
  12. Hu YQ, Liu S, Yuan HM, Li J, Yan DW, Zhang JF, Lu YT (2010) Functional comparison of catalase genes in the elimination of photorespiratory H2O2 using promoter- and 3′-untranslated region exchange experiments in the Arabidopsis cat2 photorespiratory mutant. Plant, Cell Environ 33:1656–1670CrossRefGoogle Scholar
  13. Ishiguro S, Kawai-Oda A, Ueda J, Nishida I, Okada K (2001) The DEFECTIVE IN ANTHER DEHISCIENCE gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis. Plant Cell 13:2191–2209PubMedGoogle Scholar
  14. Kim BC, Soh MC, Kang BJ, Furuya M, Nam HG (1996) Two dominant photomorphogenic mutations of Arabidopsis thaliana identified as suppressor mutations of hy2. Plant J 9:441–456PubMedCrossRefGoogle Scholar
  15. Liechti R, Farmer EE (2006) Jasmonate biochemical pathway. Sci STKE, issue 322, P. m3Google Scholar
  16. Liscum E, Reed JW (2002) Genetics of Aux/IAA and ARF action in plant growth and development. Plant Mol Biol 49:387–400PubMedCrossRefGoogle Scholar
  17. Llorente F, Muskett P, Sanchez-Vallet A, Lopez G, Ramos B, Sanchez-Rodriguez C, Jorda L, Parker J, Molina A (2008) Repression of the auxin response pathway increases Arabidopsis susceptibility to necrotrophic fungi. Mol Plant 1:496–509PubMedCrossRefGoogle Scholar
  18. Mockaitis K, Estelle M (2008) Auxin receptors and plant development: a new signaling paradigm. Annu Rev Cell Dev Biol 24:55–80PubMedCrossRefGoogle Scholar
  19. Muto H, Nagao I, Demura T, Fukuda H, Kinjo M, Yamamoto KT (2006) Fluorescence cross-correlation analyses of the molecular interaction between an Aux/IAA protein, MSG2/IAA19, and protein–protein interaction domains of auxin response factors of Arabidopsis expressed in HeLa cells. Plant Cell Physiol 47:1095–1101PubMedCrossRefGoogle Scholar
  20. Nagpal P, Walker LM, Young JC, Sonawala A, Timpte C, Estelle M, Reed JW (2000) AXR2 encodes a member of the Aux/IAA protein family. Plant Physiol 123:563–574PubMedCrossRefGoogle Scholar
  21. 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 132:4107–4118PubMedCrossRefGoogle Scholar
  22. Oono Y, Ooura C, Uchimiya H (2002) Expression pattern of Aux/IAA genes in the iaa3/shy2-1D mutant of Arabidopsis thaliana (L.). Ann Bot 89:77–82PubMedCrossRefGoogle Scholar
  23. Ouellet F, Overvoorde PJ, Theologis A (2001) IAA17/AXR3: biochemical insight into an auxin mutant phenotype. Plant Cell 13:829–841PubMedGoogle Scholar
  24. Pan X, Welti R, Wang X (2010) Quantitative analysis of major plant hormones in crude plant extracts by high-performance liquid chromatography-mass spectrometry. Nat Protoc 5:986–992PubMedCrossRefGoogle Scholar
  25. Pekker I, Alvarez JP, Eshed Y (2005) Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity. Plant Cell 17:2899–2910PubMedCrossRefGoogle Scholar
  26. Ploense SE, Wu MF, Nagpal P, Reed JW (2009) A gain-of-function mutation in IAA18 alters Arabidopsis embryonic apical patterning. Development 136:1509–1517PubMedCrossRefGoogle Scholar
  27. Ramos JA, Zenser N, Leyser O, Callis J (2001) Rapid degradation of auxin/indoleacetic acid proteins requires conserved amino acids of domain II and is proteasome dependent. Plant Cell 13:2349–2360PubMedGoogle Scholar
  28. Reed JW (2001) Roles and activities of Aux/IAA proteins in Arabidopsis. Trends Plant Sci 6:420–425PubMedCrossRefGoogle Scholar
  29. Reeves PH, Ellis CM, Ploense SE, Wu MF, Yadav V, Tholl D, Chetelat A, Haupt I, Kennerley BJ, Hodgens C, Farmer EE, Nagpal P, Reed JW (2012) A regulatory network for coordinated flower maturation. PLoS Genet 8:e1002506PubMedCrossRefGoogle Scholar
  30. Remington DL, Vision TJ, Guilfoyle TJ, Reed JW (2004) Contrasting modes of diversification in the Aux/IAA and ARF gene families. Plant Physiol 135:1738–1752PubMedCrossRefGoogle Scholar
  31. Rinaldi MA, Liu J, Enders TA, Bartel B, Strader LC (2012) A gain-of-function mutation in IAA16 confers reduced responses to auxin and abscisic acid and impedes plant growth and fertility. Plant Mol Biol 79(4–5):359–373Google Scholar
  32. Rogg LE, Lasswell J, Bartel B (2001) A gain-of-function mutation in IAA28 suppresses lateral root development. Plant Cell 13:465–480PubMedGoogle Scholar
  33. Rouse D, Mackay P, Stirnberg P, Estelle M, Leyser O (1998) Changes in auxin response from mutations in an AUX/IAA gene. Science 279:1371–1373PubMedCrossRefGoogle Scholar
  34. Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Scholkopf B, Weigel D, Lohmann JU (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37:501–506PubMedCrossRefGoogle Scholar
  35. Tabata R, Ikezaki M, Fujibe T, Aida M, Tian CE, Ueno Y, Yamamoto KT, Machida Y, Nakamura K, Ishiguro S (2010) Arabidopsis auxin response factor 6 and 8 regulate jasmonic acid biosynthesis and floral organ development via repression of class 1 KNOX genes. Plant Cell Physiol 51:164–175PubMedCrossRefGoogle Scholar
  36. Tatematsu K, Kumagai S, Muto H, Sato A, Watahiki MK, Harper RM, Liscum E, Yamamoto KT (2004) MASSUGU2 encodes Aux/IAA19, an auxin-regulated protein that functions together with the transcriptional activator NPH4/ARF7 to regulate differential growth responses of hypocotyl and formation of lateral roots in Arabidopsis thaliana. Plant Cell 16:379–393PubMedCrossRefGoogle Scholar
  37. Thakur JK, Jain M, Tyagi AK, Khurana JP (2005) Exogenous auxin enhances the degradation of a light down-regulated and nuclear-localized OsiIAA1, an Aux/IAA protein from rice, via proteasome. Biochim Biophys Acta 1730:196–205PubMedCrossRefGoogle Scholar
  38. Tian Q, Reed JW (1999) Control of auxin-regulated root development by the Arabidopsis thaliana SHY2/IAA3 gene. Development 126:711–721PubMedGoogle Scholar
  39. Tiwari SB, Hagen G, Guilfoyle TJ (2004) Aux/IAA proteins contain a potent transcriptional repression domain. Plant Cell 16:533–543PubMedCrossRefGoogle Scholar
  40. 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 9:1963–1971PubMedGoogle Scholar
  41. Ulmasov T, Hagen G, Guilfoyle TJ (1999a) Activation and repression of transcription by auxin-response factors. Proc Natl Acad Sci USA 96:5844–5849PubMedCrossRefGoogle Scholar
  42. Ulmasov T, Hagen G, Guilfoyle TJ (1999b) Dimerization and DNA binding of auxin response factors. Plant J 19:309–319PubMedCrossRefGoogle Scholar
  43. Vernoux T, Brunoud G, Farcot E, Morin V, Van den Daele H, Legrand J, Oliva M, Das P, Larrieu A, Wells D, Guedon Y, Armitage L, Picard F, Guyomarc’h S, Cellier C, Parry G, Koumproglou R, Doonan JH, Estelle M, Godin C, Kepinski S, Bennett M, De Veylder L, Traas J (2011) The auxin signalling network translates dynamic input into robust patterning at the shoot apex. Mol Syst Biol 7:508PubMedCrossRefGoogle Scholar
  44. Walter M, Chaban C, Schutze K, Batistic O, Weckermann K, Nake C, Blazevic D, Grefen C, Schumacher K, Oecking C, Harter K, Kudla J (2004) Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J 40:428–438PubMedCrossRefGoogle Scholar
  45. Weijers D, Benkova E, Jager KE, Schlereth A, Hamann T, Kientz M, Wilmoth JC, Reed JW, Jurgens G (2005) Developmental specificity of auxin response by pairs of ARF and Aux/IAA transcriptional regulators. EMBO J 24:1874–1885PubMedCrossRefGoogle Scholar
  46. Weijers D, Schlereth A, Ehrismann JS, Schwank G, Kientz M, Jurgens G (2006) Auxin triggers transient local signaling for cell specification in Arabidopsis embryogenesis. Dev Cell 10:265–270PubMedCrossRefGoogle Scholar
  47. Wu MF, 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
  48. Yang X, Lee S, So JH, Dharmasiri S, Dharmasiri N, Ge L, Jensen C, Hangarter R, Hobbie L, Estelle M (2004) The IAA1 protein is encoded by AXR5 and is a substrate of SCF(TIR1). Plant J 40:772–782PubMedCrossRefGoogle Scholar
  49. Zenser N, Ellsmore A, Leasure C, Callis J (2001) Auxin modulates the degradation rate of Aux/IAA proteins. Proc Natl Acad Sci USA 98:11795–11800PubMedCrossRefGoogle Scholar
  50. Zenser N, Dreher KA, Edwards SR, Callis J (2003) Acceleration of Aux/IAA proteolysis is specific for auxin and independent of AXR1. Plant J 35:285–294PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Jing Wang
    • 1
  • Da-Wei Yan
    • 1
  • Ting-Ting Yuan
    • 1
  • Xiang Gao
    • 1
  • Ying-Tang Lu
    • 1
    Email author
  1. 1.State Key Laboratory of Hybrid Rice, College of Life SciencesWuhan UniversityWuhanChina

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