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SPL8, a local regulator in a subset of gibberellin-mediated developmental processes in Arabidopsis

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Abstract

Gibberellins (GAs) are important plant growth regulators, regulating many plant developmental processes, including seed germination, root and stem elongation, rosette expansion, floral induction and anther development. The diverse effects of GAs on plant development make it critical to maintain an appropriate endogenous GA level and a fine-tuned GA signalling. Some global regulators in GA signalling have been identified but little is known about genes specifically involved in local implementation of GA signalling. Here we report that the Arabidopsis thaliana SBP-box gene SQUAMOSA-PROMOTER-BINDING-PROTEIN-LIKE8 (SPL8) acts as a local regulator in a subset of GA-dependent developmental processes. Previous knowledge holds that SPL8 is involved in reproductive development as deduced from its loss-of-function phenotype (Unte et al. (2003) Plant Cell 15:1009–1019). We now determined that constitutive overexpression of SPL8 affects fertility due to non-dehiscent anthers, likely resulting from a constitutive GA response, suggesting a positive role of SPL8 in GA-mediated anther development. On the other hand, SPL8 gain- and loss-of-function mutants showed opposite responses to GA and its biosynthetic inhibitor paclobutrazol (PAC) with respect to seed germination and root elongation during the seedling stage. Genes involved in GA biosynthesis and signalling are transcriptionally affected by altered SPL8 expression. Our study uncovered a tissue-dependent regulatory role for SPL8 in the response to GA signalling in plant development.

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Abbreviations

GA:

Gibberellic acid

PAC:

Paclobutrazol

JA:

Jasmonate

MeJA:

Methyl jasmonate

DAG:

Days after germination

References

  • Bikenbihl RP, Jach G, Saedler H, Huijser P (2005) Functional dissection of the plant-specific SBP-domain: overlap of the DNA-binding and nuclear localization domains. J Mol Biol 352:585–596

    Article  CAS  Google Scholar 

  • Cardon GH, Höhmann S, Klein J, Nettesheim K, Saedler H, Huijser P (1999) Molecular characterisation of the Arabidopsis SBP-box genes. Gene 237:91–104

    Article  PubMed  CAS  Google Scholar 

  • Cheng H, Qin L, Lee S, Fu X, Richards DE, Cao D, Luo D, Harberd NP, Peng J (2004) Gibberellin regulates Arabidopsis floral development via suppression of DELLA protein function. Development 131:1055–1064

    Article  PubMed  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  PubMed  CAS  Google Scholar 

  • Colombo N, Favret EA (1996) The effect of gibberellic acid on male fertility in bread wheat. Euphytica 91:297–303

    Article  CAS  Google Scholar 

  • Cowling RJ, Kamiya Y, Seto H, Harberd NP (1998) Gibberellin dose-response regulation of GA4 gene transcript levels in Arabidopsis. Plant Physiol 117:1195–1203

    Article  PubMed  CAS  Google Scholar 

  • Dill A, Thomas SG, Hu J, Steber CM, Sun TP (2004) The Arabidopsis F-box protein SLEEPY1 targets gibberellin signalling repressors for gibberellin-induced degradation. Plant Cell 16:1392–1405

    Article  PubMed  CAS  Google Scholar 

  • Filardo FF, Swain SM (2003) SPYing on GA signalling and plant development. J Plant Growth Regul 22:163–175

    Article  CAS  Google Scholar 

  • Fleet CM, Sun TP (2005) A DELLAcate balance: the role of gibberellin in plant organogenesis. Curr Opin Plant Biol 8:77–85

    Article  PubMed  CAS  Google Scholar 

  • Fridborg I, Kuusk S, Moritz T, Sundberg E (1999) The Arabidopsis dwarf mutant shi exhibits reduced gibberellin responses conferred by overexpression of a new putative zinc finger protein. Plant Cell 11:1019–1031

    Article  PubMed  CAS  Google Scholar 

  • Fu X, Harberd NP (2003) Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421:740–743

    Article  PubMed  CAS  Google Scholar 

  • Fu X, Richards DE, Fleck B, Xie D, Burton N, Harberd NP (2004) The Arabidopsis mutant sleepy1gar2-1 protein promotes plant growth by increasing the affinity of the SCFSLY1 E3 ubiquitin ligase for DELLA protein substrates. Plant Cell 16:1406–1418

    Article  PubMed  CAS  Google Scholar 

  • Hay A, Kaur H, Phillips A, Hedden P, Hake S, Tsiantis M (2002) The gibberellin pathway mediates KNOTTED1-type homeobox function in plants with different body plans. Curr Biol 12:1557–1565

    Article  PubMed  CAS  Google Scholar 

  • Hedden P, Phillips AL (2000) Gibberellin metabolism: new insights revealed by the genes. Trends Plant Sci 5:523–530

    Article  PubMed  CAS  Google Scholar 

  • Huang S, Cerny RE, Qi Y, Bhat D, Aydt CM, Hanson DD, Malloy KP, Ness LA (2003) Transgenic studies on the involvement of cytokinin and gibberellin in male development. Plant Physiol 131:1270–1282

    Article  PubMed  CAS  Google Scholar 

  • Ikeda A, Ueguchi-Tanaka M, Sonoda Y, Kitano H, Koshioka M, Futsuhara Y, Matsuoka M, Yamaguchi J (2001) slender rice, a constitutive gibberellin response mutant is caused by a null mutation of the SLR1 gene, an orthologue of the height-regulating gene GAI/RGA/RHT/D8. Plant Cell 13:999–1010

    Article  PubMed  CAS  Google Scholar 

  • Izhaki A, Borochov A, Zamski E, Weiss D (2002) Gibberellin regulates post-microsporogenesis processes in petunia anthers. Physiol Plant 115:442–447

    Article  PubMed  CAS  Google Scholar 

  • Jacobsen SE, Olszewski NE (1991) Characterization of the arrest in anther development associated with gibberellin deficiency of the gib-1 mutant of tomato. Plant Physiol 97:409–414

    Article  PubMed  CAS  Google Scholar 

  • Jacobsen SE, Olszewski NE (1993) Mutations at the SPINDLY locus of Arabidopsis alter gibberellin signal transduction. Plant Cell 5:887–896

    Article  PubMed  CAS  Google Scholar 

  • Koornneef M, Van der Veen JH (1980) Induction and analysis of gibberellin-sensitive mutants in Arabidopsis thaliana (L.) heynh. Theor Appl Genet 58:257–263

    Article  Google Scholar 

  • Lee S, Cheng H, King KE, Wang W, He Y, Hussain A, Lo J, Harberd NP, Peng J (2002) Gibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following imbibition. Genes Dev 16:646–658

    Article  PubMed  CAS  Google Scholar 

  • Magome H, Yamaguchi S, Hanada A, Kamiya Y, Oda K (2004) dwarf and delayed-flowering 1, a novel Arabidopsis mutant deficient in gibberellin biosynthesis because of overexpression of a putative AP2 transcription factor. Plant J 37:720–729

    Article  PubMed  CAS  Google Scholar 

  • McGinnis KM, Thomas SG, Soule JD, Strader LC, Zale JM, Sun TP, Steber CM (2003) The Arabidopsis SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell 15:1120–1130

    Article  PubMed  CAS  Google Scholar 

  • Meier C, Bouquin T, Nielsen ME, Raventos D, Mattsson O, Rocher A, Schomburg F, Amasino RM, Mundy J (2001) Gibberellin response mutants identified by luciferase imaging. Plant J 25:509–519

    Article  PubMed  CAS  Google Scholar 

  • Murray F, Kalla R, Jacobsen J, Gubler F (2003) A role for HvGAMYB in anther development. Plant J 33:481–491

    Article  PubMed  CAS  Google Scholar 

  • Olszewski N, Sun TP, Gubler F (2002) Gibberellin Signalling: biosynthesis, catabolism, and response pathways. Plant Cell 14:S61–S80

    PubMed  CAS  Google Scholar 

  • Peng J, Carol P, Richards DE, King KE, Cowling RJ, Murphy GP, Harberd NP (1997) The Arabidopsis GAI gene defines a signalling pathway that negatively regulates gibberellin responses. Genes Dev 11:3194–3205

    PubMed  CAS  Google Scholar 

  • Perazza D, Vachon G, Herzog M (1998) Gibberellins promote trichome formation by up-regulating GLABROUS1 in Arabidopsis. Plant Physiol 117:375–383

    Article  PubMed  CAS  Google Scholar 

  • Regan SM, Moffatt BA (1990) Cytochemical analysis of pollen development in wild-type Arabidopsis and a male-sterile mutant. Plant Cell 2:877–889

    Article  PubMed  CAS  Google Scholar 

  • Rieu I, Wolters-Arts M, Derksen J, Mariani C, Weterings K (2003) Ethylene regulates the timing of anther dehiscence in tobacco. Planta 217:131–137

    PubMed  CAS  Google Scholar 

  • Ross JJ (1994) Recent advances in the study of gibberellin mutants. Plant Growth Regul 15:193–206

    Article  CAS  Google Scholar 

  • Sanders PM, Bui AQ, Weterings K, McIntire KN, Hsu YC, Lee PY, Truong MT, Beals TP, Goldberg RB (1999) Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex Plant Reprod 11:297–322

    Article  CAS  Google Scholar 

  • Scott RJ, Spielman M, Dickinson HG (2004) Stamen structure and function. Plant Cell 16:S46–S60

    Article  PubMed  CAS  Google Scholar 

  • Sorensen A, Guerineau F, Canales-Holzeis C, Dickinson HG, Scott RJ (2002) A novel extinction screen in Arabidopsis thaliana identifies mutant plants defective in early microsporangial development. Plant J 29:581–594

    Article  PubMed  CAS  Google Scholar 

  • Steber CM, Cooney SE, McCourt P (1998) Isolation of the GA-response mutant sly1 as a suppressor of ABI1-1 in Arabidopsis thaliana. Genetics 149:509–521

    PubMed  CAS  Google Scholar 

  • Tyler L, Thomas SG, Hu J, Dill A, Alonso JM, Ecker JR, Sun TP (2004) DELLA proteins and gibberellin-regulated seed germination and floral development in Arabidopsis. Plant Physiol 135:1008–1019

    Article  PubMed  CAS  Google Scholar 

  • Ueguchi-Tanaka M, Ashikari M, Nakajima M, Itoh H, Katoh E, Kobayashi M, Chow T, Hsing YC, Kitano H, Yamaguchi I, Matsuoka M (2005) GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437:693–698

    Article  PubMed  CAS  Google Scholar 

  • Unte US, Sorensen AM, Pesaresi P, Gandikota M, Leister D, Saedler H, Huijser P (2003) SPL8, an SBP-box gene that affects pollen sac development in Arabidopsis. Plant Cell 15:1009–1019

    Article  PubMed  CAS  Google Scholar 

  • Xu YL, Li L, Gage DA, Zeevaart JAD (1999) Feedback regulation of GA5 expression and metabolic engineering of gibberellin levels in Arabidopsis. Plant Cell 11:927–935

    Article  PubMed  CAS  Google Scholar 

  • Zhu QH, Ramm K, Shivakkumar R, Dennis ES, Upadhyaya NM (2004) The ANTHER INDEHISCENCE1 gene encoding a single MYB domain protein is involved in anther development in rice. Plant Physiol 135:1514–1525

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to Susanne Höhmann for excellent technical support and Sandra Kröber for assistance in making semi-thin sections for studying anther histology. We thank Guido Jach for providing the binary vectors pGJ2148 and pGJ2171. We also thank our colleagues in the department for helpful discussions and Sabine Zachgo in particular for critically reading the manuscript. Y.Z. was supported by an International Max-Planck Research School stipend.

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Author notes

  1. Yan Zhang

    Present address: Plant Gene Expression Center, UC Berkeley, 800 Buchanan St., Albany, CA, 94710, USA

Authors and Affiliations

  1. Department of Molecular Plant Genetics, Max Planck Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, 50829, Cologne, Germany

    Yan Zhang, Stefan Schwarz, Heinz Saedler & Peter Huijser

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  1. Yan Zhang
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  2. Stefan Schwarz
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  3. Heinz Saedler
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  4. Peter Huijser
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Correspondence to Peter Huijser.

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Zhang, Y., Schwarz, S., Saedler, H. et al. SPL8, a local regulator in a subset of gibberellin-mediated developmental processes in Arabidopsis. Plant Mol Biol 63, 429–439 (2007). https://doi.org/10.1007/s11103-006-9099-6

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