Abstract
We generated 12 different mutations in the grape Gibberellin Insensitive1 (VvGAI1) sequences, transformed them into Arabidopsis under the control of 35S, Arabidopsis GAI or grape GAI1 promoter, and evaluated the impact of these mutant alleles on plant growth and development. These VvGAI1 sequence variants included some mimics of the known GAI-like mutant alleles discovered in grape, wheat, barley, corn, Brassica, and Arabidopsis. In general, plant height and related traits such as length of internodes and inflorescences were significantly reduced for most of the mutant alleles studied, regardless of which promoter was used. Interestingly, the numbers of rosette leaves and lateral branches were generally reduced when a 35S promoter was used to express the mutant alleles, but increased when an Arabidopsis or grape GAI promoter was used. Furthermore, the 35S plants often displayed curly and small leaves. In contrast, the leaves of the plants carrying mutant alleles controlled by a GAI promoter were of variable size, dark green and rarely curly. In addition, when certain VvGAI1 mutant alleles were under the control of the grape GAI1 promoter, the number of pods on inflorescences was significantly increased, but some of the pods produced few seeds due to partial sterility. On the basis of the systematic evaluation of various VvGAI1 mutant alleles in Arabidopsis, we concluded that the VvGAI1 mutant alleles mimicking the GAI or GAI-like mutant variants discovered in wheat, barley and Brassica could potentially be useful for the improvement of grapevine plant architecture.
Similar content being viewed by others
References
Achard P, Gusti A, Cheminant S, Alioua M, Dhondt S, Coppens F, Beemster GT, Genschik P (2009) Gibberellin signaling controls cell proliferation rate in Arabidopsis. Curr Biol 19:1188–1193
Asano K, Hirano K, Ueguchi-Tanaka M, Angeles-Shim RB, Komura T, Satoh H, Kitano H, Matsuoka M, Ashikari M (2009) Isolation and characterization of dominant dwarf mutants, Slr1-d, in rice. Mol Genet Genomics 281:223–231
Boss PK, Thomas MR (2002) Association of dwarfism and floral induction with a grape ‘green revolution’ mutation. Nature 416:847–850
Boss PK, Buckeridge EJ, Poole A, Thomas MR (2003) New insights into grapevine flowering. Funct Plant Biol 30:593–606
Busov V, Meilan R, Pearce DW, Rood SB, Ma C, Tschaplinski TJ, Strauss SH (2006) Transgenic modification of gai or rgl1 causes dwarfing and alters gibberellins, root growth, and metabolite profiles in Populus. Planta 224:288–299
Chandler PM, Marion-Poll A, Ellis M, Gubler F (2002) Mutants at the Slender1 locus of barley cv Himalaya. Molecular and physiological characterization. Plant Physiol 129:181–190
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
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743
Coles JP, Phillips AL, Croker SJ, Garcia-Lepe R, Lewis MJ, Hedden P (1999) Modification of gibberellin production and plant development in Arabidopsis by sense and antisense expression of gibberellin 20-oxidase genes. Plant J 17:547–556
Fleck B, Harberd NP (2002) Evidence that the Arabidopsis nuclear gibberellin signalling protein GAI is not destabilised by gibberellin. Plant J 32:935–947
Fu X, Sudhakar D, Peng J, Richards DE, Christou P, Harberd NP (2001) Expression of Arabidopsis GAI in transgenic rice represses multiple gibberellin responses. Plant Cell 13:1791–1802
Gou J, Ma C, Kadmiel M, Gai Y, Strauss S, Jiang X, and Busov V (2011) Tissue-specific expression of Populus C19 GA 2-oxidases differentially regulate above- and below-ground biomass growth through control of bioactive GA concentrations. New Phytologist. doi:10.1111/j.1469-8137.2011.03837.x
Harberd NP, Freeling M (1989) Genetics of dominant gibberellin-insensitive dwarfism in maize. Genetics 121:827–838
Harberd NP, Belfield E, Yasumura Y (2009) The angiosperm gibberellin-GID1-DELLA growth regulatory mechanism: how an “inhibitor of an inhibitor” enables flexible response to fluctuating environments. Plant Cell 21:1328–1339
Hynes LW, Peng J, Richards DE, Harberd NP (2003) Transgenic expression of the Arabidopsis DELLA proteins GAI and gai confers altered gibberellin response in tobacco. Transgenic Res 12:707–714
Itoh H, Shimada A, Ueguchi-Tanaka M, Kamiya N, Hasegawa Y, Ashikari M, Matsuoka M (2005) Overexpression of a GRAS protein lacking the DELLA domain confers altered gibberellin responses in rice. Plant J 44:669–679
Itoh H, Ueguchi-Tanaka M, Matsuoka M (2008) Molecular biology of gibberellins signaling in higher plants. Int Rev Cell Mol Biol 268:191–221
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
Koornneef M, Elgersma A, Hanhart CJ, van Loenen-Martinet EP, van Rijn L, Zeevaart JAD (1985) A gibberellin insensitive mutant of Arabidopsis thaliana. Physiol Plant 65:33–39
Liu C, Wang J, Huang T, Wang F, Yuan F, Cheng X, Zhang Y, Shi S, Wu J, Liu K (2010) A missense mutation in the VHYNP motif of a DELLA protein causes a semi-dwarf mutant phenotype in Brassica napus. Theor Appl Genet 121:249–258
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
Muangprom A, Thomas SG, Sun TP, Osborn TC (2005) A novel dwarfing mutation in a green revolution gene from Brassica rapa. Plant Physiol 137:931–938
Murase K, Hirano Y, Sun TP, Hakoshima T (2008) Gibberellin-induced DELLA recognition by the gibberellin receptor GID1. Nature 456:459–463
Nakagawa T, Suzuki T, Murata S, Nakamura S, Hino T, Maeo K, Tabata R, Kawai T, Tanaka K, Niwa Y et al (2007) Improved Gateway binary vectors: high-performance vectors for creation of fusion constructs in transgenic analysis of plants. Biosci Biotechnol Biochem 71:2095–2100
Nakajima M, Shimada A, Takashi Y, Kim YC, Park SH, Ueguchi-Tanaka M, Suzuki H, Katoh E, Iuchi S, Kobayashi M et al (2006) Identification and characterization of Arabidopsis gibberellin receptors. Plant J 46:880–889
Olszewski N, Sun TP, Gubler F (2002). Gibberellin signaling: biosynthesis, catabolism, and response pathways. Plant Cell 14(Suppl):S61–S80
Peng J, Harberd NP (1993) Derivative alleles of the Arabidopsis gibberellin-insensitive (gai) mutation confer a wild-type phenotype. Plant Cell 5:351–360
Peng J, Carol P, Richards DE, King KE, Cowling RJ, Murphy GP, Harberd NP (1997) The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes Dev 11:3194–3205
Peng J, Richards DE, Hartley NM, Murphy GP, Devos KM, Flintham JE, Beales J, Fish LJ, Worland AJ, Pelica F et al (1999a) ‘Green revolution’ genes encode mutant gibberellin response modulators. Nature 400:256–261
Peng J, Richards DE, Moritz T, Cano-Delgado A, Harberd NP (1999b) Extragenic suppressors of the Arabidopsis gai mutation alter the dose-response relationship of diverse gibberellin responses. Plant Physiol 119:1199–1208
Sasaki A, Ashikari M, Ueguchi-Tanaka M, Itoh H, Nishimura A, Swapan D, Ishiyama K, Saito T, Kobayashi M, Khush GS et al (2002) Green revolution: a mutant gibberellin-synthesis gene in rice. Nature 416:701–702
Sasaki A, Itoh H, Gomi K, Ueguchi-Tanaka M, Ishiyama K, Kobayashi M, Jeong DH, An G, Kitano H, Ashikari M et al (2003) Accumulation of phosphorylated repressor for gibberellin signaling in an F-box mutant. Science 299:1896–1898
Silverstone AL, Ciampaglio CN, Sun T (1998) The Arabidopsis RGA gene encodes a transcriptional regulator repressing the gibberellin signal transduction pathway. Plant Cell 10:155–169
Spielmeyer W, Ellis MH, Chandler PM (2002) Semidwarf (sd-1), “green revolution” rice, contains a defective gibberellin 20-oxidase gene. Proc Natl Acad Sci USA 99:9043–9048
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
Ueguchi-Tanaka M, Ashikari M, Nakajima M, Itoh H, Katoh E, Kobayashi M, Chow TY, Hsing YI, Kitano H, Yamaguchi I et al (2005) GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437:693–698
Ueguchi-Tanaka M, Nakajima M, Katoh E, Ohmiya H, Asano K, Saji S, Hongyu X, Ashikari M, Kitano H, Yamaguchi I et al (2007) Molecular interactions of a soluble gibberellin receptor, GID1, with a rice DELLA protein, SLR1, and gibberellin. Plant Cell 19:2140–2155
Wen CK, Chang C (2002) Arabidopsis RGL1 encodes a negative regulator of gibberellin responses. Plant Cell 14:87–100
Weston DE, Elliott RC, Lester DR, Rameau C, Reid JB, Murfet IC, Ross JJ (2008) The Pea DELLA proteins LA and CRY are important regulators of gibberellin synthesis and root growth. Plant Physiol 147:199–205
Willige BC, Ghosh S, Nill C, Zourelidou M, Dohmann EM, Maier A, Schwechheimer C (2007) The DELLA domain of GA INSENSITIVE mediates the interaction with the GA INSENSITIVE DWARF1A gibberellin receptor of Arabidopsis. Plant Cell 19:1209–1220
Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol 59:225–251
Yang Y, Zhong G-Y (2011) Characterization of the grape GAI promoter in Arabidopsis. In: The proceedings of the 10th international conference on grapevine breeding and genetics, the Acta Horticulturae proceedings (in press)
Zhu LH, Li XY, Welander M (2008) Overexpression of the Arabidopsis gai gene in apple significantly reduces plant size. Plant Cell Rep 27:289–296
Acknowledgments
We would like to thank Dr. Joanne Labate of USDA-Agriculture Research Service Plant Genetic Resources Unit, Geneva, New York for reviewing the manuscript and Dr. Tsuyoshi Nakagawa for providing us the pGWB502Ω gateway binary vector for this study. USDA is an equal opportunity provider and employer.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Zhong, GY., Yang, Y. Characterization of grape Gibberellin Insensitive1 mutant alleles in transgenic Arabidopsis . Transgenic Res 21, 725–741 (2012). https://doi.org/10.1007/s11248-011-9565-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11248-011-9565-z