doi: 10.15389/agrobiology.2016.5.571eng
UDC 631.523/.524:581.14:575.1
Acknowledgements:
We are grateful to Dr. O.V. Tankelyun (St. Petersburg State University) for reading the manuscript and helpful comments.
Supported by grant from Russian Science Foundation (project № 16-16-00026)
MOLECULAR BASIS OF THE DWARFISM CHARACTER IN CULTIVATED PLANTS. II. DELLA-PROTEINS: STRUCTURE AND FUNCTIONS (review)
T.E. Bilova1, D.N. Ryabova2, I.N. Anisimova2
1Saint Petersburg State University, 7-9, Universitetskaya nab., St. Petersburg, 199034 Russia,
e-mail bilova.tati-ana@gmail.com;
2Federal Research Center the N.I. Vavilov All-Russian Institute of Plant Genetic Resources, Federal Agency of Scientific Organizations, 42-44, ul. Bol’shaya Morskaya, St. Petersburg, 190000 Russia,
e-mail rdash@mail.ru, irina_ani-simova@inbox.ru
Received January 25, 2016
The wheat gene Rht (Reduced height) which predeterminated the success of «Green revolution» and has been employed in creation of plant varieties with reduced stem elongation and resistant to stem lodging, encodes a protein containing highly conserved DELLA domain (J. Peng et al., 1999). Many other high-yield dwarf varieties also possess mutations in the genes coding DELLA proteins. Since the mutations did not affect viability and reproducibility of the plants the usage of the mutations for advanced plant breeding might be very promising (M. Ueguchi-Tanaka et al., 2007). Along with dwarfism, some mutations in the genes can lead to an opposite phenotype: to tall plants with spindly stems, the so called slender forms. What phenotype (dwarf or slender plant) would be developed depends on functionality of a protein region affected by the mutation. The paper considers in depth structure, posttranslational modifications, cellular localization and functions of DELLA proteins. The proteins being participants of complex protein-protein interactions play a role of repressors in gibberellin (GA) signal transduction. In the absence/or small concentration of GA DELLA proteins interact with specific transcriptional factor (TF) targets blocking their DNA binding activity and as a result restrain plant growth. In the presence of GA stem elongation is activated because this hormone promotes destabilization of DELLA proteins, releasing TF from their repression. Thus, restrained growth of the rht mutant as well as other naturally occurring dwarf plants is associated with accumulation of DELLA proteins in a result of their high stability. In turn, enhanced stability of the proteins can be caused by mutations in functionally important domains of either DELLA proteins or other players of GA signaling such as receptor GID1 and F-box proteins (GID2 in rice; SLY1 in Arabidopsis) of E3-ubiqutin protein ligase. They all participate in complex protein-protein interaction which is necessary for DELLA protein degradation via 26S-proteasome pathway (B.C. Willige et al., 2007; K. Hirano et al., 2010). The paper reviews a role of different functional motifs of DELLA protein in transduction of GA signal: DELLA, TVHYNP, polySTV on N-terminal part of a molecule and С-terminal GRAS-domain, containing the motifs LR, VHIID, PFYRE and SAW. DELLA-proteins possess no DNA-binding site. Most probably their repressive function is associated with GRAS-domain via protein-protein interaction of LR region with target TFs (R. Zentella et al., 2007; K. Hirano et al., 2010). The polySTV domain plays a regulator role. Post-transcriptional modifications in the region are potentially able to change partners in protein-protein interaction and/or cellular localization of the DELLA proteins (M. Ueguchi-Tanaka et al., 2005; K. Hirano et al., 2010). A function of DELLA protein as an integrator of hormone signal ways and external factors is also discussed. In the context the DELLA proteins are considered as «correctors» of plant growth reaction depending on growth conditions (X.-H. Gao et al., 2011). Thus, the activity of DELLA proteins might underlie the plant phenotypic flexibility and promotes restrained plant growth under unfavorable environmental conditions.
Keywords: dwarfism, retard growth, gibberellin signal transduction, DELLA protein, repression function, proteolysis.
REFERENCES
- Ueguchi-Tanaka M., Nakajima M., Motoyuki A., Matsuoka M. Gibberellin receptor and its role in gibberellin signaling in plants. Annu. Rev. Plant Biol., 2007, 58(1): 183-198 CrossRef
- Peng J., Richards D.E., Hartley N.M., Murphy G.P., Devos K.M., Flintham J.E., Beales J., Fish L.J., Worland A.J., Pelica F., Sudhakar D., Christou P., Spape J.W., Gale M.D., Harberd N.P. «Green Revolution» genes encode mutant gibberellin response modulators. Nature, 1999, 400(6741): 256-261 CrossRef
- Kulaeva O.N. Sorosovskii obrazovatel'nyi zhurnal, 2000, 6(8): 18-23 (in Russ.).
- Achard P., Renou J.P., Berthome R., Harberd N.P., Genschik P. Plant DELLAs restrain growth and promote survival of adversity by reducing the levels of reactive oxygen species. Curr. Biol., 2008, 18(9): 656-660 CrossRef
- Hirano K., Asano K., Tsuji H., Kawamura M., Mori H., Kitano H., Ueguchi-Tanaka M., Matsuoka M. Characterization of the molecular mechanism underlying gibberellin perception complex formation in rice. Plant Cell, 2010, 22(8): 2680-2696 CrossRef
- Chen J., Cheng T., Wang P., Tian L., Wang G., Luo Y., Wang J., Yang L., Shi J. Genome-wide bioinformatics analysis of DELLA-family proteins from plants. Plant Omics, 2013, 6(3): 201-207.
- Achard P., Genschik P. Releasing the brakes of plant growth: how GAs shutdown DELLA proteins. J. Exp. Bot., 2009, 60(4): 1085-1092 CrossRef
- Wang F., Zhu D., Huang X., Li S., Gong Y., Yao Q., Fu X., Fan L.-M., Deng X.W. Biochemical insights on degradation of Arabidopsis DELLA proteins gained from a cell-free assay system. Plant Cell, 2009, 21: 2378-2390 CrossRef
- Winkler R.G., Freeling M. Physiological genetics of the dominant gibberellin-nonresponsive maize dwarfs, Dwarf8 and Dwarf9. Planta,1994, 193(3): 341-348 CrossRef
- Lawit S.J., Wych H.M., Xu D., Kundu S., Tomes D.T. Maize DELLA proteins Dwarf plant8 and Dwarf plant9 as modulators of plant development. Plant Cell Physiol., 2010, 51(11): 1854-1868 CrossRef
- Pearce S., Saville R., Vaughan S.P., Chandler P.M., Wilhelm E.P., Sparks A.C., Al-Caff N., Korolev A., Boulton M.I., Phillips A.L., Hedden P., Nicholson P., Thomas S.G. Molecular characterization of Rht-1 dwarfing genes in hexaploid wheat. Plant Physiol., 2011, 157(4): 1820-1831 CrossRef
- Muangprom A., Thomas S.G., Sun T.P., Osborn T.C. A novel dwarfing mutation in a green revolution gene from Brassica rapa. Plant Physiol., 2005, 137(3): 931-938 CrossRef
- Boss P.K., Thomas M.R. Association of dwarfism and floral induction with a grape «green revolution» mutation. Nature, 2002, 416(6883): 847-850 CrossRef
- Ikeda A., Ueguchi-Tanaka M., Sonoda Y., Kitano H., Koshioka M., Futsuhara Y., Matsuoka M., Yamaguchi J. slender Rice, a constitutive gibberellin response mutant is caused by a null mutation of the SLR1 gene, an ortholog of the height-regulating gene GAI/RGA/RHT/D8. Plant Cell, 2001, 13(5): 999-1010 CrossRef
- Chandler P.M., Marion-Poll A., Ellis M., Gubler F. Mutants at the Slender1 locus of ‘Himalaya’ barley: molecular and physiological characterization. Plant Physiol., 2002, 129(1): 181-190 CrossRef
- Weston D.E., Elliott R.C., Lester D.R., Rameau C., Reid J.B., Murfet I.C., Ross J.J. The pea DELLA proteins LA and CRY are important regulators of gibberellin synthesis and root growth. Plant Physiol., 2008, 147(1): 199-205 CrossRef
- De Lucas M., Daviere J.-M., Rodriguez-Falcon M., Pontin M., Iglesias-Pedraz J.M., Lorrain S., Fankhause C., Blazquez M.A., Titarenko E., Prat S. A molecular framework for light and gibberellin control of cell elongation. Nature, 2008, 451(7177): 480-484 CrossRef
- Bassel G.W., Mullen R.T., Bewley J.D. Procera is a putative DELLA mutant in tomato (Solanum lycopersicum): effects on the seed and vegetative plant. J. Exp. Bot., 2008, 59(3): 585-593 CrossRef
- Peng J., Carol P., Richards D.E., King K.E., Cowling R.J., Murphy G.P., Harberd N.P. The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes Dev., 1997, 11(23): 3194-3205 CrossRef
- Silverstone A.L., Ciampaglio C.N., Sun T. The Arabidopsis RGA gene encodes a transcriptional regulator repressing the gibberellin signal transduction pathway. Plant Cell,1998, 10(3): 155-169 CrossRef
- Wen C.K., Chang C. Arabidopsis RGL1 encodes a negative regulator of gibberellin responses. Plant Cell, 2002, 14(1): 87-100 CrossRef
- Tyler L., Thomas S.G., Hu J., Dill A., Alonso J.M., Ecker J.R., Sun T. DELLA proteins and gibberellin-regulated seed germination and floral development in Arabidopsis. Plant Physiol., 2004, 135(2): 1008-1019 CrossRef
- Ariizumi T., Steber C.M. Ubiquitin becomes ubiquitous in GA signaling. In: Plant physiology. L. Taiz, E. Zeiger (eds.). Sunderland, MA, 2006. V. 20: 20.3. Available http://www.ars.usda.gov/research/publications/
publications.htm?SEQ_NO_115=198851. No date. - Dill A., Sun T.-P. Synergistic derepression of gibberellin signaling by removing RGA and GAI function in Arabidopsis thaliana. Genetics, 2001, 159: 777-785.
- Ogawa M., Kusano T., Katsumi M., Sano H. Rice gibberellin-insensitive gene homolog, OsGAI, encodes a nuclear-localized protein capable of gene activation at transcriptional level. Gene, 2000, 245(1): 21-29 CrossRef
- Fleck B., Harberd N.P. Evidence that the Arabidopsis nuclear gibberellin signaling protein GAI is not destabilized by gibberellin. Plant J.,2002, 32(6): 935-947 CrossRef
- Ueguchi-Tanaka M., Ashikari M., Nakajima M., Itoh H., Katoh E., Kobayashi M., Chow T.Y., Hsing Y.I., Kitano H., Yamaguchi I., Matsuoka M. GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellins. Nature, 2005, 437(7059): 693-698 CrossRef
- Murase K., Hirano Y., Sun T.-P., Hakoshima T. Gibberellin induced DELLA recognition by the gibberellin receptor GID1. Nature, 2008, 456(7221): 459-463 CrossRef
- Hartweck L.M. Gibberellin signaling. Planta, 2008, 229(1): 1-13 CrossRef
- Itoh H., Ueguchi-Tanaka M., Sato Y., Ashikari M., Matsuoka M. The gibberellin signaling pathway is regulated by appearance and disappearance of SLENDER RICE1 in nuclei. Plant Cell, 2002, 14(1): 57-70 CrossRef
- Willige B.C., Ghosh S., Nill C., Zourelidou M., Dohmann E.M., Maier A., Schwechheimer C. The DELLA domain of GA INSENSITIVE mediates the interaction with the GA INSENSITIVE DWARF1a gibberellin receptor of Arabidopsis. Plant Cell, 2007, 19(4): 1209-1220 CrossRef
- Cassani E., Bertolini E., Badone F.C., Landoni M., Gavina D., Sirizzotti A., Pilu R. Characterization of the first dominant dwarf maize mutant carrying a single amino acid insertion in the VHYNP domain of the dwarf8 gene. Mol. Breed.,2009, 24(4): 375-385 CrossRef
- Itoh H., Shimada A., Ueguchi-Tanaka M., Kamiya N., Hasegawa Y., Ashikari M., Matsuoka M. Overexpression of a GRAS protein lacking the DELLA domain confers altered gibberellin responses in rice. Plant J., 2005, 44(4): 669-679 CrossRef
- Sun T.-P. The molecular mechanism and evolution of the review GA–GID1–DELLA signaling module in plants. Curr. Biol., 2011, 21(9): R338-R345 CrossRef
- Dill A., Thomas S.G., Hu J., Steber C.M., Sun T.-P. The Arabidopsis F-box protein SLEEPY1 targets gibberellin signaling repressors for gibberellin-induced degradation. Plant Cell, 2004, 16: 1392-1405 CrossRef
- Ramos M.L., Altieri E., Bulos M., Sala C.A. Phenotypic characterization, genetic mapping and candidate gene analysis of a source conferring reduced plant height in sunflower. Theor. Appl. Genet., 2013, 126(1): 251-263 CrossRef
- Asano K., Hirano K., Ueguchi-Tanaka M., Angeles-Shim R.B., Komura T., Satoh H., Kitano H., Matsuoka M., Ashikari M. Isolation and characterization of dominant dwarf mutants, Slr1-d, in rice. Mol. Genet. Genomics, 2009, 281: 223-231 CrossRef
- Silverstone A.L., Tseng T.-S., Swain S., Dill A., Jeong S.Y., Olszewski N.E., Sun T.-P. Functional analysis of SPINDLY in gibberellins signaling in Arabidopsis. Plant Physiol., 2007, 143(2): 987-1000 CrossRef
- Shimada A., Ueguchi-Tanaka M., Sakamoto T., Fujioka S., Takatsuto S., Yoshida S., Sazuka T., Ashikari M., Matsuoka M. The rice SPINDLY gene functions as a negative regulator of gibberellins signaling by controlling the suppressive function of the DELLA protein, SLR1, and modulating brassinosteroid synthesis. Plant J., 2006, 48(3): 390-402 CrossRef
- Sasaki A., Itoh H., Gomi K., Ueguchi-Tanaka M., Ishiyama K., Kobayashi M., Jeong D.H., An G., Kitano H., Ashikari M., Matsuoka M. Accumulation of phosphorylated repressor for gibberellin signaling in an F-box mutant. Science, 2003, 299(5614): 1896-1898 CrossRef
- Richter R., Behringer C., Muller I.K., Schwechheimer C. The GATA-type transcription factors GNC and GNL/CGA1 repress gibberellin signaling downstream from DELLA proteins and PHYTOCHROME-INTERACTING FACTORS. Genes Dev., 2010, 24(18): 2093-2104 CrossRef
- Zhang Z.-L., Ogawab M., Fleeta C.M., Zentella R., Hua J., Heoc J.-O., Limc J., Kamiyab Y., Yamaguchib S., Sun T. SCARECROW-LIKE 3 promotes gibberellin signaling by antagonizing master growth repressor DELLA in Arabidopsis. PNAS USA, 2011, 108(5): 2160-2165 CrossRef
- Itoh H., Sasaki A., Ueguchi-Tanaka K., Kobayashi M., Hasegawa Y., Minami E., Ashikari M., Matsuoka M. Dissection of the phosphorylation of rice DELLA protein, SLENDER RICE1. Plant Cell Physiol., 2005, 46(8): 1392-1399 CrossRef
- Hussain A., Cao D., Peng J. Identification of conserved tyrosine residues important for gibberellin sensitivity of Arabidopsis RGL2 protein. Planta, 2007, 226(2): 475-483 CrossRef
- Dai C., Xue H.-W. Rice early flowering1, a CKI, phosphorylates DELLA protein SLR1 to negatively regulate gibberellin signalling. The EMBO Journal, 2010, 29: 1916-1927 CrossRef
- Jacobsen S.E., Binkowski K.A., Olszewski N.E. SPINDLY, a tetratricopeptide repeat protein involved in gibberellins signal transduction in Arabidopsis. PNAS USA, 1996, 93(17): 9292-9296 CrossRef
- Pysh L.D., Wysocka-Diller J.W., Camilleri C., Bouchez D., Benfey P.N. The GRAS gene family in Arabidopsis: sequence characterization and basic expression analysis of the SCARECROW-LIKE genes. Plant J., 1999, 18(1): 111-119 CrossRef
- Tian C., Wan P., Sun S., Li J., Chen M. Genome-wide analysis of the GRAS gene family in rice and Arabidopsis. Plant Mol. Biol., 2004, 54(4): 519-532 CrossRef
- Hirsch S., Oldroyd G.E.D. GRAS-domain transcription factors that regulate plant development. Plant Signal. Behav., 2009, 4(8): 698-700 CrossRef
- Zentella R., Zhang Z.L., Park M., Thomas S.G., Endo A., Murase K., Fleet C.M., Jikumaru Y., Nambara E., Kamiya Y., Sun T.P. Global analysis of DELLA direct targets in Early Gibberellin Signaling in Arabidopsis. Plant Cell, 2007, 19(10): 3037-3057 CrossRef
- Yoshida H., Hirano K., Sato T., Mitsuda N., Nomoto M., Maeo K., Koketsu E., Mitani R., Kawamura M., Ishiguro S., Tada Y., Ohme-Takagi M., Matsuoka M., Ueguchi-Tanaka M. DELLA protein functions as a transcriptional activator through the DNA binding of the indeterminate domain family proteins. PNAS USA, 2014, 111(21): 7861-7866 CrossRef
- Bolle C. The role of GRAS proteins in plant signal transduction and development. Planta, 2004, 218(5): 683-692 CrossRef
- Gao X.-H., Xiao S.-L., Yao Q.-F., Wang Y.-J., Fu X.-D. An updated GA signaling «Relief of repression» regulatory model. Mol. Plant., 2011, 4(4): 601-606 CrossRef
- Achard P., Cheng H., De Grauwe L., Decat J., Schoutteten H., Moritz T., Van Der Straeten D., Peng J., Harberd N.P. Integration of plant responses to environmentally activated phytohormonal signals. Science, 2006, 311(5757): 91-94 CrossRef
- Feng S., Martinez C., Gusmaroli G., Wang Y., Zhou J., Wang F., Chen L.Y., Yu L., Iglesias-Pedraz J.M., Kircher S., Schafer E., Fu X.D., Fan L.M., Deng X.W. Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature, 2008, 451(7177): 475-479 CrossRef
- Alabadi D., Gallego-Bartolome J., Orlando L., Garcia-Carcel L., Rubio V., Martinez C., Frigerio M., Iglesias-Pedraz J.M., Espinosa A., Deng X.W., Blazquez M.A. Gibberellins modulate light signaling pathways to prevent Arabidopsis seedling de-etiolation in darkness. Plant J., 2008, 53(2): 324-335 CrossRef
- Arnaud N., Grain T., Sorefan K., Fuentes S., Wood T.A., Lawrenson T., Sablowski R., Ostergaard L. Gibberellins control fruit patterning in Arabidopsis thaliana. Gene Dev., 2010, 24(19): 2127-2132 CrossRef
- Ubeda-Tomás S., Swarup R., Coates J., Swarup K., Laplaze L., Beemster G.T.S., Hedden P., Bhalerao R., Bennett M.J. Root growth in Arabidopsis requires gibberellin/DELLA signalling in the endodermis. Nat. Cell Biol., 2008, 10(5): 625-628 CrossRef
- Hou X., Lee L.Y.C., Xia K., Yan Y., Yu H. DELLAs modulate jasmonate signaling via competitive binding to JAZs. Dev. Cell, 2010, 19(6): 884-894 CrossRef
- Wild M., Davière J.M., Cheminant S., Regnault T., Baumberger N., Heintz D., Baltz R., Genschik P., Achard P. The Arabidopsis DELLA RGA-LIKE3 is a direct target of MYC2 and modulates jasmonate signaling responses. Plant Cell, 2012, 24(8): 3307-3319 CrossRef