DELLA Proteins in Signalling

Abstract

DELLA proteins have emerged as important modulators of prewired transcriptional circuits in response to the environment. In vascular plants, proteasome‐dependent degradation of DELLAs is induced by gibberellins, whose levels are strongly regulated by environmental signals such as light, temperature and nutrient availability. Transcriptional regulation is exerted by DELLAs through physical interaction with DNA‐binding transcription factors and other transcriptional regulators. The key biological role of DELLAs has been proposed to regulate the balance between growth and stress responses, which justifies the inadvertent selection of hyperstable DELLA alleles during the breeding programs that lead to the Green Revolution. DELLA proteins are also present in nonvascular plants which do not synthesise active gibberellins, suggesting that the origin of DELLAs predates the emergence of gibberellin biosynthesis.

Key Concepts

  • DELLAs are nuclear proteins that modulate the activity of a large set of transcription factors through protein–protein interaction.
  • DELLA protein degradation is regulated by environmental signals mostly through gibberellin signalling.
  • DELLA proteins are ‘hubs’ that control the balance between growth and stress responses.
  • The origin of DELLA proteins predates the appearance of bioactive gibberellins.
  • Manipulation of DELLA proteins has contributed to the ‘Green Revolution’.

Keywords: Arabidopsis ; rice; gibberellin; green revolution; prefoldin; transcriptional regulation; hormone signalling

Figure 1. Domain structure of DELLA proteins. The N‐terminal domain contains the ‘DELLA’, ‘LExLE’ and ‘TVHYNP’ motifs necessary for the interaction with the GID1 GA receptor. The C‐terminal domain also called ‘GRAS domain’ contains two leucine heptad repeats (LHR1 and 2), the ‘VHIID’ motif preceded by a nuclear localisation signal, and the ‘PFYRE’ and ‘SAW’ motifs.
Figure 2. GA‐dependent degradation of DELLA proteins. The images show the nuclear fluorescence signal emitted by RGA‐YFP in the absence of GAs, in Arabidopsis hypocotyls under a confocal microscope. The rga‐Δ17 allele is stable even in the presence of GAs.
Figure 3. Mechanisms of DELLA transcriptional regulation. DELLAs can sequester TFs, or sequester TF regulators, or act as TF transcriptional coactivators at the promoters of target genes.
Figure 4. The role of DELLA proteins in the coordination of transcriptional programs in response to environmental signals. Depending on the interacting TF, DELLAs can affect different biological processes in a given plant.
Figure 5. Regulation of microtubule elongation by DELLA‐PFD interaction. DELLA‐dependent retention of PFD in the nucleus impairs proper folding of tubulin, and hence microtubule extension.
close

References

Achard P , Renou JP , Berthome R , Harberd NP and Genschik P (2008) Plant DELLAs restrain growth and promote survival of adversity by reducing the levels of reactive oxygen species. Current Biology 18: 656–660.

Arana MV , Marin‐de la Rosa N , Maloof JN , Blazquez MA and Alabadi D (2011) Circadian oscillation of gibberellin signaling in Arabidopsis . Proceedings of the National Academy of Sciences of the United States of America 108: 9292–9297.

Ariizumi T , Lawrence PK and Steber CM (2011) The role of two F‐Box proteins, SLEEPY1 and SNEEZY, in Arabidopsis gibberellin signaling. Plant Physiology 155: 765–775.

Bowman JL , Kohchi T , Yamato KT , et al. (2017) Insights into land plant evolution garnered from the Marchantia polymorpha genome. Cell 171 (287–304) e215.

Briones‐Moreno A , Hernandez‐Garcia J , Vargas‐Chavez C , et al. (2017) Evolutionary analysis of DELLA‐associated transcriptional networks. Frontiers in Plant Science 8: 626.

Claeys H , De Bodt S and Inze D (2014) Gibberellins and DELLAs: central nodes in growth regulatory networks. Trends in Plant Science 19: 231–239.

Conti L , Nelis S , Zhang C , et al. (2014) Small ubiquitin‐like modifier protein SUMO enables plants to control growth independently of the phytohormone gibberellin. Developmental Cell 28: 102–110.

Feng S , Martinez C , Gusmaroli G , et al. (2008) Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451: 475–479.

Gallego‐Bartolomé J , Minguet EG , Marín JA , et al. (2010) Transcriptional diversification and functional conservation between DELLA proteins in Arabidopsis . Molecular Biology and Evolution 27: 1247–1256.

Gu Y , Deng Z , Paredez AR , et al. (2008) Prefoldin 6 is required for normal microtubule dynamics and organization in Arabidopsis . Proceedings of the National Academy of Sciences of the United States of America 105: 18064–18069.

Hirano K , Nakajima M , Asano K , et al. (2007) The GID1‐mediated gibberellin perception mechanism is conserved in the Lycophyte Selaginella moellendorffii but not in the Bryophyte Physcomitrella patens . The Plant Cell 19: 3058–3079.

Hirano K , Kouketu E , Katoh H , et al. (2012) The suppressive function of the rice DELLA protein SLR1 is dependent on its transcriptional activation activity. The Plant Journal 71: 443–453.

Hirano Y , Nakagawa M , Suyama T , et al. (2017) Structure of the SHR‐SCR heterodimer bound to the BIRD/IDD transcriptional factor JKD. Nature plants 3: 17010.

Hou X , Lee LY , Xia K , Yan Y and Yu H (2010) DELLAs modulate jasmonate signaling via competitive binding to JAZs. Developmental Cell 19: 884–894.

Hussain A , Cao D , Cheng H , Wen Z and Peng J (2005) Identification of the conserved serine/threonine residues important for gibberellin‐sensitivity of Arabidopsis RGL2 protein. The Plant Journal 44: 88–99.

Hussain A , Cao D and Peng J (2007) Identification of conserved tyrosine residues important for gibberellin sensitivity of Arabidopsis RGL2 protein. Planta 226: 475–483.

Ikeda A , Ueguchi‐Tanaka M , Sonoda Y , et al. (2001) 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. The Plant Cell 13: 999–1010.

Itoh H , Sasaki A , Ueguchi‐Tanaka M , et al. (2005) Dissection of the phosphorylation of rice DELLA protein, SLENDER RICE1. Plant & Cell Physiology 46: 1392–1399.

Li S , Zhao Y , Zhao Z , et al. (2016) Crystal structure of the GRAS domain of SCARECROW‐LIKE7 in Oryza sativa . The Plant Cell 28: 1025–1034.

Locascio A , Blazquez MA and Alabadi D (2013a) Dynamic regulation of cortical microtubule organization through prefoldin‐DELLA interaction. Current Biology 23: 804–809.

Locascio A , Blazquez MA and Alabadi D (2013b) Genomic analysis of della protein activity. Plant & Cell Physiology 54: 1229–1237.

de Lucas M , Davière JM , Rodríguez‐Falcón M , et al. (2008) A molecular framework for light and gibberellin control of cell elongation. Nature 451: 480–484.

Marin‐de la Rosa N , Sotillo B , Miskolczi P , et al. (2014) Large‐scale identification of gibberellin‐related transcription factors defines Group VII ETHYLENE RESPONSE FACTORS as functional DELLA partners. Plant Physiology 166: 1022–1032.

Marin‐de la Rosa N , Pfeiffer A , Hill K , et al. (2015) Genome wide binding site analysis reveals transcriptional coactivation of cytokinin‐responsive genes by DELLA proteins. PLoS Genetics 11: e1005337.

Millan‐Zambrano G and Chavez S (2014) Nuclear functions of prefoldin. Open Biology 4. pii: 140085.

Murase K , Hirano Y , Sun TP and Hakoshima T (2008) Gibberellin‐induced DELLA recognition by the gibberellin receptor GID1. Nature 456: 459–463.

Peng J , Richards DE , Hartley NM , et al. (1999) ‘Green revolution’ genes encode mutant gibberellin response modulators. Nature 400: 256–261.

Qin Q , Wang W , Guo X , et al. (2014) Arabidopsis DELLA protein degradation is controlled by a type‐one protein phosphatase, TOPP4. PLoS Genetics 10: e1004464.

Silverstone AL , Tseng TS , Swain SM , et al. (2007) Functional analysis of SPINDLY in gibberellin signaling in Arabidopsis . Plant Physiology 143: 987–1000.

Sun TP and Kamiya Y (1994) The Arabidopsis GA1 locus encodes the cyclase ent‐kaurene synthetase A of gibberellin biosynthesis. The Plant Cell 6: 1509–1518.

Sun X , Jones WT , Harvey D , et al. (2010) N‐terminal domains of della proteins are intrinsically unstructured proteins in the absence of interaction with gid1 ga receptors. The Journal of Biological Chemistry 285: 11557–11571.

Ueguchi‐Tanaka M , Nakajima M , Motoyuki A and Matsuoka M (2007) Gibberellin receptor and its role in gibberellin signaling in plants. Annual Review of Plant Biology 58: 183–198.

Ueguchi‐Tanaka M , Hirano K , Hasegawa Y , Kitano H and Matsuoka M (2008) Release of the repressive activity of rice DELLA protein SLR1 by gibberellin does not require SLR1 degradation in the gid2 mutant. The Plant Cell 20: 2437–2446.

Van De Velde K , Ruelens P , Geuten K , Rohde A and Van Der Straeten D (2017) Exploiting DELLA signaling in cereals. Trends in Plant Science 22: 880–893.

Wang W , Zhang J , Qin Q , et al. (2014) The six conserved serine/threonine sites of REPRESSOR OF ga1‐3 protein are important for its functionality and stability in gibberellin signaling in Arabidopsis . Planta 240: 763–779.

Willige BC , Ghosh S , Nill C , et al. (2007) The DELLA domain of GA INSENSITIVE mediates the interaction with the GA INSENSITIVE DWARF1A gibberellin receptor of Arabidopsis . The Plant Cell 19: 1209–1220.

Yasumura Y , Crumpton‐Taylor M , Fuentes S and Harberd NP (2007) Step‐by‐step acquisition of the gibberellin‐DELLA growth‐regulatory mechanism during land‐plant evolution. Current Biology 17: 1225–1230.

Zentella R , Hu J , Hsieh WP , et al. (2016) O‐GlcNAcylation of master growth repressor DELLA by SECRET AGENT modulates multiple signaling pathways in Arabidopsis . Genes & Development 30: 164–176.

Zentella R , Sui N , Barnhill B , et al. (2017) The Arabidopsis O‐fucosyltransferase SPINDLY activates nuclear growth repressor DELLA. Nature Chemical Biology 13: 479–485.

Further Reading

Daviere JM and Achard P (2013) Gibberellin signaling in plants. Development (Cambridge, England) 140: 1147–1151.

Schwechheimer C (2011) Gibberellin signaling in plants ‐ the extended version. Frontiers in Plant Science 2: 107.

Thomas SG (2017) Novel Rht‐1 dwarfing genes: tools for wheat breeding and dissecting the function of DELLA proteins. Journal of Experimental Botany 68: 354–358.

Vera‐Sirera F , Gomez MD and Perez‐Amador MA (2015) DELLA proteins, a group of GRAS transcription regularors, mediate gibberellin signaling. In: González DH (ed.) Plant Transcription Factors; Evolutionary, Structural and Functional Aspects, pp. 313–328. Amsterdam (The Netherlands): Elsevier.

Yoshida H , Tanimoto E , Hirai T , et al. (2018) Evolution and diversification of the plant gibberellin receptor GID1. Proceedings of the National Academy of Sciences of the United States of America 115: E7844–E7853.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Blázquez, Miguel A(Mar 2019) DELLA Proteins in Signalling. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0020096.pub2]