Abstract
Gibberellic acid (GA) is a major plant hormone involved in several biological processes from the flowering to the symbiosis with microorganisms. Thus, the GA regulation is crucial for plant biology. This regulation occurs via the DELLA proteins that belong to the GRAS transcription factor family. DELLA proteins are characterised by a DELLA N-terminal and a GRAS C-terminal domains. It is well known that DELLA activity appears after the bryophytes divergence and then evolved in the vascular plant lineages. Here we present the phylogeny of DELLA across 75 species belonging to various lineages from algae, liverworts and angiosperms. Our study confirmed two main duplication events, the first occurring before the angiosperms divergence and the other specific to the eudicots lineage. Comparative analysis of DELLA subclades in angiosperms revealed the loss in Poaceae and strong alteration in other species of the DELLA functional domain in the DELLA2 clade. In addition, molecular evolution analysis suggests that each of the clades (named DELLA1.1, DELLA1.2 and DELLA2) evolved differently but copies of each subclade are under strong purifying selection. This also suggests that, although the DELLA functional domain is altered in DELLA2, DELLA2 orthologs are still functional and operate in a different way compared to DELLA1 copies. In angiosperms, additional duplication events occurred and led to duplicate copies in species, genus or family such as in the Fabaceae subfamily Papilionoideae. This duplication led to the formation of additional paralogs in the DELLA1.2 subclade (DELLA1.2.1 and DELLA1.2.2). Interestingly, both copies appeared to be under relaxing selection revealing different evolutionary fate of the DELLA duplicated copies.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Briones-Moreno A, Hernández-García J, Vargas-Chávez C et al (2017) Evolutionary analysis of DELLA-associated transcriptional networks. Front Plant Sci 8:626. https://doi.org/10.3389/fpls.2017.00626
Camacho C, Coulouris G, Avagyan V et al (2009) BLAST+: architecture and applications. BMC Bioinform 10:421. https://doi.org/10.1186/1471-2105-10-421
Cenci A, Rouard M (2017) Evolutionary analyses of GRAS transcription factors in angiosperms. Front Plant Sci 8:273. https://doi.org/10.3389/fpls.2017.00273
Chen J, Cheng T, Wang P et al (2013) Genome-wide bioinformatics analysis of DELLA-family proteins from plants. Plant Omics J 6(3):201–207
Cheng S, Xian W, Fu Y et al (2019) Genomes of subaerial zygnematophyceae provide insights into land plant evolution. Cell 179:1057-1067.e14. https://doi.org/10.1016/j.cell.2019.10.019
Crooks GE (2004) WebLogo: a sequence logo generator. Genome Res 14:1188–1190. https://doi.org/10.1101/gr.849004
Davies PJ (ed) (2010) Plant hormones. Springer, Dordrecht
Dolgikh AV, Kirienko AN, Tikhonovich IA et al (2019) The DELLA proteins influence the expression of cytokinin biosynthesis and response genes during nodulation. Front Plant Sci 10:432. https://doi.org/10.3389/fpls.2019.00432
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. https://doi.org/10.1093/nar/gkh340
Ferguson BJ, Foo E, Ross JJ, Reid JB (2011) Relationship between gibberellin, ethylene and nodulation in Pisum sativum. New Phytol 189:829–842. https://doi.org/10.1111/j.1469-8137.2010.03542.x
Finn RD, Coggill P, Eberhardt RY et al (2016) The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res 44:D279–D285. https://doi.org/10.1093/nar/gkv1344
Floss DS, Levy JG, Levesque-Tremblay V et al (2013) DELLA proteins regulate arbuscule formation in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci 110:E5025–E5034. https://doi.org/10.1073/pnas.1308973110
Fonouni-Farde C, Tan S, Baudin M et al (2016) DELLA-mediated gibberellin signalling regulates Nod factor signalling and rhizobial infection. Nat Commun 7:1–13. https://doi.org/10.1038/ncomms12636
Fu X, Richards DE, Ait-ali T et al (2002) Gibberellin-mediated proteasome-dependent degradation of the barley DELLA protein SLN1 repressor. Plant Cell 14:3191–3200. https://doi.org/10.1105/tpc.006197
Gupta R, Chakrabarty SK (2013) Gibberellic acid in plant: still a mystery unresolved. Plant Signal Behav 8:e25504. https://doi.org/10.4161/psb.25504
Hane JK, Ming Y, Kamphuis LG et al (2017) A comprehensive draft genome sequence for lupin (Lupinus angustifolius), an emerging health food: insights into plant-microbe interactions and legume evolution. Plant Biotechnol J 15:318–330. https://doi.org/10.1111/pbi.12615
Hernández-García J, Briones-Moreno A, Dumas R, Blázquez MA (2019) Origin of gibberellin-dependent transcriptional regulation by molecular exploitation of a transactivation domain in DELLA proteins. Mol Biol Evol 36:908–918. https://doi.org/10.1093/molbev/msz009
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. Plant Cell 19:3058–3079. https://doi.org/10.1105/tpc.107.051524
Hoang DT, Chernomor O, von Haeseler A et al (2018) UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol 35:518–522. https://doi.org/10.1093/molbev/msx281
Itoh H, Shimada A, Ueguchi-Tanaka M et al (2005) Overexpression of a GRAS protein lacking the DELLA domain confers altered gibberellin responses in rice: rice SLR1-like genes. Plant J 44:669–679. https://doi.org/10.1111/j.1365-313X.2005.02562.x
Jiao Y, Wickett NJ, Saravanaraj A et al (2011) Data from: ancestral polyploidy in seed plants and angiosperms. Nature 473(7345):97 100. https://doi.org/10.1038/nature09916
Jin Y, Liu H, Luo D et al (2016) DELLA proteins are common components of symbiotic rhizobial and mycorrhizal signalling pathways. Nat Commun 7(1):1–14. https://doi.org/10.1038/ncomms12433
Kalyaanamoorthy S, Minh BQ, Wong TKF et al (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14:587–589. https://doi.org/10.1038/nmeth.4285
Kenrick P, Crane PR (1997) The origin and early evolution of plants on land. Nature 389(6646):33–39. https://doi.org/10.1038/37918
Letunic I, Bork P (2016) Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 44:W242–W245. https://doi.org/10.1093/nar/gkw290
Lievens S, Goormachtig S, Den Herder J et al (2005) Gibberellins are involved in nodulation of Sesbania rostrata. Plant Physiol 139:1366–1379. https://doi.org/10.1104/pp.105.066944
Maekawa T, Maekawa-Yoshikawa M, Takeda N et al (2009) Gibberellin controls the nodulation signaling pathway in Lotus japonicus. Plant J 58:183–194. https://doi.org/10.1111/j.1365-313X.2008.03774.x
Martín-Rodríguez JA, Huertas R, Ho-Plágaro T et al (2016) Gibberellin–abscisic acid balances during arbuscular mycorrhiza formation in tomato. Front Plant Sci 7:1273. https://doi.org/10.3389/fpls.2016.01273
Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274. https://doi.org/10.1093/molbev/msu300
Pimprikar P, Carbonnel S, Paries M et al (2016) A CCaMK-CYCLOPS-DELLA complex activates transcription of RAM1 to regulate arbuscule branching. Curr Biol 26:987–998. https://doi.org/10.1016/j.cub.2016.01.069
Pond SLK, Frost SDW, Muse SV (2005) HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676–679. https://doi.org/10.1093/bioinformatics/bti079
Pysh LD, Wysocka-Diller JW, Camilleri C et al (1999) The GRAS gene family in Arabidopsis: sequence characterization and basic expression analysis of the SCARECROW-LIKE genes. Plant J 18:111–119. https://doi.org/10.1046/j.1365-313X.1999.00431.x
Sato T, Miyanoiri Y, Takeda M et al (2014) Expression and purification of a GRAS domain of SLR1, the rice DELLA protein. Protein Expr Purif 95:248–258. https://doi.org/10.1016/j.pep.2014.01.006
Sun T (2011) The molecular mechanism and evolution of the GA–GID1–DELLA signaling module in plants. Curr Biol 21:R338–R345. https://doi.org/10.1016/j.cub.2011.02.036
Suyama M, Torrents D, Bork P (2006) PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res 34:W609–W612. https://doi.org/10.1093/nar/gkl315
Takeda N, Handa Y, Tsuzuki S et al (2015) Gibberellin regulates infection and colonization of host roots by arbuscular mycorrhizal fungi. Plant Signal Behav 10:e1028706. https://doi.org/10.1080/15592324.2015.1028706
Ueguchi-Tanaka M, Nakajima M, Motoyuki A, Matsuoka M (2007) Gibberellin receptor and its role in gibberellin signaling in plants. Annu Rev Plant Biol 58:183–198. https://doi.org/10.1146/annurev.arplant.58.032806.103830
Van de Peer Y, Mizrachi E, Marchal K (2017) The evolutionary significance of polyploidy. Nat Rev Genet 18:411–424. https://doi.org/10.1038/nrg.2017.26
Wang Y, Deng D (2014) Molecular basis and evolutionary pattern of GA–GID1–DELLA regulatory module. Mol Genet Genomics 289:1–9. https://doi.org/10.1007/s00438-013-0797-x
Wen C-K, Chang C (2002) Arabidopsis RGL1 encodes a negative regulator of gibberellin responses. Plant Cell 14:87–100. https://doi.org/10.1105/tpc.010325
Wertheim JO, Murrell B, Smith MD et al (2015) RELAX: detecting relaxed selection in a phylogenetic framework. Mol Biol Evol 32:820–832. https://doi.org/10.1093/molbev/msu400
Yang Z, Nielsen R (2000) Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol 17:32–43. https://doi.org/10.1093/oxfordjournals.molbev.a026236
Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591. https://doi.org/10.1093/molbev/msm088
Yasumura Y, Crumpton-Taylor M, Fuentes S, Harberd NP (2007) Step-by-step acquisition of the gibberellin-DELLA growth-regulatory mechanism during land-plant evolution. Curr Biol 17:1225–1230. https://doi.org/10.1016/j.cub.2007.06.037
Yu N, Luo D, Zhang X et al (2014) A DELLA protein complex controls the arbuscular mycorrhizal symbiosis in plants. Cell Res 24:130–133. https://doi.org/10.1038/cr.2013.167
Acknowledgements
We acknowledge the GenOuest bioinformatics core facility (https://www.genouest.org) for providing the computing infrastructure. Part of this work was conducted at the LRSV laboratory, which belongs to the TULIP Laboratoire d’Excellence (LABEX) (ANR-10-LABX-41). JK and CL were supported by the research project Engineering Nitrogen Symbiosis for Africa (ENSA), which is funded through a grant to the University of Cambridge by the Bill & Melinda Gates Foundation (OPP1172165). JK was supported by a doctoral research grant from the University of Rennes 1 – French Ministry of Higher Education and Research. This work benefited from the International Associated Laboratory “Ecological Genomics of Polyploidy” supported by CNRS (INEE, UMR CNRS 6553 Ecobio), University of Rennes 1, Iowa State University (Ames, USA).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
10709_2020_102_MOESM2_ESM.fa
Supplementary material 2 (FA 5.1 kb). Supplementary Data S2: Protein sequences discarded prior the phylogenetic analysis (less than 200 amino acids)
Rights and permissions
About this article
Cite this article
Keller, J., Delcros, P., Libourel, C. et al. DELLA family duplication events lead to different selective constraints in angiosperms. Genetica 148, 243–251 (2020). https://doi.org/10.1007/s10709-020-00102-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10709-020-00102-6