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DELLA functions evolved by rewiring of associated transcriptional networks

Nature Plants volume 9, pages 535–543 (2023)Cite this article

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Abstract

DELLA proteins are land-plant specific transcriptional regulators that transduce environmental information to multiple processes throughout a plant’s life1,2,3. The molecular basis for this critical function in angiosperms has been linked to the regulation of DELLA stability by gibberellins and to the capacity of DELLA proteins to interact with hundreds of transcription factors4,5. Although bryophyte orthologues can partially fulfil functions attributed to angiosperm DELLA6,7, it is not clear whether the capacity to establish interaction networks is an ancestral property of DELLA proteins or is associated with their role in gibberellin signalling8,9,10. Here we show that representative DELLAs from the main plant lineages display a conserved ability to interact with multiple transcription factors. We propose that promiscuity was encoded in the ancestral DELLA protein, and that this property has been largely maintained, whereas the lineage-dependent diversification of DELLA-dependent functions mostly reflects the functional evolution of their interacting partners.

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Fig. 1: Capacity of interaction of DELLAs from different plant lineages.
Fig. 2: Heterologous complementation of DELLA function.
Fig. 3: Behaviour of DELLAs from different plant lineages as transcriptional regulators in A. thaliana.
Fig. 4: Comparison of the transcriptional regulatory activity of DELLAs across the plant lineage.

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Data availability

All materials generated in this study are freely available from the corresponding author upon request. All data are available in the main text or the supplementary materials. The RNA sequencing data generated in this study have been submitted to the NCBI BioProject database (https://www.ncbi.nlm.nih.gov/bioproject/) under accession numbers PRJNA695247 (‘Complementation of an Arabidopsis thaliana dellaKO with DELLAs from different plant species’) and PRJNA695244 (‘DELLA-dependent transcriptomes in different plant species’).

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Acknowledgements

We thank D. Weiss and S. Livne (The Hebrew University of Jerusalem) for the tomato pro mutant and advice on the selection of homozygous seedlings, and K. Hirano (Nagoya University) for the rice seeds. The Ppdellaab mutant was obtained from Y. Yasumura, E. Belfield and N.P. Harberd (University of Oxford). We also thank J. Agustí, B. Catarino and M. Sanmartín (Instituto de Biología Molecular y Celular de Plantas, Valencia) for excellent input on the manuscript. Work was performed with grants BFU2016-80621-P and PID2019-110717-GB funded by Spanish MCIN/AEI /10.13039/501100011033/ and by ‘ERDF, A way of making Europe’.

Author information

Author notes

  1. Jorge Hernández-García

    Present address: Laboratory of Biochemistry, Wageningen University, Wageningen, the Netherlands

Authors and Affiliations

  1. Instituto de Biología Molecular y Celular de Plantas (CSIC-U Politècnica de València), Valencia, Spain

    Asier Briones-Moreno, Jorge Hernández-García, Noel Blanco-Touriñán, Cristina Úrbez, David Alabadí & Miguel A. Blázquez

  2. Institut de Biologia Evolutiva (CSIC-U Pompeu Fabra), Barcelona, Spain

    Carlos Vargas-Chávez

  3. School of Biosciences, University of Birmingham, Birmingham, UK

    Alexandros Phokas & Juliet C. Coates

  4. Fundación Instituto Leloir, Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, Argentina

    Pablo D. Cerdán

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Contributions

A.B.-M., J.H.-G. and M.A.B. conceptualized the project. A.B.-M., J.H.-G., C.V.-C., N.B.-T., C.Ú. and A.P. conducted the investigation. A.B.-M., J.H.-G., C.V.-C., N.B.-T. and M.A.B. conducted the formal analysis. P.D.C., J.C.C., D.A. and M.A.B. supervised the project. J.C.C. and M.A.B. acquired the funding. A.B.-M. and M.A.B. wrote the original draft of the paper. All authors revised and edited the paper.

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Correspondence to Miguel A. Blázquez.

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Nature Plants thanks Xiangdong Fu, Javier Moreno and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Phylogenetic tree of the DELLA family.

a, Maximum likelihood phylogenetic tree of the DELLA family using representative DELLA proteins. Sequences used in Y2H assays have been highlighted with a solid red circle (when used for both homologous and heterologous tests) or an empty red circle (when only used for heterologous tests with AtTFs). Proteins included in the analysis have been previously described11, with the only exception of Anthoceros agrestis DELLA (see Methods, note that AaDELLA1 and AaDELLA2 are DELLAs from Artemisia annua in contrast to that of A. agrestis, AaDELLA). DELLA clades are named after Ref. 11. Statistical support associated with branches are SH-like aLRT values, depicted as colour-coded circles in branch nodes. b, Scheme of the evolutionary path followed by the different DELLA clades in land plants inferred from the tree in panel a. ‘Basal’ lineages are defined by the following species: Vitis vinifera, Kalanchoe laxiflora for Basal rosids; Actinidia chinensis, Beta vulgaris, Amaranthus hypochondriacus for Basal asterids; Nelumbo nucifera, Aquilegia caerulea for Basal eudicots; Phalaenopsis equestris, Spirodela polyrrhiza for basal monocots; Magnolia grandiflora, Amborella trichopoda for basal angiosperms.

Extended Data Fig. 2 Protein sequence conservation in the GRAS domain of several GRAS families.

Conservation per residue was calculated on previously available alignments from multiple land plant GRAS proteins11 using ProtSkin software52. Box plots represent values from orthologues previously assigned to each family11 (n = 50 for all families except for DELLA and SCL3 families, in which n = 53). Letters indicate statistical differences between groups after one-way ANOVA followed by Tukey’s HSD post hoc test (p < 0.01).

Extended Data Fig. 3 DELLA accumulation in complemented lines (pRGA::DELLA-YFP).

a–c, Western Blot assay of whole 7-day-old seedlings grown with 0.5 µM PAC (a, b) and leaves from 30-day-old adult plants watered with 10 µM PAC. (c). In a, dellaKO and pRGA::RGA-YFP (line #1) are shown as controls for YFP detection. Ponceau staining prior immunostaining is shown as loading control. In b and c, detection of DET3 protein was used as internal control; DELLA proteins fused to YFP were detected with the anti-GFP antibody JL-8. Arrowheads indicate expected band size. The analysis shown here was confirmed in a second independent test. d, Confocal microscopy images of complementation lines in 7-day-old seedling root tips. YFP fluorescent signal in green, dellaKO root tip shape is marked with a red dotted line. Seedlings were grown in half strength MS medium supplemented with 0.5 μM PAC. The images shown here are representative from n = 6 seedlings examined per line. Scale bar = 50 µm. e, Transcript levels of MpDELLA and AtRGA transgenes in 14-day-old M. polymorpha overexpression lines (see Fig. 2) determined by qPCR. Bars represent the mean number of transcripts per 109 transcript of MpEF1α calculated from three independent biological replicates (shown as grey dots). ND indicates non detected expression of AtRGA.

Extended Data Fig. 4 Heterologous complementation of dellaKO mutants.

Wild-type A. thaliana plants (WT), plants mutant for the five DELLA genes (AtdellaKO) and AtdellaKO plants transformed with DELLAs from the indicated species (At, Sl, Pa, Sm, or Mp) under the control of the AtRGA promoter and terminator, had their phenotypes examined in the presence of 0.5 μM PAC. a, Stem length of 30-day-old plants. n = 15 plants per genotype were measured. b, Percentage of germinated seeds, scored after 24 h at 22 °C in darkness with 1 µM PAC, in three independent experiments. Graphs show individual data points (dots) and data mean (horizontal black bar). Letters indicate statistical differences between groups after one-way ANOVA followed by Tukey’s HSD post hoc test (p < 0.01).

Extended Data Fig. 5 Heterologous and homologous interaction of putative tomato DELLA interactors.

Yeast 2-hybrid assay showing interaction (or lack of it) of the tomato orthologues of At1G74840 and AT5G01380 with AtRGA and SlPRO. H, Histidine; 3AT, 3-amino-1,2,4-triazole; AD, Activation Domain; BD, Binding Domain.

Supplementary information

Supplementary Information

Supplementary Figs. 1–3.

Reporting Summary

Supplementary Tables

Supplementary Tables 1–12. Table 1: Transcription factors and DELLA sequences used in this study. Table 2: Yeast 2-hybrid assay results. Table 3: Transcriptomic analysis of dellaKO complementation. Table 4: Gene Ontology analysis of dellaKO complementation. Table 5: TF-enrichment analysis in the set of 211 conserved DEGs of dellaKO complementation. Table 6: TF-enrichment analysis of the exclusive set of SlPRO-regulated genes. Table 7: DELLA-dependent transcriptomes in each species. Table 8: Orthologous relationships for the genes of all the species used in this study. Table 9: Gene Ontology analysis of DELLA-dependent transcriptomes in each species. Table 10: TF-enrichment analysis of DELLA-dependent transcriptomes in each species. Table 11: Oligonucleotides used in this study. Table 12: Sequences of truncated DELLA proteins used in this study.

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Briones-Moreno, A., Hernández-García, J., Vargas-Chávez, C. et al. DELLA functions evolved by rewiring of associated transcriptional networks. Nat. Plants 9, 535–543 (2023). https://doi.org/10.1038/s41477-023-01372-6

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