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SMAX1-dependent seed germination bypasses GA signalling in Arabidopsis and Striga

Abstract

Parasitic plant infestations dramatically reduce the yield of many major food crops of sub-Saharan Africa and pose a serious threat to food security on that continent1. The first committed step of a successful infestation is the germination of parasite seeds primarily in response to a group of related small-molecule hormones called strigolactones (SLs), which are emitted by host roots2. Despite the important role of SLs, it is not clear how host-derived SLs germinate parasitic plants. In contrast, gibberellins (GA) acts as the dominant hormone for stimulation of germination in non-parasitic plant species by inhibiting a set of DELLA repressors3. Here, we show that expression of SL receptors from the parasitic plant Striga hermonthica in the presence of SLs circumvents the GA requirement for germination of Arabidopsis thaliana seed. Striga receptors co-opt and enhance signalling through the HYPOSENSITIVE TO LIGHT/KARRIKIN INSENSITIVE 2 (AtHTL/KAI2) pathway, which normally plays a rudimentary role in Arabidopsis seed germination4,5. AtHTL/KAI2 negatively controls the SUPPRESSOR OF MAX2 1 (SMAX1) protein5, and loss of SMAX1 function allows germination in the presence of DELLA repressors. Our data suggest that ligand-dependent inactivation of SMAX1 in Striga and Arabidopsis can bypass GA-dependent germination in these species.

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Fig. 1: Arabidopsis seeds expressing SL receptors from S. hermonthica do not require GA to germinate.
Fig. 2: SL-activated ShHTL7 circumvents RGL2 repression of Arabidopsis seed germination.
Fig. 3: S. hermonthica SL receptors require functional MAX2 for germination.
Fig. 4: GA is not required for initiation of germination of S. hermonthica seeds.

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Data availability

The data generated from this study are included in the article and Supplementary Tables. RNA-seq data from Fig. 3 were deposited in NCBI Sequence Read Archive under accession no. PRJNA602291, ID 602291.

References

  1. Parker, C. Observations on the current status of Orobanche and Striga problems worldwide. Pest Manag. Sci. 65, 453–459 (2009).

    Article  CAS  PubMed  Google Scholar 

  2. Cook, C. E. et al. Germination of witchweed (Striga lutea Lour.): isolation and properties of a potent stimulant. Science 154, 1189–1190 (1966).

    Article  CAS  PubMed  Google Scholar 

  3. Sun, T. P. The molecular mechanism and evolution of the GA-GID1-DELLA signaling module in plants. Curr. Biol. 21, R338–R345 (2011).

    Article  CAS  PubMed  Google Scholar 

  4. Waters, M. T. et al. Specialization within the DWARF14 protein family confers distinct responses to karrikins and strigolactones in Arabidopsis. Development 139, 1285–1295 (2012).

    Article  CAS  PubMed  Google Scholar 

  5. Stanga, J. P., Smith, S. M., Briggs, W. R. & Nelson, D. C. SUPPRESSOR OF MORE AXILLARY GROWTH2 1 controls seed germination and seedling development in Arabidopsis. Plant Physiol. 163, 318–330 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Santner, A., Calderon-Villalobos, L. I. & Estelle, M. Plant hormones are versatile chemical regulators of plant growth. Nat. Chem. Biol. 5, 301–307 (2009).

    Article  CAS  PubMed  Google Scholar 

  7. Lumba, S., Holbrook-Smith, D. & McCourt, P. The perception of strigolactones in vascular plants. Nat. Chem. Biol. 13, 599–606 (2017).

    Article  CAS  PubMed  Google Scholar 

  8. Waters, M. T., Gutjahr, C., Bennett, T. & Nelson, D. C. Strigolactone signaling and evolution. Annu. Rev. Plant Biol. 68, 291–322 (2017).

    Article  CAS  PubMed  Google Scholar 

  9. Waldie, T., McCulloch, H. & Leyser, O. Strigolactones and the control of plant development: lessons from shoot branching. Plant J. 79, 607–622 (2014).

    Article  CAS  PubMed  Google Scholar 

  10. Cardoso, C., Ruyter-Spira, C. & Bouwmeester, H. J. Strigolactones and root infestation by plant-parasitic Striga, Orobanche and Phelipanche spp. Plant Sci. 180, 414–420 (2011).

    Article  CAS  PubMed  Google Scholar 

  11. Akiyama, K., Matsuzaki, K. & Hayashi, H. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435, 824–827 (2005).

    Article  CAS  PubMed  Google Scholar 

  12. Yoshida, S. & Shirasu, K. Plants that attack plants: molecular elucidation of plant parasitism. Curr. Opin. Plant Biol. 15, 708–713 (2012).

    Article  CAS  PubMed  Google Scholar 

  13. Tsuchiya, Y. et al. Probing strigolactone receptors in Striga hermonthica with fluorescence. Science 349, 864–868 (2015).

    Article  CAS  PubMed  Google Scholar 

  14. Toh, S. et al. Structure–function analysis identifies highly sensitive strigolactone receptors in Striga. Science 350, 203–207 (2015).

    Article  CAS  PubMed  Google Scholar 

  15. Conn, C. et al. Convergent evolution of strigolactone perception enabled host detection in parasitic plants. Science 349, 540–543 (2015).

    Article  CAS  PubMed  Google Scholar 

  16. Scaffidi, A. et al. Strigolactone hormones and their stereoisomers signal through two related receptor proteins to induce different physiological responses in Arabidopsis. Plant Physiol. 165, 1221–1232 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Yao, R. et al. ShHTL7 is a non-canonical receptor for strigolactones in root parasitic weeds. Cell Res. 27, 838–841 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Bennett, T. et al. Strigolactone regulates shoot development through a core signalling pathway. Biol. Open 5, 1806–1820 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Lantzouni, O., Klermund, C. & Schwechheimer, C. Largely additive effects of gibberellin and strigolactone on gene expression in Arabidopsis thaliana seedlings. Plant J. 92, 924–938 (2017).

    Article  CAS  PubMed  Google Scholar 

  20. Wallner, E. S., López-Salmerón, V. & Greb, T. Strigolactone versus gibberellin signaling: reemerging concepts? Planta 243, 1339–1350 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. de Saint Germain, A. et al. Strigolactones stimulate internode elongation independently of gibberellins. Plant Physiol. 163, 1012–1025 (2013).

    Article  CAS  Google Scholar 

  22. Tsuchiya, Y., Yoshimura, M. & Hagihara, S. The dynamics of strigolactone perception in Striga hermonthica: a working hypothesis. J. Exp. Bot. 69, 2281–2290 (2018).

    Article  CAS  PubMed  Google Scholar 

  23. Xie, X., Yoneyama, K. & Yoneyama, K. The strigolactone story. Annu. Rev. Phytopathol. 48, 93–117 (2010).

    Article  CAS  PubMed  Google Scholar 

  24. Lee, S. et al. Gibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following imbibition. Genes Dev. 16, 646–658 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Bassel, G. W. et al. Genome-wide network model capturing seed germination reveals coordinated regulation of plant cellular phase transitions. Proc. Natl Acad. Sci. USA 108, 9709–9714 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Cao, D. et al. Gibberellin mobilizes distinct DELLA-dependent transcriptomes to regulate seed germination and floral development in Arabidopsis. Plant Physiol. 142, 509–525 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Yang, Z. et al. Comparative transcriptome analyses reveal core parasitism genes and suggest gene duplication and repurposing as sources of structural novelty. Mol. Biol. Evol. 32, 767–790 (2015).

    Article  CAS  PubMed  Google Scholar 

  28. Flematti, G. R., Ghisalberti, E. L., Dixon, K. W. & Trengove, R. D. A compound from smoke that promotes seed germination. Science 305, 977 (2004).

    Article  CAS  PubMed  Google Scholar 

  29. Nelson, D. C. et al. Karrikins enhance light responses during germination and seedling development in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 107, 7095–7100 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Nelson, D. C. et al. F-box protein MAX2 has dual roles in karrikin and strigolactone signaling in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 108, 8897–8902 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Toh, S. et al. Detection of parasitic plant suicide germination compounds using a high-throughput Arabidopsis HTL/KAI2 strigolactone perception system. Chem. Biol. 21, 988 (2014).

    Article  CAS  PubMed  Google Scholar 

  32. Xu, Y. et al. Structural analysis of HTL and D14 proteins reveals the basis for ligand selectivity in Striga. Nat. Commun. 9, 1 (2018).

    Article  CAS  Google Scholar 

  33. Wallner, E.-S. et al. Strigolactone- and karrikin-independent SMXL proteins are central regulators of phloem formation. Curr. Biol. 27, 1241–1247 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Nelson, D. C. et al. Karrikins discovered in smoke trigger Arabidopsis seed germination by a mechanism requiring gibberellic acid synthesis and light. Plant Physiol. 149, 863–873 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Marín-de la Rosa, N. et al. Large-scale identification of gibberellin-related transcription factors defines group VII ETHYLENE RESPONSE FACTORS as functional DELLA partners. Plant Physiol. 166, 1022–1032 (2014).

    Article  PubMed  CAS  Google Scholar 

  36. Chung, M. H., Chen, M. K. & Pan, S. M. Floral spray transformation can efficiently generate Arabidopsis. Transgenic Res. 9, 471–486 (2000).

    Article  CAS  PubMed  Google Scholar 

  37. Harrison, S. J. et al. A rapid and robust method of identifying transformed Arabidopsis thaliana seedlings following floral dip transformation. Plant Methods 2, 19 (2006).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Gomez-Roldan, V. et al. Strigolactone inhibition of shoot branching. Nature 455, 189–194 (2008).

    Article  CAS  PubMed  Google Scholar 

  39. Suzuki, Y., Kawazu, T. & Koyama, H. RNA isolation from siliques, dry seeds, and other tissues of Arabidopsis thaliana. Biotechniques 37, 542–544 (2004).

    Article  CAS  PubMed  Google Scholar 

  40. Kim, D., Langmead, B. & Salzberg, S. L. HISAT: a fast spliced aligner with low memory requirements. Nat. Methods 12, 357–360 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Li, B. & Dewey, C. N. RSEM: accurate transcript quantification from RNA-seq data with or without a reference genome. BMC Bioinformatics 12, 323 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. de Hoon, M. J. L., Imoto, S., Nolan, J. & Miyano, S. Open source clustering software. Bioinformatics 20, 1453–1454 (2004).

    Article  CAS  PubMed  Google Scholar 

  43. Saldanha, A. J. Java Treeview—extensible visualization of microarray data. Bioinformatics 20, 3246–3248 (2004).

    Article  CAS  PubMed  Google Scholar 

  44. Long, S. S. et al. A simple staining method for observation of germinated Striga seeds. Seed Sci. Res. 18, 125–129 (2008).

    Article  Google Scholar 

  45. Graeber, K. et al. A guideline to family-wide comparative state-of-the-art quantitative RT–PCR analysis exemplified with a Brassicaceae cross-species seed germination case study. Plant Cell 23, 2045–2063 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402–408 (2001).

    Article  CAS  PubMed  Google Scholar 

  47. Winter, D. et al. An “electronic fluorescent pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2, e718 (2007).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgements

We thank D. Nelson for the gift of smax1, smax1; smxl2 and max2; smax1 seeds, and T. Sun for the RGL2 clone. We acknowledge the contribution of P. McCourt for discussions and feedback on our manuscript. We acknowledge the Arabidopsis Biological Resource Center for obtaining ga1 mutants and the Parasitic Plant Genome Project for publicly available Striga transcriptome datasets. This work was supported by the Natural Sciences and Engineering Research Council of Canada in the form of a Discovery Grant (no. 06752), an Accelerator Supplement (no. 507992) and a Research Tools and Instruments grant awarded to S.L.

Author information

Authors and Affiliations

Authors

Contributions

S.L. contributed to all aspects of the research. M.B. designed and performed experiments, and analysed and interpreted data. S.T. contributed to the general conception of the project, and performed RT–qPCR in Arabidopsis and physiological experiments on Striga. C.W. constructed transgenic Arabidopsis lines and performed cell biology experiments using confocal microscopy. Z.X. performed RT–qPCR experiments and contributed to physiological assays. G.L. analysed RNA-seq data from Arabidopsis and identified homologues of Arabidopsis genes in S. hermonthica sequence datasets. C.S.P.M. contributed compounds required to conduct physiological experiments. G.P., K.E.N., P.S. and J.D.L. contributed to the generation of Arabidopsis transgenic lines and performed germination assays. J.D.S. provided S. hermonthica sequences and helped identify Striga homologues. S.L. and M.B. wrote the manuscript. S.L. directed and supervised all of the research.

Corresponding author

Correspondence to Shelley Lumba.

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The authors declare no competing interests.

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Peer review information Nature Plants thanks Tom Bennett, Yuichiro Tsuchiya and Ruifeng Yao for their contribution to the peer review of this work.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–8.

Reporting Summary

Supplementary Table 1

List of statistical values for Figs. and Supplementary Figs.

Supplementary Table 2

Transcriptome data and lists of genes, strains and primers used in this study.

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Bunsick, M., Toh, S., Wong, C. et al. SMAX1-dependent seed germination bypasses GA signalling in Arabidopsis and Striga. Nat. Plants 6, 646–652 (2020). https://doi.org/10.1038/s41477-020-0653-z

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