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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.

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.

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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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