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Mechanisms of pre-attachment Striga resistance in sorghum through genome-wide association studies

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Abstract

Witchweeds (Striga spp.) greatly limit production of Africa’s most staple crops. These parasitic plants use strigolactones (SLs)—chemical germination stimulants, emitted from host’s roots to germinate, and locate their hosts for invasion. This information exchange provides opportunities for controlling the parasite by either stimulating parasite seed germination without a host (suicidal germination) or by inhibiting parasite seed germination (pre-attachment resistance). We sought to determine genetic factors that underpin Striga pre-attachment resistance in sorghum using the genome wide association study (GWAS) approach. Results revealed that Striga germination was associated with genes encoding hormone signaling functions, e.g., the Novel interactor of jaz (NINJA) and, Abscisic acid-insensitive 5 (ABI5). This pointed toward abscisic acid (ABA) and gibberellic acid (GA) as probable determinants of Striga germination. To test this hypothesis, we conditioned Striga using: ABA, ABA + its inhibitor fluridone (FLU), GA or water. Unexpectedly, Striga conditioned with FLU germinated after 4 days without SL. Upon germination stimulation using sorghum root exudate or the synthetic SL GR24, we found that ABA conditioned seeds had above 20-fold reduction in germination. Conversely, FLU conditioned seeds recorded above 20-fold increase in germination. Conditioning with GA reduced Striga seed germination 1.5-fold only in the GR24 treatment. Germination assays using seeds of a related parasitic plant (Alectra vogelii) showed similar degrees of stimulation and reduction of germination by the hormones further affirming the hormonal crosstalk. Our findings have far-reaching implications in the control of some of the most noxious pathogens of crops in Africa.

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Data availability

The datasets generated or analyzed during the current study are available from the corresponding author on reasonable request.

Abbreviations

ABI5:

Abscisic acid-insensitive 5

GA:

Gibberellic acid (GA)

GWAS:

Genome wide association study

NINJA:

Novel interactor of jaz

SL:

Strigolactones

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Acknowledgements

The research leading to these results received funding from the National Academies of Science (NAS) under the Partnerships for Enhanced Engagement in Research (PEER) program, Grant/Award Number: PGA- 2000008288; NAS and the United States Agency for International Development, Grant/Award Number: AID-OAA-A-11-00012. ICRISAT, Eastern and Southern Africa provided funding to conduct DArT seq. TM’s PhD fellowship is sponsored by the Pan African University (PAUSTI) through an African Union Initiative.

Funding

National Academies of Science (NAS) under the Partnerships for Enhanced Engagement in Research (PEER) program, Grant/Award Number: PGA- 2000008288; NAS and the United States Agency for International Development, Grant/Award Number: AID-OAA-A-11–00012.

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Authors

Contributions

SR and DAO conceived and designed the study. TSM, GI and SM performed Striga and Alectra germination and GWAS analysis guided by SR, DAO and SMG. EO carried out analysis of sequence data, quality control and participated in the GWAS analysis. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Damaris A. Odeny or Steven Runo.

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The authors declare that they have no competing interests.

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Supplementary Information

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438_2022_1882_MOESM1_ESM.tif

Suppl. Fig. S1 Geographic origins of the sorghum used in the GWAS study. Categories are based on the major sorghum races (TIF 9498 kb)

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Suppl Fig. 2 Bayesian Information Criterion (BIC) identification of optimal K clustering. The lowest K (K=8) is indicated by an elbow curve of BIC values (TIF 2850 kb)

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Suppl Fig. S3 Hierarchical Bayesian clustering of sorghum accessions used in the GWAS study using various K values K=7; (CV=0.35293 ) K = 8 (CV=0.35673) and K = 9 (CV=0.36229) (TIF 6641 kb)

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Mallu, T.S., Irafasha, G., Mutinda, S. et al. Mechanisms of pre-attachment Striga resistance in sorghum through genome-wide association studies. Mol Genet Genomics 297, 751–762 (2022). https://doi.org/10.1007/s00438-022-01882-6

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  • DOI: https://doi.org/10.1007/s00438-022-01882-6

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