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Structural modelling and transcriptional responses highlight a clade of PpKAI2-LIKE genes as candidate receptors for strigolactones in Physcomitrella patens

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Abstract

Main conclusion

A set of PpKAI2 - LIKE paralogs that may encode strigolactone receptors in Physcomitrella patens were identified through evolutionary, structural, and transcriptional analyses, suggesting that strigolactone perception may have evolved independently in basal land plants in a similar manner as spermatophytes.

Carotenoid-derived compounds known as strigolactones are a new class of plant hormones that modulate development and interactions with parasitic plants and arbuscular mycorrhizal fungi. The strigolactone receptor protein DWARF14 (D14) belongs to the α/β hydrolase family. D14 is closely related to KARRIKIN INSENSITIVE2 (KAI2), a receptor of smoke-derived germination stimulants called karrikins. Strigolactone and karrikin structures share a butenolide ring that is necessary for bioactivity. Charophyte algae and basal land plants produce strigolactones that influence their development. However phylogenetic studies suggest that D14 is absent from algae, moss, and liverwort genomes, raising the question of how these basal plants perceive strigolactones. Strigolactone perception during seed germination putatively evolved in parasitic plants through gene duplication and neofunctionalization of KAI2 paralogs. The moss Physcomitrella patens shows an increase in KAI2 gene copy number, similar to parasitic plants. In this study we investigated whether P. patens KAI2-LIKE (PpKAI2L) genes may contribute to strigolactone perception. Based on phylogenetic analyses and homology modelling, we predict that a clade of PpKAI2L proteins have enlarged ligand-binding cavities, similar to D14. We observed that some PpKAI2L genes have transcriptional responses to the synthetic strigolactone GR24 racemate or its enantiomers. These responses were influenced by light and dark conditions. Moreover, (+)-GR24 seems to be the active enantiomer that induces the transcriptional responses of PpKAI2L genes. We hypothesize that members of specific PpKAI2L clades are candidate strigolactone receptors in moss.

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Abbreviations

D14:

DWARF14

DE:

Differentially expressed

HTL:

HYPOSENSITIVE TO LIGHT

KAI2:

KARRIKIN INSENSITIVE2

KAR:

Karrikin

KL:

KAI2 ligand

PpKAI2L:

Physcomitrella patens KAI2-LIKE

SL:

Strigolactone

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Acknowledgments

The authors would like to thank F. -D. Boyer (Institut de Chimie des Substances Naturelles, Gif sur Yvette, France) for providing racemic GR24 and GR24 enantiomers. This research was supported by the Agence Nationale de la Recherche (contract ANR-12-BSV6-004-01), National Science Foundation Grant IOS-1350561 to D. C. N., and a National Science Foundation Graduate Research Fellowship to C. E. C. The IJPB benefits from the support of the Labex Saclay Plant Sciences-SPS (ANR-10-LABX-0040-SPS).

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Authors and Affiliations

  1. Institut Jean-Pierre Bourgin, INRA, AgroParisTech, CNRS, Université Paris-Saclay, RD10, 78026, Versailles Cedex, France

    Mauricio Lopez-Obando, Beate Hoffmann, Catherine Rameau & Sandrine Bonhomme

  2. Department of Genetics, University of Georgia, Athens, GA, 30602, USA

    Caitlin E. Conn & David C. Nelson

  3. Department of Medicine, Imperial College London, London, UK

    Rohan Bythell-Douglas

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  1. Mauricio Lopez-Obando
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  2. Caitlin E. Conn
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  3. Beate Hoffmann
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  4. Rohan Bythell-Douglas
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  5. David C. Nelson
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  6. Catherine Rameau
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Correspondence to David C. Nelson or Sandrine Bonhomme.

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Lopez-Obando, M., Conn, C.E., Hoffmann, B. et al. Structural modelling and transcriptional responses highlight a clade of PpKAI2-LIKE genes as candidate receptors for strigolactones in Physcomitrella patens . Planta 243, 1441–1453 (2016). https://doi.org/10.1007/s00425-016-2481-y

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