Strigolactone biosynthesis is evolutionarily conserved, regulated by phosphate starvation and contributes to resistance against phytopathogenic fungi in a moss, Physcomitrella patens

Eva L. Decker; Adrian Alder; Stefan Hunn; Jenny Ferguson; Mikko T. Lehtonen; Bjoern Scheler; Klaus L. Kerres; Gertrud Wiedemann; Vajiheh Safavi-Rizi; Steffen Nordzieke; Aparna Balakrishna; Lina Baz; Javier Avalos; Jari P. T. Valkonen; Ralf Reski; Salim Al-Babili

doi:10.1111/nph.14506

Strigolactone biosynthesis is evolutionarily conserved, regulated by phosphate starvation and contributes to resistance against phytopathogenic fungi in a moss, Physcomitrella patens

Eva L. Decker, Adrian Alder, Stefan Hunn, Jenny Ferguson, Mikko T. Lehtonen, Bjoern Scheler, Klaus L. Kerres, Gertrud Wiedemann, Vajiheh Safavi-Rizi, Steffen Nordzieke, Aparna Balakrishna, Lina Baz, Javier Avalos, Jari P. T. Valkonen, Ralf Reski, Salim Al-Babili

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Abstract

In seed plants, strigolactones (SLs) regulate architecture and induce mycorrhizal symbiosis in response to environmental cues. SLs are formed by combined activity of the carotenoid cleavage dioxygenases (CCDs) 7 and 8 from 9-cis-β-carotene, leading to carlactone that is converted by cytochromes P450 (clade 711; MAX1 in Arabidopsis) into various SLs. As Physcomitrella patens possesses CCD7 and CCD8 homologs but lacks MAX1, we investigated if PpCCD7 together with PpCCD8 form carlactone and how deletion of these enzymes influences growth and interactions with the environment. We investigated the enzymatic activity of PpCCD7 and PpCCD8 in vitro, identified the formed products by high performance liquid chromatography (HPLC) and LC-MS, and generated and analysed ΔCCD7 and ΔCCD8 mutants. We defined enzymatic activity of PpCCD7 as a stereospecific 9-cis-CCD and PpCCD8 as a carlactone synthase. ΔCCD7 and ΔCCD8 lines showed enhanced caulonema growth, which was revertible by adding the SL analogue GR24 or carlactone. Wild-type (WT) exudates induced seed germination in Orobanche ramosa. This activity was increased upon phosphate starvation and abolished in exudates of both mutants. Furthermore, both mutants showed increased susceptibility to phytopathogenic fungi. Our study reveals the deep evolutionary conservation of SL biosynthesis, SL function, and its regulation by biotic and abiotic cues.

Original language	English (US)
Pages (from-to)	455-468
Number of pages	14
Journal	New Phytologist
Volume	216
Issue number	2
DOIs	https://doi.org/10.1111/nph.14506
State	Published - Mar 6 2017

Bibliographical note

KAUST Repository Item: Exported on 2020-10-01
Acknowledgements: We thank Harro Bouwmeester and Carolien Ruyter-Spira for valuable discussions, Agnes Novakovic for supporting the generation and analysis of DCCD lines, and Anne Katrin Prowse for editing the language of the manuscript. This work was supported by the Deutsche Forschungsgemeinschaft (DFG; grant AL892/1- 4 and the Graduiertenkolleg 1305 ‘Plant Signal Systems’), King Abdullah University of Science and Technology (KAUST; baseline funding of S.A-B.), the Excellence Initiative of the German Federal and State Governments (grant no. EXC 294 BIOSS to R.R.), and The Academy of Finland (grant 1253126 to J.P.T.V.).

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Decker, E. L., Alder, A., Hunn, S., Ferguson, J., Lehtonen, M. T., Scheler, B., Kerres, K. L., Wiedemann, G., Safavi-Rizi, V., Nordzieke, S., Balakrishna, A., Baz, L., Avalos, J., Valkonen, J. P. T., Reski, R., & Al-Babili, S. (2017). Strigolactone biosynthesis is evolutionarily conserved, regulated by phosphate starvation and contributes to resistance against phytopathogenic fungi in a moss, Physcomitrella patens. New Phytologist, 216(2), 455-468. https://doi.org/10.1111/nph.14506

@article{7bd44bb237fd4cb6898ede9cf0c35550,

title = "Strigolactone biosynthesis is evolutionarily conserved, regulated by phosphate starvation and contributes to resistance against phytopathogenic fungi in a moss, Physcomitrella patens",

abstract = "In seed plants, strigolactones (SLs) regulate architecture and induce mycorrhizal symbiosis in response to environmental cues. SLs are formed by combined activity of the carotenoid cleavage dioxygenases (CCDs) 7 and 8 from 9-cis-β-carotene, leading to carlactone that is converted by cytochromes P450 (clade 711; MAX1 in Arabidopsis) into various SLs. As Physcomitrella patens possesses CCD7 and CCD8 homologs but lacks MAX1, we investigated if PpCCD7 together with PpCCD8 form carlactone and how deletion of these enzymes influences growth and interactions with the environment. We investigated the enzymatic activity of PpCCD7 and PpCCD8 in vitro, identified the formed products by high performance liquid chromatography (HPLC) and LC-MS, and generated and analysed ΔCCD7 and ΔCCD8 mutants. We defined enzymatic activity of PpCCD7 as a stereospecific 9-cis-CCD and PpCCD8 as a carlactone synthase. ΔCCD7 and ΔCCD8 lines showed enhanced caulonema growth, which was revertible by adding the SL analogue GR24 or carlactone. Wild-type (WT) exudates induced seed germination in Orobanche ramosa. This activity was increased upon phosphate starvation and abolished in exudates of both mutants. Furthermore, both mutants showed increased susceptibility to phytopathogenic fungi. Our study reveals the deep evolutionary conservation of SL biosynthesis, SL function, and its regulation by biotic and abiotic cues.",

author = "Decker, {Eva L.} and Adrian Alder and Stefan Hunn and Jenny Ferguson and Lehtonen, {Mikko T.} and Bjoern Scheler and Kerres, {Klaus L.} and Gertrud Wiedemann and Vajiheh Safavi-Rizi and Steffen Nordzieke and Aparna Balakrishna and Lina Baz and Javier Avalos and Valkonen, {Jari P. T.} and Ralf Reski and Salim Al-Babili",

note = "KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: We thank Harro Bouwmeester and Carolien Ruyter-Spira for valuable discussions, Agnes Novakovic for supporting the generation and analysis of DCCD lines, and Anne Katrin Prowse for editing the language of the manuscript. This work was supported by the Deutsche Forschungsgemeinschaft (DFG; grant AL892/1- 4 and the Graduiertenkolleg 1305 {\textquoteleft}Plant Signal Systems{\textquoteright}), King Abdullah University of Science and Technology (KAUST; baseline funding of S.A-B.), the Excellence Initiative of the German Federal and State Governments (grant no. EXC 294 BIOSS to R.R.), and The Academy of Finland (grant 1253126 to J.P.T.V.).",

year = "2017",

month = mar,

day = "6",

doi = "10.1111/nph.14506",

language = "English (US)",

volume = "216",

pages = "455--468",

journal = "New Phytologist",

issn = "0028-646X",

publisher = "Wiley-Blackwell Publishing Ltd",

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Decker, EL, Alder, A, Hunn, S, Ferguson, J, Lehtonen, MT, Scheler, B, Kerres, KL, Wiedemann, G, Safavi-Rizi, V, Nordzieke, S, Balakrishna, A, Baz, L, Avalos, J, Valkonen, JPT, Reski, R & Al-Babili, S 2017, 'Strigolactone biosynthesis is evolutionarily conserved, regulated by phosphate starvation and contributes to resistance against phytopathogenic fungi in a moss, Physcomitrella patens', New Phytologist, vol. 216, no. 2, pp. 455-468. https://doi.org/10.1111/nph.14506

TY - JOUR

T1 - Strigolactone biosynthesis is evolutionarily conserved, regulated by phosphate starvation and contributes to resistance against phytopathogenic fungi in a moss, Physcomitrella patens

AU - Decker, Eva L.

AU - Alder, Adrian

AU - Hunn, Stefan

AU - Ferguson, Jenny

AU - Lehtonen, Mikko T.

AU - Scheler, Bjoern

AU - Kerres, Klaus L.

AU - Wiedemann, Gertrud

AU - Safavi-Rizi, Vajiheh

AU - Nordzieke, Steffen

AU - Balakrishna, Aparna

AU - Baz, Lina

AU - Avalos, Javier

AU - Valkonen, Jari P. T.

AU - Reski, Ralf

AU - Al-Babili, Salim

N1 - KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: We thank Harro Bouwmeester and Carolien Ruyter-Spira for valuable discussions, Agnes Novakovic for supporting the generation and analysis of DCCD lines, and Anne Katrin Prowse for editing the language of the manuscript. This work was supported by the Deutsche Forschungsgemeinschaft (DFG; grant AL892/1- 4 and the Graduiertenkolleg 1305 ‘Plant Signal Systems’), King Abdullah University of Science and Technology (KAUST; baseline funding of S.A-B.), the Excellence Initiative of the German Federal and State Governments (grant no. EXC 294 BIOSS to R.R.), and The Academy of Finland (grant 1253126 to J.P.T.V.).

PY - 2017/3/6

Y1 - 2017/3/6

N2 - In seed plants, strigolactones (SLs) regulate architecture and induce mycorrhizal symbiosis in response to environmental cues. SLs are formed by combined activity of the carotenoid cleavage dioxygenases (CCDs) 7 and 8 from 9-cis-β-carotene, leading to carlactone that is converted by cytochromes P450 (clade 711; MAX1 in Arabidopsis) into various SLs. As Physcomitrella patens possesses CCD7 and CCD8 homologs but lacks MAX1, we investigated if PpCCD7 together with PpCCD8 form carlactone and how deletion of these enzymes influences growth and interactions with the environment. We investigated the enzymatic activity of PpCCD7 and PpCCD8 in vitro, identified the formed products by high performance liquid chromatography (HPLC) and LC-MS, and generated and analysed ΔCCD7 and ΔCCD8 mutants. We defined enzymatic activity of PpCCD7 as a stereospecific 9-cis-CCD and PpCCD8 as a carlactone synthase. ΔCCD7 and ΔCCD8 lines showed enhanced caulonema growth, which was revertible by adding the SL analogue GR24 or carlactone. Wild-type (WT) exudates induced seed germination in Orobanche ramosa. This activity was increased upon phosphate starvation and abolished in exudates of both mutants. Furthermore, both mutants showed increased susceptibility to phytopathogenic fungi. Our study reveals the deep evolutionary conservation of SL biosynthesis, SL function, and its regulation by biotic and abiotic cues.

AB - In seed plants, strigolactones (SLs) regulate architecture and induce mycorrhizal symbiosis in response to environmental cues. SLs are formed by combined activity of the carotenoid cleavage dioxygenases (CCDs) 7 and 8 from 9-cis-β-carotene, leading to carlactone that is converted by cytochromes P450 (clade 711; MAX1 in Arabidopsis) into various SLs. As Physcomitrella patens possesses CCD7 and CCD8 homologs but lacks MAX1, we investigated if PpCCD7 together with PpCCD8 form carlactone and how deletion of these enzymes influences growth and interactions with the environment. We investigated the enzymatic activity of PpCCD7 and PpCCD8 in vitro, identified the formed products by high performance liquid chromatography (HPLC) and LC-MS, and generated and analysed ΔCCD7 and ΔCCD8 mutants. We defined enzymatic activity of PpCCD7 as a stereospecific 9-cis-CCD and PpCCD8 as a carlactone synthase. ΔCCD7 and ΔCCD8 lines showed enhanced caulonema growth, which was revertible by adding the SL analogue GR24 or carlactone. Wild-type (WT) exudates induced seed germination in Orobanche ramosa. This activity was increased upon phosphate starvation and abolished in exudates of both mutants. Furthermore, both mutants showed increased susceptibility to phytopathogenic fungi. Our study reveals the deep evolutionary conservation of SL biosynthesis, SL function, and its regulation by biotic and abiotic cues.

UR - http://hdl.handle.net/10754/623062

UR - http://onlinelibrary.wiley.com/doi/10.1111/nph.14506/abstract

UR - http://www.scopus.com/inward/record.url?scp=85014476210&partnerID=8YFLogxK

U2 - 10.1111/nph.14506

DO - 10.1111/nph.14506

M3 - Article

C2 - 28262967

SN - 0028-646X

VL - 216

SP - 455

EP - 468

JO - New Phytologist

JF - New Phytologist

IS - 2

ER -

Strigolactone biosynthesis is evolutionarily conserved, regulated by phosphate starvation and contributes to resistance against phytopathogenic fungi in a moss, Physcomitrella patens

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