The Arabidopsis D27-LIKE1 is a cis/cis/trans-β-carotene isomerase that contributes to Strigolactone biosynthesis and negatively impacts ABA level

Yu Yang; Haneen Abuauf; Shanshan Song; Jian You Wang; Yagiz Alagoz; Juan C. Moreno; Jianing Mi; Abdugaffor Ablazov; Muhammad Jamil; Shawkat Ali; Xiongjie Zheng; Aparna Balakrishna; Ikram Blilou; Salim Al-Babili

doi:10.1111/tpj.16095

The Arabidopsis D27-LIKE1 is a cis/cis/trans-β-carotene isomerase that contributes to Strigolactone biosynthesis and negatively impacts ABA level

Yu Yang, Haneen Abuauf, Shanshan Song, Jian You Wang, Yagiz Alagoz, Juan C. Moreno, Jianing Mi, Abdugaffor Ablazov, Muhammad Jamil, Shawkat Ali, Xiongjie Zheng, Aparna Balakrishna, Ikram Blilou, Salim Al-Babili^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

7 Scopus citations

Abstract

The enzyme DWARF27 (D27) catalyzes the reversible isomerization of all-trans- into 9-cis-β-carotene, initiating strigolactone (SL) biosynthesis. Genomes of higher plants encode two D27-homologs, D27-like1 and -like2, with unknown functions. Here, we investigated the enzymatic activity and biological function of the Arabidopsis D27-like1. In vitro enzymatic assays and expression in Synechocystis sp. PCC6803 revealed an unreported 13-cis/15-cis/9-cis- and a 9-cis/all-trans-β-carotene isomerization. Although disruption of AtD27-like1 did not cause SL deficiency phenotypes, overexpression of AtD27-like1 in the d27 mutant restored the more-branching phenotype, indicating a contribution of AtD27-like1 to SL biosynthesis. Accordingly, generated d27 d27like1 double mutants showed a more pronounced branching phenotype compared to d27. The contribution of AtD27-like1 to SL biosynthesis is likely a result of its formation of 9-cis-β-carotene that was present at higher levels in AtD27-like1 overexpressing lines. By contrast, AtD27-like1 expression correlated negatively with the content of 9-cis-violaxanthin, a precursor of ABA, in shoots. Consistently, ABA levels were higher in shoots and also in dry seeds of the d27like1 and d27 d27like1 mutants. Transgenic lines expressing GUS driven by the AtD27LIKE1 promoter and transcript analysis of hormone-treated Arabidopsis seedlings revealed that AtD27LIKE1 is expressed in different tissues and affects ABA and auxin. Taken together, our work reports a cis/cis-β-carotene isomerase that affects the content of both cis-carotenoid-derived plant hormones, ABA and SLs.

Original language	English (US)
Pages (from-to)	986-1003
Number of pages	18
Journal	Plant Journal
Volume	113
Issue number	5
DOIs	https://doi.org/10.1111/tpj.16095
State	Published - Mar 2023

Bibliographical note

Funding Information:
This work was supported by Baseline funding and Competitive Research Grants 7 and 9 (CRG7, 9) from King Abdullah University of Science and Technology to S.A‐B. We thank all members of the BioActives Lab at KAUST for their helpful discussions. We also thank the members of KAUST Greenhouse core lab for their kind support and Dr Li Yang for her kind help with the isomerization of 9‐‐violaxanthin from KAUST Catalysis Center. cis

Publisher Copyright:
© 2023 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.

Keywords

9-cis-violaxanthin
ABA
D27LIKE1
strigolactones
β-carotene

ASJC Scopus subject areas

Genetics
Plant Science
Cell Biology

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10.1111/tpj.16095

Cite this

Yang, Y., Abuauf, H., Song, S., Wang, J. Y., Alagoz, Y., Moreno, J. C., Mi, J., Ablazov, A., Jamil, M., Ali, S., Zheng, X., Balakrishna, A., Blilou, I., & Al-Babili, S. (2023). The Arabidopsis D27-LIKE1 is a cis/cis/trans-β-carotene isomerase that contributes to Strigolactone biosynthesis and negatively impacts ABA level. Plant Journal, 113(5), 986-1003. https://doi.org/10.1111/tpj.16095

@article{33b2594310724875ae258316207eb000,

title = "The Arabidopsis D27-LIKE1 is a cis/cis/trans-β-carotene isomerase that contributes to Strigolactone biosynthesis and negatively impacts ABA level",

abstract = "The enzyme DWARF27 (D27) catalyzes the reversible isomerization of all-trans- into 9-cis-β-carotene, initiating strigolactone (SL) biosynthesis. Genomes of higher plants encode two D27-homologs, D27-like1 and -like2, with unknown functions. Here, we investigated the enzymatic activity and biological function of the Arabidopsis D27-like1. In vitro enzymatic assays and expression in Synechocystis sp. PCC6803 revealed an unreported 13-cis/15-cis/9-cis- and a 9-cis/all-trans-β-carotene isomerization. Although disruption of AtD27-like1 did not cause SL deficiency phenotypes, overexpression of AtD27-like1 in the d27 mutant restored the more-branching phenotype, indicating a contribution of AtD27-like1 to SL biosynthesis. Accordingly, generated d27 d27like1 double mutants showed a more pronounced branching phenotype compared to d27. The contribution of AtD27-like1 to SL biosynthesis is likely a result of its formation of 9-cis-β-carotene that was present at higher levels in AtD27-like1 overexpressing lines. By contrast, AtD27-like1 expression correlated negatively with the content of 9-cis-violaxanthin, a precursor of ABA, in shoots. Consistently, ABA levels were higher in shoots and also in dry seeds of the d27like1 and d27 d27like1 mutants. Transgenic lines expressing GUS driven by the AtD27LIKE1 promoter and transcript analysis of hormone-treated Arabidopsis seedlings revealed that AtD27LIKE1 is expressed in different tissues and affects ABA and auxin. Taken together, our work reports a cis/cis-β-carotene isomerase that affects the content of both cis-carotenoid-derived plant hormones, ABA and SLs.",

keywords = "9-cis-violaxanthin, ABA, D27LIKE1, strigolactones, β-carotene",

author = "Yu Yang and Haneen Abuauf and Shanshan Song and Wang, {Jian You} and Yagiz Alagoz and Moreno, {Juan C.} and Jianing Mi and Abdugaffor Ablazov and Muhammad Jamil and Shawkat Ali and Xiongjie Zheng and Aparna Balakrishna and Ikram Blilou and Salim Al-Babili",

note = "Funding Information: This work was supported by Baseline funding and Competitive Research Grants 7 and 9 (CRG7, 9) from King Abdullah University of Science and Technology to S.A‐B. We thank all members of the BioActives Lab at KAUST for their helpful discussions. We also thank the members of KAUST Greenhouse core lab for their kind support and Dr Li Yang for her kind help with the isomerization of 9‐‐violaxanthin from KAUST Catalysis Center. cis Publisher Copyright: {\textcopyright} 2023 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.",

year = "2023",

month = mar,

doi = "10.1111/tpj.16095",

language = "English (US)",

volume = "113",

pages = "986--1003",

journal = "Plant Journal",

issn = "0960-7412",

publisher = "Wiley",

number = "5",

}

Yang, Y, Abuauf, H, Song, S , Wang, JY , Alagoz, Y, Moreno, JC, Mi, J, Ablazov, A , Jamil, M, Ali, S, Zheng, X , Balakrishna, A , Blilou, I & Al-Babili, S 2023, 'The Arabidopsis D27-LIKE1 is a cis/cis/trans-β-carotene isomerase that contributes to Strigolactone biosynthesis and negatively impacts ABA level', Plant Journal, vol. 113, no. 5, pp. 986-1003. https://doi.org/10.1111/tpj.16095

TY - JOUR

T1 - The Arabidopsis D27-LIKE1 is a cis/cis/trans-β-carotene isomerase that contributes to Strigolactone biosynthesis and negatively impacts ABA level

AU - Yang, Yu

AU - Abuauf, Haneen

AU - Song, Shanshan

AU - Wang, Jian You

AU - Alagoz, Yagiz

AU - Moreno, Juan C.

AU - Mi, Jianing

AU - Ablazov, Abdugaffor

AU - Jamil, Muhammad

AU - Ali, Shawkat

AU - Zheng, Xiongjie

AU - Balakrishna, Aparna

AU - Blilou, Ikram

AU - Al-Babili, Salim

N1 - Funding Information: This work was supported by Baseline funding and Competitive Research Grants 7 and 9 (CRG7, 9) from King Abdullah University of Science and Technology to S.A‐B. We thank all members of the BioActives Lab at KAUST for their helpful discussions. We also thank the members of KAUST Greenhouse core lab for their kind support and Dr Li Yang for her kind help with the isomerization of 9‐‐violaxanthin from KAUST Catalysis Center. cis Publisher Copyright: © 2023 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.

PY - 2023/3

Y1 - 2023/3

N2 - The enzyme DWARF27 (D27) catalyzes the reversible isomerization of all-trans- into 9-cis-β-carotene, initiating strigolactone (SL) biosynthesis. Genomes of higher plants encode two D27-homologs, D27-like1 and -like2, with unknown functions. Here, we investigated the enzymatic activity and biological function of the Arabidopsis D27-like1. In vitro enzymatic assays and expression in Synechocystis sp. PCC6803 revealed an unreported 13-cis/15-cis/9-cis- and a 9-cis/all-trans-β-carotene isomerization. Although disruption of AtD27-like1 did not cause SL deficiency phenotypes, overexpression of AtD27-like1 in the d27 mutant restored the more-branching phenotype, indicating a contribution of AtD27-like1 to SL biosynthesis. Accordingly, generated d27 d27like1 double mutants showed a more pronounced branching phenotype compared to d27. The contribution of AtD27-like1 to SL biosynthesis is likely a result of its formation of 9-cis-β-carotene that was present at higher levels in AtD27-like1 overexpressing lines. By contrast, AtD27-like1 expression correlated negatively with the content of 9-cis-violaxanthin, a precursor of ABA, in shoots. Consistently, ABA levels were higher in shoots and also in dry seeds of the d27like1 and d27 d27like1 mutants. Transgenic lines expressing GUS driven by the AtD27LIKE1 promoter and transcript analysis of hormone-treated Arabidopsis seedlings revealed that AtD27LIKE1 is expressed in different tissues and affects ABA and auxin. Taken together, our work reports a cis/cis-β-carotene isomerase that affects the content of both cis-carotenoid-derived plant hormones, ABA and SLs.

AB - The enzyme DWARF27 (D27) catalyzes the reversible isomerization of all-trans- into 9-cis-β-carotene, initiating strigolactone (SL) biosynthesis. Genomes of higher plants encode two D27-homologs, D27-like1 and -like2, with unknown functions. Here, we investigated the enzymatic activity and biological function of the Arabidopsis D27-like1. In vitro enzymatic assays and expression in Synechocystis sp. PCC6803 revealed an unreported 13-cis/15-cis/9-cis- and a 9-cis/all-trans-β-carotene isomerization. Although disruption of AtD27-like1 did not cause SL deficiency phenotypes, overexpression of AtD27-like1 in the d27 mutant restored the more-branching phenotype, indicating a contribution of AtD27-like1 to SL biosynthesis. Accordingly, generated d27 d27like1 double mutants showed a more pronounced branching phenotype compared to d27. The contribution of AtD27-like1 to SL biosynthesis is likely a result of its formation of 9-cis-β-carotene that was present at higher levels in AtD27-like1 overexpressing lines. By contrast, AtD27-like1 expression correlated negatively with the content of 9-cis-violaxanthin, a precursor of ABA, in shoots. Consistently, ABA levels were higher in shoots and also in dry seeds of the d27like1 and d27 d27like1 mutants. Transgenic lines expressing GUS driven by the AtD27LIKE1 promoter and transcript analysis of hormone-treated Arabidopsis seedlings revealed that AtD27LIKE1 is expressed in different tissues and affects ABA and auxin. Taken together, our work reports a cis/cis-β-carotene isomerase that affects the content of both cis-carotenoid-derived plant hormones, ABA and SLs.

KW - 9-cis-violaxanthin

KW - ABA

KW - D27LIKE1

KW - strigolactones

KW - β-carotene

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U2 - 10.1111/tpj.16095

DO - 10.1111/tpj.16095

M3 - Article

C2 - 36602437

AN - SCOPUS:85147017730

SN - 0960-7412

VL - 113

SP - 986

EP - 1003

JO - Plant Journal

JF - Plant Journal

IS - 5

ER -

The Arabidopsis D27-LIKE1 is a cis/cis/trans-β-carotene isomerase that contributes to Strigolactone biosynthesis and negatively impacts ABA level

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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