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Functional characterization of the pinoresinol–lariciresinol reductase-2 gene reveals its roles in yatein biosynthesis and flax defense response

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Abstract

Main conclusion

This study provides new insights into the biosynthesis regulation and in planta function of the lignan yatein in flax leaves.

Pinoresinol–lariciresinol reductases (PLR) catalyze the conversion of pinoresinol into secoisolariciresinol (SECO) in lignan biosynthesis. Several lignans are accumulated in high concentrations, such as SECO accumulated as secoisolariciresinol diglucoside (SDG) in seeds and yatein in aerial parts, in the flax plant (Linum usitatissimum L.) from which two PLR enzymes of opposite enantioselectivity have been isolated. While LuPLR1 catalyzes the biosynthesis of (+)-SECO leading to (+)-SDG in seeds, the role(s) of the second PLR (LuPLR2) is not completely elucidated. This study provides new insights into the in planta regulation and function of the lignan yatein in flax leaves: its biosynthesis relies on a different PLR with opposite stereospecificity but also on a distinct expression regulation. RNAi technology provided evidence for the in vivo involvement of the LuPLR2 gene in the biosynthesis of (−)-yatein accumulated in flax leaves. LuPLR2 expression in different tissues and in response to stress was studied by RT-qPCR and promoter-reporter transgenesis showing that the spatio-temporal expression of the LuPLR2 gene in leaves perfectly matches the (−)-yatein accumulation and that LuPLR2 expression and yatein production are increased by methyl jasmonate and wounding. A promoter deletion approach yielded putative regulatory elements. This expression pattern in relation to a possible role for this lignan in flax defense is discussed.

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Abbreviations

GUS:

β-Glucuronidase

MeJA:

Methyl jasmonate

4-MUG:

4-Methylumbelliferyl-β-d-glucuronide

PLR:

Pinoresinol–lariciresinol reductase

SA:

Salicylic acid

SDG:

Secoisolariciresinol diglucoside

SECO:

Secoisolariciresinol

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Acknowledgements

This research was funded by Conseil Départemental d’Eure et Loir, Ligue Contre le Cancer Comité d’Eure et Loir, Région Centre Val de Loire and Ministère Enseignement Supérieur, Recherche et Technologies. We wish to thank JP Trouvé (Coopérative Terre de Lin) for donating seeds. The authors thank Carol Robins (Scientific English) for English editing.

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  1. Cyrielle Corbin, Samantha Drouet, and Ivan Mateljak contributed equally to this work.

Authors and Affiliations

  1. Laboratoire de Biologie des Ligneux et des Grandes Cultures (LBLGC), INRA USC1328, Université d’Orléans, 21 rue de Loigny la Bataille, 28000, Chartres, France

    Cyrielle Corbin, Samantha Drouet, Ivan Mateljak, Lucija Markulin, Cédric Decourtil, Sullivan Renouard, Tatiana Lopez, Joël Doussot, Frédéric Lamblin, Daniel Auguin, Eric Lainé & Christophe Hano

  2. Ecole SITI, Département CASER, Le CNAM, Paris, France

    Joël Doussot

  3. Interfaculty Institute of Biochemistry, Hoppe-Seyler-St. 4, 72076, Tübingen, Germany

    Elisabeth Fuss

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Correspondence to Christophe Hano.

Electronic supplementary material

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425_2017_2701_MOESM1_ESM.pptx

Online Resource S1 ClustalW alignment of the LuPLR2 gene putative promoter region isolated by chromosome walking and the corresponding sequence deposited in the Phytozome database resulting from the flax genome sequencing project (Wang et al. 2012) (PPTX 55 kb)

425_2017_2701_MOESM2_ESM.pptx

Online Resource S2 Putative cis-acting elements located in the 1,207 nucleotide sequence of the 5’ non-coding region of the LuPLR2 gene detected using the data available on the PlantPAN (PPTX 48 kb)

425_2017_2701_MOESM3_ESM.docx

Online Resource S3 a Comparison of the normalized LuPLR1 and LuPLR2 gene expression measured by RT-qPCR in flax leaves and b during the first seed developmental stages. Developmental stages are described by Hano et al. (2006). WS is for whole seed. Briefly, WS0-1: 4–10 days after flowering, from no visible to 0.5-mm embryo, WS2: 16 days after flowering, from 2- to 3-mm embryo, WS3: 20 days after flowering, from 4- to 5-mm embryo. Data are expressed as the mean of n=4 independent experiments ± standard deviation of the mean (DOCX 29 kb)

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Corbin, C., Drouet, S., Mateljak, I. et al. Functional characterization of the pinoresinol–lariciresinol reductase-2 gene reveals its roles in yatein biosynthesis and flax defense response. Planta 246, 405–420 (2017). https://doi.org/10.1007/s00425-017-2701-0

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