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A genome-wide analysis of the flax (Linum usitatissimum L.) dirigent protein family: from gene identification and evolution to differential regulation

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Identification of DIR encoding genes in flax genome. Analysis of phylogeny, gene/protein structures and evolution. Identification of new conserved motifs linked to biochemical functions. Investigation of spatio-temporal gene expression and response to stress.

Abstract

Dirigent proteins (DIRs) were discovered during 8-8′ lignan biosynthesis studies, through identification of stereoselective coupling to afford either (+)- or (−)-pinoresinols from E-coniferyl alcohol. DIRs are also involved or potentially involved in terpenoid, allyl/propenyl phenol lignan, pterocarpan and lignin biosynthesis. DIRs have very large multigene families in different vascular plants including flax, with most still of unknown function. DIR studies typically focus on a small subset of genes and identification of biochemical/physiological functions. Herein, a genome-wide analysis and characterization of the predicted flax DIR 44-membered multigene family was performed, this species being a rich natural grain source of 8-8′ linked secoisolariciresinol-derived lignan oligomers. All predicted DIR sequences, including their promoters, were analyzed together with their public gene expression datasets. Expression patterns of selected DIRs were examined using qPCR, as well as through clustering analysis of DIR gene expression. These analyses further implicated roles for specific DIRs in (−)-pinoresinol formation in seed-coats, as well as (+)-pinoresinol in vegetative organs and/or specific responses to stress. Phylogeny and gene expression analysis segregated flax DIRs into six distinct clusters with new cluster-specific motifs identified. We propose that these findings can serve as a foundation to further systematically determine functions of DIRs, i.e. other than those already known in lignan biosynthesis in flax and other species. Given the differential expression profiles and inducibility of the flax DIR family, we provisionally propose that some DIR genes of unknown function could be involved in different aspects of secondary cell wall biosynthesis and plant defense.

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Acknowledgements

This work was supported by Région Centre Val de Loire, Conseil Départemental d’Eure et Loir, Ligue contre le Cancer (Comité d’Eure et Loir) and French Ministry Enseignement Supérieur et Recherche and by the Chemical Sciences, Geosciences and Biosciences Division, DOE Office of Basic Energy Sciences (DE-FG-0397ER20259). A portion of the research was performed using the Environmental Molecular Sciences Laboratory (EMSL), a DOE Office of Science User Facility sponsored by the Office of Biological and Environmental Research and located at Pacific Northwest National Laboratory (PNNL) in Richland WA.

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  1. Norman G. Lewis and Christophe Hano have equal contribution of the senior authors.

Authors and Affiliations

  1. Laboratoire de Biologie des Ligneux et des Grandes Cultures, INRA USC1328, Université d’Orléans, 28000, Chartres, France

    Cyrielle Corbin, Samantha Drouet, Lucija Markulin, Daniel Auguin, Éric Lainé & Christophe Hano

  2. COSM’ACTIFS, CNRS GDR3711, 28000, Chartres, France

    Cyrielle Corbin, Samantha Drouet, Lucija Markulin, Daniel Auguin, Éric Lainé & Christophe Hano

  3. Institute of Biological Chemistry, Washington State University, Pullman, WA, 99164-6340, USA

    Laurence B. Davin & Norman G. Lewis

  4. Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, WA, 99354, USA

    John R. Cort

  5. Pôle Universitaire d’Eure et Loir, 21 Rue de Loigny la Bataille, 28000, Chartres, France

    Christophe Hano

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  1. Cyrielle Corbin
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  6. Laurence B. Davin
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Contributions

CC contributions included realization of the experiments, participation in data analysis and in joint manuscript writing and revisions. SD and LM contributions included participation to the experiments. DA contributions included participation in protein sequence analysis and in joint manuscript writing and revisions. EL contributions included participation in data analysis and interpretation and in joint manuscript writing and revisions. LBD, JRC and NGL contributions included insights on lignin/lignan biosynthesis, participation in data analysis and interpretation and in joint manuscript writing and revisions. CH contributions included conception, design and participation in the experiments, participation in data analysis and interpretation and in joint manuscript writing and revisions. All the authors approved the manuscript.

Corresponding authors

Correspondence to Norman G. Lewis or Christophe Hano.

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Electronic supplementary material

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Supplementary material 1 Primers for expression analysis of flax selected-DIR (DOCX 44 KB)

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Supplementary material 2 Accession number of the different genes selected as putatively involved in secondary cell wall biosynthesis and remodeling. (DOCX 57 KB)

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Supplementary material 3 Phylogenic tree of minimum evolution of flax DIRs using MEGA6. The alignment of amino acid sequences was conducted in MEGA6 with MUSCLE. The percentages of replicate trees in which associated sequences cluster together in the bootstrap test (percentage of 1000 replicates) are shown next to the branches. Color boxes correspond to phylogenic groups as defined by Ralph et al. (2007). Considering the name and the Phytozome identity, the dirigent-like protein domain PF03018 are identified by a blue box in the schematic protein structure where numbers in small type (e.g. 181, etc.) correspond to the length of the respective proteins. (PPTX 12509 KB)

Supplementary material 4 Selected DIR ortholog genes reported in literature (DOCX 42 KB)

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Supplementary material 5 Sequence alignment of flax DIRs. a. Global MUSCLE sequence alignment performed using Jalview suite. Red and green boxes correspond to the enlarged region A in b. and region B in c. respectively. Conserved motifs I, II, III, IV and V are indicated by a solid black line. Red crosses refer to Phe residues putatively responsible in stereoselectivity (Kim et al. 2012). Orange dots represent highly conserved polar residues (Kim et al. 2015). Blue stars correspond to differing amino acids in (+)- or (–)-pinoresinol forming DIRs (Kim et al. 2015). Green diamonds symbolize functional N-glycosylation sites (Kazenwadel et al. 2013). Colored residues refer to the highly conserved F192, F243 and F287 residues in green; G282, G283, G285 and G292 in pink; H80, H320, H324, H326 and H327 in blue, respectively. (PPTX 602 KB)

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Supplementary material 6 Number of cis-acting elements identified in the flax DIR gene promoters by PLACE analysis (DOCX 116 KB)

Supplementary material 7 List of cis-acting elements located in the DIR gene promoter regions (DOCX 55 KB)

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Supplementary material 8 Conserved motifs identified in flax DIR promoters by MEME global analysis. a. Location of the three identified conserved motifs (respectively symbolized by cyan, blue or red boxes) in promoter sequences that are represented by a continuous line and corresponding P value. Scale of promoter sequence is indicated at the bottom, and the transcription start is located on the right extremity. b. TOMTOM analysis results for the three conserved DNA motifs detected in the DIR gene promoter sequences. (PPTX 2356 KB)

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Supplementary material 9 Conserved motifs identified in flax DIR promoters revealed following TOMTOM analysis. p = proximal (500 last bp in 3′); d = distal (next 1000 bp in 5′). (PPTX 84 KB)

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Supplementary material 10 a. Schematic representation of possible monolignol-derived product biosynthesis in plant cell [adapted from Wang et al. (2013)] and b. regulation network controlling secondary cell wall biosynthesis (adapted from ADDIN EN.CITE (Cassan-Wang et al. 2013; Nakano et al. 2015; Wang and Dixon 2012; Zhao and Dixon 2011; Zhong and Ye 2009). BGLU, β-Glucosidases; CAD, Cinnamyl Alcohol Dehydrogenase; CCR, Cinnamoyl-CoA Reductase; CES, Cellulose Synthase; CTL, Chitinase and Chitinase-Like; DIR, dirigent protein; GT, glucosyltransferase; LAC, laccase; PCBER, PhenylCoumaran Benzylic Ether Reductase; PME, Pectin Methyl Esterases; PMEI, Pectin Methyl Esterase Inhibitors; POX, peroxidase. (PPTX 91 KB)

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Corbin, C., Drouet, S., Markulin, L. et al. A genome-wide analysis of the flax (Linum usitatissimum L.) dirigent protein family: from gene identification and evolution to differential regulation. Plant Mol Biol 97, 73–101 (2018). https://doi.org/10.1007/s11103-018-0725-x

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