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Novel lignin-based extracellular barrier in glandular trichome

Nature Plants volume 10, pages 381–389 (2024)Cite this article

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Abstract

Successful biochemical reactions in organisms necessitate compartmentalization of the requisite components. Glandular trichomes (GTs) act as compartments for the synthesis and storage of specialized compounds. These compounds not only are crucial for the survival of plants under biotic and abiotic stresses but also have medical and commercial value for humans. However, the mechanisms underlying compartmentalization remain unclear. Here we identified a novel structure that is indispensable for the establishment of compartments in cucumber GTs. Silica, a specialized compound, is deposited on the GTs and is visible on the surface of the fruit as a white powder, known as bloom. This deposition provides resistance against pathogens and prevents water loss from the fruits1. Using the cucumber bloomless mutant2, we discovered that a lignin-based cell wall structure in GTs, named ‘neck strip’, achieves compartmentalization by acting as an extracellular barrier crucial for the silica polymerization. This structure is present in the GTs of diverse plant species. Our findings will enhance the understanding of the biosynthesis of unique compounds in trichomes and provide a basis for improving the production of compounds beneficial to humans.

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Fig. 1: Silica polymerization occurs in the GT of WT.
Fig. 2: CsCASP1 is localized to the plasma membrane of the GT neck cell.
Fig. 3: Lignin-based cell wall structure is present on the lateral surface of the neck cell in GTs.
Fig. 4: Neck strip functions as an apoplastic barrier in the GT of cucumber.

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Data availability

The RNA sequencing data are deposited to National Center for Biotechnology Information under BioProject ID PRJNA925542. Source data are provided with this paper.

Code availability

The code for RNA sequencing is deposited at https://doi.org/10.5281/zenodo.10344857.

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Acknowledgements

We thank M. Saiki, C. Masuda and Y. Kawara for providing technical support, and we also thank M. Tanaka and Y. Shikanai for their guidance on the immunolocalization experiment. Funding: Japan Society for the Promotion of Science (JSPS) KAKENHI grant 21H02087, 17H03782 (T.K.). Japan–China Scientific Cooperation Program between JSPS and NSFC (3201154000) (T.W., T.K.). Japan Society for the Promotion of Science (JSPS) KAKENHI grant 18H05490, 19H05637 (T.F.). Hunan Provincial Recruitment Program of Foreign Experts (T.W., T.F.). National Natural Science Foundation of China (U21A20234) (B.L.). National Natural Science Foundation of China (31972429) (T.W.). Hunan Provincial Natural Science Foundation of China (2021JJ10032) (T.W.). Scientific Research on Innovative Areas IBmS: Japan Society for the Promotion of Science (JSPS) KAKENHI (JP19H05771) (M.S.).

Author information

Author notes

  1. These authors contributed equally: Ning Hao, Hongxin Yao.

Authors and Affiliations

  1. College of Horticulture/Yuelu Mountain Laboratory of Hunan Province, Hunan Agricultural University, Changsha, China

    Ning Hao, Hongxin Yao, Chunhua Wang, Jiajian Cao & Tao Wu

  2. Graduate School of Agricultural and Life Sciences, University of Tokyo, Tokyo, Japan

    Ning Hao, Michio Suzuki, Toru Fujiwara & Takehiro Kamiya

  3. MOE Key Laboratory of Environment Remediation and Ecological Health, College of Environmental and Resource Science, Zhejiang University, Hangzhou, China

    Baohai Li

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Contributions

Conceptualization: N.H., T.W, T.F. and T.K. Methodology: N.H. and T.K. Investigation: N.H., H.Y., C.W., M.S., J.C. and T.K. Visualization: N.H. and T.K. Funding acquisition: T.W., T.F. and T.K. Project administration: T.W., T.F. and T.K. Supervision: T.W., T.F. and T.K. Writing – original draft: N.H. and T.K. Writing – review and editing: N.H., T.W., B.L., T.F. and T.K.

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Correspondence to Tao Wu or Takehiro Kamiya.

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Extended data

Extended Data Fig. 1 Phenotypic analysis of csmyb36 mutant lines.

(a) Mutation sites and gRNA target regions in CsMYB36. CsMYB36-CR1 and CsMYB36-CR2 are two independent CRIPSR lines of CsMYB36. (b) 10 DAA fruit phenotype of the CsMYB36 mutant lines. The representative images were shown among 3 biologically independent samples. (c) Quantitative analysis of bloom on the fruit surface of WT and ygp mutant (means ± SD). n = 3 biologically independent samples, unpaired two-tails Student’s t-test (****P < 0.0001). (d) Quantitative analysis of bloom on the fruit surface of WT and two independent CRISPR lines of CsMYB36 (means ± SD). n = 5 biologically independent samples, Student’s t-test (****P < 0.0001). (e) Expression level of CsCASP1 in CsMYB36 CRISPR lines in the fruit of 0 DAA (means ± SD). n = 3 biologically independent samples. (f) Si concentration in the cucumber fruit of WT and CsMYB36 CRISPR lines by ICP-MS analysis (means ± SD). n = 5 biologically independent samples, Student’s t-test (ns, P ≥ 0.05). Dots represent individual data. Scale bars, (B) 5 cm.

Source data

Extended Data Fig. 2 Bloom formation was determined by the shoot genotype.

Comparison of the amount of bloom on the 10 DAA fruit of grafting plants between the WT and ygp mutant (mean ± SD); n = 3 biologically independent samples, Student’s t-test (ns, P ≥ 0.05; ****P < 0.0001).

Source data

Extended Data Fig. 3 SEM-EDS analysis on the surface of GT on the cucumber fruit surface.

The SEM-EDS analysis was performed on the red point (spot) on the GT of the WT (A, B),ygp mutant (C, D), WT for CRISPR lines (E, F), CsMYB36-CR1 (G, H), and CsMYB36-CR2 (I, J). One of two images taken with different samples is shown here. Zero DAA fruits were used for the analysis. (B), (D), (F), (H) and (J) show the percentage of mass concentration for every genotype in (A), (C), (E), (G)and (I), respectively. Each dot in (B), (D), (F), (H) and (J) represents one image. The experiment for (A), (C), (E), (G) and (I) was repeated independently twice and results are similar. Scale bars: (A, C, E, G, I) 6 µm.

Extended Data Fig. 4 CsMYB36 can directly bind to the CsCASP1 promoter.

(a) Schematic diagrams of four predicted MYB transcription factor binding motifs at the promoter sequence of CsCASP1. Two fragments (CsCASP1-1 and CsCASP1-2) containing two cis-element was fused into prey vector, respectively. (b) Binding of CsMYB36 to CsCASP1 promoter sequence using yeast one-hybrid assays. Yeast cultures grown in YPDA media (OD600 = 0.2 × 10°, × 10−1, × 10−2) were spotted to SD-TLH media containing 0, 10, 20, 30 mM 3AT, respectively. (c) Schematic diagrams of the effector and reporter constructs used for dual-luciferase assays. (d) Representative images of dual-luciferase reporter assay. Luminescence was captured after infiltration of each construct into Nicotiana benthamiana leaves. The left side of the leaf is for CsCASP1-1, and the right side of the leaf is for CsCASP1-2. MYB36-SK + LUC and empty-62-SK + LUC are the negative control. Empty 62-SK+CsCASP1-1-LUC and CsCASP1-2-LUC are the background control. (e) Quantification of dual-luciferase reporter assay of CsMYB36 and CsCASP1-2. The data are means ± SD, n = 4 biologically independent samples, Student’s t-test (*, P < 0.05). Dots represent individual data.

Source data

Extended Data Fig. 5 Localization of CsCASP1 on the cucumber fruit surface of WT.

(a-c) Z-stack confocal image of Calcofluor White (cellulose) (A) and anti-CsCASP1 antibody (B) in the GT of WT fruit. (c) Merged image of (A) and (B). The experiment for (A) to (C) was repeated at least three times and the results were consistent. Cucumber fruit samples are approximately 3–4 days before anthesis. Scale bars: (A–C) 50 μm.

Extended Data Fig. 6 Lignin deposition in the GT was not detected in the ygp mutant and CsMYB36 CRISPR lines.

(a–i) Z-stack confocal image of Calcofluor White (A, D, G) and Basic Fuchsin (B, E, H) staining, in the fruit peel of ygp mutant, CsMYB36-CR1, CsMYB36-CR2, respectively. (c, f, i) is the merged image of (A) and (B), (D) and (E), (G) and (H), respectively. The experiment for (A) to (I) was repeated independently at least three times and the results are similar. Cucumber fruit samples were collected approximately 3–4 days before anthesis. Scale bars: (A–I) 10 µm.

Extended Data Fig. 7 Cuticle layer on the surface of GT.

GT on the fruit peel was stained with Calcofluor White (cellulose) (a) and Nile Red (cuticle) staining (b) and observed via confocal microscopy. (c) Merged image. The experiment for (A) to (C) was repeated independently twice and the results were consistent. Cucumber fruit samples were collected approximately 3–4 days before anthesis. Scale bars, 10 µm.

Extended Data Fig. 8 Plasmodesmata in cucumber fruit GTs.

(a) Electron microscopy image of a GT stained with KMnO4. The experiment for (A) was repeated independently three times and the results are similar. The image is the same as Fig. 3d. (b–i) Magnified region of the boxes in (A). The white arrowheads in (B–E) indicate the presence of plasmodesmata. GC, gland cell; NC, neck cell; SC, stalk cell; BC, basal cell; EC, epidermal cell. Scale bars: (A) 10 µm and (B–I) 1 µm.

Extended Data Fig. 9 CsCASP1 immunolocalization pattern in the root of WT and ygp mutant.

(a-c) Immunolocalization using anti-CsCASP1 antibody in the root of WT (A-C). (d-f) Immunolocalization using anti-CsCASP1 antibody in the root of ygp mutant. The experiment for (A) and (F) was repeated at least twice and the results are similar. Scale bars: 50 µm.

Extended Data Fig. 10 CS phenotype observation in the root of WT and ygp mutant.

(a-c) Lignin and cellulose staining by Calcofluor White (A) and basic fuchsin (B) in the root of WT. The experiment for (A) and (C) was repeated at least twice and the results are similar. (C) is merge image of (A) and (B). A’, B’ and C’ are the magnified image of the white box in A, B and C, respectively. (d-f) Lignin and cellulose staining by Calcofluor White (D) and basic fuchsin (E) in the root of ygp mutant. The experiment for (D) and (F) was repeated at least twice and the results are similar. (F) is merge image of (D) and (E). A’, B’ and C’ are the magnified image of the white box in A, B and C, respectively. D’, E’ and F’ are magnified image of D, E and F, respectively. Scale bars: 50 µm.

Supplementary information

Supplementary Information

Supplementary Figs. 1–3.

Reporting Summary

Supplementary Tables 1–3

List of down-regulated genes (FDR < 0.05) in the fruit peel of ygp mutant. Accession numbers of the genes used in the phylogenetic tree. Primers used in this study.

Source data

Source Data Fig. 1

Statistical source data.

Source Data Fig. 2

Statistical source data.

Source Data Extended Data Fig. 1

Statistical source data.

Source Data Extended Data Fig. 2

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Source Data Extended Data Fig. 4

Statistical source data.

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Hao, N., Yao, H., Suzuki, M. et al. Novel lignin-based extracellular barrier in glandular trichome. Nat. Plants 10, 381–389 (2024). https://doi.org/10.1038/s41477-024-01626-x

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