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Deciphering the core shunt mechanism in Arabidopsis cuticular wax biosynthesis and its role in plant environmental adaptation

Nature Plants volume 11, pages 165–175 (2025)Cite this article

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Abstract

Plant cuticular waxes serve as highly responsive adaptations to variable environments1,2,3,4,5,6,7. Aliphatic waxes consist of very-long-chain (VLC) compounds produced from 1-alcohol- or alkane-forming pathways5,8. The existing variation in 1-alcohols and alkanes across Arabidopsis accessions revealed that 1-alcohol amounts are negatively correlated with aridity factors, whereas alkanes display the opposite behaviour. How carbon resources are allocated between the 1-alcohol and alkane pathways responding to environmental stimuli is still largely unknown. Here, in Arabidopsis, we report a novel 1-alcohol biosynthesis pathway in which VLC acyl-CoAs are first reduced to aldehydes by CER3 and then converted into 1-alcohols via a newly identified putative aldehyde reductase SOH1. CER3, previously shown to interact with CER1 in alkane synthesis, is identified to interact with SOH1 as well, channelling wax precursors into either alcohol- or alkane-forming pathways, and the directional shunting of these precursors is tightly regulated by the SOH1–CER3–CER1 module in response to environmental conditions.

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Fig. 1: Synthesis of primary alcohols in Arabidopsis and other species.
Fig. 2: Identification of SOH1 and SOH1-LIKE as part of an alcohol-forming pathway.
Fig. 3: Primary (1-)alcohols compete with alkanes for VLC acyl-CoAs during wax biosynthesis and negatively affect the cuticular water barrier.
Fig. 4: Natural variation in primary (1-)alcohols and alkanes of Arabidopsis leaves correlates with environmental conditions of the accessions’ geographical origin.

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Data availability

All data required to assess the conclusions of this study are available in the paper or its Supplementary Information. Other relevant data are available from the corresponding authors upon request. Source data are provided with this paper.

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (grant nos. 32370300 and 32070282).

Author information

Author notes

  1. These authors contributed equally: Shipeng Li, Xuanhao Zhang, Haodong Huang.

Authors and Affiliations

  1. State Key Laboratory of Biocatalysis and Enzyme Engineering, School of Life Sciences, Hubei University, Wuhan, China

    Shipeng Li, Xuanhao Zhang, Haodong Huang, Pingfang Yang, Huayan Zhao & Shiyou Lü

  2. Hubei Hongshan Laboratory, Wuhan, China

    Shipeng Li, Xuanhao Zhang, Haodong Huang & Shiyou Lü

  3. Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, China

    Mou Yin

  4. School of Plant Sciences, College of Agriculture and Life Sciences, The University of Arizona, Tucson, AZ, USA

    Matthew A. Jenks

  5. Department of Biochemistry and Molecular Biology, University of Nevada, Reno, NV, USA

    Dylan K. Kosma

  6. College of Life Sciences, Shandong Normal University, Jinan, China

    Xianpeng Yang

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Contributions

S. Lu, H.Z., S. Li and X.Y. designed the study and wrote the paper. S. Li, X.Z., X.Y. and H.H. performed the experiments. S. Li, X.Z., M.Y. and X.Y. analysed the data. P.Y., M.A.J. and D.K.K. analysed data and wrote the paper.

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Correspondence to Xianpeng Yang, Huayan Zhao or Shiyou Lü.

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Nature Plants thanks Yanjun Guo and Mi Chung Suh for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Phylogenetic tree of putative AHRs from Arabidopsis.

Using E.coli YbbO as a query sequence, the protein sequences of the putative Arabidopsis AHRs were found in the Arabidopsis genome and the phylogenetic tree was generated by MEGA using the neighbor-joining method. YbbO and AT5g02540 (SOH1) were highlighted in red.

Extended Data Fig. 2 The expression pattern of SOH1, SOH1-LIKE and CER4.

a and b, Cell-type specific expression patterns of SOH1 (a) and SOH1-LIKE (b) obtained from Cell Type Specific Arabidopsis eFP Browser (https://bar.utoronto.ca/efp). c, Relative expression of SOH1, SOH1-LIKE and CER4 in whole leaf, leaf epidermis, whole stem and stem epidermis. These results were independently replicated at least twice, yielding similar outcomes each time. Data are represented as mean ± s.d., n = 3 of biological replicates. d, Expression pattern of SOH1, SOH1-LIKE and CER4 in different tissues of Arabidopsis. These results were independently replicated at least twice, yielding similar outcomes each time. Data are represented as mean ± s.d., n = 3 of biological replicates.

Extended Data Fig. 3 Identification of wax primary (1-) alcohol synthesis gene SOH1 and SOH1-LIKE.

a, The 1-alcohol coverage on leaves of soh1-2 mutant. Wax coverage is expressed as microgram per square decimeter leaf surface area. These results were independently replicated at least twice, yielding similar outcomes each time. Data are shown as mean ± s.d., n = 3 of biological replicates. ***P < 0.001 (Student’s two-tailed t-test). Exact P values are listed in the source data. b, Phylogenetic tree of SOH1 paralogues from Arabidopsis. Phylogenetic tree was generated by MEGA using the neighbor-joining method. SOH1 and SOH1-LIKE were highlighted in red. c, The 1-alcohol coverage on leaves of different SOH1-LIKE overexpression lines. Wax coverage is expressed as microgram per square decimeter leaf surface area. These results were independently replicated at least twice, yielding similar outcomes each time. Data are shown as mean ± s.d., n = 3 of biological replicates. **P < 0.01; ***P < 0.001 (Student’s two-tailed t-test). Exact P values are listed in the source data. d, The 1-alcohol coverage on leaves of Col-0, cer4-4, soh1-1 soh1-like and cer4-4 soh1-1 soh1-like mutants. Wax coverage is expressed as microgram per square decimeter leaf surface area. These results were independently replicated at least twice, yielding similar outcomes each time. Data are shown as mean ± s.d., n = 3 of biological replicates. ND, not detectable. **P < 0.01; ***P < 0.001 (Student’s two-tailed t-test). Exact P values are listed in the source data. e, The 1-alcohol coverage on stems of Col-0, soh1-1, soh1-like and soh1-1 soh1-like mutants. Wax coverage is expressed as microgram per square decimeter stem surface area. These results were independently replicated at least twice, yielding similar outcomes each time. Data are shown as mean ± s.d., n = 5 of biological replicates. Not significant (Student’s two-tailed t-test). Exact P values are listed in the source data.

Source data

Extended Data Fig. 4 SOH1-LIKE physically interacts with CER3 forming an alcohol-generating complex.

a, Interaction between SOH1-LIKE and CER3 identified by luciferase complementation imaging (LCI) assay. In this experiment, different combinations including SOH1-LIKE-nLUC/cLUC-CER3, BlpR-nLUC/cLUC-KanR, SOH1-LIKE-nLUC/cLUC-KanR and BlpR-nLUC/cLUC-CER3 were transiently transformed into N. benthamiana cells. BlpR (phosphinothricin acetyltransferase) and KanR (aminoglycoside phosphotransferase) were used as negative control. These results were independently replicated at least twice with similar outcomes. b, Interaction of SOH1-LIKE with CER3 verified by the split ubiquitin yeast two-hybrid assay (SUY2H). Dilutions of yeast cells expressing different combinations were dotted on media lacking Leucine and Tryptophan (-LW) for checking the growth state and on selective media lacking Leucine, Tryptophan and Histidine (-LWH) for checking the interaction. These results were independently replicated at least twice with similar outcomes. c, C26, C28 and C30 alcohols generated by the yeast cells co-expressing SOH1, SOH1-LIKE and both of them with CER3. Gas chromatography-flame ionization detection (GC-FID) of the alcohol fractions after separation of total lipid from different yeast strains using thin layer chromatography (TLC). These results were independently replicated three times with similar outcomes.

Extended Data Fig. 5 Maximum likelihood tree of SOH1 and homologs.

Gene name follows the pattern “familyspecies_gene ID”. Maximum likelihood phylogenies were inferred using RAXML-NG v.0.7.0b. Figtree v.1.4.3 was employed for tree adjustment. The SOH1 and other related SOH1-LIKE members are labeled following their gene ID and highlighted in red.

Extended Data Fig. 6 Functional characterization of SOH1-LIKEs from Oryza sativa and Physcomitrium patens.

a and b, PpSOH1-LIKE1 and OsSOH1-LIKE physically interact with AtCER3 in N. benthamiana cell by luciferase complementation imaging (LCI) assay, N-terminus of luciferase fused PpSOH1-LIKE1 and OsSOH1-LIKE, AtCER3 fused C-terminus luciferase co-transformed N. benthamiana cells exhibit luciferase activity, BlpR (phosphinothricin acetyltransferase) and KanR (aminoglycoside phosphotransferase) were used as negative control. These results were independently replicated at least twice with similar outcomes. c, C26, C28 and C30 alcohols generated by the yeast cells co-expressing PpSOH1-LIKE1 or OsSOH1-LIKE with AtCER3. Gas chromatography-flame ionization detection (GC-FID) of the alcohol fractions after separation of total lipid from different yeast strains using thin layer chromatography (TLC). These results were independently replicated three times with similar outcomes. d and e, primary alcohol coverage in the leaves of different PpSOH1-LIKE1 (d) and OsSOH1-LIKE (e) overexpression lines, respectively. Wax coverage is expressed as microgram per square decimeter of leaf surface area. These results were independently replicated at least twice, yielding similar outcomes each time. Data are shown as mean ± s.d., n = 4 of biological replicates. *P < 0.05; **P < 0.01; ***P < 0.001 (Student’s two-tailed t-test). Exact P values are listed in the source data. f and g, alkane coverage in the leaves of different PpSOH1-LIKE1 (f) and OsSOH1-LIKE (g) overexpression lines. Wax coverage is expressed as microgram per square decimeter of leaf surface area. These results were independently replicated at least twice, yielding similar outcomes each time. Data are shown as mean ± s.d., n = 4 of biological replicates. *P < 0.05 (Student’s two-tailed t-test). Exact P values are listed in the source data.

Source data

Extended Data Fig. 7 Primary alcohols compete with alkanes in forming process.

a, Wax coverage on the leaf of Col-0 (WT), SOH1-LIKE OE-1, SOH1-LIKE OE-2. Wax coverage is expressed as microgram per square decimeter of leaf surface area. These results were independently replicated at least twice, yielding similar outcomes each time. Data are shown as mean ± s.d., n = 3 of biological replicates. ***P < 0.001 (Student’s two-tailed t-test). Exact P values are listed in the source data. b, Wax coverage on the stem of Col-0 (WT), SOH1-LIKE OE-1, SOH1-LIKE OE-2. Wax coverage is expressed as microgram per square decimeter of stem surface area. These results were independently replicated at least twice, yielding similar outcomes each time. Data are shown as mean ± s.d., n = 3 of biological replicates. *P < 0.05; ***P < 0.001 (Student’s two-tailed t-test). Exact P values are listed in the source data. c and d, Relative wax coverage (%) on leaves of different Col-0 (WT), soh1-1 soh1-like double mutant SOH1 OE-1 and SOH1 OE-2 lines under normal condition (c) or after drought treatment (d). Others include Acids and Aldehydes. These results were independently replicated at least twice, yielding similar outcomes each time. Data are represented as mean ± s.d., (c) n = 3; (d) n = 4 of biological replicates. Different letters indicate statistically significant differences (P < 0.05, one-way ANOVA). Exact P values are listed in the source data.

Source data

Extended Data Fig. 8 Box plots of the relative level of individual wax monomers (percentage of each in total wax) in 190 natural accessions.

In the box plots, the central lines represent the median percentage values, the upper and lower box limits represent the 75th and 25th percentiles, and the upper and lower whiskers extend to 1.5 times the interquartile range, respectively.

Extended Data Fig. 9 Stability of SOH and CER1 proteins and interaction intensity with CER3 under heat stress.

a, SOH1, CER1 and SOH1-LIKE protein stability under drought and high-temperature treatment. SOH1-eYFP, CER1-eYFP and SOH1-LIKE-eYFP proteins were extracted from SOH1 OE-1, CER1 OE-1 and SOH1-LIKE OE-1 transgenic lines respectively. b, Quantitative analysis of the interaction intensity of SOH1 and CER1 respectively with CER3 by dual-luciferase reporter system under control (CK) and high-temperature (HT) treatment. CER1-nLUC/cLUC-CER3 were transiently transformed into cer1-2 mutant leaf cells. SOH1-nLUC/cLUC-CER3 were transiently transformed into soh1-1 soh1-like mutant leaf cells. These results were independently replicated at least twice, yielding similar outcomes each time. Data are shown as mean ± s.d., n = 4 of biological replicates. ***P < 0.001 (Student’s two-tailed t-test). Exact P values are listed in the source data.

Source data

Extended Data Fig. 10 Gene expression patterns and wax accumulation under long-term high-temperature treatment.

a-d, Expression patterns of SOH1, SOH1-LIKE, CER1 and CER3 gene under different high temperature treatment time points. Data are represented as mean ± s.d., n = 3 of biological replicates. e-h, 1-alcohols and alkanes coverage of Col-0 leaves under different high temperature treatment time points. Wax coverage is expressed as microgram per square decimeter of leaf surface area. These results were independently replicated at least twice, yielding similar outcomes each time. Data are shown as mean ± s.d., n = 4 of biological replicates. NS, not significant; *P < 0.05; **P < 0.01; ***P < 0.001 (Student’s two-tailed t-test). Exact P values are listed in the source data. i-l, Ratios of 1-alcohols to alkanes in response to high temperature at different time points. These results were independently replicated at least twice, yielding similar outcomes each time. Data are represented as mean ± s.d., n = 4 of biological replicates. Different letters indicate statistically significant differences (P < 0.05, one-way ANOVA). Exact P values are listed in the source data.

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Supplementary Figs. 1–25, Tables 1 and 2 and uncropped scans of blots for Extended Data Fig. 9a.

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Li, S., Zhang, X., Huang, H. et al. Deciphering the core shunt mechanism in Arabidopsis cuticular wax biosynthesis and its role in plant environmental adaptation. Nat. Plants 11, 165–175 (2025). https://doi.org/10.1038/s41477-024-01892-9

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