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The evolutionary innovation of root suberin lamellae contributed to the rise of seed plants

Nature Plants volume 9, pages 1968–1977 (2023)Cite this article

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Abstract

Seed plants overtook ferns to become the dominant plant group during the late Carboniferous, a period in which the climate became colder and dryer1,2. However, the specific innovations driving the success of seed plants are not clear. Here we report that the appearance of suberin lamellae (SL) contributed to the rise of seed plants. We show that the Casparian strip and SL vascular barriers evolved at different times, with the former originating in the most recent common ancestor (MRCA) of vascular plants and the latter in the MRCA of seed plants. Our results further suggest that most of the genes required for suberin formation arose through gene duplication in the MRCA of seed plants. We show that the appearance of the SL in the MRCA of seed plants enhanced drought tolerance through preventing water loss from the stele. We hypothesize that SL provide a decisive selective advantage over ferns in arid environments, resulting in the decline of ferns and the rise of gymnosperms. This study provides insights into the evolutionary success of seed plants and has implications for engineering drought-tolerant crops or fern varieties.

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Fig. 1: SL are present in roots of only seed plants.
Fig. 2: SL were not able to be induced by ABA in pteridophytes.
Fig. 3: Evolution and functional analysis of suberin-related genes in plant kingdom.
Fig. 4: SL contributes to drought tolerance of plants by preventing water leakage during transport in roots.

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All the data required to assess the conclusions of this study are available in the paper or the 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

We thank J. Murray for suggestions and editing on this manuscript. We thank J. Vermeer and N. Geldner for kindly providing the A. thaliana mutant gelpquint-2 and the transgenetic line proCASP1::CDEF. We thank L. Xu, X. Gao, Z. Zhang, J. Li, W. Lan, S. Bu, W. Cai and S. Yin for their technical support. We also thank Y. He and the Experimental Auxiliary System, BL10U1 of Shanghai Synchrotron Radiation Facility for their support in using Raman microspectroscopy. This work was supported by the National Natural Science Foundation of China (grant nos. 31930024, 32070282 and U19A2026), Chinese Academy of Sciences (grant no. XDB27010103) and the Newton Fund (grant no. NAF\R1\201264).

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Author notes

  1. Tao Feng

    Present address: Biosystematics Group, Wageningen University & Research, Wageningen, the Netherlands

  2. These authors contributed equally: Yu Su, Tao Feng.

Authors and Affiliations

  1. National Key Laboratory of Plant Molecular Genetics, Shanghai Center for Plant Stress Biology, CAS Centre for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai, China

    Yu Su, Chu-Bin Liu, Ya-Ling Wang, Mei-Ling Han, Xing Huang, Jia-Chen Wu, Tao Song, Lin Xu & Dai-Yin Chao

  2. University of Chinese Academy of Sciences, Beijing, China

    Yu Su, Chu-Bin Liu, Xing Huang, Jia-Chen Wu & Tao Song

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

    Tao Feng, Haodong Huang, Xiaojuan Fu, Xuanhao Zhang, Xianpeng Yang & Shiyou Lü

  4. Shanghai Chenshan Plant Science Research Center, Shanghai Chenshan Botanical Garden, Chinese Academy of Sciences, Shanghai, China

    Hui Shen

  5. Hubei Hongshan Laboratory, Wuhan, China

    Shiyou Lü

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Contributions

D.-Y.C., S.L., Y.S. and T.F. designed the study and wrote the manuscript. Y.S., T.F., C.-B.L., Y.-L.W., H.H., M.-L.H., X.F., X.Z., X.H., J.-C.W. and T.S. performed the experiments. Y.S., T.F. and C.-B.L. analysed the data. H.S., X.Y. and L.X. provided feedback on the manuscript.

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Correspondence to Shiyou Lü or Dai-Yin Chao.

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Extended data

Extended Data Fig. 1 Basic Fuchsin staining in root endodermis of the 18 species.

a, b, The positions for observing CS staining in dichotomous branching (a) and lateral branching (b) species as indicated by magenta or blue bars. c, Basic fuchsin staining pictures of endodermal cell walls at the positions as shown in (a) and (b). Species marked in magenta correspond to magenta bars in (a) and those marked in white correspond to blue bars in (b). These results were independently repeated three times. Lyj, Lycopodium japonicum; Sek, Selaginella kraussiana; Iss, Isoetes sinensis; Eqh, Equisetum hyemale; Opv, Ophioglossum vulgatum; Anf, Angiopteris fokiensis; Sac, Salvinia cucullata; Cer, Ceratopteris richardii; Nea, Nephrolepis auriculata; Pot, Polystichum tsus-simense; Adc, Adiantum capillus-veneris; Gib, Ginkgo biloba; Cyr, Cycas revoluta; Pib, Pinus bungeana; Tac, Taxus chinensis; Meg, Metasequoia glyptostroboides; Ors, Oryza sativa; Art, Arabidopsis thaliana. en, endodermis. Arrows pointed to the position of the Casparian strip. Scale bars: 10 µm.

Extended Data Fig. 2 Representative transmission electron microscopy pictures of endodermal cell walls.

a, b, The positions for observing CS staining in dichotomous branching (a) and lateral branching (b) species as indicated by magenta or blue bars. c, d, Ultrastructural observation of endodermal cells at the positions as shown in (a) and (b) after plasmolysis. Species marked in magenta correspond to magenta bars in (a) and those marked in white correspond to blue bars in (b). Plasmolysis was induced by incubating root sections in 0.8 M mannitol for 1 hour. c, The overview TEM pictures of endodermal cells after plasmolysis. Magenta dotted boxes show the cell wall between adjacent endodermal cells. Black asterisks (*) show the apoplastic space generated by plasmolysis. These results were independently repeated three times. en, endodermis; co, cortex; ste, stele; Scale bars: 5 µm. d, Details of the CS and the CSD-CS attachment.The arrows indicate attachment of CSD to CS after plasmolysis. These results were independently repeated three times. CS, Casparin strip. Scale bars: 500 nm. Lyj, Lycopodium japonicum; Sek, Selaginella kraussiana; Iss, Isoetes sinensis; Eqh, Equisetum hyemale; Opv, Ophioglossum vulgatum; Anf, Angiopteris fokiensis; Sac, Salvinia cucullata; Cer, Ceratopteris richardii; Nea, Nephrolepis auriculata; Pot, Polystichum tsus-simense; Adc, Adiantum capillus-veneris; Gib, Ginkgo biloba; Cyr, Cycas revoluta; Pib, Pinus bungeana; Tac, Taxus chinensis; Meg, Metasequoia glyptostroboides; Ors, Oryza sativa; Art, Arabidopsis thaliana.

Extended Data Fig. 3 Fluorol yellow staining in root endodermis at fully developed of the vascular plants.

a, b, The positions for observing CS staining in dichotomous branching (a) and lateral branching (b) species as indicated by colourful bars. c, d, FY 088 staining of roots at the positions as shown in (a) and (b). Species marked in magenta correspond to magenta bars in (a) and those marked in green and yellow species correspond to green and yellow bars respectively in (b). c, The overview FY 088 staining pictures of roots. These results were independently repeated three times. en, endodermis; Scale bars: 50 µm. d, Details of FY 088 staining pictures of the endodermal cells from three independent experiment. en, endodermis. Scale bars: 10 µm. Lyj, Lycopodium japonicum; Sek, Selaginella kraussiana; Iss, Isoetes sinensis; Eqh, Equisetum hyemale; Opv, Ophioglossum vulgatum; Anf, Angiopteris fokiensis; Sac, Salvinia cucullata; Cer, Ceratopteris richardii; Nea, Nephrolepis auriculata; Pot, Polystichum tsus-simense; Adc, Adiantum capillus-veneris; Gib, Ginkgo biloba; Cyr, Cycas revoluta; Pib, Pinus bungeana; Tac, Taxus chinensis; Meg, Metasequoia glyptostroboides; Ors, Oryza sativa; Art, Arabidopsis thaliana.

Extended Data Fig. 4 Phylogenetic tree of MYB41 family in plants.

The tree was inferred using maximum likelihood method with model Q.plant+R9. Numbers near nodes are bootstrap support values. The Arabidopsis MYB genes that are known to be involved in root suberization are in red. The genes used for function test are indicated by red star symbol.

Extended Data Fig. 5 The expression of 35S::MYBs-eYFP in tobacco leaves.

Expression and subcellular localization of the MYB homologs in epidermal cells of N. benthamiana leaves were observed under a confocal microscope. These results were independently repeated three times. DAPI was used as a nucler marker. The corresponding genes were cloned from Selaginella kraussiana, Salvinia cucullata, Adiantum capillus-veneris, Ginkgo biloba and Arabidopsis thaliana. Scale bars: 20 μm.

Extended Data Fig. 6 Raw data for Fig. 4c.

Raman spectra of D2O obtained from the mannitol after a 2-hour treatment. Shaded areas show the extent of one standard deviation on both sides of the mean values, n = 3. These results were independently repeated three times with similar outcomes.

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Su, Y., Feng, T., Liu, CB. et al. The evolutionary innovation of root suberin lamellae contributed to the rise of seed plants. Nat. Plants 9, 1968–1977 (2023). https://doi.org/10.1038/s41477-023-01555-1

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