Aliphatic suberin confers salt tolerance to Arabidopsis by limiting Na+ influx, K+ efflux and water backflow

Wang, Pei; Wang, Chun-Mei; Gao, Li; Cui, Yan-Nong; Yang, Hai-Li; de Silva, Nayana D. G.; Ma, Qing; Bao, Ai-Ke; Flowers, Timothy J.; Rowland, Owen; Wang, Suo-Min

doi:10.1007/s11104-020-04464-w

Regular Article
Published: 26 February 2020

Aliphatic suberin confers salt tolerance to Arabidopsis by limiting Na⁺ influx, K⁺ efflux and water backflow

Pei Wang^1,2^na1,
Chun-Mei Wang¹^na1,
Li Gao¹,
Yan-Nong Cui¹,
Hai-Li Yang¹,
Nayana D. G. de Silva³,
Qing Ma¹,
Ai-Ke Bao¹,
Timothy J. Flowers⁴,
Owen Rowland^1,3 &
Suo-Min Wang ORCID: orcid.org/0000-0003-0027-8822¹

Plant and Soil volume 448, pages 603–620 (2020)Cite this article

1136 Accesses
16 Citations
Metrics details

Abstract

Background and aims

Uncontrolled uptake of Na⁺ is the reason that many species are sensitive to salinity. Suberin is a protective barrier found in the walls of root endodermal cells that appears to be important for salt tolerance, yet its specific protective mechanism has not been fully elucidated.

Methods

Here we investigated the role of aliphatic suberin in protecting plants against salt stress by using a mutant of Arabidopsis, cyp86a1, which exhibits a significant reduction of root aliphatic suberin.

Results

We found that NaCl significantly increased suberization in roots of hydroponic-grown wild-type plants, but not in cyp86a1. Cyp86a1 exhibited a salt-sensitive phenotype. Compared with wild-type, Na⁺ accumulation in shoots was higher in cyp86a1. We provide evidence that increased Na⁺ uptake was via the root transcellular pathway. Furthermore, cyp86a1 accumulated less K⁺ in shoots than wild-type under NaCl stress, which was a consequence of increased K⁺ efflux from the root vasculature. Additionally, we provide evidence that aliphatic suberin reduces inflow of water across the root endodermis under non-stress conditions but reduces the backflow of water to the medium under salt stress.

Conclusions

Finally, we propose a model for the role of aliphatic suberin in restricting Na⁺ influx, K⁺ efflux and water backflow in plants under saline conditions.

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Abbreviations

CTM:: Composite transport model
GC-MS:: Gas chromatography-mass spectrometer
Gs:: Stomatal conductance
ICP-OES:: Inductively coupled plasma - optical emission spectrometer
Jv _r :: The volume flow of xylem sap per unit root surface area
Lp _r :: Root hydraulic conductivity
NMT:: Non-invasive micro-test technology
Pn:: Net photosynthesis rate
PTS:: Trisodium-8-hydroxy-1,3,6-pyrenetrisulphonic acid
SA:: Selective absorption
ST:: Selective transport
Tr:: Transpiration rate
WUE:: Water use efficiency

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Acknowledgements

We thank Dr. Xiaolong Chen (Lanzhou University) for technical assistance and Prof. Fengmin Li (Lanzhou University) for providing WinRHIZO software. This research was supported by grants from the National Natural Science Foundation of China (31730093 and 31802122) and the Fundamental Research Funds for the Central Universities (lzujbky-2018-k01 and 2019HQZZ17).

Author information

Pei Wang and Chun-Mei Wang contributed equally to this work.

Authors and Affiliations

State Key Laboratory of Grassland Agro-ecosystems; Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs; College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou, 730020, People’s Republic of China
Pei Wang, Chun-Mei Wang, Li Gao, Yan-Nong Cui, Hai-Li Yang, Qing Ma, Ai-Ke Bao, Owen Rowland & Suo-Min Wang
Institution of Qinghai-Tibetan Plateau, Collaborative Innovation Center for Ecological Animal Husbandry of Qinghai-Tibetan Plateau, Southwest Minzu University, Chengdu, 510041, People’s Republic of China
Pei Wang
Department of Biology and Institute of Biochemistry, Carleton University, Ottawa, ON, K1S 5B6, Canada
Nayana D. G. de Silva & Owen Rowland
Department of Evolution Behaviour and Environment, School of Life Sciences, University of Sussex, Falmer, Brighton, Sussex, BN1 9QG, UK
Timothy J. Flowers

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Pei Wang
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Chun-Mei Wang
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Li Gao
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Yan-Nong Cui
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Hai-Li Yang
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Nayana D. G. de Silva
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Qing Ma
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Ai-Ke Bao
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Timothy J. Flowers
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Owen Rowland
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Suo-Min Wang
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Correspondence to Owen Rowland or Suo-Min Wang.

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Supplemental Fig. S1

The growth status of wild-type and cyp86a1 mutant plants grown under different NaCl concentrations in soil. Seeds were germinated and grown on 1/2 MS plates, 7-d-old seedlings were transferred to soil and grown for 21 d, then treated with different salt treatments (0–30 mM NaCl) for 21 d prior to the images being taken (PDF 170 kb)

Supplemental Fig. S2

Chemical composition of suberin monomers in roots of wild-type and cyp86a1 mutant plants under different concentrations of NaCl. (a) All aliphatic suberin monomers and total aromatic monomers; (b) All ω-hydroxyacid monomers identified; (c) All α,ω-diacid monomers identified. The growth conditions and treatments are the same as for Fig. 2c. Mean values are shown in μg·mg⁻¹ delipidated dry residue (DR) ± SD of three biological replicates, each replicate is made up by 0.4–0.5 g of fresh roots (~10 pooled plants). Columns with different letters indicate significant difference at p < 0.05 (Duncan’s test) (PDF 1186 kb)

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Wang, P., Wang, CM., Gao, L. et al. Aliphatic suberin confers salt tolerance to Arabidopsis by limiting Na⁺ influx, K⁺ efflux and water backflow. Plant Soil 448, 603–620 (2020). https://doi.org/10.1007/s11104-020-04464-w

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Received: 28 November 2019
Accepted: 14 February 2020
Published: 26 February 2020
Issue Date: March 2020
DOI: https://doi.org/10.1007/s11104-020-04464-w

Keywords

Salt tolerance
Suberin
Apoplastic barrier
Arabidopsis
CYP86A1
Root hydraulic conductivity (Lp_r)