Skip to main content
Log in

Comparative analysis of periderm suberin in stems and roots of Tetraena mongolica Maxim and Zygophyllum xanthoxylum (Bunge) Engl

  • Original Article
  • Published:
Trees Aims and scope Submit manuscript

Abstract

Key message

The chemical analysis and the expression patterns of related genes were determined to reveal and compare the adaptation mechanism of T. mongolica and Z. xanthoxylum to arid environments.

Abstract

Tetraena mongolica Maxim, the only member of the Tetraena genus in the Zygophyllaceae, is endemic to the northwest of China and is normally accompanied by another plant species in the same taxonomic family, Z. xanthoxylum (Bunge) Engl, and they play a key role in the ecology of the local environment. In order to survive in the local arid environment, many plants have developed a variety of adaptive mechanisms, including the formation of effective protective barrier, such as suberin in the stems and roots that can prevent plants from losing water and improve their adaptability to water-deficient environments. Previous studies have shown that Z. xanthoxylum had stronger drought tolerance than T. mongolica. Here, the water loss rates, the chemical composition of suberin and associated fatty acids in the periderms of stems and roots from T. mongolica and Z. xanthoxylum were determined. The expression level of genes related to suberin and associated fatty acid metabolism of the two species were also analyzed through transcriptome sequencing. The results showed that the stem and root periderms of these two species had similar chemical composition of suberin and fatty acids; however, much higher amount of suberin monomers and fatty acids were found in T. mongolica. Accordingly, transcriptome sequencing showed that more of the differentially expressed genes (DEGs) associated with suberin and associated fatty acid biosynthesis were up-regulated in the stem periderms of T. mongolica; however, minority of DEGs were up-regulated in root periderms of T. mongolica, compared with Z. xanthoxylum. This study lays an important foundation for revealing the adaptation mechanism of T. mongolica and Z. xanthoxylum to arid environments and for comparing the adaptability differences of these two species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

The transcriptome sequencing raw data were deposited in the National Center for Biotechnology Information with the Accession PRJNA647792 and PRJNA647989.

Abbreviations

DEGs:

Differentially expressed genes

FPKM:

Fragment per kilobase of exon model per million mapped reads

GC:

Gas chromatography

KEGG:

Kyoto encyclopedia of genes and genomes

qRT-PCR:

Quantitative reverse transcription PCR

VLCFA:

Very long chain fatty acids

References

  • Bao AK, Du BQ, Touil L, Kang P, Wang QL, Wang SM (2016) Co-expression of tonoplast Cation/H(+) antiporter and H(+)-pyrophosphatase from xerophyte Zygophyllum xanthoxylum improves alfalfa plant growth under salinity, drought and field conditions. Plant Biotechnol J 14:964–975

    Article  CAS  PubMed  Google Scholar 

  • Baxter I, Hosmani PS, Rus A, Lahner B, Borevitz JO, Muthukumar B, Mickelbart MV, Schreiber L, Franke RB, Salt DE (2009) Root suberin forms an extracellular barrier that affects water relations and mineral nutrition in Arabidopsis. PLoS Genet 5:e1000492

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Beisson F, Li Y, Bonaventure G, Pollard M, Ohlrogge JB (2007) The acyltransferase GPAT5 is required for the synthesis of suberin in seed coat and root of Arabidopsis. Plant Cell 19:351–368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beisson F, Li Y, Pollard M (2012) Solving the puzzles of cutin and suberin polymer biosynthesis. Curr Opin Plant Biol 15:329–337

    Article  CAS  PubMed  Google Scholar 

  • Bonaventure G, Beisson F, Ohlrogge J, Pollard M (2004) Analysis of the aliphatic monomer composition of polyesters associated with Arabidopsis epidermis: occurrence of octadeca-cis-6, cis-9-diene-1,18-dioate as the major component. Plant J 40:920–930

    Article  CAS  PubMed  Google Scholar 

  • Chen M, Zhao XY (2017) Effect of pollen and resource limitation on reproduction of Zygophyllum xanthoxylum in fragmented habitats. Ecol Evol 7:9076–9084

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen N, Feng J, Song B, Tang S, He J, Zhou Y, Shi S, Xu X (2019) De novo transcriptome sequencing and identification of genes related to salt and PEG stress in Tetraena mongolica Maxim. Trees 33:1639–1656

    Article  CAS  Google Scholar 

  • Dakhma WS, Zarrouk M, Cherif A (1995) Effects of drought-stress on lipids in rape leaves. Phytochemistry 40:1383–1386

    Article  CAS  Google Scholar 

  • Enstone DE, Peterson CA, Ma F (2002) Root endodermis and exodermis: structure, function, and responses to the environment. J Plant Growth Regul 21:335–351

    Article  CAS  Google Scholar 

  • Fich EA, Segerson NA, Rose JK (2016) The plant polyester cutin: biosynthesis, structure, and biological roles. Annu Rev Plant Biol 67:207–233

    Article  CAS  PubMed  Google Scholar 

  • Franke R, Schreiber L (2007) Suberin–a biopolyester forming apoplastic plant interfaces. Curr Opin Plant Biol 10:252–259

    Article  CAS  PubMed  Google Scholar 

  • Freire CS, Silvestre AJ, Neto CP (2007) Demonstration of long-chain n-alkyl caffeates and delta7-steryl glucosides in the bark of Acacia species by gas chromatography-mass spectrometry. Phytochem Anal 18:151–156

    Article  CAS  PubMed  Google Scholar 

  • Gou M, Hou G, Yang H, Zhang X, Cai Y, Kai G, Liu C-J (2017) The MYB107 transcription factor positively regulates suberin biosynthesis. Plant Physiol 173:1045–1058

    Article  CAS  PubMed  Google Scholar 

  • Graça J (2015) Suberin: the biopolyester at the frontier of plants. Front Chem 3:62

    Article  PubMed  PubMed Central  Google Scholar 

  • Heinämäki J, Pirttimaa MM, Alakurtti S, Pitkänen HP, Kanerva H, Hulkko J, Paaver U, Aruväli J, Yliruusi J, Kogermann K (2017) Suberin fatty acids from outer birch bark: Isolation and physical material characterization. J Nat Prod 80:916–924

    Article  PubMed  CAS  Google Scholar 

  • Höfer R, Briesen I, Beck M, Pinot F, Schreiber L, Franke R (2008) The Arabidopsis cytochrome P450 CYP86A1 encodes a fatty acid ω-hydroxylase involved in suberin monomer biosynthesis. J Exp Bot 59:2347–2360

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T, Yamanishi Y (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36:D480-484

    Article  CAS  PubMed  Google Scholar 

  • Kang J, Zhao W, Zhu X (2016) Silicon improves photosynthesis and strengthens enzyme activities in the C(3) succulent xerophyte Zygophyllum xanthoxylum under drought stress. J Plant Physiol 199:76–86

    Article  CAS  PubMed  Google Scholar 

  • Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12:357–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kolattukudy PE (2001) Polyesters in higher plants. Adv Biochem Eng Biotechnol 71:1–49

    CAS  PubMed  Google Scholar 

  • Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63:1593–1608

    Article  CAS  PubMed  Google Scholar 

  • Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lee SB, Jung SJ, Go YS, Kim HU, Kim JK, Cho HJ, Park OK, Suh MC (2009) Two Arabidopsis 3-ketoacyl CoA synthase genes, KCS20 and KCS2/DAISY, are functionally redundant in cuticular wax and root suberin biosynthesis, but differentially controlled by osmotic stress. Plant J 60:462–475

    Article  CAS  PubMed  Google Scholar 

  • Leite C, Oliveira V, Miranda I, Pereira H (2020) Cork oak and climate change: disentangling drought effects on cork chemical composition. Sci Rep 10:7800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform 12:323

    Article  CAS  Google Scholar 

  • Li Y, Beisson F, Koo AJ, Molina I, Pollard M, Ohlrogge J (2007) Identification of acyltransferases required for cutin biosynthesis and production of cutin with suberin-like monomers. Proc Natl Acad Sci USA 104:18339–18344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li M, Zhao M, Wu H, Wu W, Xu Y (2013) Cloning, characterization and functional analysis of two type 1 diacylglycerol acyltransferases (DGAT1s) from Tetraena mongolica. J Integr Plant Biol 55:490–503

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-∆∆CT Method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Ma Q, Yue LJ, Zhang JL, Wu GQ, Bao AK, Wang SM (2012) Sodium chloride improves photosynthesis and water status in the succulent xerophyte Zygophyllum xanthoxylum. Tree Physiol 32:4–13

    Article  CAS  PubMed  Google Scholar 

  • Ma Q, Bao AK, Chai WW, Wang WY, Zhang JL, Li YX, Wang SM (2016) Transcriptomic analysis of the succulent xerophyte Zygophyllum xanthoxylumin response to salt treatment and osmotic stress. Plant Soil 402:343–361

    Article  CAS  Google Scholar 

  • Ma Q, Hu J, Zhou XR, Yuan HJ, Kumar T, Luan S, Wang SM (2017) ZxAKT1 is essential for K(+) uptake and K(+) /Na(+) homeostasis in the succulent xerophyte Zygophyllum xanthoxylum. Plant J 90:48–60

    Article  CAS  PubMed  Google Scholar 

  • Nejat N, Mantri N (2017) Plant immune system: crosstalk between responses to biotic and abiotic stresses the missing link in understanding plant defence. Curr Issues Mol Biol 23:1–16

    Article  PubMed  Google Scholar 

  • Pollard M, Beisson F, Li Y, Ohlrogge JB (2008) Building lipid barriers: Biosynthesis of cutin and suberin. Trends Plant Sci 13:236–246

    Article  CAS  PubMed  Google Scholar 

  • Rains MK, Gardiyehewa de Silva ND, Molina I (2018) Reconstructing the suberin pathway in poplar by chemical and transcriptomic analysis of bark tissues. Tree Physiol 38:340–361

    Article  CAS  PubMed  Google Scholar 

  • Rios P, Cabral V, Santos S, Mori F, Graca J, Products W (2014) The chemistry of Kielmeyera coriacea outer bark: a potential source for cork. Eur J Wood Wood pro 72:509–519

    Article  CAS  Google Scholar 

  • Schreiber L (2010) Transport barriers made of cutin, suberin and associated waxes. Trends Plant Sci 15:546–553

    Article  CAS  PubMed  Google Scholar 

  • Schreiber L, Franke R, Hartmann K (2005) Wax and suberin development of native and wound periderm of potato (Solanum tuberosum L.) and its relation to peridermal transpiration. Planta 220:520–530

    Article  CAS  PubMed  Google Scholar 

  • Serra O, Soler M, Hohn C, Sauveplane V, Pinot F, Franke R, Schreiber L, Prat S, Molinas M, Figueras M (2009) CYP86A33-targeted gene silencing in potato tuber alters suberin composition, distorts suberin lamellae, and impairs the periderm’s water barrier function. Plant Physiol 149:1050–1060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi S, Wang Y, Zhou H, Zhou J (2012) Comparative analysis of water related parameters and photosynthetic characteristics in the endangered plant Tetraena mongolica Maxim. and the closely related Zygophyllum xanthoxylon (Bunge) Maxim. Acta Ecol Sin 32:1163–1173

    Article  CAS  Google Scholar 

  • Shi F, Zhou X, Yao MM, Zhou Q, Ji SJ, Wang Y (2019) Low-temperature stress-induced aroma loss by regulating fatty acid metabolism pathway in “Nanguo” pear. Food Chem 297:124927

    Article  CAS  PubMed  Google Scholar 

  • Sun WX, Zhang Q, Jiang JQ (2010) Chemical constituents of Daphne giraldii Nitsche. J Integr Plant Biol 48:1498–1501

    Article  Google Scholar 

  • Tarazona S, Garcã-A-Alcalde F, Dopazo J, Ferrer A, Conesa A (2011) Differential expression in RNA-seq: a matter of depth. Genome Res 21:2213–2223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vishwanath SJ, Delude C, Domergue F, Rowland O (2015) Suberin: biosynthesis, regulation, and polymer assembly of a protective extracellular barrier. Plant Cell Rep 34:573–586

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Lu M, Duan L (2005) Modified hot phenol method for extracting total RNA from seedling root of cotton. Acta Botan Boreali-Occiden Sin 25:723–726

    CAS  Google Scholar 

  • Wang G, Lin Q, Xu Y (2007) Tetraena mongolica Maxim can accumulate large amounts of triacylglycerol in phloem cells and xylem parenchyma of stems. Phytochemistry 68:2112–2117

    Article  CAS  PubMed  Google Scholar 

  • Wu GQ, Xi JJ, Wang Q, Bao AK, Ma Q, Zhang JL, Wang SM (2011) The ZxNHX gene encoding tonoplast Na(+)/H(+) antiporter from the xerophyte Zygophyllum xanthoxylum plays important roles in response to salt and drought. J Plant Physiol 168:758–767

    Article  CAS  PubMed  Google Scholar 

  • Xu X, Xiao L, Feng J, Chen N, Chen Y, Song B, Xue K, Shi S, Zhou Y, Jenks MA (2016) Cuticle lipids on heteromorphic leaves of Populus euphratica Oliv. growing in riparian habitats differing in available soil moisture. Physiol Plant 158:318–330

    Article  CAS  PubMed  Google Scholar 

  • Xu X, Chen N, Feng J, Zhou M, He J, Zou Y, Shi S, Zhou Y, Jenks MA (2020) Comparative analyses of leaf cuticular lipids of two succulent xerophytes of the Ordos Plateau (Gobi Desert), Tetraena mongolica maxim and Zygophyllum xanthoxylum (Bunge) Engl. Environ Exp Bot 177:104129

    Article  CAS  Google Scholar 

  • Xue D, Zhang X, Lu X, Chen G, Chen ZH (2017) Molecular and evolutionary mechanisms of cuticular wax for plant drought tolerance. Front Plant Sci 8:621

    Article  PubMed  PubMed Central  Google Scholar 

  • Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang J, Li S, Li R, Bolund L, Wang J (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34:W293–W297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yeats TH, Rose JK (2013) The formation and function of plant cuticles. Plant Physiol 163:5–20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yin H, Li M, Li D, Khan S, Hepworth SR, Wang S (2019) Transcriptome analysis reveals regulatory framework for salt and osmotic tolerance in a succulent xerophyte. BMC Plant Biol 19:88–88

    Article  PubMed  PubMed Central  Google Scholar 

  • Yu L, Fan J, Xu C (2019) Peroxisomal fatty acid β-oxidation negatively impacts plant survival under salt stress. Plant Signal Behav 14:1561121

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yuan HJ, Ma Q, Wu GQ, Wang P, Hu J, Wang SM (2015) ZxNHX controls Na+ and K+ homeostasis at the whole-plant level in Zygophyllum xanthoxylum through feedback regulation of the expression of genes involved in their transport. Ann Bot 115:495–507

    Article  CAS  PubMed  Google Scholar 

  • Zhang YJ, Yang C (2000) Comparative analysis of genetic diversity in the endangered shrub Teraena mongolica and its related congener Zygophyllum xanthoxylon. Acta Phytoecol Sin 24:425–429

    Google Scholar 

  • Zhang YF, Chi Y, Bo LI, Chen JK (2003) Interpopulation difference in growth and reproduction of endemic species Tetraena mongolica in Ordos Plateau. Acta Ecol Sin 23:436–443

    Google Scholar 

  • Zhi Y, Sun Z, Sun P, Zhao K, Guo Y, Zhang D, Zhang B (2018) How much genetic variation is stored in the endangered and fragmented shrub Tetraena mongolica Maxim? PeerJ 6:e5645

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou HB, Wang YC, Shi SL, Zhou JH (2011) Response of antioxidant system in leaves of Tetraena mongolica and Zygophyllum xanthoxylon seedlings to drought stress. Acta Bot Boreali-Occidentalia Sin 31:1188–1194

    CAS  Google Scholar 

  • Zhu GP, Li HQ, Zhao L, Man L, Liu Q (2016) Mapping the ecological dimensions and potential distributions of endangered relic shrubs in western Ordos biodiversity center. Sci Rep 6:26268–26268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This research was supported by the National Natural Science Foundation of China (Grant no. 31971409), the First Class University and Discipline Construction Project of Minzu University of China (Yldxxk201819).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xiaojing Xu.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest to declare that are relevant to the content of this article.

Ethical standards

T. mongolica is endemic to the western part of Inner Mongolia and Ningxia, Gansu province and also subjected as nationally endangered in China. Before collecting the plant materials and performing the experiments, an oral permission was got from the local management of forestry after applying with introduction letters from College of Life and Environmental Sciences, Minzu University of China.

Additional information

Communicated by Gärtner.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Fig. S1.

Typical leaf and branching morphology of T. mongolica (a) and Z. xanthoxylum (b) growing in natural habitats of Mengxi, Ordos County, Inner Mongolia. Supplementary file1 (JPG 2400 KB)

Fig. S2.

The suberin monomer content in the periderms of stems (a) and roots (b) from T. mongolica and Z. xanthoxylum. Values represent the amount in μg/cm2 of area for each suberin monomer. Supplementary file2 (JPG 2581 KB)

Fig. S3.

The Unigene KEGG function distribution in the periderms of stems (a) and roots (b) from T. mongolica and Z. xanthoxylum. Supplementary file3 (JPG 2493 KB)

Fig. S4.

The lipid metabolism pathways of All-Unigenes in the periderms of stems (a) and roots (b) from T. mongolica and Z. xanthoxylum. Supplementary file4 (JPG 2086 KB)

Supplementary file5 (XLSX 12 KB)

Supplementary file6 (XLSX 11 KB)

Supplementary file7 (XLSX 14 KB)

Supplementary file8 (XLSX 21 KB)

Supplementary file9 (XLSX 21 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhou, M., Chen, N., Zou, Y. et al. Comparative analysis of periderm suberin in stems and roots of Tetraena mongolica Maxim and Zygophyllum xanthoxylum (Bunge) Engl. Trees 36, 325–339 (2022). https://doi.org/10.1007/s00468-021-02208-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-021-02208-6

Keywords

Navigation