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Overexpression of the pear PbSPMS gene in Arabidopsis thaliana increases resistance to abiotic stress

Plant Cell, Tissue and Organ Culture (PCTOC) volume 140, pages 389–401 (2020)Cite this article

Abstract

The fruit of ‘Dangshansuli’ pear is yellowish green in colour, while that of its mutant ‘Xiusu’ is russet in colour. A differentially expressed gene, PbSPMS, was screened from the transcriptomes of the exocarps of ‘Dangshansuli’ and ‘Xiusu’ fruit. To understand the role of PbSPMS in the russet exocarp formation of ‘Xiusu’, the expression of the PbSPMS gene in the exocarp of ‘Dangshansuli’ and ‘Xiusu’ at different stages of development was analysed. The functions of the PbSPMS gene in phenolic synthesis and suberin and polyamine (PA) deposition in Arabidopsis plants and the responses to drought and salt stress were also studied. The results showed that the relative area of vascular bundles of the transgenic PbSPMS Arabidopsis plants was larger than that of the wild-type (WT) plants and that the secondary thickened cell wall of the xylem was thicker in the transgenic Arabidopsis plants than in the WT plants. The contents of PAs, phenolics and suberin in the PbSPMS Arabidopsis plants were greater than those in the WT plants. Under drought and salt stress, the introduction of PbSPMS facilitated the rapid accumulation of spermidine (Spd) and spermine (Spm) within a short period of time in A. thaliana, and the contents of Spd and Spm were significantly greater in the transgenic plants than in the WT plants, showing that PbSPMS participates in the stress response rapidly to reduce the negative effects of stress. Moreover, exogenous PbSPMS increased the contents of proline (Pro), H2O2, peroxidase (POD) and soluble sugars in the plants. With prolonged stress time, the contents of all the compounds increased gradually, and the longer the stress time was, the more significant the drought resistance of the PbSPMS transgenic plants. Overall, the results demonstrated that PbSPMS contributes to phenolic synthesis and suberin and PA deposition in Arabidopsis plants and improves plant resistance to both drought and salt stress.

Key message

An pear gene, PbSPMS might be involved in phenolic and suberin compound biosynthesis, and response to salinity and drought stress in transgenic Arabidopsis thaliana.

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Abbreviations

DAFB:

Days after full bloom

PbSPMS :

Pyrus bretschneideri SPMS gene

SPMS :

Spermine synthase

Spd:

Spermidine

Spm:

Spermine

Put:

Putrescine

Pro:

Proline

POD:

Peroxidase

PAs:

Polyamines

WT:

Wild-type Arabidopsis thaliana (Columbia)

References

  • Agudelo-Romero P, Bortollot C, Pais MS, Tiburcio AF, Fortes AM (2013) Study of polyamines during grape ripening indicate an important role of polyamine catabolism. Plant Physiol Biochem 67:105–119

    CAS  Article  Google Scholar 

  • Biasi R, Bagni N, Costa G (2010) Endogenous polyamines in apple and their relationship to fruit set and fruit growth. Physiol Plant 73:201–205

    Article  Google Scholar 

  • Chen B, Wang C, Tian Y, Chu Q, Hu C (2015) Anatomical characteristics of young stems and mature leaves of dwarf pear. Sci Hortic 186:172–179

    Article  Google Scholar 

  • Cheng L, Zou Y, Ding S, Zhang J, Yu X, Cao J et al (2009) Polyamine accumulation in transgenic tomato enhances the tolerance to high temperature stress. J Integr Plant Biol 51:489–499

    CAS  Article  Google Scholar 

  • Cheng XQ, Zhu XF, Tian WG, Cheng WH, Hakim Sun J et al (2017) Genome-wide identification and expression analysis of polyamine oxidase genes in upland cotton (Gossypium hirsutum L.). Plant Cell Tissue Organ Cult 129:237–249

    CAS  Article  Google Scholar 

  • Falasca G, Franceschetti M, Bagni N, Altamura MM, Biasi R (2010) Polyamine biosynthesis and control of the development of functional pollen in kiwifruit. Plant Physiol Biochem 48:565–573

    CAS  Article  Google Scholar 

  • Fernandes EM, Aroso IM, Mano JF, Covas JA, Reis RL (2014) Functionalized cork-polymer composites (CPC) by reactive extrusion using suberin and lignin from cork as coupling agents. Composites B 67:371–380

    CAS  Article  Google Scholar 

  • Ferreira R, Garcia H, Sousa AF, Guerreiro M, Duarte FJS, Freire C et al (2014) Unveiling the dual role of the cholinium hexanoate ionic liquid as solvent and catalyst in suberin depolymerisation. RSC Adv 4:2993–3002

    CAS  Article  Google Scholar 

  • Gonzalez ME, Marco F, Minguet EG, Carrasco Sorli P, Blázquez MA, Carbonell J et al (2011) Perturbation of spermine synthase gene expression and transcript profiling provide new insights on the role of the tetraamine spermine in Arabidopsis defense against Pseudomonas viridiflava. Plant Physiol 156:2266–2277

    CAS  Article  Google Scholar 

  • Guo JX, Wang SF, Yu XY, Dong R, Li YZ, Mei XR et al (2018) Polyamines regulate strawberry fruit ripening by abscisic acid, auxin, and ethylene. Plant Physiol 177:339–351

    CAS  Article  Google Scholar 

  • Haque A, Ferdousy NE, Sharif-Ar-Raffi SA, Sagor GH (2018) Differential role of spermine and thermospermine in Arabidopsis thaliana in response to abiotic stresses. J Bangladesh Agric Univ 16:244–249

    Article  Google Scholar 

  • Harindra Champa WA, Gill MIS, Mahajan BVC, Bedi S (2015) Exogenous treatment of spermine to maintain quality and extend postharvest life of table grapes (Vitis vinifera L.) cv. flame seedless under low temperature storage. LWT Food Sci Technol 60:412–419

    CAS  Article  Google Scholar 

  • Heng W, Wang ZT, Jiang XH, Jia B, Liu P, Liu L et al (2016) The role of polyamines during exocarp formation in a russet mutant of ‘Dangshansuli’ pear (Pyrus bretchnederi Rehd.). Plant Cell Rep 35:1841–1852

    CAS  Article  Google Scholar 

  • Heng W, Huang H, Li F, Hou Z, Zhu L (2017) Comparative analysis of the structure, suberin and wax composition and key gene expression in the epidermis of ‘dangshansuli’ pear and its russet mutant. Acta Physiol Plant 39:150

    Article  Google Scholar 

  • Imai A, Akiyama T, Kato T, Sato S, Tabata S, Yamamoto KT et al (2004) Spermine is not essential for survival of Arabidopsis. FEBS Lett 556:148–152

    CAS  Article  Google Scholar 

  • Kitashiba H, Hao YJ, Honda C, Moriguchi T (2005) Two types of spermine synthase gene: MdACL5 and MdSPMS are differentially involved in apple fruit development and cell growth. Gene 361:101–111

    CAS  Article  Google Scholar 

  • Lester GE (2000) Polyamines and their cellular anti-senescence properties in honey dew muskmelon fruit. Plant Sci 160:105–112

    CAS  Article  Google Scholar 

  • Lin DB, Liu ZQ, Zhang SC (1994) Effects of polyamines on cold hardiness development of citrus. Acta Hortic Sin 21:222–226

    Google Scholar 

  • Liu JH, Nada K, Pang XM, Honda C, Kitashiba H, Moriguchi T (2006) Role of polyamines in peach fruit development and storage. Tree Physiol 26:791–798

    CAS  Article  Google Scholar 

  • Liu JH, Inoue H, Moriguchi T (2008) Salt stress-mediated changes in free polyamine titers and expression of genes responsible for polyamine biosynthesis of apple in vitro shoots. Environ Exp Bot 62:28–35

    CAS  Article  Google Scholar 

  • Maiale S, Sánchez DH, Guirado A, Vidal A, Ruiz OA (2004) Spermine accumulation under salt stress. Plant Physiol 161:35–42

    CAS  Article  Google Scholar 

  • Malik AU, Singh Z (2004) Endogenous free polyamines of mangos in relation to development and ripening. J Am Soc Hortic Sci 129:280–286

    Article  Google Scholar 

  • Marco F, Buso E, Carrasco P (2014) Overexpression of SAMDC1 gene in Arabidopsis thaliana increases expression of defense-related genes as well as resistance to Pseudomonas syringae and Hyaloperonospora arabidopsidis. Front Plant Sci 5:1–9

    Article  Google Scholar 

  • Maruri-Lopez I, Hernandez-Sanchez IE, Ferrando A, Carbonell J, Jimenez-Bremont JF (2015) Characterization of maize spermine synthase 1 (ZmSPMS1): evidence for dimerization and intracellular location. Plant Physiol Biochem 97:264–271

    CAS  Article  Google Scholar 

  • Moller SG, McPherson MJ (1998) Developmental expression and biochemical analysis of the Arabidopsis atao1 gene encodingan H2O2-generating diamine oxidase. Plant J 13:781–791

    CAS  Article  Google Scholar 

  • Ono Y, Kim WD, Watanabe K, Sasaki A, Niitsu M, Berberich T et al (2012) Constitutively and highly expressed Oryza sativa polyamine oxidases localize in peroxisomes and catalyze polyamine back conversion. Amino Acids 42:867–876

    CAS  Article  Google Scholar 

  • Schieber A, Keller P, Carle R (2001) Determination of phenolic acids and flavonoids of apple and pear by high-performance liquid chromatography. J Chromatogr A 910:265–273

    CAS  Article  Google Scholar 

  • Su GX, Yu BJ, Zhang WH, Liu YL (2007) Higher accumulation of γ-aminobutyric acid induced by salt stress through stimulating the activity of diamine oxidases in Glycine max (L.) Merr. roots. Plant Physiol Biochem 45:560–566

    Article  Google Scholar 

  • Valero D, Martinez-Romero D, Serrano M (2002) The role of polyamines in the improvement of the shelf life of fruit. Trends Food Sci Technol 13:228–234

    CAS  Article  Google Scholar 

  • Wang MH, Ding MQ, Chen AQ, Zhang YT, Rong JK (2014) Over expression of a cotton GaSus3 gene enhancing the salt stress tolerance of Arabidopsis thaliana. Acta Phytophysiol Sin 50:901–908

    CAS  Google Scholar 

  • Wei J, Tanabe K (1994) Effect of temperature on polyamine, ACC contents, EFE activities and ethylene production in post-harvested pear fruits. Acta Hortic Sin 21:139–144

    Google Scholar 

  • Wen XP, Pang XM, Matsuda N, Kita M, Inoue H, Hao YJ et al (2008) Over-expression of the apple Spd synthase gene in pear confers multiple abiotic stress tolerance by altering polyamine titers. Transgenic Res 17:251–263

    CAS  Article  Google Scholar 

  • Yoda H, Yamaguchi Y, Sano H (2003) Induction of hypersensitive cell death by hydrogen peroxide produced through polyamine degradation in tobacco plants. Plant Physiol 132:1973–1981

    CAS  Article  Google Scholar 

  • Zhang Z, Honda C, Kita M, Hu C, Nakayama M, Moriguchi T (2003) Structure and expression of spermidine synthase genes in apple: two cDNAs are spatially and developmentally regulated through alternative splicing. Mol Genet Genomics 286:799–807

    Article  Google Scholar 

  • Zhao LL, Song LQ, Liu Z, Xie XB, Zhai H, Hao YJ (2008) Changes of polyamines in the leaves of 4 apple rootstocks during low temperature stress. J Fruit Sci 25:151–156

    CAS  Google Scholar 

  • Zhu L, Zhu Y, Jia B, Zhang S (2009) Study on pear (Pyrus spp.) germplasm resources collected at the protection district of ‘Dangshansuli’ by ISSR markers. Hortic Environ Biotechnol 50:334–340

    CAS  Google Scholar 

Download references

Acknowledgements

This project was supported by the National Natural Science Foundation of China (31101519, 31972985) and the earmarked fund for China Agriculture Research System (CARS-29-14). The authors thank American Journal Experts for the helpful suggestions and revisions of the manuscript.

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Author notes

  1. Xianghong Jiang and Junyu Zhan should be regarded as joint first authors.

Authors and Affiliations

  1. School of Horticulture, Anhui Agricultural University, Hefei, Anhui, People’s Republic of China

    Xianghong Jiang, Junyu Zhan, Qi Wang, Xinyi Wu, Xiaonan Chen, Bing Jia, Pu Liu, Li Liu, Zhenfeng Ye, Liwu Zhu & Wei Heng

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Contributions

HW and JXH conceived and designed the study. ZJY and WQ constructed and transformed gene vectors, screened and purified transgenic Arabidopsis seeds. ZJY and JB collected fruits and prepared for RNA. WXY and CXN performed RT-qPCR. LP and YZF contributed to bioinformatic analysis. JXH contributed to the writing of the manuscript and data analysis. ZJY and ZLW revised the manuscript. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Liwu Zhu or Wei Heng.

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Jiang, X., Zhan, J., Wang, Q. et al. Overexpression of the pear PbSPMS gene in Arabidopsis thaliana increases resistance to abiotic stress. Plant Cell Tiss Organ Cult 140, 389–401 (2020). https://doi.org/10.1007/s11240-019-01735-y

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  • DOI: https://doi.org/10.1007/s11240-019-01735-y

Keywords

  • Pear
  • PbSPMS
  • Polyamine
  • Phenols
  • Suberin
  • Resistance