Skip to main content

Advertisement

SpringerLink
Log in

Exogenous spermidine maintains the chloroplast structure of cucumber seedlings and inhibits the degradation of photosynthetic protein complexes under high-temperature stress

  • Original Article
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Cucumbers (Cucumis sativus L.) are thermophilic horticulture crop but do not tolerate high temperature. The photosynthesis of cucumber under high temperature is highly susceptible to damage. To study the physiological mechanism of exogenous spermidine (Spd) on cucumber photosynthesis under heat stress, the sensitive cucumber cultivar ‘Jinchun no. 2’ was grown in substrate culture at a high temperature in an artificial climate box and treated with 1.0 mmol L−1 Spd under high-temperature stress (42/32 °C). The results showed that exogenous Spd alleviated the photosynthetic damage caused by heat shock, added the chlorophyll content and maintained the chloroplast structures relatively intact. Western blotting analysis showed that exogenous Spd inhibited the degradation of photosynthetic proteins, slowed the dissociation of the protein complexes, and maintained the stability of light-harvesting complexes (LHCs) in cucumber leaves under high-temperature stress. Twenty-two differentially expressed thylakoid membrane proteins involved in different photosynthetic processes were successfully authenticated by sodium dodecyl sulphate (SDS)-urea-PAGE and Blue native-polyacrylamide gel electrophoresis (BN-PAGE). The results showed that exogenous Spd regulated the expression of photosynthetic and bursal somatic membrane proteins, which resulted in adaptive changes under high-temperature stress at the transcriptional and translational levels, inhibited the degradation of thylakoid membrane proteins in cucumber leaves, and maintained the stable structure of the thylakoid membrane. Collectively, these results suggested that exogenous Spd alleviated high temperature-induced photosynthesis damage by improving the expression and synthesis of thylakoid membrane proteins, mitigating the dissociation of LHCII–Chl and thylakoid membrane protein complexes and maintaining the integrity and functional stability of the photosynthetic organ structure.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

Abbreviations

2-D BN/SDS-PAGE:

Two-dimensional blue-native/SDS–polyacrylamide gel electrophoresis

BN-PAGE:

Blue native-polyacrylamide gel electrophoresis

CBB:

Coomassie Blue

Chl:

Chlorophyll

Chlase:

Chlorophyllase

Cyt b6/f :

Cytochrome b6/f

DW:

Dry weight

EDTA:

Ethylenediaminetetraacetic acid

FW:

Fresh weight

GL:

Grana lamellae

LHCII:

Light-harvesting complex II

LHCB:

Light-harvesting chlorophyll a/b binding protein

LHCs:

Light-harvesting complexes

MGBG:

Mitoguazone

P:

Osmiophilic particles

PAs:

Polyamines

PPFD:

Photosynthetic photon flux density

PSI:

Photosystem I

PSII:

Photosystem II

PVDF:

Polyvinylidene fluoride

Put:

Putrescine

SDS:

Sodium dodecyl sulphate

SDS-PAGE:

Sodium dodecyl sulphate–polyacrylamide gel electrophoresis

SG:

Starch granules

Spd:

Spermidine

Spm:

Spermine

References

  • Abdelmageed AHA, Gruda N (2009) Influence of high temperatures on gas exchange rate and growth of eight tomato cultivars under controlled heat stress conditions. Eur J Horticul Sci 74:152–159

    CAS  Google Scholar 

  • Andersson B, Barber J (1996) Mechanisms of photodamage and protein degradation during photoinhibition of photosystem II. Adv Photosynth Respir 5:101–121

    Article  CAS  Google Scholar 

  • Andersson J, Wentworth M, Walters RG, Howard CA, Ruban AV, Horton P, Jansson S (2003) Absence of the Lhcb1 and Lhcb2 proteins of the light-harvesting complex of photosystem II-effects on photosynthesis, grana stacking and fitness. Plant J Cell Mol Biol 35:350–361

    Article  CAS  Google Scholar 

  • Barros T, Kühlbrandt W (2009) Crystallisation, structure and function of plant light-harvesting. Compl II Biochim Biophys Acta (BBA) Bioenerg 1787:753–772

    Article  CAS  Google Scholar 

  • Cheng L, Zou Y (2009) Polyamine accumulation in transgenic tomato enhances the tolerance to high temperature stress. J Integr Plant Biol 51:489–499

    Article  CAS  PubMed  Google Scholar 

  • Demetriou G, Neonaki C, Navakoudis E et al (2007) Salt stress impact on the molecular structure and function of the photosynthetic apparatus—the protective role of polyamines. Biochim Biophys Acta BBA 1767:272–280

    Article  CAS  PubMed  Google Scholar 

  • Edreva A, Yordanov I, Kardjieva R, Gesheva E (1998) Heat shock responses of bean plants: involvement of free radicals, antioxidants and free radical/active oxygen scavenging systems. Biol Plant 41:185–191

    Article  CAS  Google Scholar 

  • Fernandez-Lopez JA, Almela L, Lopez-Roca JM, Alcaraz C (1991) Iron deficiency in citrus limon: effects on photo-chlorophyllase synthetic pigments and chlorophyllase activity. J Plant Nutr 14:1133–1144

    Article  CAS  Google Scholar 

  • Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838

    Article  CAS  PubMed  Google Scholar 

  • Garab G, Cseh Z, Kovács L (2002) Light-induced trimer to monomer transition in the main light-harvesting antenna complex of plants: thermo-optic mechanism. Biochemistry 41(51):15121

    Article  CAS  PubMed  Google Scholar 

  • Gill SS, Tuteja N (2010) Polyamines and abiotic stress tolerance in plants. Plant Signal Behav 5:26–33

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gounaris K, Brain APR, Quinn PJ, Williams WP (1983) Structural and functional changes associated with heat-induced phase-separations of non-bilayer lipids in chloroplast thylakoid membranes. FEBS Lett 153:47–52

    Article  CAS  Google Scholar 

  • Gu W, Xie X, Gao S, Zhou W, Pan G, Wang G (2013) Comparison of different cells of Haematococcus pluvialis reveals an extensive acclimation mechanism during its aging process: from a perspective of photosynthesis. PLoS One 8:e67028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haldimann P, Feller U (2004) Inhibition of photosynthesis by high temperature in oak (Quercus pubescens L.) leaves grown under natural conditions closely correlates with a reversible heat-dependent reduction of the activation state of ribulose-1,5-bisphosphate carboxylase/oxygen. Plant Cell Enviro 27:1169–1183

    Article  CAS  Google Scholar 

  • Hamdani S, Yaakoubi H, Carpentier R (2011) Polyamines interaction with thylakoid proteins during stress. J Photochem Photobiol B Biol 104:314–319

    Article  CAS  Google Scholar 

  • Hasanuzzaman M, Nahar K, Fujita M, Anjum NA, Gill SS, Gill R (2014) Regulatory role of polyamines in growth, development and abiotic stress tolerance in plants. Ann N Y Acad Sci 190:322–329

    Google Scholar 

  • Hörtensteiner S (2009) Stay-green regulates chlorophyll and chlorophyll-binding protein degradation during senescence. Trends Plant Sci 14:155–162

    Article  PubMed  Google Scholar 

  • Hubbart S, Ajigboye OO, Horton P, Murchie EH (2012) The photoprotective protein PsbS exerts control over CO2 assimilation rate in fluctuating light in rice. Plant J 71:402–412

    CAS  PubMed  Google Scholar 

  • Ingle RA, Smith JAC, Sweetlove LJ (2005) Responses to nickel in the proteome of the hyperaccumulator plant Alyssum lesbiacum. Biometals 18:627–641

    Article  CAS  PubMed  Google Scholar 

  • Ioannidis NE, Sfichi L, Kotzabasis K (2006) Putrescine stimulates chemiosmotic ATP synthesis. Biochem Biophys Acta 1757:821

    CAS  PubMed  Google Scholar 

  • Jansson S, Virgin I, Gustafsson P, Andersson B, Öqulst G (1992) Light-induced changes of photosystem II activity in dark-grown Scots pine seedlings. Physiol Plant 84:6–12

    Article  CAS  Google Scholar 

  • Kapri-Pardes E, Naveh L, Adam Z (2007) The thylakoid lumen protease Deg1 is involved in the repair of photosystem II from photoinhibition in Arabidopsis. Plant Cell 19:1039–1047

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lan S, Wu L, Zhang D, Hu C (2012) Composition of photosynthetic organisms and diurnal changes of photosynthetic efficiency in algae and moss crusts. Plant Soil 351:325–336

    Article  CAS  Google Scholar 

  • Lan S, Wu L, Zhang D, Hu C (2014) Desiccation provides photosynthetic protection for crust cyanobacteria Microcoleus vaginatus from high temperature. Physiol Plant 152:345–354

    Article  CAS  PubMed  Google Scholar 

  • Liliana S, Nikolaos L, Kiriakos K (2004) Thylakoid-associated polyamines adjust the UV-B sensitivity of the photosynthetic apparatus by means of light-harvesting Complex II changes. Photochem Photobiol 80:499–506

    Article  Google Scholar 

  • Lipinska B, Fayet O, Baird L (1989) Identification, characterization, and mapping of the escherichia coli htra gene, whose product is essential for bacterial growth only at elevated temperatures. J Bacteriol 171(3):1574–1584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Marutani Y, Yamauchi Y, Miyoshi A, Inoue K, Ikeda K, Mizutani M, Sugimoto Y (2014) Regulation of photochemical energy transfer accompanied by structural changes in thylakoid membranes of heat-stressed wheat. Int J Mol Sci 15:23042–23058

    Article  PubMed  PubMed Central  Google Scholar 

  • Murkowski A (2001) Heat stress and spermidine: effect on chlorophyll fluorescence in tomato plants. Biol Plant 44:53–57

    Article  CAS  Google Scholar 

  • Navakoudis E, Lütz C, Langebartels C, Lütz-Meindl U, Kotzabasis K (2003) Ozone impact on the photosynthetic apparatus and the protective role of polyamines. Biochim Biophys Acta (BBA) Gen Subj 1621:160–169

    Article  CAS  Google Scholar 

  • Nield J, Redding K, Hippler M (2004) Remodeling of light-harvesting protein complexes in chlamydomonas in response to environmental changes. Eukaryot Cell 3:1370–1380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oda M (1993) Effects of humidity and soil moisture content on chlorophyll fluorescence of cucumber seedlings exposed to high air temperature. J Jpn Soc Horticult Sci 62:399–405

    Article  CAS  Google Scholar 

  • Ogweno JO et al (2008) Brassinosteroids Alleviate heat-induced inhibition of photosynthesis by increasing carboxylation efficiency and enhancing antioxidant systems in Lycopersicon esculentum. J Plant Growth Regul 27:49–57

    Article  CAS  Google Scholar 

  • Porra RJ (2002) The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b. Photosynth Res 73:149–156

    Article  CAS  PubMed  Google Scholar 

  • Purohit GK, Mahanty A (2016) Evaluation of housekeeping genes as references for quantitative real-time PCR analysis of gene expression in the murrel Channa striatus under high-temperature stress. Fish Physiol Biochem 42:1–11

    Article  Google Scholar 

  • Rast A, Heinz S, Nickelsen J (2015) Biogenesis of thylakoid membranes. Biochim Biophys Acta (BBA) Bioenerg 1847:821–830

    Article  CAS  Google Scholar 

  • Reisinger V, Eichacker LA (2006) Analysis of membrane protein complexes by Blue Native PAGE. Proteomics 6(Suppl 2):6–15

    Article  PubMed  Google Scholar 

  • Ruban AV et al (2003) Plants lacking the main light-harvesting complex retain photosystem II macro-organization. Nature 421:648–652

    Article  CAS  PubMed  Google Scholar 

  • Sang QQ, Shu S, Shan X, Guo SR, Sun J (2016) Effects of exogenous spermidine on antioxidant system of tomato seedlings exposed to high temperature stress Russian. J Plant Physiol 63:645–655

    CAS  Google Scholar 

  • Schelbert S, Aubry S, Burla B, Agne B, Kessler F, Krupinska K, Hörtensteiner S (2009) Pheophytin pheophorbide hydrolase (pheophytinase) is involved in chlorophyll breakdown during leaf senescence in Arabidopsis. Plant Cell 21:767–785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sfakianaki M, Sfichi L, Kotzabasis K (2006) The involvement of LHCII-associated polyamines in the response of the photosynthetic apparatus to low temperature. J Photochem Photobiol B Biol 84:181–188

    Article  CAS  Google Scholar 

  • Shan X, Guo SR (2016) Effects of exogenous spermidine on carbon and nitrogen metabolism in tomato seedlings under high temperature. J Am Soc Hortic Sci 141:4381–4388

    Google Scholar 

  • Shu S, Guo SR, Sun J, Yuan LY (2012) Effects of salt stress on the structure and function of the photosynthetic apparatus in Cucumis sativus and its protection by exogenous putrescine. Physiol Plant 146:285–296

    Article  CAS  PubMed  Google Scholar 

  • Standfuss J, Ac TVS, Lamborghini M, Kühlbrandt W (2005) Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5 A resolution. EMBO J 24:919–928

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Talanova VV, Topchieva LV, Titov AF (2006) Effect of abscisic acid on the resistance of cucumber seedlings to combined exposure to high temperature and chloride. Biol Bull 33:619–622

    Article  CAS  Google Scholar 

  • Tian J, Wang LP, Yang YJ, Sun J, Guo SR (2012) Exogenous spermidine alleviates the oxidative damage in cucumber seedlings subjected to high temperatures. J Am Soc Horticult 137:11–19

    CAS  Google Scholar 

  • Vani B, Saradhi PP, Mohanty P (2001) Alteration in chloroplast structure and thylakoid membrane composition due to heat treatment of rice seedlings: correlation with the functional changes. J Plant Physiol 158:583–592

    Article  CAS  Google Scholar 

  • Wu XX, Yao XF (2014) Brassinosteroids protect photosynthesis and antioxidant system of eggplant seedlings from high-temperature stress. Acta Physiol Plant 36:251–261

    Article  CAS  Google Scholar 

  • Yamori W, Shikanai T (2016) Physiological functions of cyclic electron transport around photosystem I in sustaining photosynthesis and plant growth. Annu Rev Plant Biol 67(1):81–106

    Article  CAS  PubMed  Google Scholar 

  • Yamori W, Noguchi K, Hikosaka K, Terashima I (2010) Phenotypic plasticity in photosynthetic temperature acclimation among crop species with different cold tolerances. Plant Physiol 152:388–399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamori W, Hikosaka K, Way DA (2014) Temperature response of photosynthesis in C3, C4, and CAM plants: temperature acclimation and temperature adaptation. Photosynth Res 119:101–117

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was financially supported by the National Natural Science Foundation of China (Nos. 31471869, 31401919, and 31272209), the Priority Academic Program Development of Jiangsu Higher Education Institutions (PDPA), the China Agriculture Research System (CARS-25-C-03) and the Research Fund for the Doctoral Program of Higher Education (20130097120015).

Author information

Author notes

  1. Liwei Wang and Heng Zhou have contributed equally to this work.

Authors and Affiliations

  1. Key Laboratory of Southern Vegetable Crop Genetic Improvement in Ministry of Agriculture College of Horticulture, Nanjing Agriculture University, Nanjing, 210095, People’s Republic of China

    Liwei Wang, Heng Zhou, Shirong Guo, Yahong An, Sheng Shu & Jin Sun

  2. Jiangsu Province Engineering Laboratory for Modern Facility Agriculture Technology and Equipment, Nanjing, 210095, People’s Republic of China

    Liwei Wang, Heng Zhou, Shirong Guo, Yahong An, Sheng Shu & Jin Sun

  3. Center for Environment, Health and Field Science, Chiba University, Kashiwa-no-ha 6-2-1, Kashiwa, Chiba, Japan

    Na Lu

Authors
  1. Liwei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Heng Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shirong Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yahong An
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sheng Shu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Na Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jin Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jin Sun.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest to declare.

Additional information

Communicated by E. Schleiff.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (JPEG 8457 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, L., Zhou, H., Guo, S. et al. Exogenous spermidine maintains the chloroplast structure of cucumber seedlings and inhibits the degradation of photosynthetic protein complexes under high-temperature stress. Acta Physiol Plant 40, 47 (2018). https://doi.org/10.1007/s11738-018-2624-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-018-2624-9

Keywords

Search

Navigation