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Effects of exogenous spermidine on photosynthetic capacity and expression of Calvin cycle genes in salt-stressed cucumber seedlings

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Abstract

We investigated the effects of exogenous spermidine (Spd) on growth, photosynthesis and expression of the Calvin cycle-related genes in cucumber seedlings (Cucumis sativus L.) exposed to NaCl stress. Salt stress reduced net photosynthetic rates (P N ), actual photochemical efficiency of PSII (ΦPSII) and inhibited plant growth. Application of exogenous Spd to salinized nutrient solution alleviated salinity-induced the inhibition of plant growth, together with an increase in P N and ΦPSII. Salinity markedly reduced the maximum carboxylase activity of ribulose-1,5-bisphosphate carboxylase/oxygenase (Vcmax), the maximal velocity of RuBP regeneration (Jmax), triose-phosphate utilization capacity (TPU) and carboxylation efficiency (CE). Spd alleviated the negative effects on CO2 assimilation induced by salt stress. Moreover, Spd significantly increased the activities and contents of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) and fructose-1,6-biphosphate aldolase (ALD; aldolase) in the salt-stressed cucumber leaves. On the other hand, salinity up-regulated the transcriptional levels of ribulose-1,5-bisphosphate (RCA), glyceraldehyde-3-phosphate dehydrogenase (GAPDH) and phosphoribrokinase (PRK) and down-regulated the transcriptional levels of ribulose-1,5-bisphosphate carboxylase/oxygenase large subunit (RbcL), ribulose-1,5-bisphosphate carboxylase/oxygenase small subunit (RbcS), ALD, triose-3-phosphate isomerase (TPI), fructose-1,6-bisphosphate phosphatase (FBPase) and 3-phosphoglyceric acid kinase (PGK). However, Spd application to salt-stressed plant roots counteracted salinity-induced mRNA expression changes in most of the above-mentioned genes. These results suggest that Spd could improve photosynthetic capacity through regulating gene expression and activity of key enzymes for CO2 fixation, thus confers tolerance to salinity on cucumber plants.

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References

  • Abbasi FM, Komatsu S (2004) A proteomic approach to analyze salt-responsive proteins in rice leaf sheath. Proteomics 4:2072–2081

    Article  PubMed  CAS  Google Scholar 

  • Barhoumi Z, Djebali W, Chaïbi W, Abdelly C, Smaoui A (2007) Salt impact on photosynthesis and leaf ultrastructure of Aeluropus littoralis. J Plant Res 126:859–867

    Google Scholar 

  • Beauchemin R, Gauthier A, Harnois J, Boisvert S, Govindachary S, Carpentier R (2007) Spermine and spermidine inhibition of photosystem II: disassembly of the oxygen evolving complex and onsequent perturbation in electron donation from TyrZ to P680+ and the quinone acceptors Q −A to QB. Biochim Biophys Acta 1767:905–912

    Article  PubMed  CAS  Google Scholar 

  • Besford RT, Richardson CM, Campos JL, Tiburcio AF (1993) Effect of polyamines on stabilization of molecular complexes in thylakoid membranes of osmotically stressed oat leaves. Planta 189:201–206

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantization of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Chattopadhayay MK, Tiwari BS, Chattopadhyay G, Bose A, Sengupta DN, Ghosh B (2002) Protective role of exogenous polyamines on salinity-stressed rice (Oryza sativa) plants. Physiol Plant 116:192–199

    Article  PubMed  CAS  Google Scholar 

  • Chen LF, Lu W, Sun J, Guo SR, Zhang ZX, Yang YJ (2011) Effects of exogenous spermidine on photosynthesis and carbohydrate accumulation in roots and leaves of cucumber (Cucumis sativus L.) seedlings under salt stress. Chin J Nanjing Agric University 34:31–36

    Google Scholar 

  • Christine AR (2003) The Calvin cycle revisited. Photosynth Res 75:1–10

    Article  Google Scholar 

  • Duan JJ, Li J, Guo SR, Kang YY (2008) Exogenous spermidine affects polyamine metabolism in salinity-stressed Cucumis sativus roots and enhances short-term salinity tolerance. J Plant Physiol 165:1620–1635

    Article  PubMed  CAS  Google Scholar 

  • Dubois JB, Fiscus EL, Booker FL, Flowers MD, Reid CD (2007) Optimizing the statistical estimation of the parameters of the Farquhar–von Caemmerer–Berry model of photosynthesis. New Phytol 176:402–414

    Article  PubMed  Google Scholar 

  • Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Ann Rev Plant Physiol 33:317–345

    Article  CAS  Google Scholar 

  • Feng LL, Han YJ, Liu G, An BG, Yang J, Yang GH, Li YS, Zhu YG (2007) Overexpression of sedoheptulose-1,7-bisphosphatase enhances photosynthesis and growth under salt stress in transgenic rice plants. Funct Plant Biol 34:822–834

    Article  CAS  Google Scholar 

  • Fridlyand LE, Scheibe R (1999) Regulation of the Calvin cycle for CO2 fixation as an example for general control mechanisms in metabolic cycles. BioSystems 51:79–93

    Article  PubMed  CAS  Google Scholar 

  • Geissler N, Hussin S, Koyro HW (2009) Interactive effects of NaCl salinity and elevated atmospheric CO2 concentration on growth, photosynthesis, water relations and chemical composition of the potential cash crop halophyte (Aster tripolium L.). Environ Exp Bot 65:220–231

    Article  CAS  Google Scholar 

  • Gil R, Boscaiu M, Lull C, Bautista I, Lidón A, Vicente O (2013) Are soluble carbohydrates ecologically relevant for salt tolerance in halophytes? Funct Plant Biol 40:805–818

    CAS  Google Scholar 

  • Haake V, Zrenner R, Sonnewald U, Stitt M (1998) A moderate decrease of plastid aldolase activity inhibits photosynthesis, alters the levels of sugars and starch, and inhibits growth of potato plants. Plant J 14:147–157

    Article  PubMed  CAS  Google Scholar 

  • He Y, Yu CL, Zhou L, Chen Y, Liu A, Jin JH, Hong J, Qi YH, Jiang D (2014) Rubisco decrease is involved in chloroplast protrusion and Rubisco-containing body formation in soybean (Glycine max.) under salt stress. Plant Physiol Biochem 74:118–124

    Article  PubMed  CAS  Google Scholar 

  • HuangXX Bie ZL (2010) Cinnamic acid-inhibited ribulose-1,5-bisphosphate carboxylase activity is mediated through decreased spermine and changes in the ratio of polyamines in cowpea. J Plant Physiol 167:47–53

    Article  Google Scholar 

  • Jiang XY, Song J, Fan H, Zhao KF (2000) Regulation of exogenous calcium and spermidine on ion balance and polyamine levels in maize seedlings under NaCl stress. Acta Phytophysiolocica Sinica 26:539–544

    CAS  Google Scholar 

  • Kang RJ, Shi DJ, Cong W, Ma WM, Cai ZL, Fan QY (2005) Effects of co-expression of two higher plants genes ALD and TPI in Anabaena sp. PCC7120 on photosynthetic CO2 fixation. Enzyme Microbial Tech 36:600–604

    Article  CAS  Google Scholar 

  • Kasukabe Y, He LX, Nada K, Misawa SH, Ihara I, Tachibana S (2004) Overexpression of spermidine synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stress regulated genes in transgenic Arabidopsis thaliana. Plant Cell Physiol 45:712–722

    Article  PubMed  CAS  Google Scholar 

  • Kelly GJ, Latzko E (1976) Regulatory as peats of photosynthetic carbon metabolism. Ann Rev Plant Physiol 27:185–191

    Article  Google Scholar 

  • Kooten O, Snel J (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 25:147–150

    Article  PubMed  Google Scholar 

  • Kusano T, Yamaguchi K, Berberich T, Takahashi Y (2007) Advance in polyamine research in 2007. J Plant Res 120:345–350

    Article  PubMed  CAS  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680

    Article  PubMed  CAS  Google Scholar 

  • Lee SW, Hahn TR (2002) Two light-responsive elements of pea chloroplastic fructose-1,6-bisphosphatase gene involved in the red-light-specific gene expression in transgenic tobaccos. Biochim Biophys Acta 1579:8–17

    Article  PubMed  CAS  Google Scholar 

  • Li J, Gao XH, Guo SR, Zhang RH, Wang X (2007) Effects of exogenous spermidine on photosynthesis of salt-stressed Cuellmis sativus seedlings. Chin J Ecol 26:1595–1599

    CAS  Google Scholar 

  • Lorimer GH (1981) Ribulosebisphosphate carboxylase: amino acid sequence of a peptide bearing the activator carbon dioxide. Biochemistry 20:1236–1240

    Article  PubMed  CAS  Google Scholar 

  • Lu CM, Qiu NW, Wang BS, Zhang J (2003) Salinity treatment shows no effects on photosystem II photochemistry, but increases the resistance of photosystem II to heat stress in halophyte Suaeda salsa. J Exp Bot 54:851–860

    Article  PubMed  CAS  Google Scholar 

  • Lu KX, Cao BH, Feng XP, He Y, Jiang DA (2009) Photosynthetic response of salt-tolerant and sensitive soybean varieties. Photosynthetica 47:381–387

    Article  CAS  Google Scholar 

  • Maliro MFA, McNeil D, Redden B, Kollmorgen JF, Pittock C (2008) Sampling strategies and screening of chickpea (Cicer arietinum L.) germplasm for salt tolerance. Genet Resour Crop Evol 55:53–63

    Article  Google Scholar 

  • Marston JP, Cliff MJ, Reed MA, Blackburn GM, Hounslow AM, Craven CJ, Waltho JP (2010) Structural tightening and interdomain communication in the catalytic cycle of phosphoglycerate kinase. J Mol Biol 396:345–360

    Article  PubMed  CAS  Google Scholar 

  • Mittal S, Kumari N, Sharma V (2012) Differential response of salt stress on Brassica juncea: photosynthetic performance, pigment, proline, D1 and antioxidant enzymes. Plant Physiol Biochem 54:17–26

    Article  PubMed  CAS  Google Scholar 

  • Mustroph A, Albrecht G (2003) Tolerance of crop plants to oxygen deficiency stress: fermentative activity and photosynthetic capacity of entire seedlings under hypoxia and anoxia. Physiol Plant 117:508–520

    Article  PubMed  CAS  Google Scholar 

  • Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349

    Article  PubMed  CAS  Google Scholar 

  • Praxedes SC, DaMatta FM, Loureiro ME, Ferrãob MAG, Cordeiroa AT (2006) Effects of long-term soil drought on photosynthesis and carbohydrate metabolism in mature robusta coffee (Coffea canephora Pierre var. kouillou) leaves. Environ Exp Bot 56:263–273

    Article  CAS  Google Scholar 

  • Roychoudhury A, Basu S, Sengupta DN (2011) Amelioration of salinity stress by exogenously applied spermidine or spermine in three varieties of indica rice differing in their level of salt tolerance. J Plant Physiol 168:317–328

    Article  PubMed  CAS  Google Scholar 

  • Sharkey TD, SeemannJ R, Beny JA (1986) Regulation of ribulose-l,5-bisphosphate-carboxylase activity in response to changing partial pressure of O2 and light in Phaseolus vulgaris. Plant Physiol 81:788–791

    Article  PubMed  CAS  PubMed Central  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 L. and its protection by exogenous putrescine. Physiol Plant 146:285–296

    Article  PubMed  CAS  Google Scholar 

  • Shu S, Yuan LY, Guo SR, Sun J, Yuan YH (2013) Effects of exogenous spermine on chlorophyll fluorescence, antioxidant system and ultrastructure of chloroplasts in Cucumis sativus L. under salt stress. Plant Physiol Biochem 63:209–216

    Article  PubMed  CAS  Google Scholar 

  • Sudhir P, Murthy SDS (2004) Effects of salt stress on basic processes of photosynthesis. Photosynthetica 42:481–486

    Article  CAS  Google Scholar 

  • Takahashi Y, Cong R, Sagor GHM, Niitsu M, Berberich T, Kusano T (2010) Characterization of five polyamine oxidase isoforms in Arabidopsis thaliana. Plant Cell Rep 29:955–965

    Article  PubMed  CAS  Google Scholar 

  • Uematsu K, Suzuki N, Iwamae T, Inui M, Yukawa H (2012) Increased fructose 1,6-bisphosphate aldolase in plastids enhances growth and photosynthesis of tobacco plants. J Exp Bot 63:3001–3009

    Article  PubMed  CAS  Google Scholar 

  • Wang H, Gu M, Cui J, Shi K, Zhou Y, Yu J (2009) Effects of light quality on CO2 assimilation, chlorophyll-fluorescence quenching, expression of Calvin cycle genes and carbohydrate accumulation in Cucumis sativus. J Photochem Photobiol B: Biol 96:30–37

    Article  CAS  Google Scholar 

  • Yamane K, Mitsuya S, Taniguchi M, Miyake H (2012) Salt-induced chloroplast protrusion is the process of exclusion of ribulose-1,5-bisphosphate carboxylase/oxygenase from chloroplasts into cytoplasm in leaves of rice. Plant Cell Environ 35:1663–1671

    Article  PubMed  CAS  Google Scholar 

  • Yang X, Liang Z, Wen X, Lu C (2008) Genetic engineering of the biosynthesis of glycinebetaine leads to increased tolerance of photosynthesis to salt stress in transgenic tobacco plants. Plant Mol Biol 66:73–86

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was funded by National Basic Research Program of China (973 Program, No. 2009CB119000) and National Natural Science Foundation of China (No. 31071831; No. 31272209) and Supported by the China earmarked fund for Modern Agro-industry Technology Research System (CARS-25-C-03) and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD) and sponsored by Research Fund for the Doctoral Program of Higher Education (20130097120015).

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  1. College of Horticulture, Nanjing Agricultural University, Key Laboratory of Southern Vegetable Crop Genetic Improvement, Ministry of Agriculture, Weigang No.1, Nanjing, 210095, Jiangsu, People’s Republic of China

    Sheng Shu, Lifang Chen, Wei Lu, Jin Sun, Shirong Guo, Yinhui Yuan & Jun Li

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  1. Sheng Shu
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  2. Lifang Chen
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  7. Jun Li
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Correspondence to Shirong Guo.

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Shu, S., Chen, L., Lu, W. et al. Effects of exogenous spermidine on photosynthetic capacity and expression of Calvin cycle genes in salt-stressed cucumber seedlings. J Plant Res 127, 763–773 (2014). https://doi.org/10.1007/s10265-014-0653-z

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