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Exogenous spermidine delays chlorophyll metabolism in cucumber leaves (Cucumis sativus L.) under high temperature stress

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Abstract

This study evaluated the effects of exogenous spermidine (Spd) on chlorophyll (Chl) biosynthesis and catabolism in the leaves of cucumber (Cucumis sativus L.) seedlings under high temperature stress. Substrate culture experiments were performed using the high temperature-sensitive variety ‘Jinchun No. 2’ in an artificial climate chamber at 42/32 °C with foliar applications of 1.0 mmol L−1 Spd. The results suggested that high temperature stress markedly reduced the leaf Chl concentrations and inhibited plant growth; the harmful effect of high temperature on the cucumber seedlings was mitigated by exogenous Spd, which increased the leaf Chl concentration and promoted plant growth. Under high temperature stress, the conversion of porphobilinogen (PBG) into uroporphyrinogen III (UroIII) in the Chl biosynthetic pathway and the catabolic process of Chl were accelerated. Following the application of exogenous Spd, the conversion of PBG into UroIII was suppressed, and the accumulation of certain intermediates, e.g., protoporphyrin IX (ProtoIX) and Mg-protoporphyrin IX (Mg-ProtoIX), was decreased in the Chl biosynthetic pathway. Additionally, exogenous Spd reduced chlorophyllase (Chlase) and Mg-dechelatase (MDCase) activity and transcript levels and markedly downregulated pheophorbide A oxygenase (PaO), red Chl catabolite reductase (RCCR), Chl b reductase 1 (CBR1) and stay-green reductase 1 (SGR1) transcript levels. These results indicate that although high temperature stress accelerated Chl biosynthesis, it concurrently facilitated Chl catabolism in cucumber leaves. Exogenous Spd delayed the conversion of PBG into UroIII in the Chl biosynthetic pathway, effectively preventing oxidative bleaching of Chl in cucumber leaves. Meanwhile, Spd clearly decreased PaO pathway-related enzyme activity and transcript levels, thereby slowing Chl catabolism and increasing Chl concentrations.

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Abbreviations

ALA:

δ-Aminolevulinic acid

CBR:

Chl b reductase

CCEs:

Chl catabolic enzymes

Chl:

Chlorophyll

Chlase:

Chlorophyllase

Chlide a:

Chlorophyllide a

CLH :

Chlorophyllase

HMBS :

Hydroxymethylbilane synthase

MDCase:

Mg-dechelatase

Mg-ProtoIX:

Mg-protoporphyrin IX

NCCs:

Nonfluorescent Chl catabolites

LHCII:

Photosystem II

LHCP II–Chl:

Chl–protein complex

pFCCs:

Primary fluorescent Chl catabolites

PBG:

Porphobilinogen

PaO:

Pheophorbide A oxygenase

PAs:

Polyamines

PBGD:

Porphobilinogen deaminase

Pchl:

Proto Chl

Pheide a:

Pheophorbide a

Pheide b:

Pheophorbide b

ProtoIX:

Protoporphyrin IX

RCCR:

Red Chl catabolite reductase

RCCs:

Red Chl catabolites

ROS:

Reactive oxygen species

SGR1:

Stay-green reductase 1

Spd:

Spermidine

UroIII:

Uroporphyrinogen III

UROS:

Uroporphyrinogen III synthase

References

  • Alcazar R, Altabella T, Marco F, Bortolotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF (2010) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231:1237–1249

    Article  CAS  PubMed  Google Scholar 

  • Armstrong GA, Runge S, Frick G, Sperling U, Apel K (1995) Identification of NADPH:protochlorophyllide oxidoreductases A and B: a branched pathway for light-dependent chlorophyll biosynthesis in Arabidopsis thaliana. Plant Physiol 108:1505–1517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Battersby AR, Leeper FJ (2002) Biosynthesis of the pigments of life: mechanistic studies on the conversion of porphobilinogen to uroporphyrinogen III. Chem Rev 90:1261–1274

    Article  Google Scholar 

  • Beale SI (2005) Green genes gleaned. Trends Plant Sci 10:309–312

    Article  CAS  PubMed  Google Scholar 

  • Bogorad L (1962) Porphyrin synthesis. Methods Enzymol 5:885–895

    Article  CAS  Google Scholar 

  • Boyer JS (1982) Plant productivity and environment. Science 218:443–448

    Article  CAS  PubMed  Google Scholar 

  • Costa ML, Civello PM, Chaves AR, Martinez GA (2002) Characterization of Mg-dechelatase activity obtained from Fragaria × ananassa fruit. Plant Physiol Biochem 40:111–118

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  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. Plant Physiol 165:1620–1635

    Article  CAS  Google Scholar 

  • Enriqueta A, María R, Domingo José I, Maria Isabel MM, Damasceno CMB, Theodore William T, Rose JKC, Manuel T, Manuel C (2008) An evaluation of the basis and consequences of a stay-green mutation in the navel negra citrus mutant using transcriptomic and proteomic profiling and metabolite analysis. Plant Physiol 147:1300–1315

    Article  Google Scholar 

  • Fang ZY, Bouwkamp JC, Solomos T (1998) Chlorophyllase activities and chlorophyll degradation during leaf senescence in non-yellowing mutant and wild type of Phaseolus vulgaris L. J Exp Bot 49:503–510

    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 

  • Foyer CH, Shigeoka S (2010) Focus issue on enhancing photosynthesis: understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol 155:93–100

    Article  PubMed  PubMed Central  Google Scholar 

  • Frydman RB, Frydman B (1979) Disappearance of porphobilinogen deaminase activity in leaves before the onset of senescence. Plant Physiol 63:1154–1157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ginsburg S, Matile P (1993) Identification of catabolites of chlorophyll-porphyrin in senescent rape cotyledons. Plant Physiol 102:521–527

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ginsburg S, Schellenberg M, Matile P (1994) Cleavage of chlorophyll-porphyrin (requirement for reduced ferredoxin and oxygen). Plant Physiol 105:545–554

    CAS  PubMed  PubMed Central  Google Scholar 

  • Harpaz-Saad S, Azoulay T, Arazi T, Ben-Yaakov E, Mett A, Shiboleth YM, Hörtensteiner S, Gidoni D, Gal-On A, Goldschmidt EE, Eyal Y (2007) Chlorophyllase is a rate-limiting enzyme in chlorophyll catabolism and is posttranslationally regulated. Plant Cell 19:1007–1022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hendry GAF, Brown SB (1987) Tansley review no. 11. The degradation of chlorophyll-A biological enigma. New Phytol 107:255–302

    Article  CAS  Google Scholar 

  • Hodgins RR, van Huystee RB (1986) Rapid simultaneous estimation of protoporphyrin and Mg-porphyrins in higher plants. J Plant Physiol 125:311–323

    Article  CAS  Google Scholar 

  • Hortensteiner S (2006) Chlorophyll degradation during senescence. Annu Rev Plant Biol 57:55–77

    Article  CAS  PubMed  Google Scholar 

  • Hortensteiner S, Krautler B (2011) Chlorophyll breakdown in higher plants. Biochim Biophys Acta 1807:977–988

    Article  CAS  PubMed  Google Scholar 

  • Hummel I, El-Amrani A, Gouesbet G, Hennion F, Couee I (2004) Involvement of polyamines in the interacting effects of low temperature and mineral supply on Pringlea antiscorbutica (Kerguelen cabbage) seedlings. J Exp Bot 55:1125–1134

    Article  CAS  PubMed  Google Scholar 

  • Klein S, Harel E, Ne’eman E, Katz E, Meller E (1975) Accumulation of delta-aminolevulinic acid and its relation to chlorophyll synthesis and development of plastid structure in greening leaves. Plant Physiol 56:486–496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krishnan R, Ramakrishnan B, Reddy KR, Reddy VR (2011) High-temperature effects on rice growth, yield, and grain quality. Adv Agron 111:87–206

    Article  CAS  Google Scholar 

  • Kumar TA, Charan TB (1998) Temperature-stress-induced impairment of chlorophyll biosynthetic reactions in cucumber and wheat. Plant Physiol 117:851–858

    Article  Google Scholar 

  • Lin DD, Zhang GF, Yu JB, Feng J (2011) Analyses of photosynthetic pigment content and chlorophyll fluorescence parameter in leaves of different clones of Cinnamomum camphora. J Plant Resour Environ 20:56–61

    Google Scholar 

  • Mathis JN, Burkey KO (1989) Light intensity regulates the accumulation of the major light-harvesting chlorophyll-protein in greening seedlings. Plant Physiol 90:560–566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matile P, Hortensteiner S, Thomas H (1999) Chlorophyll degradation. Annu Rev Plant Physiol Plant Mol Biol 50:67–95

    Article  CAS  PubMed  Google Scholar 

  • Min YU, Cheng-Xiao HU, Wang YH (2006) Effects of molybdenum on the precursors of chlorophyll biosynthesis in winter wheat cultivars under low temperature. Sci Agric Sin 39:702–708

    Google Scholar 

  • Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767:414–421

    Article  CAS  PubMed  Google Scholar 

  • Nozomi N, Ryouichi T, Soichirou S, Ayumi T (2005) Identification of a vinyl reductase gene for chlorophyll synthesis in Arabidopsis thaliana and implications for the evolution of Prochlorococcus species. Plant Cell 17:233–240

    Article  Google Scholar 

  • Oda M (1993) Effects of humidity and soil moisture content on chlorophyll fluorescence of cucumber seedlings exposed to high air temperature. Engei Gakkai Zasshi 62:399–405

    Article  CAS  Google Scholar 

  • Oda M, Thilakaratne DM, Li ZJ, Sasaki H (1994) Effects of abscisic acid on high-temperature stress injury in cucumber. J Japanese Soc Hortic Sci 63:393–399

    Article  CAS  Google Scholar 

  • Park SY, Yu JW, Park JS, Jinjie L, Yoo SC, Lee NY, Lee SK, Jeong SK, Seo HS, Koh HJ (2007) The senescence-induced staygreen protein regulates chlorophyll degradation. Plant Cell 19:1649–1664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng Q, Zhou Q (2009) Influence of lanthanum on chloroplast ultrastructure of soybean leaves under ultraviolet-B stress. J Rare Earths 27:304–307

    Article  Google Scholar 

  • Pfannschmidt T, Brautigam K, Wagner R, Dietzel L, Schroter Y, Steiner S, Nykytenko A (2009) Potential regulation of gene expression in photosynthetic cells by redox and energy state: approaches towards better understanding. Ann Bot 103:599–607

    Article  CAS  PubMed  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 

  • Roca M, James C, Pruzinska A, Hortensteiner S, Thomas H, Ougham H (2004) Analysis of the chlorophyll catabolism pathway in leaves of an introgression senescence mutant of Lolium temulentum. Phytochemistry 65:1231–1238

    Article  CAS  PubMed  Google Scholar 

  • Sakuraba Y, Kim D, Kim YS, Hortensteiner S, Paek NC (2014) Arabidopsis STAYGREEN-LIKE (SGRL) promotes abiotic stress-induced leaf yellowing during vegetative growth. FEBS Lett 588:3830–3837

    Article  CAS  PubMed  Google Scholar 

  • Schelbert S, Aubry S, Burla B, Agne B, Kessler F, Krupinska K, Hortensteiner 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 

  • Seemann JR, Berry JA, Downton WJ (1984) Photosynthetic response and adaptation to high temperature in desert plants: a comparison of gas exchange and fluorescence methods for studies of thermal tolerance. Plant Physiol 75:364–368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen W, Nada K, Tachibana S (2000) Involvement of polyamines in the chilling tolerance of cucumber cultivars. Plant Physiol 124:431–439

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

    Article  CAS  PubMed  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 

  • Tanaka A, Tanaka R (2006) Chlorophyll metabolism. Curr Opin Plant Biol 9:248–255

    Article  CAS  PubMed  Google Scholar 

  • Tanaka R, Tanaka A (2007) Tetrapyrrole biosynthesis in higher plants. Annu Rev Plant Biol 58:321–346

    Article  CAS  PubMed  Google Scholar 

  • Tewari AK, Tripathy BC (1998) Temperature-stress-induced impairment of chlorophyll biosynthetic reactions in cucumber and wheat. Plant Physiol 117:851–858

    Article  CAS  Google Scholar 

  • Tian J, Guo SR, Wang LP, Liu SR, Sun J (2010) Exogenous spermidine mitigates the disruption of photosynthesis and chloroplast ultrastructure caused by high temperature stress in cucumber seedlings. Acta Hortic Sin 37 (Supplement)

  • 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 Hortic Sci 137:11–19

    Article  CAS  Google Scholar 

  • Vered N, Jaime K (2002) Temperature affects plant development, flowering and tuber dormancy in calla lily (Zantedeschia). J Hortic Sci Biotechnol 77:170–176

    Article  Google Scholar 

  • Vezitskii AY, Shcherbakov RA (2002) Interconversions of chlorophylls a and b synthesized from exogenous chlorophyllides a and b in etiolated and post-etiolated rye seedlings. Russ J Plant Physiol 49:605–609

    Article  CAS  Google Scholar 

  • Wang X, Lin WJ, Izumi K, Jiang Q, Lai KP, Xu D, Fang LY, Lu T, Li L, Xia S (2012) Increased infiltrated macrophages in benign prostatic hyperplasia (BPH): role of stromal androgen receptor in macrophage-induced prostate stromal cell proliferation. J Biol Chem 287:18376–18385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weaver LM, Gan S, Quirino B, Amasino RM (1998) A comparison of the expression patterns of several senescence-associated genes in response to stress and hormone treatment. Plant Mol Biol 37:455–469

    Article  CAS  PubMed  Google Scholar 

  • Wettstein DV (1995) Chlorophyll biosynthesis. NATO ASI 7:1039–1057

    Google Scholar 

  • Zapata PJ, Serrano M, Pretel MT, Amorós A, Botella M (2004) Polyamines and ethylene changes during germination of different plant species under salinity. Plant Sci 167:781–788

    Article  CAS  Google Scholar 

  • Zhao Q, Liu J, Khabarov N, Obersteiner M, Westphal M (2014) Impacts of climate change on virtual water content of crops in China. Ecol Inf 19:26–34

    Article  Google Scholar 

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Acknowledgments

This work was supported by the National Natural Science Foundation of China (Nos. 31471869, 31401919, and 31272209), the Central Research Institutes of Basic Research Fund (6J0745), the Priority Academic Program Development of Jiangsu Higher Education Institutions (PDPA), and the China Agriculture Research System (CARS-25-C-03) and was sponsored by the Research Fund for the Doctoral Program of Higher Education (20130097120015).

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Authors and Affiliations

  1. College of Horticulture, Nanjing Agriculture University, Nanjing, 210095, People’s Republic of China

    Heng Zhou, Shirong Guo, Yahong An, Xi Shan, Ying Wang, Sheng Shu & Jin Sun

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

    Heng Zhou, Shirong Guo, Yahong An, Xi Shan, Ying Wang, Sheng Shu & Jin Sun

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  1. Heng Zhou
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  2. Shirong Guo
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Correspondence to Jin Sun.

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Zhou, H., Guo, S., An, Y. et al. Exogenous spermidine delays chlorophyll metabolism in cucumber leaves (Cucumis sativus L.) under high temperature stress. Acta Physiol Plant 38, 224 (2016). https://doi.org/10.1007/s11738-016-2243-2

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  • DOI: https://doi.org/10.1007/s11738-016-2243-2

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