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Effects of low temperature and low irradiance on the physiological characteristics and related gene expression of different pepper species

  • Original Papers
  • Published:
Photosynthetica

Abstract

Pepper is a thermophilous and heliophilic vegetable. In China, pepper is grown in greenhouse during winter and spring under lower temperature and irradiation. In this study, we investigated the effects of low temperature and low irradiance (LTLI) on the physiological characteristics and the expression of related genes in five pepper species, Capsicum annuum L. (CA), C. baccatum L. (CB), C. chinense Jacquin (CC), C. frutescens L. (CF), and C. pubescens Ruiz & Pavon (CP) in order to screen for greenhouse species that is resistant to such adverse conditions. We observed significant reductions not only in photosynthetic pigments and stomatal conductance but also in proline, total soluble sugar, enzyme activity, and root activity; disordered arrangements of leaf palisade and spongy tissues; and first rising and then falling expression of C-repeat binding factor (CBF3) and cold-regulated genes (CORc410). These results indicate that pepper is not resistant to LTLI. We also found that CP showed significantly higher photosynthetic activity, more proline and total soluble sugar, higher enzyme activity, higher root activity, higher CBF3 and CORc410 expression levels, more tightly packed leaf palisade and spongy tissues, and thicker bundle sheath than the other four species did under LTLI, while CF exhibited the lowest values for these indicators. It demonstrated significant differences in the ability to resist to LTLI among different species, with CP showing the strongest resistance, followed by CB. Therefore, we recommend the introduction of CP and CB to greenhouse cultivation to further screen for low temperature and low light-resistant pepper varieties to increase pepper production by strengthening intervariety hybridization.

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Abbreviations

CA:

Capsicum annuum L.

Car:

carotenoids

CAT:

catalase

CB:

Capsicum baccatum L.

CBF3 :

C-repeat binding factor

CC:

Capsicum chinense Jacquin

CF:

Capsicum frutescens L.

Chl:

chlorophyll

CORc410 :

cold-regulated gene

CP:

Capsicum pubescens Ruiz & Pavon

E :

transpiration rate

Fm :

maximal fluorescence

Fm′:

maximal fluorescence under light

FM:

fresh mass

F0 :

minimal initial fluorescence

F0′:

minimal fluorescence

g s :

stomatal conductance

GR:

glutathione reductase

LTLI:

low temperature and low irradiance

qN :

nonphotochemical quenching

qP :

photochemical quenching

P N :

net photosynthetic rate

SOD:

superoxide dismutase

POD:

peroxidase

WUE:

water-use efficiency

ΦPSII :

actual photochemical efficiency of PSII in the light

References

  • An F.Q., Yu L.F., Li F.H.: [Influence of low light and low temperature on microstructure of summer squash’s leaves.] — Crops 27: 45–47, 2011. [In Chinese]

    Google Scholar 

  • An L.H., Chen L.Z., Hu Q.Q. et al.: [Effects of cold stress to three non-heading chinese cabbage OguCMS and biochemical indexes of its maintaining line.] — Chin.Vege. 1: 19–23, 2010. [In Chinese]

    Google Scholar 

  • Arnon D.I.: Copper enzymes in isolated chloroplasts phenoloxidases in Beta vulgaris. — Plant Physiol. 24: 1–15, 1949.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bai C.Y., Gao S.F., Zhang Y., Chen C.: [Analysis of anatomical leaf structure and drought resistance in 12 varieties of walnut.] — Acta Agric. Boreal. 19: 125–128, 2010. [In Chinese]

    Google Scholar 

  • Bartley G.E., Scolnik P.A.: Plant carotenoids: pigments for photoprotection, visual attraction, and human health. — Plant Cell 7: 1027–1038, 1995.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Britton G.: Structure and properties of carotenoids in relation to function. — FASEB J. 9: 1551–1558, 1995.

    CAS  PubMed  Google Scholar 

  • Cai Y.L., Song Y.C.: [Adaptive characteristics and behavior of Dalbergia millettii liana in subtropical evergreen broad-leaved forest of eastern China.] — Acta Ecol. Sin. 21: 216–224, 2001. [In Chinese]

    Google Scholar 

  • Carvallo M.A., Pino M.T., Jeknić Z. et al.: A comparison of the low temperature transcriptomes and CBF regulons of three plant species that differ in freezing tolerance: Solanum commersonii, Solanum tuberosum, and Arabidopsis thaliana. — J. Exp. Bot. 62: 3807–3819, 2011.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chai W.C., Ma R.L., Jiao, Y.S., Xing, G.M.: [Influences of low temperature stress on pepper’s growth index and physiological index.] — Acta Bot. Boreal. 25: 168–171, 2010. [In Chinese]

    Google Scholar 

  • Chinnusamy V., Zhu J., Zhu, K.: Cold stress regulation of gene expression in plants. — Trends Plant Sci. 12: 444–451, 2007.

    Article  CAS  PubMed  Google Scholar 

  • Deng, H.B., Che F.L., Xiao Y.H. et al.: [Effects of low temperature stress during flowering period on pollen characters and flag leaf physiological and biochemical characteristics of rice.] — Chin. J. Appl. Ecol. 22: 66–72, 2011. [In Chinese]

    CAS  Google Scholar 

  • Fan P.G., Li L.S., Duan W. et al.: Photosynthesis of young apple trees in response to low sink demand under different air temperatures. — Tree Physiol. 30: 313–325, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Fowler S., Thomashow M.F.: Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. — Plant Cell 14: 1675–1690, 2002.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Friend D.J.C.: The control of chlorophyll accumulation in leaves of marquis wheat by temperature and light intensity. I. The rate of chlorophyll accumulation and maximal absolute chlorophyll contents. — Physiol. Plantarum 13: 776–785, 1960.

    Article  CAS  Google Scholar 

  • Genty B., Briantais J.M., Baker N.R.: The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. — Biochim. Biophys. Acta 900: 87–92, 1989.

    Article  Google Scholar 

  • Gilmour S.J., Sebolt A.M., Salazar M.P. et al.: Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. — Plant Physiol. 124: 1854–1865, 2000.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Guy C.L.: Cold acclimation and freezing stress tolerance: Role of protein metabolism. — Annu. Rev. Plant Phys. 41: 187–223, 1990.

    Article  CAS  Google Scholar 

  • Hetherington S.E., He J., Smillie R.M.: Photoinhibition at low temperature in chilling-sensitive and resistant plants. — Plant Physiol. 90: 1609–1615, 1990.

    Article  Google Scholar 

  • Hatano-Iwasaki A., Ogawa K.: Overexpression of GSH1 gene mimics transcriptional response to low temperature during seed vernalization treatment of Arabidopsis. — Plant Cell Physiol. 53: 1195–1203, 2012.

    Article  CAS  PubMed  Google Scholar 

  • He H.J., Kou S.R., Wang X.J.: [Effects of drought stress on photosynthetic characteristics and yield components of different plant types of corn.] — Agric. Res. Arid Areas 29: 63–66, 2011. [In Chinese]

    Google Scholar 

  • He L.G.: [Expression and analysis of cold-responsive CBF-like genes in citrus and related species under low temperature.] — Ph. D. Dissertation, Huzhong Agric. Univ., 2010. [In Chinese]

  • Hodgson R.A., Raison J.K.: Inhibition of photosynthesis by chilling in moderate light: a comparison of plants sensitive and insensitive to chilling. — Planta 178: 545–552, 1989.

    Article  CAS  PubMed  Google Scholar 

  • Kendall S.L., Hellwege A., Marriot P. et al.: Induction of dormancy in Arabidopsis summer annuals requires parallel regulation of DOG1 and hormone metabolism by low temperature and CBF transcription factors. — Plant Cell 23: 2568–2580, 2011.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Li M., Yang D., Li W.: Leaf gas exchange characteristics and chlorophyll fluorescence of three wetland plants in response to long-term soil flooding. — Photosynthetica 45: 222–228, 2007.

    Article  Google Scholar 

  • Liang F., Zheng C.S., Sun X.Z., Wang W.L.: [Effects of low temperature- and weak light stress and its recovery on the photosynthesis and chlorophyll fluorescence parameters of cut flower chrysanthemum.] — Chin. J. Appl. Ecol. 21: 29–35, 2010. [In Chinese]

    CAS  Google Scholar 

  • Lin C., Wang L.H., Fan T.Y., Kuo F.W.: Lipid content and composition during the oocyte development of two gorgonian coral species in relation to low temperature preservation. — PLOS ONE 7: e38689, 2012.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Liu H.S., Han J.F., Meng F.T., Du X.T.: [Effects of several physiological index related to resistance in sesame leaves under water-logging stress in soil.] — Plant Physiol. Commun. 37: 106–108, 2001a. [In Chinese]

    CAS  Google Scholar 

  • Liu P., Meng Q.W., Zou Q. et al.: Effects of cold-hardening on chilling-induced photoinhibition of photosynthesis and on xanthophyll cycle pigments in sweet pepper. — Photosynthetica 39: 467–472, 2001b.

    Article  CAS  Google Scholar 

  • Liu W., Ai X.Z., Liang W.J. et al.: [Effects of salicylic acid on the leaf photosynthesis and antioxidant enzyme activities of cucumber seedlings under low temperature and light intensity.] — Chin. J. Appl. Ecol. 20: 441–445, 2009. [In Chinese]

    CAS  Google Scholar 

  • Onyango L.A., Dunstan R.H., Gottfries J. et al.: Effect of low temperature on growth and ultra-structure of staphylococcus spp. — PLOS ONE 7: e29031, 2012.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ou L.J., Zhang Z.Q., Dai X.Z., Zou XX.: Molecular characteristics and expression of cytoplasmic genes in cytoplasmic male sterility of pepper (Capsicum annuum L.). — Acta Physiol. Plant. 34: 2033–2037, 2012.

    Article  CAS  Google Scholar 

  • Peng S.Q., Liu Y.L., Xie S.X.: [Response of water using efficiency and membrane permeability to drought stress in different varieties of Flos lonicerae.] — North. Hortic. 35: 156–158, 2011. [In Chinese]

    Google Scholar 

  • Peng W.X., Wang W.Q., Liang Y.H. et al.: [The effect of water stress on the microstructure of Glycyrrhica uralensis.] — J. Hebei Agric. Univ. 26: 46–48, 2003. [In Chinese]

    CAS  Google Scholar 

  • Pickersgill B.: Genetic resources and breeding of Capsicum spp. — Euphytica 96: 129–133, 1997.

    Article  Google Scholar 

  • Prince J.P., Lackney V.K., Angeles C. et al.: A survey of DNA polymorphism within the genus Capsicum and the fingerprinting of pepper cultivars. — Genome 38: 224–231, 1995.

    Article  CAS  PubMed  Google Scholar 

  • Thomashow M.F.: Molecular genetics of cold acclimation in higher plant. — Adv. Genet. 28: 99–131, 1990.

    Article  CAS  Google Scholar 

  • Thomashow M.F.: Plant cold acclimation: freezing tolerance genes and regulationary. — Annu. Rev. Plant Physiol. 50: 571–599, 1999.

    Article  CAS  Google Scholar 

  • Thomashow M.F., Gilmour S.J., Stoekinger E.J. et al.: Role of the Arabidopsis CBF transcriptional activators in cold acclimation. — Physiol. Plantarum 112:171–175, 2001.

    Article  CAS  Google Scholar 

  • Tsuneo K., Junko I.S., Hidehiro H. et al.: Influence of low air humidity and low root temperature on water uptake, growth and aquaporin expression in rice plants. — Plant Cell Physiol. 53: 1418–1431, 2012.

    Article  Google Scholar 

  • Wang Z.H., Guo X.P., Lv S.F. et al.: [Effects of soil drought on starch accumulation of grain and activity of corresponding starch synthesis enzymes in different winter wheat varieties.] — Agric. Res. Arid Areas 29: 67–74, 2011. [In Chinese]

    CAS  Google Scholar 

  • Xin Z.G., Browse J.: Cold comfort farm: the acclimation of plants to freezing temperatures. — Plant Cell Environ. 23: 893–902, 2000.

    Article  Google Scholar 

  • Xie J.M., Yu J.H., Xie M.H., Feng Z.: [Changes of three osmotic regulatory metabolites in leaves of pepper under low temperature and poor light stress and relations between its and varietal tolerance.] — Acta Bot. Boreal. 29: 105–110, 2009. [In Chinese]

    Google Scholar 

  • Xie J.M., Yu J.H., Huang G.B., Feng Z.: [Correlations between changes of absorption and transformation of light energy by PSII in pepper leaves and the variety tolerance under low temperature and weak light.] — Sci. Agric. Sin. 44: 1855–1862, 2011. [In Chinese]

    Google Scholar 

  • Xie J.M., Yu J.H., Huang G.B., Feng Z.: [Relationship between carotenoid content and low-light-tolerance or chilling- and low-light-tolerance of pepper varieties.] — Sci. Agric. Sin. 43: 4036–4044, 2010. [In Chinese]

    CAS  Google Scholar 

  • Xu R., Miao M.M., Cao B.S.: [Effect of low temperature and pollination on cucumber yield formation.] — Chin. Vege. 1: 53–56, 2010. [In Chinese]

    Google Scholar 

  • Yang S.: [Expression and functional analysis of the CBF3 in sweet pepper under chilling stress.] — Ph. D. Dissertation, Shandong Agric. Univ., 2011. [In Chinese]

  • Yang R., Guan X.L., Zhang R.L. et al.: [Changes of Ca2+ and Ca2+-ATPase in the mesophyll cells of Euonymus japonicus ‘Cuzhi’ under cold stress.] — Acta Hortic. Sin. 40: 1139–1152, 2013. [In Chinese]

    CAS  Google Scholar 

  • Yang S., Tang X.F., Ma N.N. et al.: Heterology expression of the sweet pepper CBF3 gene confers elevated tolerance to chilling stress in transgenic tobacco. — J. Plant Physiol. 168: 1804–1812, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Yu L.F., An F.Q., Li F.H., Tan D.H.: [Effect of low light and low temperature on anatomical structure of summer squash leaves.] — J. Changjiang Vege. 25: 44–46, 2011. [In Chinese]

    Google Scholar 

  • Zhang H.Y., Mao X.G., Wang C.S., Jing R.L.: Overexpression of a common wheat gene TaSnRK2.8 enhances tolerance to drought, salt and low temperature in Arabidopsis. — PLOS ONE 5: e16041, 2010.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zongren M.: [Study on free proline accumulation of seedling in many species of plant under water stress.] — Prata. Sci. 11: 15–18, 1994. [In Chinese]

    Google Scholar 

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Authors and Affiliations

  1. Vegetable Institution of Hunan Academy of Agricultural Science, Hunan Changsha, 410125, China

    L. J. Ou, G. Wei, Z. Q. Zhang, X. Z. Dai & X. X. Zou

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  1. L. J. Ou
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  2. G. Wei
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  4. X. Z. Dai
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  5. X. X. Zou
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Correspondence to X. X. Zou.

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Acknowledgements: This work was supported by China Agriculture Research System (CARS-25-A-8).The first two authors contributed equally to the paper.

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Ou, L.J., Wei, G., Zhang, Z.Q. et al. Effects of low temperature and low irradiance on the physiological characteristics and related gene expression of different pepper species. Photosynthetica 53, 85–94 (2015). https://doi.org/10.1007/s11099-015-0084-7

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