Article | . 2018 Vol. 36, Issue. 5
Detection of Temperature Stress Using Chlorophyll Fluorescence Parameters and Stress-related Chlorophyll and Proline Content in Paprika (Capsicum annuum L.) Seedlings



Department of Horticulture, College of Agriculture & Life Sciences, Chonbuk National University1
Department of Bioindustrial Machinery Engineering, College of Agriculture & Life Sciences, Chonbuk National University2
Institute for Agricultural Machinery & ICT Convergence, Chonbuk National University3
Institute of Agricultural Science & Technology, Chonbuk National University4




2018.. 619:629


PDF XML




Thirty three-day-old paprika (Capsicum annuum L.) seedlings were grown under different temperature conditions (low: 10°C, moderate: 25°C, and high: 35°C) in a closed plant production system for 32 days and their chlorophyll (Chl) fluorescence and growth parameters, and Chl and proline contents were measured at 0, 1, 2, 4, 8, 16, 24, and 32 days after the initiation of treatment. Minimal fluorescence (F0) sharply increased from 8 days and continued until the end of the experimental period under all three temperature treatments, with the highest increase at the low temperature condition. Maximum quantum yield (Fv/Fm) and the efficiency of excitation capture of open photosystem II (PSII) center (F’v/F’m) significantly decreased at low temperature compared with those at moderate and high temperatures. Non-photochemical quenching (NPQ) and the ratio of the fluorescence decrease (Rfd) were significantly affected, particularly at the high temperature, followed by the low and moderate temperatures; quantum yield of non-regulated energy dissipation in PSII (ϕNO) increased under all treatments. Furthermore, Chl content showed a relatively greater decrease at the low temperature compared to the high temperature throughout the experiment; moderate temperature showed a stable chlorophyll content throughout the experiment. Proline concentration increased significantly at the high and low temperatures, but not under moderate temperature. Plant height and shoot and root weight were the lowest at the low temperature. Overall, our results suggest that paprika plants were more severely affected by low temperature than high temperature with respect to photosynthetic activity as well as growth, which was significantly slowed at low temperature.



1. Allakhverdiev SI, Kreslavski VD, Klimov VV, Los DA, Carpentier R, Mohanty P (2008) Heat stress: an overview of molecular responses in photosynthesis. Photosynth Res 98:541-550. doi:10.1007/s11120-008-9331-0  

2. Anjum SA, Xie X-Y, Wang L-C, Saleem MF, Man C, Lei W (2011) Morphological, physiological and biochemical responses of plants to drought stress. Afr J Agric Res 6:2026-2032. doi:10.5897/AJAR10.027  

3. Asada K, Endo T, Mano J, Miyake C (1998) Molecular mechanism for relaxation of and protection from light stress. In K Satoh, N Murata, ed, Stress Responses of Photosynthetic Organisms. Elsevier, Amsterdam, The Netherlands, pp 37-52. doi:10.1016/B978-0-444- 82884-2.50006-6  

4. Baker NR, Rosenqvist E (2004) Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot 55:1607-1621. doi:10.1093/jxb/erh196  

5. Berry J, Bjorkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Ann Rev Plant Physiol 31:491-543. doi:10.1146/annurev.pp.31.060180.002423  

6. Bhandari SR, Lee MJ, Rhee HC, Choi GL, Oh SS, Lee JT, Lee JG (2018) Rapid monitoring of proline accumulation in paprika leaf sap relative to leaf position and water stress. Hortic Environ Biotechnol 59:483-489. doi:10.1007/s13580-018-0063-6  

7. Bielczynski LW, Lacki MK, Hoefnagels I, Gambin A, Croce R (2017) Leaf and plant age affects photosynthetic performance and photoprotective capacity. Plant Physiol 175:1634-1648. doi:10.1104/pp.17.00904  

8. Boyer JS (1982) Plant productivity and environment. Science 218:443-448. doi:10.1126/science.218.4571.443  

9. Briantais JM, Dacosta J, Goulas Y, Ducruet JM, Moya I (1996) Heat stress induces in leaves an increase of the minimum level of chlorophyll fluorescence, F: a time-resolved analysis. Photosynth Res 48:189-196. doi:10.1007/BF00041008  

10. Camejo D, Rodrıguez P, Morales MA, Dell Amico JM, Torrecillas A, Alarcon JJ (2005) High temperature effects on photosynthetic activity of two tomato cultivars with different heat susceptibility. J Plant Physiol 162:281-289. doi:10.1016/j.jplph.2004.07.014  

11. Chen WR, Zheng JS, Li YQ, Guo WD (2012) Effects of high temperature on photosynthesis, chlorophyll fluorescence, chloroplast ultrastructure and antioxidant activities in fingered citron. Russ J Plant Phys 59:732-740. doi:10.1134/S1021443712060040  

12. Feller U, Vaseva II (2014) Extreme climatic events: impacts of drought and high temperature on physiological processes in agronomically important plants. Front Environ Sci 2:1-16. doi:10.3389/fenvs.2014.00039  

13. Feng B, Liu P, Li G, Dong ST, Wang FH, Kong LA, Zhang JW (2014) Effect of heat stress on the photosynthetic characteristics in flag leaves at the grain-filling stage of different heat-resistant winter wheat varieties. J Agron Crop Sci 200:143-155. doi:10.1111/jac.12045  

14. Georgieva K, Yordanov I (1993) Temperature dependence of chlorophyll fluorescence parameters of pea seedlings. J Plant Physiol 142:151-155. doi:10.1016/S0176-1617(11)80955-7  

15. Gorbe E, Calatayud A (2012) Applications of chlorophyll fluorescence imaging technique in horticultural research: a review. Sci Hortic 138:24-35. doi:10.1016/j.scienta.2012.02.002  

16. 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/oxygenase. Plant Cell Environ 27:1169-1183. doi:10.1111/j.1365-3040.2004.01222.x  

17. Haq NU, Raza S, Luthe DS, Heckathorn SA, Shakeel SN (2013) A dual role for the chloroplast small heat shock protein of Chenopodium album including protection from both heat and metal stress. Plant Mol Biol Rep 31:398-408. doi:10.1007/s11105-012-0516-5  

18. Hogewoning SW, Harbinson J (2007) Insights on the development, kinetics, and variation of photoinhibition using chlorophyll fluorescence imaging of a chilled, variegated leaf. J Exp Bot 58:453-463. doi:10.1093/jxb/erl219  

19. Huang L, Jiang G-B, Zhu Y, Dang C-H, Wang H-X, Zhang Y-X, Wang L-S, Li G-Z, Zou J-X, et al (2018) Effects of high temperature on leaf gas exchange and chlorophyll fluorescence parameters of the north high bush blueberry. Chin J Ecol 35:871-879. doi:10.13292/ j.l000-4890.201604.022  

20. Janka E, Korner O, Rosenqvist E, Ottosen C-O (2013) High temperature stress monitoring and detection using chlorophyll a fluorescence and infrared thermography in chrysanthemum (Dendranthema grandiflora). Plant Physiol Biochem 67:87-94. doi:10.1016/j.plaphy. 2013.02.025  

21. Kalisz A, Jezdinsky A, Pokluda R, Sekara A, Grabowska A, Gil J (2016) Impacts of chilling on photosynthesis and chlorophyll pigment content in Juvenile basil cultivars. Hortic Environ Biotechnol 57:330-339. doi:10.1007/s13580-016-0095-8  

22. Kim J-S, Ahn J, Lee S-J, Moon BK, Ha T-Y, Kim S (2011) Phytochemicals and antioxidant activity of fruits and leaves of paprika (Capsicum annuum L., var. Special) cultivated in Korea. J Food Sci 76:193-198. doi:10.1111/j.1750-3841.2010.01891.x  

23. Kim S, Park JJ, Moon BK (2015) Phytochemicals and quality characteristics of candied paprika (Capsicum annuum L.) during storage. Int J Food Sci Technol 50:1847-1854. doi:10.1111/ijfs.12849  

24. Krause G, Santarius K (1975) Relative thermostability of the chloroplast envelope. Planta 127:285-299. doi:10.1007/BF00380726  

25. Lichtenthaler HK, Buschmann C, Knapp M (2005) How to correctly determine the different chlorophyll fluorescence parameters and the chlorophyll fluorescence decrease ration Rfd of leaves with the PAM fluorometer. Photosynthetica 43:379-393. doi:10.1007/ s11099-005-0062-6  

26. Mathur S, Jajoo A, Mehta P, Bharti S (2011) Analysis of elevated temperature-induced inhibition of photosystem II using chlorophyll a fluorescence induction kinetics in wheat leaves (Triticum aestivum). Plant Biol 13:1-6. doi:10.1111/j.1438-8677.2009.00319.x  

27. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence - a practical guide. J Exp Bot 51:659-668. doi:10.1093/jexbot/51.345.659  

28. Nankishore A, Farrell AD (2016) The response of contrasting tomato genotypes to combined heat and drought stress. J Plant Physiol 202:75-82. doi:10.1016/j.jplph.2016.07.006  

29. Ogweno JO, Song X-S, Hu W-H, Shi K, Zhou Y-H, Yu J-Q (2009) Detached leaves of tomato differ in their photosynthetic physiological response to moderate high and low temperature stress. Sci Hortic 123:17-22. doi:10.1016/j.scienta.2009.07.011  

30. Olvera-Gonzalez E, Alaniz-Lumbreras D, Ivanov-Tsonchev R, Villa-Hernandez V, de la Rosa-Vargas I, Lopez-Cruz I, Silos-Espino H, Lara-Herrera A (2013) Chlorophyll fluorescence emission of tomato plants as a response to pulsed light based LEDs. Plant Growth Regul 69:117-123. doi:10.1007/s10725-012-9753-8  

31. Ortiz R, Sayre KD, Govaerts B, Gupta R, Subbarao GV, Ban T, et al (2008) Climate change: can wheat beat the heat? Agric Ecosyst Environ 126:46-58. doi:10.1016/j.agee.2008.01.019  

32. Oxborough K (2004) Imaging of chlorophyll a fluorescence: theoretical and practical aspects of an emerging technique for the monitoring of photosynthetic performance. J Exp Bot 55:1195-1205. doi:10.1093/jxb/erh145  

33. Partelli FL, Vieira HD, Viana AP, Batista-Santos P, Rodrigues AP, Leitao AE, Ramalho JC (2009) Low temperature impact on photosynthetic parameters of coffee genotypes. Pesq Agropec Bras 44:1404-1415. doi:10.1590/S0100-204X2009001100006  

34. Phyo AK, Chung N-J (2017) Influence of high temperature on chlorophyll fluorescence and its varietal variation in rice. Phillipine J Crop Sci 42:59-68  

35. Schreiber U, Klughammer C (2008) Non-photochemical fluorescence quenching and quantum yields in PS I and PS II: analysis of heat-induced limitations using Maxi-Imaging-PAM and dual-PAM-100. PAM Appl Notes 1:15-18  

36. Sharma DK, Fernandez JO, Rosenqvist E, Ottosen C-O (2014) Genotypic response of detached leaves versus intact plants for chlorophyll fluorescence parameters under high temperature stress in wheat. J Plant Physiol 171:576:586. doi:10.1016/j.jplph.2013.09.025  

37. Szabados L, Savoure A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89-97. doi:10.1016/j.tplants.2009.11.009  

38. Toomey HM (2013) Chlorophyll fluorescence and thermal stress in Archaias angulatus (Class Foraminifera). MS Thesis, College of Marine Science, University of South Florida, USA. pp 1-130  

39. Trovato M, Mattioli R, Costantino P (2008) Multiple roles of proline in plant stress tolerance and development. Rend Lincei Sci Fis Nat 19:325-346. doi:10.1007/s12210-008-0022-8  

40. Verslues PE, Sharma S (2010) Proline metabolism and its implications for plant-environment interaction. The Arabidopsis Book. 8:e0140. doi:10.1199/tab.0140  

41. Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: an overview. Environ Exp Bot 61:199-223. doi:10.1016/ j.envexpbot.2007.05.011  

42. Wang J, Cui L, Wang Y, Li J (2009) Growth, lipid peroxidation and photosynthesis in two tall fescue cultivars differing in heat tolerance. Biol Plant 53:237-242. doi:10.1007/s10535-009-0045-8  

43. Warren CR (2008) Rapid measurement of chlorophylls with a mircoplate reader. J Plant Nutr 31:1321-1332. doi:10.1080/01904160802135092  

44. Weng J-H, Lai M-F (2005) Estimating heat tolerance among plant species by two chlorophyll fluorescence parameters. Photosynthetica 43:439-444. doi:10.1007/s11099-005-0070-6  

45. Yamada M, Hidaka T, Fukamachi H (1996) Heat tolerance in leaves of tropical fruit crops as measured by chlorophyll fluorescence. Sci Hortic 67:39-48. doi:10.1016/S0304-4238(96)00931-4  

46. Yang X, Song J, Fillmore S, Pang X, Zhang Z (2011) Effect of high temperature on color, chlorophyll fluorescence and volatile biosynthesis in green-ripe banana fruit. Postharvest Biol Technol 62:246-257. doi:10.1016/j.postharvbio.2011.06.011  

47. Zhou R, Wu Z, Wang X, Rosenqvist E, Wang Y, Zhao T, Ottosen C-O (2018) Evaluation of temperature stress tolerance in cultivated and wild tomatoes using photosynthesis and chlorophyll fluorescence. Hortic Environ Biotechnol 59:499-509. doi:10.1007/s13580-018-0050-y  

48. Zribi L, Fatma G, Fatma R, Salwa R, Hassan N, Nejib RM (2009) Application of chlorophyll fluorescence for the diagnosis of salt stress in tomato “Solanum lycopersicum (variety Rio Grande)”. Sci Hortic 120:367-372. doi:10.1016/j.scienta.2008.11.025