Skip to main navigation menu Skip to main content Skip to site footer
ASPHC Baner

Vol. 17 No. 6 (2018)

Articles

CHANGES IN CHLOROPHYLL a FLUORESCENCE AND PIGMENTS COMPOSITION IN OAK LEAVES WITH GALLS OF TWO CYNIPID SPECIES (Hymenoptera, Cynipidae)

DOI: https://doi.org/10.24326/asphc.2018.6.15
Submitted: December 20, 2018
Published: 2018-12-20

Abstract

Gall-inducing insects may cause multiple physiological changes in host plants, such as the loss of photosynthetic pigments and reduced photosynthetic capacity. However, the direction of these changes is usually insect species-dependent. Therefore, the objective of this research was to characterize the indirect effects of galls induced by asexual generation of Neuroterus numismalis (Fourc.) and N. quercusbaccarum L. on photosynthesis by comparing changes in photosynthetic and photoprotective pigments and chlorophyll a fluorescence in foliar tissue with and without galls in naturally growing pedunculate oak trees (Quercus robur L.). The presence of galls of both Cynipidae species caused a significant decrease of chlorophyll a, b and carotenoids contents. Moreover, photosynthetic parameters (F0, Fm, Fv/Fm, Y, qP, qN) were significantly decreased. These results provide valuable information for diagnosing the oak infections using a non-invasive method, such as chlorophyll a fluorescence and predicting the effect of infections on photosynthetic productivity.

References

  1. Aldea, M., Hamilton, J.G., Resti, J.P., Zangerl, A.R., Berenbaum, M.R., Frank, T.D., DeLucia, E.H. (2006). Comparison of photosynthetic damage from arthropod herbivory and pathogen infection in understory hardwood saplings. Oecologia, 149, 221−232 DOI: 10.1007/s00442-006-0444-x.
  2. Ashraf, M., Harris, P.J.C. (2013). Photosynthesis under stressful environments: An overview. Photosynthetica, 51(2), 163–190. DOI: 10.1007/s11099-013-0021-6.
  3. Barry, K.M., Newnham, G.J. (2012). Quantification of chlorophyll and carotenoid pigments in eucalyptus foliage with the radiative transfer model PROSPECT 5 is affected by anthocyanin and epicuticular waxes. Proceedings of the Geospatial Science Research Symposium, RMIT University, Melbourne, 1–7.
  4. Belyaeva, N.E., Bulychev, A.A., Riznichenko, G.Y., Rubin, A.B. (2016). Thylakoid membrane model of the Chl a fluorescence transient and P700 induction kinetics in plant leaves. Photosynth. Res., 130, 491–515. DOI: 10.1007/s11120-016-0289-z.
  5. Bird, J.P., Melika, G., Nicholls, J.A., Stone, G.N., Buss, E.A. (2013). Life history, natural enemies, and management of Disholcaspis quercusvirens (Hymenoptera: Cynipidae) on live oak trees. J. Econ. Entomol., 106(4), 1747–1756, https://doi.org/10.1603/EC12206.
  6. Bogard, L. (1976). Chlorophyll biosynthesis In: Chemistry and biochemistry of plant pigments, Goodwin T.W. (ed.). Vol. II. Academic Press, New York, 64–148.
  7. Carneiro, R.G.S., Isaias, R.M.S. (2011). Gradients of metabolite accumulation and redifferentiation of nutritive cells associated with vascular tissues in galls induced by sucking insects. AoB Plants, 7, plv086. DOI: 10.1093/aobpla/plv086.
  8. Carneiro, R.G.S., Castro, A.C., Isaias, R.M.S. (2014). Unique histochemical gradients in a photosynthesis-deficient plant gall. S. Afr. J. Bot., 92, 97–104.
  9. Castro, A.C., Oliveira, D.C., Moreira, A.S.F.P., Lemos-Filho, J.P., Isaias, R.M.S. (2012). Source-sink relationship and photosynthesis in the horn-shaped gall and its host plant Copaifera langsdorffii Desf. (Fabaceae). S. Afr. J. Bot., 83, 121–126.
  10. Dinç, E., Ceppi, M.G., Tóth, S.Z., Bottka, S., Schansker, G. (2012). The chl fluorescence intensity is remarkably insensitive to changes in the chlorophyll content of the leaf as long as the chl a/b ratio remains unaffected. Biochim. Biophys. Acta, 1817, 770–779. DOI: 10.1016/j.bbabio.2012.02.003.
  11. Gailite, A., Andersone, U., Ievinsh, G. (2005). Arthropod-induced neoplastic formations on trees change photosynthetic pigment levels and oxidative enzyme activities. J. Plant Interact., 1(1), 61–67.
  12. Giersch, C., Krause, H. (1991). A simple model relating photoinhibitory fluorescence quenching in chloroplasts to a population of altered Photosystem II reaction centres. Photosynth. Res., 30, 115–121.
  13. Gitelson, A.A., Gamonb, J.A., Solovchenko, A. (2017). Multiple drivers of seasonal change in PRI: Implications for photosynthesis 1. Leaf level. Remote Sens. Environ., 191, 110–116. DOI:10.1016/j.rse.2016.12.014.
  14. Golan, K., Rubinowska, K., Kmieć, K., Kot, I., Górska-Drabik, E., Łagowska, B., Michałek, W. (2015). Impact of scale insect infestation on the content of photosynthetic pigments and chlorophyll fluorescence in two host plant species. Arthropod-Plant Interact., 9, 55–65. DOI: 10.1007/s11829-014-9339-7.
  15. Guidi, L., Degl’Innocenti, E. (2012). Chlorophyll a fluorescence in abiotic stress. In: Crop stress and its management: perspectives and strategies, Venkateswarlu, B., Shanker, A., Shanker, C., Maheswari, M. (ed.). Springer, Dordrecht.
  16. Gururani, M.A., Venkatesh, J., Tran, L.S.P. (2015). Regulation of photosynthesis during abiotic stress-induced photoinhibition. Mol. Plant, 8(9), 1304–1320.
  17. Gutsche, A.R., Heng-Moss, T.M., Higley, L.G., Sarath, G., Mornhinweg, D.W. (2009). Physiological responses of resistant and susceptible barley, Hoirdeum vulgare to the Russian wheat aphid, Diuraphis noxia (Mordvilko). Arthropod-Plant Interact., 3, 233–240. DOI: 10.1007/s11829-009-9067-6.
  18. Haiden, S.A., Hoffmann, J.H., Cramer, M.D. (2012). Benefits of photosynthesis for insects in galls. Oecologia, 170, 987–997.
  19. Hannoufa, A., Hossain, Z. (2012). Regulation of carotenoid accumulation in plants. Biocatal. Agric. Biotechnol., 1, 198–202.
  20. Harper, L.J., Schönrogge, K., Lim, K.Y., Francis, P., Lichtenstein, C.P. (2004). Cynipid galls: insect-induced modifications of plant development create novel plant organs. Plant Cell Environ., 27, 327–335.
  21. Hartley, S.E. (1998). The chemical composition of plant galls: are levels of nutrients and secondary compounds controlled by the gall-former? Oecologia, 113, 492–501.
  22. Havaux, M. (2013). Carotenoid oxidation products as stress signals in plants. Plant J., 79, 597–606. DOI: 10.1111/tpj.12386.
  23. Hsu, M.H., Chen, C.C., Lin, K.H., Huang, M.Y., Yang, C.M., Huang, W.D. (2015). Photosynthetic responses of Jatropha curcas to spider mite injury. Photosynthetica, 53 (3), 349–355. DOI: 10.1007/s11099-015-0132-3.
  24. Huang, M.Y., Chou, H.M., Chang, Y.T., Yang, C.M. (2014a). The number of cecidomyiid insect galls affects the photosynthesis of Machilus thunbergii host leaves. J. Asia Pac. Entomol., 17, 151–154.
  25. Huang, M.Y., Huang, W.D., Chou, H.M., Lin, K.H., Chen, C.C., Chen, P.J., Chang, Y.T., Yang, C.M. (2014b). Leaf-derived cecidomyiid galls are sinks in Machilus thunbergii (Lauraceae) leaves. Physiol. Plant., 152(3), 475−485. DOI:10.1111/ppl.12186.
  26. Huang, M.Y., Huang, W.D., Chou, H.M., Chen, C.C., Chen, P.J., Chang, Y.T., Yang, C.M. (2015). Structural, biochemical, and physiological characterization of photosynthesis in leaf-derived cupshaped galls on Litsea acuminate. BMC Plant Biol., 15, 61. DOI: 10.1186/s12870-015-0446-0.
  27. Isaias, R.M.S., Oliveira, D.C., Moreira, A.S.F.P., Soraes, G.L.G., Carneiro, R.G.S. (2015). The imbalance of redox homeostasis in arthropod-induced plant galls: Mechanisms of stress generation and dissipation. Biochim. Biophys. Acta Gen. Subj., 1850(8), 1509–1517. DOI: 10.1016/j.bbagen.2015.03.007.
  28. Jason, J.G., Thomas, G.R., Pharr, D.M. (2004). Photosynthesis, chlorophyll fluorescence, and carbohydrate content of Illicium taxa grown under varied irradiance. J. Am. Soc. Hortic. Sci., 129, 46–53.
  29. Juneau, P., Green, B.R., Harrison, P.J. (2005). Simulation of Pulse-Amplitude-Modulated (PAM) fluorescence: Limitations of some PAM-parameters in studying environmental stress effects. Photosynthetica, 43(1), 75–83.
  30. Kalaji, H.M., Carpentier, R., Allakherdiev, S.I., Bosa, K. (2012). Fluorescence parameters as early indicators of light stress in barley. J. Photochem. Phytobiol. B Biol., 112, 1–6.
  31. Kampichler, C., Teschner, M. (2002). The spatial distribution of leaf galls of Mikiola fagi (Diptera: Cecidomyiidae) and Neuroterus quercusbaccarum (Hymenoptera: Cynipidae) in the canopy of a Central European mixed forest. Eur. J. Entomol., 99, 79–84.
  32. Karageorgou, P., Manetas, Y. (2006). The importance of being red when young: anthocyanins and the protection of young leaves of Quercus coccifera from insect herbivory and excess light. Tree Physiol., 26, 613–621.
  33. Katilmiş, Y., Azmaz, M. (2015). Investigation on the inquilines (Hymenoptera: Cynipidae, Synergini) of oak galls from inner western Anatolia, Turkey. Turk. J. Zool., 39, 168–173. DOI:10.3906/zoo-1403-68.
  34. Kmieć, K., Rubinowska, K., Michałek, W., Sytykiewicz, H. (2018). The effect of galling aphids feeding on photosynthesis photochemistry of elm trees (Ulmus sp.). Photosynthetica, 56(4), 989–997. DOI:10.1007/ s11099-018-0813-9.
  35. Kmieć, K., Kot, I., Golan, K., Górska-Drabik, E., Łagowska, B., Rubinowska, K., Michałek, W. (2016). Physiological response of orchids to mealybugs (Hemiptera: Pseudococcidae) infestation. J. Econ. Entomol., 109(6), 2489–2494, https://doi.org/10.1093/jee/tow236.
  36. Kovácsné-Koncz, N., Szabó, L.J., Máthe, C., Jámbrik, K., Hamvas, M. (2011). Histological study of quercus galls of Neuroterus quercusbaccarum (L.) (Hymenoptera: Cynipidae). Acta Biol. Szeged., 55(2), 247–253.
  37. Kot, I., Jakubczyk, A., Karaś, M., Złotek, U. (2018). Biochemical responses induced in galls of three Cynipidae species in oak trees. Bull. Entomol. Res., 108, 494–500. DOI: 10.1017/S0007485317001055.
  38. Kovinich, N., Kayanja, G., Chanoca, A., Otegui, M.S., Grotewold, E. (2015). Abiotic stresses induce different localizations of anthocyanins in Arabidopsis. Plant Signal. Behav., 10(7), e1027850. DOI: 10.1080/15592324.2015.1027850.
  39. Leszczyński, B. (2001). Rola allelozwiązków w oddziaływaniach owady – rośliny. In: Biochemiczne oddziaływania środowiskowe, Oleszek, W., Głowniak, K., Leszczyński, B. (eds.). Wyd. AM, Lublin, 61–85.
  40. Lichtenthaler, H.K., Wellburn, A.R. (1983). Determination of total carotenoids and chlorophyll a and b of leaf extract in different solvents. Biochem. Soc. Trans., 11, 591–592.
  41. Malkin, R., Niyogi, K. (2000). Photosynthesis. In: Biochemistry and molecular biology of plants, Buchanan B., Gruissem W., Jones R. (eds). American Society of Plant Physiologists, Rockville.
  42. Melika, G., Abrahamson, W.G. (2002). Review of the world genera of oak cynipid wasps (Hymenoptera: Cynipidae). In: Parasitic wasps: evolution, systematics, biodiversity and biological control, Melika, G., Thuroczy, Cs. (ed.). Agroinform, Budapest, 150–190.
  43. Melo, H.F., Souza, E.R., Cunha, J.C. (2017). Fluorescence of chlorophyll a and photosynthetic pigments in Atriplex nummularia under abiotic stresses. Rev. Bras. Eng. Agric. Ambient., 21(4), 232–237. DOI: 10.1590/1807-1929/agriambi.v21n4p232-237.
  44. Merzlyak, M.N., Solovchenko, A.E., Gitelson, A.A. (2003). Reflectance spectral features and non-destructive estimation of chlorophyll, carotenoid and anthocyanin content in apple fruit. Postharvest Biol. Technol., 27, 197–211.
  45. Mete, Ö., Demirsoy, A. (2012). A preliminary study on the gallwasp fauna of Kemaliye (Erzincan, Turkey) and a new record for Turkey. J. Biol. Chem., Special Issue, 351–363.
  46. Mibei, E.K., Ambuko, J., Giovannoni, J.J., Onyango, A.N., Owino, W.O. (2017). Carotenoid profiling of the leaves of selected African eggplant accessions subjected to drought stress Food Sci. Nutr., 5(1), 113–122. DOI: 10.1002/fsn3.370.
  47. Misyura, M., Colasanti, J., Rothstein, S.J. (2013). Physiological and genetic analysis of Arabidopsis thaliana anthocyanin biosynthesis mutants under chronic adverse environmental conditions. J. Exp. Bot., 64(1), 229–240. DOI: 10.1093/jxb/ers328.
  48. Młodzińska, E. (2009). Survey of plant pigments: molecular and environmental determination of plant colors. Acta Biol. Cracov. Bot., 51(1), 7–16.
  49. Mukherjee, S., Lokesh, G., Aruna, A.S., Sharma, S.P., Sahay, A. (2016). Studies on the foliar biochemical changes in the gall (Trioza fletcheri minor) infested tasar food plants Terminalia arjuna and Terminalia tomentosa. J. Entomol. Zool. Stud., 4(1), 154–158.
  50. Oliveira, D.C., Isaias, R.M.S., Moreira, A.S.F.P., Magalhães, T.A., Lemos-Filho, J.P. (2011). Is the oxidative stress caused by Aspidosperma spp. Galls capable of altering leaf photosynthesis? Plant Sci., 180, 489–495.
  51. Oliveira, D.C., Isaias, R.M.S., Fernandes, G.W., Ferreira, B.G., Carneiro, R.G.S., Fuzaro, L. (2016). Manipulation of host plant cells and tissues by gall-inducing insects and adaptive strategies used by different feeding guilds. J. Ins. Physiol., 84, 103–113.
  52. Oliveira, D.C., Moreira, A.S.F.P., Isaias, R.M.S., Martini, V., Rezende, U.C. (2017). Sink status and photosynthetic rate of the leaflet galls induced by Bystracoccus mataybae (Eriococcidae) on Matayba guianensis (Sapindaceae). Front. Plant Sci., 8, 1249.
  53. Patankar, R., Starr, G., Mortazavi, B., Oberbauer, S.F., Rosenblum, A. (2013). The effects of mite galling on the ecophysiology of two arctic willows. Arct. Antarct. Alp. Res., 45(1), 99–106. DOI.org/10.1657/ 1938-4246-45.1.99.
  54. Rabino, I., Mancinelli, A. (1986). Light, temperature and anthocyanin production. Plant Physiol., 81, 922–924. http://dx.doi.org/10.1104/pp.81.3.922.
  55. Ramakrishna, A., Ravishankar, G.A. (2011). Influence of abiotic stress signals on secondary metabolites in plants. Plant Signal Behav., 6(11), 1720–1731. DOI: 10.4161/psb.6.11.17613.
  56. Roháček, K., Soukupová, J., Barták, M. (2008). Chlorophyll fluorescence: A wonderful tool to study plant physiology and plant stress. Plant Cell Compartments – Selected Topics, 41–104.
  57. Samsone, I., Andersone, U., Ievinsh, G. (2011). Gall midge Rhabdophaga rosaria – induced rosette galls on Salix: morphology, photochemistry of photosynthesis and defense enzyme activity. Environ. Exp. Biol., 9, 29–36.
  58. Schreiber, U. (2004). Pulse amplitude modulation (PAM) fluorometry and saturation pulse method: an overview. In: Chlorophyll a fluorescence: a signature of photosynthesis, Papageorgiou, G.C. (ed). Kluwer Academic, Dordrecht, 279–319.
  59. Shangguan, Z., Shao, M., Dyckmans, J. (2000). Effects of nitrogen nutrition and water deficit on net photosynthetic rate and chlorophyll fluorescence in winter wheat. J. Plant Physiol., 156(1), 46–51.
  60. Solovchenko, A. (2010). Photoprotection in Plants: Optical Screening-Based Mechanisms. Springer, Heidelberg−Dordrecht−London−New York.
  61. Stone, G.N., Schönrogge, K., Atkinson, R.J., Bellido, D., Pujade-Villar, J. (2002). The population biology of oak gall wasps (Hymenoptera: Cynipidae). Annu. Rev. Entomol., 47, 633–668.
  62. Terletskaya, N., Zobova, N., Stupko, V., Shuyskaya, E. (2017). Growth and photosynthetic reactions of different species of wheat seedlings under drought and salt stress. Period. Biol., 119(1), 37–45. DOI: 10.18054/pb.v119i1.4408.
  63. Vassilev, A., Manolov, P. (1999). Chlorophyll fluorescence of barley (H. vulgare L.) seedlings grown in excess of Cd. Bulg. J. Plant Physiol., 25(3–4), 67–76.
  64. War, A.R., Paulraj, M.G., Ahmad, T., Buhroo, A.A., Hussain, B., Ignacimuthu, S., Sharma, H.C. (2012) Mechanisms of plant defense against insect herbivores. Plant Signal. Behav., 7(10), 1306–1320.
  65. Yang, C.M., Yang, M.M., Hsu, J.M., Jane, W.N. (2003). Herbivorous insect causes deficiency of pigment-protein complexes in an oval-pointed cecidomyiid gall of Machilus thunbergi leaf. Bot. Bull. Acad. Sin., 44, 315–321.
  66. Yüzbaşioǧlu, E., Dalyan, E., Akpinar, I. (2017). Changes in photosynthetic pigments, anthocyanin content and antioxidant enzyme activities of maize (Zea mays L.) seedlings under high temperature stress conditions. J. Nat. Sci., 18(2), 97−104. DOI: 10.23902/trkjnat. 289527.

Downloads

Download data is not yet available.

Most read articles by the same author(s)

1 2 > >> 

Similar Articles

<< < 5 6 7 8 9 10 11 12 13 14 > >> 

You may also start an advanced similarity search for this article.