Photosynthetica 2018, 56(4):989-997 | DOI: 10.1007/s11099-018-0813-9

The effect of galling aphids feeding on photosynthesis photochemistry of elm trees (Ulmus sp.)

K. Kmieĉ1,*, K. Rubinowska2, W. Micha³ek2, H. Sytykiewicz3
1 Department of Entomology, University of Life Sciences in Lublin, Lublin, Poland
2 Department of Plant Physiology, University of Life Sciences in Lublin, Lublin, Poland
3 Department of Biochemistry and Molecular Biology, Siedlce University of Natural Sciences and Humanities, Siedlce, Poland

Changes of chlorophyll (Chl) a fluorescence and photosynthetic pigment contents were analysed in galled leaves (visibly damaged and undamaged parts) and intact leaves. The values of minimal fluorescence of the dark-adapted state, maximal quantum yield of PSII photochemistry, effective quantum yield of PSII photochemical conversion, and photochemical quenching coefficient decreased in Ulmus pumila L. leaves galled by Tetraneura ulmi (L.) and in U. glabra Huds. galled by Eriosoma ulmi (L.). Colopha compressa (Koch.) feeding affected these parameters only in damaged parts of U. laevis Pall. galled leaves. The increasing number of T. ulmi galls progressively decreased photosynthetic performance. In gall tissues of all analysed aphid species, the lowest photosynthetic pigment content was found, indicating that the photosynthetic capacity must have been low in galls. Significant reduction of Chl and carotenoid contents were observed in damaged and undamaged portions of galled leaves only in the case of T. ulmi feeding.

Additional key words: biotic stress; Eriosomatinae; fluorescence parameters; host plant response

Received: June 30, 2017; Accepted: November 29, 2017; Prepublished online: December 1, 2018; Published: November 1, 2018  Show citation

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Kmieĉ, K., Rubinowska, K., Micha³ek, W., & Sytykiewicz, H. (2018). The effect of galling aphids feeding on photosynthesis photochemistry of elm trees (Ulmus sp.). Photosynthetica56(4), 989-997. doi: 10.1007/s11099-018-0813-9
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References

  1. Aldea M., Hamilton J.G., Resti J.P. et al.: Comparison of photosynthetic damage from arthropod herbivory and pathogen infection in understory hardwood saplings.-Oecologia 149: 221-232, 2006. Go to original source...
  2. Allakhverdiev S.I., Klimov V.V., Carpentier R.: Evidence for the involvement of cyclic electron transport in the protection of photosystem II against photoinhibition: Influence of a new phenolic compound.-Biochemistry 36: 4149-4154, 1997. Go to original source...
  3. Allakhverdiev S.I., Tsuchiya T., Watabe K. et al.: Redox potentials of primary electron acceptor quinone molecule (QA) -and conserved energetics of photosystem II in cyanobacteria with chlorophyll a and chlorophyll d.-P. Natl. Acad. Sci. USA 108: 8054-8058, 2011. Go to original source...
  4. Allakhverdiev S.I.: Recent progress in the studies of structure and function of photosystem II.-J. Photoch. Photobio. B 104: 1-8, 2011. Go to original source...
  5. Álvarez R., González-Sierra S., Candelas A. et al.: Histological study of galls induced by aphids on leaves of Ulmus minor: Tetraneura ulmi induces globose galls and Eriosoma ulmi induces pseudogalls.-Arthropod-Plant Inte. 7: 643-650, 2013. Go to original source...
  6. Ashraf M., Harris P.J.C.: Photosynthesis under stressful environments: An overview.-Photosynthetica 51: 163-190, 2013. Go to original source...
  7. Baczek-Kwinta R., Koziel A., Seidler-Lozykowska K.: Are the fluorescence parameters of German chamomile leaves the first indicators of the anthodia yield in drought conditions?-Photosynthetica 49: 87-97, 2011. Go to original source...
  8. Blackman R.L., Eastop V.F.: Aphids of the World's Plants: An Online Identification and Information Guide. Available online: https://doi.org/www.aphidsonworldsplants.info (Accessed 19 May 2017).
  9. Botha A.M., Lacock L., van Niekerk C. et al.: Is photosynthetic transcriptional regulation in Triticum aestivum L. cv. 'TungelaDN' a contributing factor for tolerance to Diuraphis noxia (Homoptera: Aphididae)?-Plant Cell Rep. 25: 41-54, 2006. Go to original source...
  10. Castro A.C., Oliveira D.C., Moreira A.S.F.P. et al.: Source-sink relationship and photosynthesis in the horn-shaped gall and its host plant Copaifera langsdorffii Desf. (Fabaceae).-South Afr. J. Bot. 83: 121-126, 2012. Go to original source...
  11. de Oliveira D.C., Isaias R.M., Moreira A.S. et al.: Is the oxidative stress caused by Aspidosperma spp. galls capable of altering leaf photosynthesis?-Plant Sci. 180: 489-495, 2011. Go to original source...
  12. El-Akkad S.S.: Biochemical changes induced in Populus nigra leaves by galling aphid Pemphigous populi.-Int. J. Agric. Biol. 6: 650-664, 2004.
  13. Elzinga D.A., De Vos M., Jander G.: Suppression of plant defenses by a Myzus persicae (Green Peach Aphid) salivary effector protein.-Mol. Plant Microbe. In. 27: 747-756, 2014. Go to original source...
  14. Fernandes G.W., Coelho M.S., Lüttge U.: Photosynthetic efficiency of Clusia arrudae leaf tissue with and without Cecidomyiidae galls.-Braz. J. Biol. 70: 723-728, 2010. Go to original source...
  15. Franzen L.D., Gutsche A.R., Heng-Moss T.M. et al.: Physiological responses of wheat and barley to Russian wheat aphid, Diuraphis noxia (Mordvilko) and bird cherry-oat aphid, Rhopalosiphym padi (L.) (Hemiptera: Aphididae).-Arthopod-Plant Inte. 2: 227-235, 2008. Go to original source...
  16. Gailite A., Andersone U., Ievinsh G.: Arthropod-induced neoplastic formations on trees change photosynthetic pigment levels and oxidative enzyme activities.-J. Plant Interact. 1: 61-67, 2005. Go to original source...
  17. Golan K., Rubinowska K., Kmiec K. et al.: Impact of scale insect infestation on the content of photosynthetic pigments and chlorophyll fluorescence in two host plant species.-Arthropod-Plant Inter. 9: 55-65, 2015. Go to original source...
  18. Guo Y.Y., Yu H.Y., Kong D.S. et al.: Effects of drought stress on growth and chlorophyll fluorescence of Lycium ruthenicum Murr. seedlings.-Photosynthetica 54: 524-531, 2016. Go to original source...
  19. Guo Y.Y., Tian S.S., Liu S.S. et al.: Energy dissipation and antioxidant enzyme system protect photosystem II of sweet sorghum under drought stress.-Photosynthetica 56: 861-872, 2018. Go to original source...
  20. Harris M.O., Freeman T.P., Moore J. A. et al.: H-Gene-Mediated resistance to Hessian fly exhibits features of penetration resistance to fungi.-Phytopathology 100: 279-289, 2010. Go to original source...
  21. Heng-Moss T.M., Ni X., Macedo T. et al.: Comparison of chlorophyll and carotenoid concentrations among Russian wheat aphid (Homoptera: Aphididae) -infested wheat isolines.-J. Econ. Entomol. 96: 475-481, 2003. Go to original source...
  22. Huang M.Y., Chou H.M., Chang Y.T. et al.: The number of cecidomyiid insect galls affects the photosynthesis of Machilus thunbergii host leaves.-J. Asia-Pac. Entomol. 17: 151-154, 2014b. Go to original source...
  23. Huang M.Y., Huang W.D., Chou H.M. et al.: Herbivorous insects alter the chlorophyll metabolism of galls on host plants.-J. Asia-Pac. Entomol. 17: 431-434, 2014a. Go to original source...
  24. Huang M.Y., Huang W.D., Chou H.M. et al.: Structural, biochemical, and physiological characterization of photosynthesis in leaf-derived cup-shaped galls on Litsea acuminata.-BMC Plant Biol. 15: 61-73, 2015. Go to original source...
  25. Huang M.Y., Lin K.H., Yang M.M. et al.: Chlorophyll fluorescence, spectral properties, and pigment composition of galls on leaves of Machilus thunbergii.-Int. J. Plant Sci. 172: 323-329, 2011. Go to original source...
  26. Iatrou G., Cook C.M., Stamou G. et al.: Chlorophyll fluorescence and leaf chlorophyll content of bean leaves injured by spider mites (Acari: Tetranychidae).-Exp. Appl. Acarol. 19: 581-591, 1995. Go to original source...
  27. Jiang C.D., Jiang G.M., Wang X. et al.: Increased photosynthetic activities and thermostability of photosystem II with leaf development of elm seedlings (Ulmus pumila) probed by the fast fluorescence rise OJIP.-Environ. Exp. Bot. 58: 261-268, 2006. Go to original source...
  28. Kalaji H.M., Schansker G., Ladle R.J. et al.: Frequently asked questions about in vivo chlorophyll fluorescence: practical issues.-Photosynth. Res. 122: 121-158, 2014. Go to original source...
  29. Khattab H., Khattab I.: Responses of Eucalypt trees to the insect feeding (gall-forming psyllid).-Int. J. Agric. Biol. 7: 979-984, 2005.
  30. Kmiec K., Kot I., Sytykiewicz H. et al.: Aphids' galls -damage or decorative value of host plants?-Scientific Proceedings of the 5th International Scientific Horticulture Conference, Nitra, Slovakia 21-23 September. Pp. 44-48, 2016.
  31. Kmiec K., Kot I.: [Occurence of aphids from Eriosomatinae subfamily on elms in the green area in Lublin.]-Ann. Univ. Mariae Curie-Sklodowska, 20: 7-13, 2010. [In Polish] Go to original source...
  32. Kmiec K., Kot I.: Tetraneura ulmi (L.) (Hemiptera, Eriosomatinae) on elm as its primary host.-Aphids Other Hemipter. Ins. 13: 145-149, 2007.
  33. Kmiec K., Sempruch C., Chrzanowski G. et al.: The effect of Tetraneura ulmi L. galling process on the activity of amino acid decarboxylases and the content of biogenic amines in Siberian elm tissues.-Bull. Entomol. Res. 18: 1-8, 2017. Go to original source...
  34. Kot I., Kmiec K.: Galls induced by insects on oaks and elms in the Lublin region, Poland.-Electron. J. Pol. Agric. Univ. 16: 3, 2013.
  35. Larson K.C., Whitham T.G.: Competition between gall aphids and natural plant sinks: plant architecture affects resistance to galling.-Oecologia 109: 575-582, 1997. Go to original source...
  36. Larson K.C., Whitham T.G.: Manipulation of food resources by a gall-forming aphid: the physiology of sink-source interactions.-Oecologia 88: 15-21, 1991. Go to original source...
  37. Larson K.C.: The impact of two gall-forming arthropods on the photosynthetic rates of their hosts.-Oecologia 115: 161-166, 1998. Go to original source...
  38. Lichtenthaler H.K., Wellburn A.R.: Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents.-Biochem. Soc. T. 11: 591-592, 1983. Go to original source...
  39. Maxwell K., Johnson G.N.: Chlorophyll fluorescence-a practical guide.-J. Exp. Bot. 51: 659-668, 2000. Go to original source...
  40. Murchie E.H., Lawson T.: Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications.-J. Exp. Bot. 64: 3983-3998, 2013. Go to original source...
  41. Nabity P.D., Hillstrom M.L., Lindroth R.L. et al.: Elevated CO2 interacts with herbivory to alter chlorophyll fluorescence and leaf temperature in Betula papyrifera and Populus tremuloides.-Oecologia 169: 905-913, 2012. Go to original source...
  42. Nabity P.D., Zavala J.A., DeLucia E.H.: Indirect suppression of photosynthesis on individual leaves by arthropod herbivory.-Ann. Bot.-London 103: 655-663, 2009. Go to original source...
  43. Netto A.T., Campostrini E., de Oliveira J.G. et al.: Photosynthetic pigments, nitrogen, chlorophyll a fluorescence and SPAD-502 readings in coffee leaves.-Sci. Hortic.-Amsterdam 104: 199-209, 2005. Go to original source...
  44. Ni X., Quisenberry S.S., Heng-Moss T. et al.: Dynamic change in photosynthetic pigments and chlorophyll degradation elicited by cereal aphid feeding.-Entomol. Exp. Appl. 105: 43-53, 2002. Go to original source...
  45. Retuerto R., Fernandez-Lema B., Rodriguez-Roiloa S. et al.: Increased photosynthetic performance in holly trees infested by scale insects.-Funct. Ecol. 18: 664-669, 2004. Go to original source...
  46. Rohácek K.: Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning, and mutual relationship.-Photosynthetica 40: 13-29, 2002. Go to original source...
  47. Sakov V.S., Krivchenko A.I., Rozengart E.V. et al.: Successes in application of pulse-amplitude modulated fluorescence.-In: Sakov V.S., Krivchenko A.I., Rozengart E.V. et al. (ed.): Derivative Spectrophotometry and PAM-Fluorescence in Comparative Biochemistry. Pp. 47-176. Springer International Publ., Cham 2015. Go to original source...
  48. Samsone I., Andersone U., Ievinsh G.: Gall midge Rhabdophaga rosaria -induced rosette galls on Salix: morphology, photochemistry of photosynthesis and defense enzyme activity.-Environ. Exp. Biol. 9: 29-36, 2011.
  49. Samsone I., Andersone U., Ievinsh G.: Variable effect of arthropod-induced galls on photochemistry of photosynthesis, oxidative enzyme activity and ethylene production in tree leaf tissues.-Environ. Exp. Biol. 10: 15-26, 2012.
  50. Samsone I., Andersone U., Vikmane M. et al.: Nondestructive methods in plant biology: an accurate measurement of chlorophyll content by a chlorophyll meter.-Acta Univ. Latv. 723: 145-154, 2007.
  51. Schreiber U., Neubauer C., Schliwa U.: PAM fluorometer based on medium-frequency pulsed Xe-flash measuring light: a highly sensitive new tool in basic and applied photosynthesis research.-Photosynth Res. 36: 65-72, 1992. Go to original source...
  52. Statistica StatSoft Inc.: Data Analysis Software System. Version 13.1. Available online at www.ststsoft.com, 2016.
  53. Suzuki D.K., Fukushi Y., Akimoto S.: Do aphid galls provide good nutrients for the aphids?: Comparisons of amino acid concentrations in galls among Tetraneura species (Aphididae: Eriosomatinae).-Arthropod-Plant Inte. 3: 241-247, 2009. Go to original source...
  54. Urban J.: Bionomics and harmfulness of Tetraneura ulmi (L.) (Aphidinea, Pemphigidae) in elms.-J. Forest Sci. 49: 159-181, 2003. Go to original source...
  55. Warabieda W., Borkowska B.: Chlorophyll a fluorescence as a diagnostic tool for assessment of apple resistance against twospotted spider mite (Tetranychus urticae Koch.).-Electron. J. Pol. Agric. Univ. 7: 1, 2004.
  56. Wojciechowski W., Depa L., Kanturski M. et al.: An annotated checklist of the Aphids (Hemiptera: Aphidomorpha) of Poland.-Pol. J. Entomol. 84: 83-420, 2015. Go to original source...
  57. Wool D.: Galling aphids: specialization, biological complexity, and variation.-Annu. Rev. Entomol. 49: 175-192, 2004. Go to original source...
  58. Yang C.M., Yang M.M., Huang M.Y. et al.: Life time deficiency of photosynthetic pigment-protein complexes CP1, A1, AB1, and AB1 in two cecidomyiid galls derived from Machilus thunbergii leaves.-Photosynthetica 45: 589-593, 2007. Go to original source...
  59. Yuan R.N., Shu S., Guo S.R. et al.: The positive roles of exogenous putrescine on chlorophyll metabolism and xanthophyll cycle in salt-stressed cucumber seedlings.-Photosynthetica 56: 557-566, 2018. Go to original source...
  60. Zhou S., Lou Y.R., Tzin V. et al.: Alteration of plant primary metabolism in response to insect herbivory.-Plant Physiol. 169: 1488-1498, 2015. Go to original source...