Photosynthetica 2020, 58(3):827-835 | DOI: 10.32615/ps.2020.033
Photochemical performance and source-sink relationships in galls induced by Pseudophacopteron longicaudatum (Hemiptera) on leaves of Aspidosperma tomentosum (Apocynaceae)
- 1 Laboratory of Plant Anatomy, Development and Interaction (LADEVI), Federal University of Uberlândia - UFU, Campus Umuarama, Uberlândia, MG, Brazil
- 2 Laboratory of Plant Physiology (LAFIVE), Institute of Biology, Federal University of Uberlândia - UFU, Campus Umuarama, Uberlândia, MG, Brazil
- 3 Laboratory of Plant Anatomy, Federal University of Jataí, Institute of Bioscience, Campus City University, Jataí, Goiás, Brazil
The establishment of the galling insect generates a biotic stress that leads to tissue transformation. However, galls can maintain chlorophyll (Chl) and consequently photosynthesize. Herein, we evaluated the consequences of the biotic stress generated by the galling insect Pseudophacopteron longicaudatum on photosynthetic rate during the leaf galls development on Aspidosperma tomentosum. In addition, we quantified polysaccharides and water content in order to evaluate the capacity of gall tissues to drain photoassimilates. The non-galled leaves contained more Chl and carotenoids per gram of fresh mass. Galls had lower values of maximum PSII quantum yield, fluorescence decline ratio, and nonphotochemical quenching compared to non-galled tissue. These results showed a significant reduction of photosynthesis photochemistry in galled tissues although total soluble sugar did not differ between gall and non-galled leaves. Water-soluble polysaccharides, relative water content, and leaf specific mass were significantly higher in galls and increased through their development, suggesting a sink relationship.
Additional key words: gall photosynthesis; green island; herbivory; Kautsky effect; oxidative stress.
Received: September 26, 2019; Revised: March 30, 2020; Accepted: April 3, 2020; Prepublished online: May 20, 2020; Published: June 11, 2020 Show citation
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References
- Alvares C.A., Stape J.L., Sentelhas P.C. et al.: Köppen's climate classification map for Brazil. - Meteorol. Z. 22: 711-728, 2013.
Go to original source... - B±czek-Kwinta R., Kozie³ A., Seidler-£o¿ykowska 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... - Baker N.R., Oxborough K.: Chlorophyll fluorescence as a probe of photosynthetic productivity. - In: Papageorgiou G.C., Govindjee (ed.): Chlorophyll a Fluorescence: A Signature of Photosynthesis. Advances in Photosynthesis and Respiration. Pp. 65-82. Springer, Dordrecht 2004.
Go to original source... - Bhattacharjee S.: Sites of generation and physicochemical basis of formation of reactive oxygen species in plant cell. - In: Gupta S.D. (ed.): Reactive Oxygen Species and Antioxidants in Higher Plants. Pp. 1-30. CRC Press, Boca Raton 2010.
Go to original source... - Bielski R.L., Turner L.A.: Separation and estimation of amino acids in crude plant extracts by thin-layer electrophoresis and chromatography. - Anal. Biochem. 17: 278-293, 1966.
Go to original source... - Bolhàr-Nordenkampf H.R, Long S.P, Baker N.R. et al.: Chlorophyll fluorescence as a probe of the photosynthetic competence of leaves in the field: a review of current instrumentation. - Funct. Ecol. 3: 497-514, 1989.
Go to original source... - Bragança G.P., Oliveira D.C., Isaias R.M.S.: Compartmentalization of metabolites and enzymatic mediation in nutritive cells of Cecidomyiidae galls on Piper arboreum Aubl. (Piperaceae). -J. Plant Stud. 6: 11, 2016.
Go to original source... - Bronner R.: The role of nutritive cells in the nutrition of Cynipids and Cecidomyiids. - In: Shorthouse J.D., Rohfritsch O. (ed.): Biology of Insect-Induced Galls. Pp. 60-86. Oxford University Press, Oxford 1992.
- Buchanan-Wollaston V., Earl S., Harrison E. et al.: The molecular analysis of leaf senescence - a genomics approach. - Plant Biotechnol. J. 1: 3-22, 2003.
Go to original source... - Campos P.T., Costa M.C.D., Isaias R.M.S. et al.: Phenological relationships between two insect galls and their host plants: Aspidosperma australe and A. spruceanum (Apocynaceae). - Acta Bot. Bras. 24: 727-733, 2010.
Go to original source... - Carneiro R.G.S., Castro A.C., Isaias R.M.S.: Unique histo-chemical gradients in a photosynthesis-deficient plant gall. - S. Afr. J. Bot. 92: 97-104, 2014b.
Go to original source... - Carneiro R.G.S., Oliveira D.C., Isaias R.M.S.: Developmental anatomy and immunocytochemistry reveal the neo-ontogenesis of the leaf tissues of Psidium myrtoides (Myrtaceae) towards the globoid galls of Nothotrioza myrtoidis (Triozidae). - Plant Cell Rep. 33: 2093-2106, 2014a.
Go to original source... - 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). - S. Afr. J. Bot. 83: 121-126, 2012.
Go to original source... - Castro A.C., Oliveira D.C., Moreira A.S.F.P., Isaias R.M.S.: Synchronism between Aspidosperma macrocarpon (Apocy-naceae) resources allocation and the establishment of the gall inducer Pseudophacopteron sp. (Hemiptera: Psylloidea). - Rev. Biol. Trop. 61: 1891-1900, 2013.
Go to original source... - Chow P.S., Landhäusser S.M.: A method for routine measurements of total sugar and starch content in woody plant tissues. - Tree Physiol. 24: 1129-1136, 2004.
Go to original source... - Cosgrove D.: Biophysical control of plant cell growth. - Ann. Rev. Plant Physio. 37: 377-405, 1986.
Go to original source... - Demmig-Adams B., Gilmore A.M., Adams III W.W.: In vivo function of carotenoids in higher plants. - FASEB J. 10: 403-412, 1996.
Go to original source... - Dias G.G., Moreira G.R.P., Ferreira B.G., Isaias R.M.S.: Why do the galls induced by Calophya duvauae Scott on Schinus polygamus (Cav.) Cabrera (Anacardiaceae) change colors? - Biochem. Syst. Ecol. 48: 111-122, 2013.
Go to original source... - El-Akkad S.S.: Biochemical changes induced in Populus nigra leaves by galling aphid Pemphigous populi. - Int. J. Agric. Biol. 6: 650-664, 2004.
- Ferreira B.G., Isaias R.M.S.: Floral-like destiny induced by a galling Cecidomyiidae on the axillary buds of Marcetia taxifolia (Melastomataceae). - Flora 209: 391-400, 2014.
Go to original source... - Florentine S.K., Raman A., Dhileepan K.: Effects of gall induction by Epiblema strenuana on gas exchange, nutrients, and energetics in Parthenium hysterophorus. - BioControl 50: 787-801, 2005.
Go to original source... - Foyer C.H., Noctor G.: Oxidant and antioxidant signaling in plants: A re-evaluation of the concept of oxidative stress in a physiological context. - Plant Cell Environ. 28: 1056-1071, 2005.
Go to original source... - Genty B., Briantais J.M., Baker N.R.: The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. - BBA-Gen. Subjects 990: 87-92, 1989.
Go to original source... - Huang M.Y., Chou H.M., Chang Y.T., Yang C.M.: The number of cecidomyiid insect galls affects the photosynthesis of Machilus thunbergii host leaves. - J. Asia-Pac. Entomol. 17: 151-154, 2014.
Go to original source... - Isaias R.M.S., Carneiro R.G.S., Oliveira D.C., Santos J.C.: Illustrated and annotated checklist of Brazilian gall morpho-types. - Neotrop. Entomol. 42: 230-239, 2013.
Go to original source... - Isaias R.M.S., Oliveira D.C., Carneiro R.G.S.: Role of Euphalerus ostreoides (Hemiptera: Psylloidea) in manipulating leaflet ontogenesis of Lonchocarpus muehlbergianus (Fabaceae). - Botany 89: 581-592, 2011.
Go to original source... - Isaias R.M.S., Oliveira D.C., Moreira A.S.F.P. et al.: The imbalance of redox homeostasis in arthropod-induced plant galls: Mechanisms of stress generation and dissipation. - BBA-Gen. Subjects 1850: 1509-1517, 2015.
Go to original source... - Kaiser W., Huguet E., Casas J. et al.: Plant green-island phenotype induced by leaf-miners is mediated by bacterial symbionts. - P. Roy. Soc. Lond. B Bio. 277: 2311-2319, 2010.
Go to original source... - Kalaji H.M., Jajoo A., Oukarroum A. et al.: Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. - Acta Physiol. Plant 38: 102, 2016.
Go to original source... - Kmieæ K., Rubinowska K., Micha³ek W., Sytykiewicz H.: The effect of galling aphids feeding on photosynthesis photochemistry of elm trees (Ulmus sp.). - Photosynthetica 56: 989-997, 2018.
Go to original source... - 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... - Lichtenthaler H.K., Miehé J.A.: Fluorescence imaging as a diagnostic tool for plant stress. - Trends Plant Sci. 2: 316-320, 1997.
Go to original source... - 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... - Lüttge U., Haridasan M., Fernandes G.W. et al.: Photosynthesis of mistletoes in relation to their hosts at various sites in tropical Brazil. - Trees 12: 167-174, 1998.
Go to original source... - Malenovskı I., Burckhardt D., Queiroz D.L. et al.: Descriptions of two new Pseudophacopteron species (Hemiptera: Psylloidea: Phacopteronidae) inducing galls on Aspidosperma (Apocynaceae) in Brazil. - Acta Ent. Mus. Nat. Pra. 55: 513-538, 2015.
- Mani M.S.: Ecology of Plant Galls. Pp. 434. Springer, Dordrecht 1964.
Go to original source... - Martini V.C., Fuzaro L., Goncalves L.A. et al.: Pseudophacopteron longicaudatum (Hemiptera) induces intralaminar leaf galls on Aspidosperma tomentosum (Apocynaceae): a qualitative and quantitative structural overview. - An. Acad. Bras. Ciênc., 2020, in press.
- Maxwell K., Johnson G.N.: Chlorophyll fluorescence - a practical guide. - J. Exp. Bot. 51: 659-668, 2000.
Go to original source... - McCready R.M., Guggolz J., Silveira V., Owens H.S.: Determina-tion of starch and amylase in vegetables. Application to peas. - Anal. Chem. 22: 1156-1158, 1950.
Go to original source... - Moreira A.S.F.P., Queiroz A.C.L., Barros F.V. et al.: Do leaf traits in two Dalbergia species present differential plasticity in relation to light according to their habitat of origin? - Aust. J. Bot. 61: 592-599, 2014.
Go to original source... - Moura M.Z.D., Soares G.L.G., Isaias R.M.S.: Species-specific changes in tissue morphogenesis induced by two arthropod leaf gallers in Lantana camara L. (Verbenaceae). - Aust. J. Bot. 56: 153-160, 2008.
Go to original source... - 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, 2008.
Go to original source... - Niyogi K.K.: Safety valves for photosynthesis. - Curr. Opin. Plant Biol. 3: 455-460, 2000.
Go to original source... - Ogburn R.M., Edwards E.J.: Quantifying succulence: a rapid, physiologically meaningful metric of plant water storage. - Plant Cell Environ. 35: 1533-1542, 2012.
Go to original source... - Oliveira D.C., Christiano J.C.S., Soares G.L.G. et al.: Reactions of chemical and structural defenses of Lonchocarpus muehlbergianus Hassl. (Fabaceae) to the action of the galler Euphalerus ostreoides Crawf. (Hemiptera: Psyllidae). - Rev. Bras. Bot. 29: 657-667, 2006. [In Portuguese]
Go to original source... - Oliveira D.C., Isaias R.M.S., Fernandes G.W. et al.: Manipulation of host plant cells and tissues by gall-inducing insects and adaptive strategies used by different feeding guilds. - J. Insect Physiol. 84: 103-113, 2016.
Go to original source... - Oliveira D.C., Isaias R.M.S., Moreira A.S.F.P. 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... - Oliveira D.C., Isaias R.M.S.: Redifferentiation of leaflet tissues during midrib gall development in Copaifera langsdorffii (Fabaceae). - S. Afr. J. Bot. 76: 239-248, 2010.
Go to original source... - Oliveira D.C., Magalhães T.A., Ferreira B.G. et al.: Variation in the degree of pectin methylesterification during the development of Baccharis dracunculifolia kidney-shaped gall. - PLoS ONE 9: e94588, 2014.
Go to original source... - Oliveira D.C., Moreira A.S.F.P., Isaias R.M.S. et al.: Sink status and photosynthetic rate of the leaflet galls induced by Bystracoccus mataybae (Eriococcidae) on Matayba guianensis (Sapindaceae). - Front. Plant Sci. 8: 1249, 2017.
Go to original source... - Oxborough K.: 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, 2004.
Go to original source... - Pavloviè A.: The effect of electrical signals on photosynthesis and respiration. - In: Volkov A.G. (ed): Plant Electrophysiology: Signaling and Responses. Pp. 33-62. Springer-Verlag, Berlin 2012.
Go to original source... - Pincebourde S., Casas J.: Hypoxia and hypercarbia in endo-phagous insects: larval position in the plant gas exchange network is key. - J. Insect Physiol. 84: 137-153, 2016.
Go to original source... - R Core Team: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria 2017. Available at: https://www.R-project.org/
- Retuerto R., Fernandez-Lema B., Obeso J.R.: Increased photosynthetic performance in holly trees infested by scale insects. - Funct. Ecol. 18: 664-669, 2004.
Go to original source... - Rezende U.C., Moreira A.S.F.P., Kuster V.C.. Oliveira D.C.: Structural, histochemical and photosynthetic profiles of galls induced by Eugeniamyia dispar (Diptera, Cecidomyiidae) on the leaves of Eugenia uniflora (Myrtaceae). - Rev. Biol. Trop. 66: 1469-1480, 2018.
Go to original source... - Roháèek K.: Chlorophyll fluorescence parameters: the defini-tions, photosynthetic meaning, and mutual relationship. - Photosynthetica 40: 13-29, 2002.
Go to original source... - Shannon J.C.: Carbon-14 distribution in carbohydrates of immature Zea mays. Kernels following 14CO2 treatment of intact plants. - Plant Physiol. 43: 1215-1220, 1968.
Go to original source... - Shorthouse J.D., Wool D., Raman A.: Gall-inducing insects - Nature's most sophisticated herbivores. - Basic Appl. Ecol. 6: 407-411, 2005.
Go to original source... - Stirbet A.: On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and photosystem II: basics and applications of the OJIP fluorescence transient. - J. Photoch. Photobio. B 104: 236-257, 2011.
Go to original source... - Turner N.: Techniques and experimental approaches for the measurement of plant water status. - Plant Soil 58: 339-366, 1981.
Go to original source... - Witkowski E.T.F., Lamont B.B.: Leaf specific mass confounds leaf density and thickness. - Oecologia 88: 486-493, 1991.
Go to original source... - Woo H.R., Kim H.J., Lim P. O. et al.: Leaf senescence: Systems and dynamics aspects. - Annu. Rev. Plant Biol. 70: 347-376, 2019.
Go to original source... - Zangerl A.R., Hamilton J.G., Miller T.J. et al.: Impact of folivory on photosynthesis is greater than the sum of its holes. - P. Natl. Acad. Sci. USA 99: 1088-1091, 2002.
Go to original source...




