Abstract
Main conclusion
The weevil gall contains two distinct regions, differing in hydrolytic and antioxidant enzymes activity and profiles, which is also functionally distinct from the non-infected Cuscuta stems.
Weevils of the genus Smicronyx are gall-forming insects, widely distributed on parasitic flowering plants of the genus Cuscuta. Thus, they are considered epiparasites and potential method for biological control of their agriculturally harmful hosts. Although several reports on gall formation in Cuscuta spp. exist, the metabolic and functional changes, occurring in the gall, remained largely unknown. Smicronyx sp. galls, collected from a wild Cuscuta campestris population, were dissected into two distinct regions, inner and outer cortex, defined by the higher chlorophyll content of the inner cortex. Based on hydrolytic and antioxidant enzymes activity and isoenzymatic profiles as analyzed after electrophoretic separation, we suggested that the gall differs in its metabolic activity from the non-infected plant tissue. While the outer cortex serves as a region of nutrient storage and mobilization, the inner cortex is directly involved in larvae nutrition. The increase in metabolic activity resulted in significantly increased superoxide dismutase activity in the gall, while several other antioxidant enzymes diminished. The present research offers new insights into the functionally differing regions of Smicronyx galls and the metabolic changes, induced in C. campestris in result of the gall formation.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Anikin V, Nikelshparg M, Nikelshparg E, Konyukhov I (2017) Photosynthetic activity of the dodder Cuscuta campestris (Convolvulaceae) in case of plant inhabitation by the gallformed weevil Smicronyx smreczynskii (Coleoptera, Curculionidae). Izvestiya Saratov Univ New Ser Chem Biol Ecol 17(1):42–47
Benvenuti S, Dinelli G, Bonetti A, Catizone P (2005) Germination ecology, emergence and host detection in Cuscuta campestris. Weed Res 45(4):270–278
Biswas SM, Chakraborty N, Pal B (2014) Foliar gall and antioxidant enzyme responses in Alstonia scholaris, R. Br. after psylloid herbivory—an experimental and statistical analysis. Glob J Bot Sci 2:12–20
Carneiro RG, Isaias RM (2015) Gradients of metabolite accumulation and redifferentiation of nutritive cells associated with vascular tissues in galls induced by sucking insects. Ann Bot Plants. https://doi.org/10.1093/aobpla/plv086
de Oliveira DC, Moreira ASFP, dos Santos Isaias RM (2014) Functional gradients in insect gall tissues: studies on Neotropical host plants. In: Fernandes JW, Santos JK (eds) Neotropical insect galls. Springer, Dordrecht, pp 35–49
Dorchin N, Cramer MD, Hoffmann JH (2006) Photosynthesis and sink activity of wasp-induced galls in Acacia pycnantha. Ecology 87(7):1781–1791
Dsouza M, Ravishankar B (2014) Nutritional sink formation in galls of Ficus glomerata Roxb. (Moraceae) by the insect Pauropsylla depressa (Psyllidae, Hemiptera). Trop Ecol 55(1):129–136
Fallahpour F, Koocheki A, Mahallati MN, Rastegar MF, Ghorbani R (2016) Biological control of dodder (Cuscuta campestris L.) by fungi pathogens. Būm/shināsī-i kishāvarzī 2(3):408–416
Foyer CH, Shigeoka S (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol 155(1):93–100
Giron D, Huguet E, Stone GN, Body M (2016) Insect-induced effects on plants and possible effectors used by galling and leaf-mining insects to manipulate their host-plant. J Insect Physiol 84:70–89
Haupt S, Oparka KJ, Sauer N, Neumann S (2001) Macromolecular trafficking between Nicotiana tabacum and the holoparasite Cuscuta reflexa. J Exp Bot 52(354):173–177
Isaias RMS, Carneiro RGS, Oliveira DC, Santos JC (2013) Illustrated and annotated checklist of Brazilian gall morphotypes. Neotrop Entomol 42(3):230–239
Isaias RMS, Oliveira DC, Moreira ASFP, Soares GLG, Carneiro RGS (2015) The imbalance of redox homeostasis in arthropod-induced plant galls: mechanisms of stress generation and dissipation. Biochim et Biophys Acta (BBA) Gen Subj 1850(8):1509–1517
Jeschke WD, Räth N, Bäumel P, Czygan F-C, Proksch P (1994) Modelling the flow and partitioning of carbon and nitrogen in the holoparasite Cuscuta reflexa Roxb. and its host Lupinus albus L. I. Methods for estimating net flows. J Exp Bot 45(6):791–800
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227(5259):680–685
Manchenko GP (2002) Handbook of detection of enzymes on electrophoretic gels. CRC Press, Boca Raton
Parker C (2012) Parasitic weeds: a world challenge. Weed Sci 60(2):269–276
Pawłowski TA, Staszak AM, Karolewski P, Giertych MJ (2017) Plant development reprogramming by cynipid gall wasp: proteomic analysis. Acta Physiol Plant 39(5):114
Rakleova G, Keightley A, Panchev I, Tsacheva I, Tchorbadjieva M (2010) Cysteine proteinases and somatic embryogenesis in suspension cultures of orchardgrass (Dactylis glomerata L.). Gen Appl Plant Physiol 36(1–2):100–109
Sae-Tang P, Hihara Y, Yumoto I, Orikasa Y, Okuyama H, Nishiyama Y (2016) Overexpressed superoxide dismutase and catalase act synergistically to protect the repair of PSII during photoinhibition in Synechococcus elongatus PCC 7942. Plant Cell Physiol 57(9):1899–1907
Sandler HA (2010) Managing Cuscuta gronovii (swamp dodder) in cranberry requires an integrated approach. Sustainability 2(2):660–683
Srivastava S, Tripathi RD, Dwivedi UN (2004) Synthesis of phytochelatins and modulation of antioxidants in response to cadmium stress in Cuscuta reflexa—an angiospermic parasite. J Plant Physiol 161(6):665–674
Sue M, Ishihara A, Iwamura H (2000) Purification and characterization of a hydroxamic acid glucoside β-glucosidase from wheat (Triticum aestivum L.) seedlings. Planta 210(3):432–438
Sumanta N, Haque CI, Nishika J, Suprakash R (2014) Spectrophotometric analysis of chlorophylls and carotenoids from commonly grown fern species by using various extracting solvents. Res J Chem Sci 2231:606X
Svubova R, Lukacova Z, Kastier P, Blehova A (2017) New aspects of dodder–tobacco interactions during haustorium development. Acta Physiol Plant 39(3):66
Tepe I, Celebi SZ, Kaya I, Ozkan RY (2017) Control of smoothseed alfalfa dodder (Cuscuta approximata) in alfalfa (Medicago sativa). Int J Agric Biol 19(1):199–203
Tjiurutue MC, Sandler HA, Kersch-Becker MF, Theis N, Adler LA (2016) Cranberry resistance to dodder parasitism: induced chemical defenses and behavior of a parasitic plant. J Chem Ecol 42(2):95–106
Van der Kooij T, Krause K, Dörr I, Krupinska K (2000) Molecular, functional and ultrastructural characterisation of plastids from six species of the parasitic flowering plant genus Cuscuta. Planta 210(5):701–707
Zhang M, Fang Y, Ji Y, Jiang Z, Wang L (2013) Effects of salt stress on ion content, antioxidant enzymes and protein profile in different tissues of Broussonetia papyrifera. S Afr J Bot 85:1–9
Zhekova E, Petkova D, Ivanova I (2014) Smicronyx smreczynskii F. Solari, 1952 (Insecta: Curculionidae): possibilities for biological control of two Cuscuta species (Cuscutaceae) in district of Ruse. Acta Zool Bulg 66(3):431–432
Zimmermann C (1962) Autotrophic development of dodder (Cuscuta pentagona Englm.) in vitro. Crop Sci 2(5):449–450
Acknowledgements
The present study was financially supported by the National Science Fund of the Bulgarian Ministry of Education and Science, Grant DNTS China 01/5 and the Inter-governmental S&T Cooperation Proposal between Bulgaria and China (No. 15-2).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Zagorchev, L.I., Albanova, I.A., Tosheva, A.G. et al. Metabolic and functional distinction of the Smicronyx sp. galls on Cuscuta campestris. Planta 248, 591–599 (2018). https://doi.org/10.1007/s00425-018-2926-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-018-2926-6