Abstract
Alterations in cell wall composition imply in new structural and functional traits in gall developmental sites, even when the inducer is a sucking exophytophagous insect with strict feeding sites as the aphid associated to Malus domestica Borkh. This host plant is an economically important, fruit-bearing species, susceptible to gall induction by the sucking aphid Eriosoma lanigerum Hausmann, 1802. Herein, the immunocytochemical detection of arabinogalactan-proteins (AGPs), pectins, and hemicelluloses using monoclonal antibodies was performed in samples of non-galled roots and stems, and of root and stem galls on M. domestica. The dynamics of these cell wall components was discussed under the structural and functional traits of the galls proximal, median, and distal regions, according to the proximity of E. lanigerum colony feeding site. In the proximal region, the epitopes of AGPs and homogalacturonans (HGs) are related to cell growth and divisions, which result in the overproduction of parenchyma cells both in root and stem galls. In the proximal and median regions, the co-occurrence of HGs and arabinans in the cell walls of parenchyma and secondary tissues favors the nutrient flow and water-holding capacity, while the xylogalacturonans and hemicelluloses may function as additional carbohydrate resources to E. lanigerum. The immunocytochemical profile of the cell walls support the feeding activity of E. lanigerum mainly in the gall proximal region. The similarity of the cell wall components of the gall distal region and the non-galled portions, both in roots and stems, relates to the decrease of the cecidogenetic field the more distant the E. lanigerum colony is.
Graphical Abstract
Similar content being viewed by others
Data availability
The authors declare that the data supporting the findings of this study are available within the paper and its Supplementary Information files. Should any raw data files be needed in another format they are available from the corresponding author upon reasonable request.
References
Adhikari U (2022) Distribution, biology, nature of damage and management of woolly apple aphid, Eriosoma lanigerum (Hausmann), (Hemiptera: Aphididae) in apple orchard: a review. Revi Food Agri 3:92–99. https://doi.org/10.26480/rfna.02.2022.92.99
Albersheim P, Darvill AG, O’Neill MA, Schols HA, Voragen AGJ (1996) An hypothesis: the same six polysaccharides are components of the primary cell walls of all higher plants. Prog Biotechnol 14:47–53. https://doi.org/10.1016/S0921-0423(96)80245-0
Álvarez R, Encina A, Pérez-Hidalgo N (2009) Histological aspects of three Pistacia terebinthus galls induced by three different aphids: Paracletus cimiciformis, Forda marginata and Forda formicaria. Plant Sci 176:303–314. https://doi.org/10.1016/j.plantsci.2008.11.006
Asante SK, Danthanarayana W, Heatwole H (1991) Bionomics and population growth statistics of apterous virginoparae of woolly apple aphid, Eriosoma lanigerum, at constant temperatures. Entomol Exp Appl 60:261–270. https://doi.org/10.1111/j.1570-7458.1991.tb01546.x
Aspinall G, Fanous H (1984) Structural investigations on the non-starchy polysaccharides of apples. Carbohyd Polym 4(3):193–214. https://doi.org/10.1016/0144-8617(84)90011-0
Ateyyat MA, Al-Antary TM (2009) Susceptibility of nine apple cultivars to woolly apple aphid, Eriosoma lanigerum (Homoptera: Aphididae) in Jordan. Int J Pest Manag 55:79–84. https://doi.org/10.1080/09670870802546164
Beliën T, Bangels E, Peusens G, Berkvens N, Viaene N, Goossens D (2011) Towards improved control of woolly apple aphid (Eriosoma lanigerum) in integrated fruit production. Acta Horticulturae 917:15–22. https://doi.org/10.17660/ActaHortic.2011.917.1
Berglund J, Mikkelsen D, Flanagan BM, Gaunitz DS, Henriksson G, Lindström ME, Yakubov GE, Gidley MJ, Vilaplana F (2020) Wood hemicelluloses exert distinct biomechanical contributions to cellulose fibrillar networks. Nat Commun 11:4692. https://doi.org/10.1038/s41467-020-18390-z
Biello R, Singh A, Cindayniah J, Fernández GFF, Mugford ST, Powell G, Hogenhout SA, Mathers TC (2021) A chromosome-level genome assembly of the woolly apple aphid, Eriosoma lanigerum Hausmann (Hemiptera: Aphididae). Mol Ecol Resour 21:316–326. https://doi.org/10.1111/1755-0998.13258
Bissing DR (1974) Haupt’s gelatin adhesive mixed with formalin for affixing paraffin sections to slides. Stain Technol 49:116–117
Bragança GPP, Alencar CF, Freitas MSC, Isaias RMS (2020) Hemicelluloses and associated compounds determine gall functional traits. Plant Biol 22:981–991. https://doi.org/10.1111/plb.13151
Brown MW, Schmitt JJ, Ranger S, Hogmire HW (1995) Yield reduction in apple by edaphic woolly apple aphid (Homoptera: Aphididae) populations. J Econ Entomol 88(127–337):133. https://doi.org/10.1093/jee/88.1.127
Bukatsch F (1972) Bemerkungen zur Doppelf¨arbung Astrablau-Safranin. Mikrokosmos 61:255
Caffall KH, Mohnen D (2009) The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr Res 344:1879–1900. https://doi.org/10.1016/j.carres.2009.05.021
Carneiro RGS, Isaias RMS (2015) Gradients of metabolite accumulation and redifferentiation of nutritive cells associated with vascular tissues in galls induced by sucking insects. AoB Plants 7:plv086. https://doi.org/10.1093/aobpla/plv086
Carneiro RGS, Oliveira DC, Isaias RMS (2014) 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. https://doi.org/10.1007/s00299-014-1683-7
Carneiro RGS, Pacheco P, Isaias RMS (2015) Could the extended phenotype extend to the cellular and subcellular levels in insect-induced galls? PLoS ONE 10:e0129331. https://doi.org/10.1371/journal.pone.0129331
Carneiro RGS, Isaias RMS (2015b) Cytological cycles and fates in Psidium myrtoides are altered towards new cell metabolism and functionalities by the galling activity of Nothotrioza myrtoidis. Protoplasma 252:637–646. https://doi.org/10.1007/s00709-014-0709-x
Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861. https://doi.org/10.1038/nrm1746
Costa EC, Oliveira DC, Ferreira DKL, Isaias RMS (2021) Structural and nutritional peculiarities related to lifespan differences on four Lopesia induced bivalve-shaped galls on the single super-host Mimosa gemmulata. Front Plantsci 12:660557. https://doi.org/10.3389/fpls.2021.660557
Denardi F, Spengler MM (2001) Comportamento da cultivar de macieira Fuji (Malus domestica, Borkh.) sobre três diferentes porta-enxertos. Rev Bras Frutic 23:630–633. https://doi.org/10.1590/S0100-29452001000300037
Denardi F, Kvitschal MV, Hawerroth MC (2015) Porta-enxertos de macieira: passado, presente e futuro. Agropecuária Catarinense 28(2):89–95
Ferreira BG, Bragança GP, Isaias RMS (2019) Cytological attributes of storage tissues in nematode and eriophyid galls: pectin and hemicellulose functional insights. Protoplasma 257:229–244. https://doi.org/10.1007/s00709-019-01431-w
Ferreira T, Rasband W (2011) The ImageJ user guide. 1:44. http://rsbweb.nih.gov/ij/docs/user-guide.pdf
Formiga AT, Oliveira DC, Ferreira BG, Magalhães TA, Castro AC, Fernandes GW, Isaias RMS (2013) The role of pectic composition of cell walls in the determination of the new shape-functional design in galls of Baccharis reticularia (Asteraceae). Protoplasma 250:899–908. https://doi.org/10.1007/s00709-012-0473-8
Freitas MS (2022) Galhas induzidas por Eriosoma lanigerum Hausmann (Hemiptera: Aphididae) em Malus domestica Borkh. (Rosaceae). Dissertação de Mestrado. Universidade Federal de Minas Gerais- UFMG. Belo Horizonte.https://hdl.handle.net/1843/40651. Accessed 03 Mar 2022
Ge F, Dietrich C, Dai W (2016) Mouthpart structure in the woolly apple aphid Eriosoma lanigerum (Hausmann) (Hemiptera: Aphidoidea: Pemphigidae). Arthropod Struct Dev 45:230e241. https://doi.org/10.1016/j.asd.2016.01.005
Jones L, Seymour GB, Knox JP (1997) Localization of pectic galactan in tomato cell walls using a monoclonal antibody specific to (1–4)-b-galactan. Plant Physiol 113:1405–1412. https://doi.org/10.1104/pp.113.4.1405
Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. J Cell Sci 27:137–138
Kikuchi A, Edashige Y, Ishii T, Satoh S (1996) A xylogalacturonan whose level is dependent on the size of cell clusters is present in the pectin from cultured carrot cells. Planta 200:369–372. https://doi.org/10.1007/bf00231391
Kraus JE, Arduin M (1997) Manual Básico de Métodos em Morfologia Vegetal. EDUR, Seropédica. Lampugnani, E.R.
Lamport DTA, Tan L, Held MA, Kieliszewski MJ (2018) Pollen tube growth and guidance: Occam’s razor sharpened on a molecular arabinogalactan glycoprotein Rosetta Stone. New Phytol 217:491–500. https://doi.org/10.1111/nph.14845
Levesque-Tremblay G, Pelloux J, Braybrook SA, Müller K (2015) Tuning of pectin methylesterification: consequences for cell wall biomechanics and development. Planta 242:791–811
Lordan J, Alegre S, Gatius F, Sarasúa M, Alins G (2015) Woolly apple aphid Eriosoma lanigerum Hausmann ecology and its relationship with climatic variables and natural enemies in Mediterranean areas. Bull Entomol Res 105:60–69. https://doi.org/10.1017/S0007485314000753
Madalon F, Damascena A, Madalon R, Araujo Junior L, Carvalho J, Pratissoli D (2020) First report of Eriosoma lanigerum (Hausmann, 1802) (Hemiptera: Aphididae) on the apple tree crop in Espirito Santo State, Brazil. Int J Adv Eng Res Sci 7:297–300. https://doi.org/10.22161/ijaers.73.44
Majewska-Sawka A, Nothnagel EA (2000) The multiple roles of Arabinogalactan proteins in plant development. Plant Physiol 122(1):3–10. https://doi.org/10.1104/pp.122.1.3
Marcus SE, Verhertbruggen Y, Herve C, Ordaz-Ortiz JJ, Farkas V, Pedersen HL, Willats WGT, Knox JP (2008) Pectic homogalacturonan masks abundant sets of xyloglucan epitopes in plant cell walls. BMC Plant Biol 8:60. https://doi.org/10.1186/1471-2229-8-60
Marcus SE, Blake AW, Benians TTAS, Lee KJD, Poyser C, Donaldson L, Leroux O, Rogowski A, Petersen HL, Boraston A, Gilbert HG, Willats WGT, Knox JP (2010) Restricted access of proteins to mannan polysaccharides in intact plant cell walls. Plant J 64:191–203. https://doi.org/10.1111/j.1365-313X.2010.04319.x
Martini VC, Moreira ASFP, Kusterb VC, Oliveira DC (2019) Galling insects as phenotype manipulators of cell wall composition during the development of galls induced on leaves of Aspidosperma tomentosum (Apocynaceae). S Afr J Bot 127:226–233. https://doi.org/10.1016/j.sajb.2019.09.006
Mastroberti AA, Mariath JEA (2008) Immunocytochemistry of the mucilage cells of Araucaria angustifolia (Bertol.) Kuntze (Araucariaceae). Rev Brasil Bot 31:1–13
McAllan JW, Adams JB (1961) The significance of pectinase in plant penetration by aphids. Can J Zool 39:3. https://doi.org/10.1139/z61-034
McCartney L, Marcus SE, Knox JP (2005) Monoclonal antibodies to plant cell wall xylans and arabinoxylans. J Histochem Cytochem 53:543–546. https://doi.org/10.1369/jhc.4B6578.2005
Miles PW (1972) The saliva of Hemiptera. Adv in Insect Phys 9:183–255. https://doi.org/10.1016/S0065-2806(08)60277-5
Miles PW (1999) Aphid saliva. Biol Rev 74:41–85
Mondal H (2020) Aphid saliva: a powerful recipe for modulating host resistance towards aphid clonal propagation. Arthropod-Plant Interactions 14:547–558. https://doi.org/10.1007/s11829-020-09769-2
Moore JP, Farrant JM, Driouich A (2008) A role for pectin-associated arabinans in maintaining the flexibility of the plant cell wall during water deficit stress. Plant Signal Behav 3:102–104. https://doi.org/10.4161/psb.3.2.4959
Mueller TF, Blommers LHM, Mols PJM (1992) Woolly apple aphid (Eriosoma lanigerum Hausm, Hom, Aphidae) parasitism by Aphelinus mali Hal (Hym, Aphelinidae) in relation to host stage and host colony size, shape and location. Appl Entomology 114:143–154. https://doi.org/10.1111/j.1439-0418.1992.tb01109.x
Nogueira RM, Costa EC, Silva JS, Isaias RMS (2022) A phenological trick and cell wall bricks toward adaptive strategies of Mimosa tenuiflora-Lopesia mimosae interaction in Caatinga environment. Flora 294:152121. https://doi.org/10.1016/j.flora.2022.152121
Nothnagel EA (1997) Proteoglycans and related components in plant cells. Int Rev Cytol 174:195–291. https://doi.org/10.1016/s0074-7696(08)62118-x
O’Donoghue EM, Sutherland PW (2012) Cell wall polysaccharide distribution in Sandersonia aurantiaca flowers using immunedetection. Protoplasma 249:843–849. https://doi.org/10.1007/s00709-011-0307-0
Oliveira DL, Alvarenga AA, Gonçalves ED, Malta MR (2014a) Qualidade da maçã cv. Eva produzida em duas regiões de Minas Gerais. Braz J Food Technol 17:269–272
Oliveira DC, Magalhães TA, Ferreira BG, Teixeira CT, Formiga AT, Fernandes GW, Isaias RMS (2014b) Variation in the degree of pectin methylesterification during the development of Baccharis dracunculifolia kidney-shaped gall. PLoS ONE 9:e94588. https://doi.org/10.1371/journal.pone.0094588
Paiva JGA, Fank-De-Carvalho SM, Magalhães MP, Graciano-Ribeiro D (2006) Verniz vitral incolor 500®: uma alternativa de meio de montagem economicamente viável. Acta Bot Bras 20:257–264
Petri JL, Hawerroth FJ, Fazio G, Francescatto P, Leite BG (2017) Avanços na propagação de fruteiras no Brasil e no mundo-macieira. Rev Bras Frutic 41:3. https://doi.org/10.1590/0100-29452019004
Pringle KL, Heunis JM (2001) Woolly apple aphid in South Africa: biology, seasonal cycles, damage and control. DFGA 51:22–23
Raman A (2012) Gall induction by hemipteroid insects. J Plant Interact 7:29–44. https://doi.org/10.1080/17429145.2011.630847
Rennie EA, VibeScheller H (2014) Xylan biosynthesis. Curr Opin Biotechnol 26:100–107. https://doi.org/10.1016/j.copbio.2013.11.013
Ridley BL, O’Neill MA, Mohnen D (2001) Pectins: structure, biosynthesis, and oligogalacturonide-related signaling. Phytochemistry 57:929–967. https://doi.org/10.1016/s0031-9422(01)00113-3
Sandanayaka WR, Bus VG (2005) Evidence of sexual reproduction of woolly apple aphid, Eriosoma lanigerum, in New Zealand. J Insect Sci 5:27. https://doi.org/10.1093/jis/5.1.27
Schols HA, Bakx EJ, Schipper D, Voragen AGJ (1995) A xylogalacturonan subunit present in the modified hairy regions of apple pectin. Carbohydr Res 279:265–279. https://doi.org/10.1016/0008-6215(95)00287-1
Seifert GJ, Roberts K (2007) The biology of Arabinogalactan proteins. Annu Rev Plant Biol 58:137–161. https://doi.org/10.1146/annurev.arplant.58.03
Shaw PW, Walker JTS (1996) Biological control of woolly apple aphid by Aphelinus mali in an integrated fruit production programme in Nelson. In: Proceedings of the 49th New Zealand Plant Protection Society Conference, Nelson, New Zealand, p 59–63. https://doi.org/10.30843/nzpp.1996.49.11425
Sherwani A. Mukhtar M. Wani AA (2016) Insect pests of apple and their management insect pests of apple and their management. Insect Pest Management of Fruit Crops. New Delhi: Biotech Books, pp. 295-306
Showalter AM (2001) Arabinogalactan-proteins: structure, expression and function. Cell Mol Life Sci 58:1399–1417. https://doi.org/10.1007/pl00000784
Silva J, Ferraz R, Dupree P, Showalter AM, Coimbra S (2020) Three decades of advances in Arabinogalactan-protein biosynthesis. Front Plant Sci 11:610377. https://doi.org/10.3389/fpls.2020.610377
Silva AFM, Lana LG, Kuster VC, Oliveira DC (2021) Chemical composition of cell wall changes during developmental stages of galls on Matayba guianensis (Sapindaceae): perspectives obtained by immunocytochemistry analysis. Sci Nature 108:16. https://doi.org/10.1007/s00114-021-01732-2
Silva-Sanzana C, Celiz-Balboa J, Garzo E, Marcus SE, Parra-Rojas JP, Rojas B, Blanco-Herrera F (2019) Pectin methyesterases modulate plant homogalacturonan status in defenses against the aphid Myzus persicae. The Plant Cell 31:1913–1929. https://doi.org/10.1105/tpc.19.00136
Smallwood M, Yates EA, Willats WGT, Martin H, Knox JP (1996) Immunochemical comparison of membrane-associated and secreted arabinogalactan-proteins in rice and carrot. Planta 198:452–459
Staniland L (1924) The immunity of apple stocks from attacks of woolly aphis (Eriosoma lanigerum, Hausmann). Part II. The causes of the relative resistance of the stocks. Bull Entomol Res 15:157–170. https://doi.org/10.1017/S0007485300031527
Stokwe NF, Malan AP (2016) Woolly apple aphid, Eriosoma lanigerum (Hausmann), in South Africa: biology and management practices, with focus on the potential use of entomopathogenic nematodes and fungi. Afr Entomol 24:267–278. https://doi.org/10.4001/003.024.0267
Su S, Higashiyama T (2018) Arabinogalactan proteins and their sugar chains: functions in plant reproduction, research methods, and biosynthesis. Plant Reprod 31:67–75. https://doi.org/10.1007/s00497-018-0329-2
Teixeira CT, Oliveira DC, Kuster VC, Isaias RMS (2018) Immunocytochemical demonstration of cell wall components related to tissue compartments in the globoid galls induced by Clinodiplosis sp. (Cecidomyiidae) on Croton floribundus Spreng. (Euphorbiaceae). Botany 96:1–29. https://doi.org/10.1139/cjb-2017-0123
Tjallingii WF (2006) Salivary secretions by aphids interacting with proteins of phloem wound responses. J Exp Bot 57:739–745. https://doi.org/10.1093/jxb/erj088
Van Hengel AJ (2001) N-Acetylglucosamine and glucosamine-containing arabinogalactan proteins control somatic embryogenesis. Plant Physiol 125:1880–1890. https://doi.org/10.1104/pp.125.4.1880
Verhertbruggen Y, Marcus SE, Haeger A, Verhoef R, Schols HA, MacCleary BV, McKee L, Knox JP (2009) Developmental complexity of arabinan polysaccharides and their processing in plant cell walls. Plant J 59:413–425
Voiniciuc C, Pauly M, Usadel B (2018) Monitoring polysaccharide dynamics in the plant cell wall. Plant Physiol 176:2590–2600. https://doi.org/10.1104/pp.17.01776
Wei HY, Ye YX, Huang HJ, Chen MS, Yang ZX, Chen XM, Zhang CX (2022) Chromosome-level genome assembly for the horned-gall aphid provides insights into interactions between gall-making insect and its host plant. Ecol Evol 12:e8815. https://doi.org/10.1002/ece3.8815
Willats WGT, Marcus SE, Knox JP (1998) Generation of a monoclonal antibody specific to (1–5)-a-L-arabinan. Carbohydr Res 308:149–152. https://doi.org/10.1016/S0008-6215(98)00070-6
Willats WGA, McCartney L, Mackie L, Knox JP (2001) Pectin: cell biology and prospects for functional analysis. Plant Mol Biol 47:9–27. https://doi.org/10.1023/A:1010662911148
Willats WGT, McCartney L, Steele-King CG, Marcus SE, Mort A, Huisman M, Alebeek GV, Schols HA, Voragen AGJ, Le Goff AL, Bonnin E, Thibault J, Knox P (2004) A xylogalacturonan epitope is specifically associated with plant cell detachment. Planta 218:673–681. https://doi.org/10.1007/s00425-003-1147-8
Wolf S, Greiner S (2012) Growth control by cell wall pectins. Protoplasma 249:169–175. https://doi.org/10.1007/s00709-011-0371-5
Wolf S, Mouille G, Pelloux J (2009) Homogalacturonan methyl-esterification and plant development. Mol Plant 2:851–860. https://doi.org/10.1093/mp/ssp066
Xu C, Zhao L, Pan XS, Amaj J (2011) Developmental localization and methylesterification of pectin epitopes during somatic embryogenesis of banana (Musa spp. AAA). PLoS One 6:e22992 https://doi.org/10.1371/journal.pone.0022992
Zandleven J, Beldman G, Bosveld M, Schols HA, Voragen AGJ (2006) Enzymatic degradation studies of xylogalacturonans from apple and potato, using xylogalacturonan hydrolase. Carbohyd Polym 65:495–503
Zykwinska A, Ralet MC, Garnier C, Thibault JF (2005) Evidence for in vitro binding of pectic side chains to cellulose. Plant Physiol 139:397–407. https://doi.org/10.1104/pp.105.065912
Funding
We thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brazil (CAPES) – Finance Code 001, Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (304535/2019–2), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) (APQ-02617–15), for financial support.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have no relevant financial or non-financial interests to disclose.
Competing Interests
There is no competing interest.
Additional information
Communicated by Handling Editor: Alexander Schulz.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Nogueira, R.M., Freitas, M.d.S.C., Picoli, E.A.d.T. et al. Implications of cell wall immunocytochemical profiles on the structural and functional traits of root and stem galls induced by Eriosoma lanigerum on Malus domestica. Protoplasma (2024). https://doi.org/10.1007/s00709-024-01939-w
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00709-024-01939-w