Abstract
The development of plant organs depends on cell division, elongation, structural and chemical changes, and reorganization of cell wall components. As phenotype manipulators, galling insects can manipulate the structure and metabolism of host tissues to build the gall. The gall formation depends on the rearrangement of cell wall components to allow cell growth and elongation, key step for the knowledge regarding gall development, and shape acquisition. Herein, we used an immunocytochemical approach to investigate the chemical composition of the cell wall during the development of galls induced by Bystracoccus mataybae (Eriococcidae) on leaflets of Matayba guianensis (Sapindaceae). Different developmental stages of non-galled leaflets (n = 10) and of leaflet galls (n = 10) were collected from the Cerrado (Brazilian savanna) for anatomical and immunocytochemical analysis. We found that the epitopes of (1 → 4) β-D-galactans and (1 → 5) α-L-arabinans were evident in the tissues of the young and senescent galls. These epitopes seem to be associated with the mechanical stability maintenance and increased gall porosity. As well, the degree of methyl-esterification of pectins changed from the young to the senescent galls and revealed the conservation of juvenile cell and tissue features even in the senescent galls. The extensins detected in senescent galls seem to support their rigidity and structural reinforcement of these bodies. Our results showed a disruption in the pattern of deposition of leaflet cell wall for the construction of M. guianensis galls, with pectin and protein modulation associated with the change of the developmental gall stages.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data and material were produced for the authors of the current article, being original and without being published before. All data are presented in the “Results” section.
Code availability
Not applicable
References
Albersheim P, Darvill A, Roberts K, Sederoff A, Staehelin A (2011) Plant cell walls. Garland Science, Taylor and Francis Group, New York, 430p
Allen C, Tans-Kersten J, Yanfeen G (1998) Ralstonia solanacearum pectin methylesterase is required for growth on methylated pectin but not for bacterial with virulence. Appl Environ Microbiol 64:4918–4923. https://doi.org/10.1128/AEM.64.12.4918-4923.1998
Amar AB, Cobanov P, Ghorbel A, Mliki A, Reustle GM (2010) Involvement of arabinogalactan proteins in the control of cell proliferation of Curcubita pepo suspension cultures. Biol Plantarum 54:321–324. https://doi.org/10.1007/s10535-010-0055-6
Arjyal BP, Katerelos DG, Filiou C, Galiotis C (2000) Measurement and modeling of stress concentration around a circular notch. Exp Mech 40:248–255. https://doi.org/10.1007/BF02327496
Atmodjo MA, Hao Z, Mohnen D (2013) Evolving views of pectin biosynthesis. Ann Ver Plant Biol 64:747–779. https://doi.org/10.1146/annurev-arplant-042811-105534
Belton OS (1997) NMR and the mobility of water in polysaccharide gels. Int J Biol Macromol 21:81–88. https://doi.org/10.1016/S0141-8130(97)00045-7
Bouton S, Leboeuf E, Mouille G, Leydecker MT, Talbotec J, Granier F, Lahaye M, Höfte H, Truong HN (2002) QUASIMODO1 encodes a putative membrane-bound glycosyltransferase required for normal pectin synthesis and cell adhesion in Arabidopsis. Plant Cell 14:2577–2590. https://doi.org/10.1105/tpc.004259
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, 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
Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3:1–30. https://doi.org/10.1111/j.1365-313x.1993.tb00007.x
Cassab GI (1998) Plant cell wall proteins. Annu Rev Plant Physiol Plant Mol Biol 49:281–309. https://doi.org/10.1146/annurev.arplant.49.1.281
Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861. https://doi.org/10.1038/nrm1746
Cosgrove DJ (2016) Catalysts of plant cell wall loosening. F1000Res 5: F1000 Faculty Rev-119. https://doi.org/10.12688/f1000research.7180.1
Drakakaki G (2015) Polysaccharide deposition during cytokinesis: challenges and future perspectives. Plant Sci 236:177–184. https://doi.org/10.1016/j.plantsci.2015.03.018
Ferreira BG, Álvarez R, Bragança GP, Alvarenga DR, Pérez-Hidalgo N, Isaias RMS (2019) Feeding and other gall facets: patterns and determinants in gall structure. Bot Rev 85:78–106. https://doi.org/10.1007/s12229-019-09207-w
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
Gao M, Showalter AM (2000) Immunolocalization of LeAGP-1, a modulator arabinogalactan protein, reveals its developmentally regulated expression in tomato. Planta 210:865–874. https://doi.org/10.1007/s004250050691
Giannoutsou E, Sotiriou P, Apostolakos P, Galatis B (2013) Early local differentiation of the cell wall matrix defines the contact sites in lobed mesophyll cells of Zea mays. Ann Bot 112:1067–1081. https://doi.org/10.1093/aob/mct175
Isaias RMS, Oliveira DC, Carneiro RGS, Kraus JE (2014) Developmental anatomy of galls in the neotropics, arthropods stimuli versus host plant constraints. In: Fernandes GW, Santos JC (eds) Neotropical insect galls. Springer, Netherlands, pp 15–34
Jarvis MC, Briggs SPH, Knox JP (2003) Intercellular adhesion and cell separation in plants. Plant Cell Environ 26:977–989. https://doi.org/10.1046/j.1365-3040.2003.01034.x
Jones L, Seymour GB, Knox JP (1997) Localization of pecticgalactan in tomato cell walls using a monoclonal antibody specific to (1R4) b-D-galactan. Plant Physiol 113:1405–1412. https://doi.org/10.1104/pp.113.4.1405
Jones L, Milne JL, Ashford D, McQueen-Mason SJ (2003) Cell wall arabinan is essential for guard cell function. Proc Natl Acad Sci USA 100:11783–11788. https://doi.org/10.1073/pnas.1832434100
Knox JP, Linstead PJ, King J, Cooper C, Roberts K (1990) Pectin esterification is spatially regulated both within cell walls and between developing tissues of roots apices. Planta 181:512–521. https://doi.org/10.1007/BF00193004
Lamport DTA, Kieliszewski MJ, Showalter AM (2006) Salt stress upregulates periplasma arabinogalactan proteins, using salt stress to analyse AGP function. New Phytol 169:479–492. https://doi.org/10.1111/j.1469-8137.2005.01591.x
Lewis NG, Yamamoto E (1990) Lignin: occurrence, biogenesis and biodegradation. Ann Rev Plant Physiol Plant Mol Biol 41:455–496. https://doi.org/10.1146/annurev.pp.41.060190.002323
Magalhães TA, Oliveira DC, Suzuki AY, Isaias RMS (2014) Patterns of cell elongation in the determination of the final shape in galls of Baccharopelma dracunculifoliae (Psyllidae) on Baccharis dracunculifolia DC (Asteraceae). Protoplasma 251:747–753. https://doi.org/10.1007/s00709-013-0574-z
Majewska-Sawka A, Nothnagel EA (2000) The multiple roles of arabinogalactan proteins in plant development. Plant Physiol 122:3–9. https://doi.org/10.1104/pp.122.1.3
Mani MS (1964) Ecology of plant galls. Dr. W. Junk Publishers, The Hague, 434p
Martini VC, Moreira ASFP, Kuster 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 Bras de Bot 31:1–13. https://doi.org/10.1590/S0100-84042008000100002
Meijer M, Murray JAH (2001) Cell cycle controls and the development of plant form. Curr Opin Plant Biol 4:44–49. https://doi.org/10.1016/S1369-5266(00)00134-5
Mohnen D (2008) Pectin structure and biosynthesis. Curr Opin Plant Biol 11:266–277. https://doi.org/10.1016/j.pbi.2008.03.006
Oliveira DC, Magalhães TA, Carneiro RGS, Alvim MN, Isaias RMS (2010) Do Cecidomyiidae galls of Aspidosperma spruceanum (Apocynaceae) fit the preestablished cytological and histochemical patterns? Protoplasma 242:81–93. https://doi.org/10.1007/s00709-010-0128-6
Oliveira DC, Magalhães TA, Ferreira BG, Teixeira CT, Formiga AT, Fernandes GW, Isaias RMS (2014) Variation in the degree of pectin methylesterification during the development of Baccharis dracunculifolia kidney-shaped gall. PLoS One 9:94588. https://doi.org/10.1371/journal.pone.0094588
Oliveira DC, Isaias RMS, Fernandes GW, Ferreira BG, Carneiro RGS, Fuzaro L (2016) 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. https://doi.org/10.1016/j.jinsphys.2015.11.012
Ordaz-Ortiz JJ, Marcus SE, Knox JP (2009) Cell wall microstructure analysis implicates hemicellulose polysaccharides in cell adhesion in tomato fruit pericarp parenchyma. Mol Plant 2:910–921. https://doi.org/10.1093/mp/ssp049
Orfila C, Knox JP (2000) Spatial regulation of pectic polysaccharides in relation to pit fields in cell walls of tomato fruit pericarp. Plant Physiol 122:775–781. https://doi.org/10.1104/pp.122.3.775
Orfila C, Seymour GB, Willats WGT et al (2001) Altered middle lamella homogalacturonan and disrupted deposition of (1→5) -alpha-L-arabinan in the pericarp of Cnr, a ripening mutant of tomato. Plant Physiol 126:210–221. https://doi.org/10.1104/pp.126.1.210
Pfeffer L, Rezende UC, Baronio GJ, Oliveira DC (2018) Building two houses on a single host plant: galling insect synchronizes its life cycle with plant phenology. Oecol Aust 22:438–448. https://doi.org/10.4257/oeco.2018.2204.07
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
Rose JC (2003) The plant cell wall. Blackwell, Garsington Road, Oxford. Ann Bot 94:645. https://doi.org/10.1093/aob/mch185
Sabba RP, Lulai EC (2005) Immunocytological analysis of potato tuber periderm and changes in pectin and extension epitopes associated with periderm maturation. J Am Soc Hortic Sci 130:936–942. https://doi.org/10.21273/JASHS.130.6.936
Sano SM, Almeida SP, Ribeiro JF (2008) Cerrado: Ecologia e flora. Embrapa, Brasília
Sarkar P, Bosneaga E, Auer M (2009) Plant cell walls throughout evolution: towards a molecular understanding of their design principles. J Exp Bot 60:3615–3635. https://doi.org/10.1093/jxb/erp245
Seifert GJ, Roberts K (2007) The biology of Arabinogalactan proteins. Ann Rev Plant Biol 58:137–161. https://doi.org/10.1146/annurev.arplant.58.032806.103801
Shorthouse JD, Wool D, Raman A (2005) Gall-inducing insects–nature’s most sophisticated herbivores. Basic Appl Ecol 6:407–411. https://doi.org/10.1016/j.baae.2005.07.001
Silva AFM, Kuster VC, Rezende UC, Oliveira DC (2019) The early developmental stages of gall-inducing insects define final gall structural and histochemical profiles: the case of Bystracoccus mataybae galls on Matayba guianensis. Botany. https://doi.org/10.1139/cjb-2019-0017
Singleton VL, Orthofer R, Lamuela-Raventos RM (1999) Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Methods Enzymol 299:152–178. https://doi.org/10.1016/S0076-6879(99)99017-1
Smallwood M, Yates EA, Willats WGA, Martin H, Knox JP (1996) Immunochemical comparison of membrane associated and secreted arabinogalactan-proteins in rice and carrot. Planta 198:452–459. https://doi.org/10.1007/BF00620063
Sotiriou P, Giannoutsou E, Panteris E, Apostolakos P, Galatis B (2016) Cell wall matrix polysaccharide distribution and cortical microtubule organization: two factors controlling mesophyll cell morphogenesis in land plants. Ann Bot 117:401–419. https://doi.org/10.1093/aob/mcv187
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 floribundusSpreng. (Euphorbiaceae). Botany 96:9–18. https://doi.org/10.1139/cjb-2017-0123
Verhertbruggen Y, Marcus SE, Haeger A, Ordaz-Ortiz J, Knox JP (2009) An extend set of monoclonal antibodies to pectichomogalacturonan. Carbohydr Res 344:1858–1862. https://doi.org/10.1016/j.carres.2008.11.010
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
Willats WGT, McCartney L, Mackie W, 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 et al (2004) Axylogalacturonan epitope is specifically associated with plant cell detachment. Planta 218:673–681. https://doi.org/10.1007/s00425-003-1147-8
Williats WGA, Marcus SE, Knox JP (1998) Generation of monoclonal antibody specific to (1–5) -α-L-arabian. Carbohydr Res 308:149–152. https://doi.org/10.1016/S0008-6215(98)00070-6
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
Wydra K, Beri H (2006) Structural changes of homogalacturonan, rhamnogalacturonan I and arabinogalactan protein in xylem cell walls of tomato genotypes in reaction to Ralstonia solanacearum. Physiol Mol Plant Pathol 68:41–50. https://doi.org/10.1016/j.pmpp.2006.06.001
Yates EA, Valdor JF, Haslam SM, Dell A, Mackie W, Knox JP (1996) Characterization of carbohydrate structural features recognized by anti-arabinogalactan-protein monoclonal antibodies. Glycobiology 6:131–139. https://doi.org/10.1093/glycob/6.2.131
Funding
This study was financed in part by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brazil (CAPES) finance code 001 and Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG). The Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) granted the fellowship to D.C. Oliveira.
Author information
Authors and Affiliations
Contributions
DCO and AFMS conceived and designed the research. AFMS, LGL, VCK, and DCO conducted the immunocytochemistry experiments. AFMS and VCK assembled and formatted the figures. AFMS, NCMS, VCK, and DCO wrote the manuscript.
Corresponding author
Ethics declarations
Ethics approval
Not applicable
Consent to participate
All authors consent the participation.
Consent for publication
All authors consent the publication of the current article.
Conflict of interest
The authors declare no competing interests.
Additional information
Communicated by Communicated by: Łukasz Stępień .
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
de Melo Silva, A.F., Lana, L.G., Kuster, V.C. et al. Chemical composition of cell wall changes during developmental stages of galls on Matayba guianensis (Sapindaceae): perspectives obtained by immunocytochemistry analysis. Sci Nat 108, 16 (2021). https://doi.org/10.1007/s00114-021-01732-2
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00114-021-01732-2