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Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

Dynamics of cell wall components and histochemical profile of a rust fungi gall (Basidiomycota: Pucciniales) on Byrsonima variabilis A.Juss. (Malpighiaceae)

Reisila S. Migliorini Mendes A B , Elaine C. Costa A , Lucas C. Oliveira https://orcid.org/0000-0001-5481-1341 A , Flávia M. Gomes B , Denis C. Oliveira C and Rosy M. S. Isaias https://orcid.org/0000-0001-8500-3320 A *
+ Author Affiliations
- Author Affiliations

A Departamento de Botânica, Universidade Federal de Minas Gerais, Instituto de Ciências Biológicas, Avenida Antônio Carlos, 6627, Pampulha. Belo Horizonte, Minas Gerais 31270-901, Brazil.

B Departamento de Ciências Biológicas, Universidade do Estado de Minas Gerais – Unidade Ibirité, Avenida São Paulo, 3996, Vila Rosário, Ibirité, Minas Gerais 32400-000, Brazil.

C Universidade Federal de Uberlândia, Instituto de Biologia, Campus Umuarama, Rua Ceará s/n, Uberlândia, Minas Gerais 38402-018, Brazil.

* Correspondence to: rosy@icb.ufmg.br

Handling Editor: Andrew Denham

Australian Journal of Botany 71(2) 93-109 https://doi.org/10.1071/BT21123
Submitted: 13 October 2021  Accepted: 7 February 2023   Published: 20 March 2023

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Context: An obligate biotrophic parasitism with a rust fungus led to gall formation on Byrsonima variabilis.

Aims: The hypothesis that the host leaf–rust fungi interaction alters the dynamics of plant cell walls and the histochemical profile toward favouring the plant cell-to-fungi cell translocation of metabolites is tested.

Methods: Gall samples were sectioned and submitted to anatomical, histometric, histochemical, and immunocytochemical techniques to evaluate structural alterations and the detection of primary and secondary metabolites, as well as the epitopes of glycoproteins, pectins, and hemicelluloses.

Key results: Fungi gall development results in the hypertrophy of the stomatal chamber and the hyperplasia of epidermis and spongy parenchyma. The cell-to-cell translocation of metabolites from plant mesophyll cells toward the rust fungi gall is favoured by the epitopes of homogalacturonans (HGs) and (1 → 5) α-l-arabinans detected in the hyphae passage sites in the pycnial and aecial stages. The arabinogalactan-proteins (AGPs) may favour mycelial nutrition and differentiation, and cell wall adhesion. HGs and arabinans confer porosity to mesophyll cell walls, which favours the traffic of molecules toward the rust fungi gall.

Conclusions: The unexpected labelling of AGPs, HGs, and arabinans in fungi cell walls is a novelty regarding the plant–fungi interaction. The primary metabolites detected in rust fungi support hyphae growth and spore maturation.

Implications: The immunolabelling of host plant cell wall components on fungi cell walls indicates the integrative role of some plant cell wall components in the biological process of pathogen colonisation in leaf tissues.

Keywords: AGPs, gall anatomy, histochemistry, histometry, immunocytochemistry, pectins, plant–fungi interaction.


References

Aime MC, Bell CD, Wilson AW (2018) Deconstructing the evolutionary complexity between rust fungi (Pucciniales) and their plant hosts. Studies in Mycology 89, 143–152.
Deconstructing the evolutionary complexity between rust fungi (Pucciniales) and their plant hosts.Crossref | GoogleScholarGoogle Scholar |

Albersheim P, Darvill A, Roberts K, Sederoff R, Staehelin A (2011) ‘Plant cell walls: from chemistry to biology.’ (Garland Science: New York, NY, USA) https://doi.org/10.1093/aob/mcr128

Araújo WS, Sobral FL, Maracahipes L (2014) Insect galls of the Parque Nacional das Emas (Mineiros, GO, Brazil). Check List 10, 1445–1451.
Insect galls of the Parque Nacional das Emas (Mineiros, GO, Brazil).Crossref | GoogleScholarGoogle Scholar |

Baker JR (1958) Note on the use of Bromophenol Blue for the histochemical recognition of protein. Journal of Cell Science 99, 459–460.
Note on the use of Bromophenol Blue for the histochemical recognition of protein.Crossref | GoogleScholarGoogle Scholar |

Berndt R, Uhlmann E (2006) New species, reports, observations, and taxonomical changes of southern African rust fungi. Mycological Progress 5, 154–177.
New species, reports, observations, and taxonomical changes of southern African rust fungi.Crossref | GoogleScholarGoogle Scholar |

Bowman SM, Free SJ (2006) The structure and synthesis of the fungal cell wall. BioEssays 28, 799–808.
The structure and synthesis of the fungal cell wall.Crossref | GoogleScholarGoogle Scholar |

Bragança GPP, Alencar CF, Freitas MSC, Isaias RMS (2020) Hemicelluloses and associated compounds determine gall functional traits. Plant Biology 22, 981–991.
Hemicelluloses and associated compounds determine gall functional traits.Crossref | GoogleScholarGoogle Scholar |

Bragança GPP, Ferreira BG, Isaias RMS (2022) Distinct cytological mechanisms for food availability in three Inga ingoides (Fabaceae)—Cecidomyiidae gall systems. Protoplasma 259, 155–162.
Distinct cytological mechanisms for food availability in three Inga ingoides (Fabaceae)—Cecidomyiidae gall systems.Crossref | GoogleScholarGoogle Scholar |

Brundrett MC, Kendrick B, Peterson CA (1991) Efficient lipid staining in plant material with Sudan Red 7B or fluoral yellow 088 in polyethylene glycolglycerol. Biotechnic Histochemistry 66, 111–116.
Efficient lipid staining in plant material with Sudan Red 7B or fluoral yellow 088 in polyethylene glycolglycerol.Crossref | GoogleScholarGoogle Scholar |

Bukatsch F (1972) Bermerkungenzur Doppelfärbung Astrablau-Safranin. Mikrokosmos 61, 255

Carvalho Júnior AA, Hennen JF, Hennen MM, Figueiredo MB (2008) Fungos causadores de ferrugens (Uredinales) em áreas de cerrado no estado de São Paulo, Brasil. Rodriguésia 59, 1–55.
Fungos causadores de ferrugens (Uredinales) em áreas de cerrado no estado de São Paulo, Brasil.Crossref | GoogleScholarGoogle Scholar |

Cassab GI (1998) Plant cell wall proteins. Annual Review of Plant Physiology and Plant Molecular Biology 49, 281–309.
Plant cell wall proteins.Crossref | GoogleScholarGoogle Scholar |

Castilleux R, Plancot B, Gügi B, Attard A, Loutelier-Bourhis C, Lefranc B, Nguema-Ona E, Arkoun M, Yvin JC, Driouich A, Vicré M (2020) Extensin arabinosylation is involved in root response to elicitors and limits oomycete colonization. Annals of Botany 125, 751–763.
Extensin arabinosylation is involved in root response to elicitors and limits oomycete colonization.Crossref | GoogleScholarGoogle Scholar |

Cavalier DM, Oliver L, Neumetzler L, Yamauchi K, Reineck A, Freschour G, Zanbotina OA, Hanh MG, Burgest I, Pauly M, Raikhel NV, Keegstra K (2008) Disrupting two Arabidopsis thaliana xylosyltransferase genes results in plants deficient in xyloglucan, a major primary cell wall component. The Plant Cell 20, 1519–1537.
Disrupting two Arabidopsis thaliana xylosyltransferase genes results in plants deficient in xyloglucan, a major primary cell wall component.Crossref | GoogleScholarGoogle Scholar |

Chen W, Wellings C, Chen X, Kang Z, Liu T (2014) Wheat stripe (yellow) rust caused by Puccinia striiformis f. sp. tritici. Molecular Plant Pathology 15, 433–446.
Wheat stripe (yellow) rust caused by Puccinia striiformis f. sp. tritici.Crossref | GoogleScholarGoogle Scholar |

Clausen MH, Ralet MC, Willats WGT, McCartney L, Marcus SE, Thibault JF, Knox JP (2004) A monoclonal antibody to feruloylated-(1→4)-b-D-galactan. Planta 219, 1036–1041.
A monoclonal antibody to feruloylated-(1→4)-b-D-galactan.Crossref | GoogleScholarGoogle Scholar |

Close DC, McArthur C (2002) Rethinking the role of many plant phenolics – protection from photodamage, not herbivores? Oikos 99, 166–172.
Rethinking the role of many plant phenolics – protection from photodamage, not herbivores?Crossref | GoogleScholarGoogle Scholar |

Coelho MS, Carneiro MAA, Branco CA, Fernandes GW (2013) Gall-inducing insects from Serra do Cabral, Minas Gerais, Brazil. Biota Neotropica 13, 102–109.
Gall-inducing insects from Serra do Cabral, Minas Gerais, Brazil.Crossref | GoogleScholarGoogle Scholar |

Cooper B, Campbell KB, Beard HS, Garrett WM, Islam N (2016) Putative rust fungal effector proteins in infected bean and soybean leaves. Phytopathology 106, 491–499.
Putative rust fungal effector proteins in infected bean and soybean leaves.Crossref | GoogleScholarGoogle Scholar |

Cosgrove DJ (1997) Assembly and enlargement of the primary cell wall in plants. Annual Review of Cell and Developmental Biology 13, 171–201.
Assembly and enlargement of the primary cell wall in plants.Crossref | GoogleScholarGoogle Scholar |

Cosgrove DJ, Jarvis MC (2012) Comparative structure and biomechanics of plant primary and secondary cell walls. Frontiers in Plant Science 3, 204
Comparative structure and biomechanics of plant primary and secondary cell walls.Crossref | GoogleScholarGoogle Scholar |

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. Frontiers in Plant Science 12, 660557
Structural and nutritional peculiarities related to lifespan differences on four Lopesia induced bivalve-shaped galls on the single super-host Mimosa gemmulata.Crossref | GoogleScholarGoogle Scholar |

De Bary A (1866) ‘Morphologie und Physiologie der Pilze, Flechten und Myxomyceten.’ (Wilhelm Engelmann: Leipzig, Königreich Sachsen) Available at https://archive.org/details/morphologieundph00bary [Accessed 21 March 2022]

Edwards HH, Blond MR (2011) Penetration and establishment of Phakopsora pachyrhizi in soybean leaves as observed by transmission electron microscopy. Phytopathology 101, 894–900.
Penetration and establishment of Phakopsora pachyrhizi in soybean leaves as observed by transmission electron microscopy.Crossref | GoogleScholarGoogle Scholar |

Ferreira BG, Bragança GPP, Isaias RMS (2020) Cytological attributes of storage tissues in nematode and eriophyid galls: pectin and hemicellulose functional insights. Protoplasma 257, 229–244.
Cytological attributes of storage tissues in nematode and eriophyid galls: pectin and hemicellulose functional insights.Crossref | GoogleScholarGoogle Scholar |

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 new shape-functional design in galls of Baccharis reticularia (Asteraceae). Protoplasma 250, 899–908.
The role of pectic composition of cell walls in the determination of new shape-functional design in galls of Baccharis reticularia (Asteraceae).Crossref | GoogleScholarGoogle Scholar |

Ganie SA, Ahammed GJ (2021) Dynamics of cell wall structure and related genomic resources for drought tolerance in rice. Plant Cell Reports 40, 437–459.
Dynamics of cell wall structure and related genomic resources for drought tolerance in rice.Crossref | GoogleScholarGoogle Scholar |

Gow NAR, Latge JP, Munro CA (2017) The fungal cell wall: structure, biosynthesis, and function. Microbiology Spectrum 5, 5–3.
The fungal cell wall: structure, biosynthesis, and function.Crossref | GoogleScholarGoogle Scholar |

Guimarães LSP, Hirakata VN (2012) Uso do Modelo de Equações de Estimativas Generalizadas na análise de dados longitudinais. Revista HCPA 32, 503–511. https://www.lume.ufrgs.br/handle/10183/158366

Guimarães ALA, Cruz SMS, Vieira ACM (2014) Structure of floral galls of Byrsonima sericea (Malpighiaceae) induced by Bruggmanniella byrsonimae (Cecidomyiidae, Diptera) and their effects on host plants. Plant Biology 16, 467–475.
Structure of floral galls of Byrsonima sericea (Malpighiaceae) induced by Bruggmanniella byrsonimae (Cecidomyiidae, Diptera) and their effects on host plants.Crossref | GoogleScholarGoogle Scholar |

Hatcher PE (1995) Three-way interactions between plant pathogenic fungi, herbivorous insects and their host plants. Biological Reviews of the Cambridge Philosophical Society 70, 639–694.
Three-way interactions between plant pathogenic fungi, herbivorous insects and their host plants.Crossref | GoogleScholarGoogle Scholar |

Health MC (1997) Signalling between pathogenic rust fungi and resistant or susceptible host plants. Annals of Botany 80, 713–720.
Signalling between pathogenic rust fungi and resistant or susceptible host plants.Crossref | GoogleScholarGoogle Scholar |

Heller A (2020) Host–parasite interaction during subepidermal sporulation and pustule opening in rust fungi (Pucciniales). Protoplasma 257, 783–792.
Host–parasite interaction during subepidermal sporulation and pustule opening in rust fungi (Pucciniales).Crossref | GoogleScholarGoogle Scholar |

Højsgaard S, Halekoh U, Yan J (2006) The R Package geepack for generalized estimating equations. Journal of Statistical Software 15, 1–11.
The R Package geepack for generalized estimating equations.Crossref | GoogleScholarGoogle Scholar |

Johansen DA (1940) ‘Plant microtechnique.’ (McGraw-Hill Book: New York, NY, USA)

Jones L, Seymour GB, Knox JP (1997) Localization of pectic galactan in tomato cell walls using a specific monoclonal antibody for the (1 → 4)-β-d-galactan. Plant Physiology 113, 1405–1412.
Localization of pectic galactan in tomato cell walls using a specific monoclonal antibody for the (1 → 4)-β-d-galactan.Crossref | GoogleScholarGoogle Scholar |

Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. Journal of Cell Biology 27, 137–138.

Kendrick B (2001) Fungi and the history of mycology. In ‘eLS’. (John Wiley & Sons, Ltd) https://doi.org/10.1002/9780470015902.a0002320.pub2

Klose J, De Sá MM, Kronstad JW (2004) Lipid-induced filamentous growth in Ustilago maydis. Molecular Microbiology 52, 823–835.
Lipid-induced filamentous growth in Ustilago maydis.Crossref | GoogleScholarGoogle Scholar |

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 root apices. Planta 181, 512–521.
Pectin esterification is spatially regulated both within cell walls and between developing tissues of root apices.Crossref | GoogleScholarGoogle Scholar |

Kolattukudy PE, Ettinger WF, Sebastian J (1987) Cuticular lipids in plant-microbe interactions. In ‘The metabolism, structure, and function of plant lipids’. (Eds PK Stumpf, JB Mudd, WD Nes) pp. 473–480. (Springer: Boston, MA, USA) https://doi.org/10.1007/978-1-4684-5263-1_86

Kolmer JA, Ordonez ME, Groth JV (2009) ‘The Rust Fungi.’ In ‘eLS’, (John Wiley & Sons, Ltd.: Chichester, UK) https://doi.org/10.1002/9780470015902.a0021264

Kraus JE, Arduin M (1997) ‘Manual Básico de métodos em morfologia vegetal.’ (EDUR [Editora da Universidade Federal Rural do Rio de Janeiro]: Seropédica)

Latgé JP (2007) The cell wall: a carbohydrate armour for the fungal cell. Molecular Microbiology 66, 279–290.
The cell wall: a carbohydrate armour for the fungal cell.Crossref | GoogleScholarGoogle Scholar |

Lenth RV (2021) emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.6.0.90003.. Available at https://github.com/rvlenth/emmeans

Leroux O, Leroux F, Bagniewska-Zadworna A, Knox JP, Claeys M, Bals S, Viane RLL (2011) Ultrastructure and composition of cell wall appositions in the roots of Asplenium (Polypodiales). Micron 42, 863–870.
Ultrastructure and composition of cell wall appositions in the roots of Asplenium (Polypodiales).Crossref | GoogleScholarGoogle Scholar |

Liepman AH, Nairn CJ, Willats WGT, Sorensen I, Roberts AW, Keegstra K (2007) Functional genomic analysis supports conservation of function among cellulose synthase-like a gene family members and suggests diverse roles of mannans in plants. Plant Physiology 143, 1881–1893.
Functional genomic analysis supports conservation of function among cellulose synthase-like a gene family members and suggests diverse roles of mannans in plants.Crossref | GoogleScholarGoogle Scholar |

Lorrain C, Gonçalves dos Santos KC, Germain H, Hecker A, Duplessis S (2019) Advances in understanding obligate biotrophy in rust fungi. New Phytologist 222, 1190–1206.
Advances in understanding obligate biotrophy in rust fungi.Crossref | GoogleScholarGoogle Scholar |

Ma Y, Zeng W, Bacic A, Johnson K (2018) AGPs through time and space. In ‘Annual plant reviews online’. (Ed. JA Roberts), pp. 767–804. (John Wiley & Sons, Ltd) https://doi.org/10.1002/9781119312994.apr0608

Mallory FB (1961) ‘Pathological technique.’ pp. 126–128. (Hafner Publishing Co.: New York, NY, USA)

Mani MS (1964) ‘Ecology of plant galls.’ (Uitgeverij Dr. W. Junk Publishers: Den Haag, Netherlands)

Marcus SE, Verhertbruggen Y, Hervé C, Ordaz-Ortiz JJ, Farkas V, Pedersen HJ, Willats WGT, Knox JP (2008) Pectic homogalacturonan masks abundant sets of xyloglucan epitopes in plant cell walls. BMC Plant Biology 8, 60
Pectic homogalacturonan masks abundant sets of xyloglucan epitopes in plant cell walls.Crossref | GoogleScholarGoogle Scholar |

Marcus SE, Blake AW, Benians TAS, Lee KJD, Poyser C, Donaldson L, Leroux O, Rogowski A, Petersen HL, Boraston A, Gilbert A, Gilbert HJ, Willats WGT, Knox JP (2010) Restricted access of proteins to mannan polysaccharides in intact plant cell walls. The Plant Journal 64, 191–203.
Restricted access of proteins to mannan polysaccharides in intact plant cell walls.Crossref | GoogleScholarGoogle Scholar |

Marques JPR, Soares MKM, Appezzato-Da-Glória B (2013) New staining technique for fungal infected plant tissues. Turkish Journal of Botany 37, 784–787.
New staining technique for fungal infected plant tissues.Crossref | GoogleScholarGoogle Scholar |

Mastroberti AA, Mariath JEA (2008) Developmental of mucilage cells of Araucaria angustifolia (Araucariaceae). Protoplasma 232, 233–245.
Developmental of mucilage cells of Araucaria angustifolia (Araucariaceae).Crossref | GoogleScholarGoogle Scholar |

McCartney L, Ormerod AP, Gidley MJ, Knox JP (2000) Temporal and spatial regulation of pectic (1→4)-β-D-galactan in cell walls of developing pea cotyledons: implications for mechanical properties. The Plant Journal 22, 105–113.
Temporal and spatial regulation of pectic (1→4)-β-D-galactan in cell walls of developing pea cotyledons: implications for mechanical properties.Crossref | GoogleScholarGoogle Scholar |

McCartney L, Marcus SE, Knox JP (2005) Monoclonal antibodies to plant cell wall xylans and arabinoxylans. Journal of Histochemistry & Cytochemistry 53, 543–546.
Monoclonal antibodies to plant cell wall xylans and arabinoxylans.Crossref | GoogleScholarGoogle Scholar |

Mendgen K, Hahn M (2002) Plant infection and the establishment of fungal biotrophy. Trends in Plant Science 7, 352–356.
Plant infection and the establishment of fungal biotrophy.Crossref | GoogleScholarGoogle Scholar |

Meyer J (1987) ‘Plant galls and gall inducers.’ (Gebrüder Bornträger: Stuttgart, Berlin)

Moore-Landecker E (2002) Fungal spores. In eLS, 10.1002/9780470015902.a0000378.pub2

Moreira LRS, Filho EXF (2008) An overview of mannan structure and mannan-degrading enzyme systems. Applied Microbiology and Biotechnology 79, 165–178.
An overview of mannan structure and mannan-degrading enzyme systems.Crossref | GoogleScholarGoogle Scholar |

Nilsson S (Ed.) (1983) ‘Atlas of airborne fungal spores in Europe.’ (Springer-Verlag: Berlin) https://doi.org/10.1007/9783-642-68803-4

Oliveira DC, Isaias RMS (2010) Cytological and histochemical gradients induced by sucking galls insect in galls of Aspidosperma australe Arg. Muell. (Apocynaceae). Plant Science 178, 350–358.
Cytological and histochemical gradients induced by sucking galls insect in galls of Aspidosperma australe Arg. Muell. (Apocynaceae).Crossref | GoogleScholarGoogle Scholar |

Oliveira DC, Carneiro RGS, Magalhães TA, Isaias RMS (2011) Cytological and histochemical gradients on two Copaifera langsdorffii Desf. (Fabaceae) Cecidomyiidae gall systems. Protoplasma 248, 829–837.
Cytological and histochemical gradients on two Copaifera langsdorffii Desf. (Fabaceae) Cecidomyiidae gall systems.Crossref | GoogleScholarGoogle Scholar |

O’Donoghue EM, Sutherland PW (2012) Cell wall polysaccharide distribution in Sandersonia aurantiaca flowers using immuno-detection. Journal of Experimental Botany 249, 843–849.
Cell wall polysaccharide distribution in Sandersonia aurantiaca flowers using immuno-detection.Crossref | GoogleScholarGoogle Scholar |

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 Botanica Brasilica 20, 257–264.
Verniz vitral incolor 500®: uma alternativa de meio de montagem economicamente viável.Crossref | GoogleScholarGoogle Scholar |

Pennell RI, Roberts K (1990) Sexual development in the pea is presaged by altered expression of arabinogalactan protein. Nature 344, 547–549.
Sexual development in the pea is presaged by altered expression of arabinogalactan protein.Crossref | GoogleScholarGoogle Scholar |

Petersen RH (1974) Rust fungus life cycle. The Botanical Review 40, 453–513.
Rust fungus life cycle.Crossref | GoogleScholarGoogle Scholar |

Petre B, Joly DL, Duplessis S (2014) Effector proteins of rust fungi. Frontiers in Plant Science 5, 416
Effector proteins of rust fungi.Crossref | GoogleScholarGoogle Scholar |

Polonio Á, Pérez-García A, Martínez-Cruz J, Fernández-Ortuño D, de Vicente A (2020) The haustorium of phytopathogenic fungi: a short overview of a specialized cell of obligate biotrophic plant parasites. In ‘Progress in Botany’, Vol. 82. (Eds FM Cánovas, U Lüttge, MC Risueño, H Pretzsch) pp. 337–355. (Springer: Cham, Switzerland). https://doi.org/10.1007/124_2020_45

Quilliam RS, Shattock RC (2003) Haustoria of microcyclic rust fungi Uromyces ficariae and Puccinia tumida and other gall-forming species, U. dactylidis (macrocyclic) and P. smyrnii (demicyclic). Plant Pathology 52, 104–113.
Haustoria of microcyclic rust fungi Uromyces ficariae and Puccinia tumida and other gall-forming species, U. dactylidis (macrocyclic) and P. smyrnii (demicyclic).Crossref | GoogleScholarGoogle Scholar |

R Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing. Available at https://www.R-project.org/ [Accessed 12 June 2020]

Sabba RP, Lulai EC (2005) Immunocytological analysis of potato tuber periderm and changes in pectin and extension epitopes associated with periderm maturation. The Journal of the American Society for Horticultural Science 130, 936–942.
Immunocytological analysis of potato tuber periderm and changes in pectin and extension epitopes associated with periderm maturation.Crossref | GoogleScholarGoogle Scholar |

Sass JE (1951) ‘Botanical microtechnique.’ 2nd edn. (Iowa State College Press: Ames, IA, USA) Available at https://archive.org/details/botanicalmicrote00sass [Accessed 12 August 2019]

Scheller HV, Ulvskov P (2010) Hemicelluloses. Annual Review of Plant Biology 61, 263–289.
Hemicelluloses.Crossref | GoogleScholarGoogle Scholar |

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. The Science of Nature 108, 16
Chemical composition of cell wall changes during developmental stages of galls on Matayba guianensis (Sapindaceae): perspectives obtained by immunocytochemistry analysis.Crossref | GoogleScholarGoogle Scholar |

Singh VB (1969) Studies on aecial development in rust fungi: Puccinia polliniae. Canadian Journal of Botany 47, 741–743.
Studies on aecial development in rust fungi: Puccinia polliniae.Crossref | GoogleScholarGoogle Scholar |

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.
Immunochemical comparison of membrane associated and secreted arabinogalactan-proteins in rice and carrot.Crossref | GoogleScholarGoogle Scholar |

Souza ESC, Aime MC, Elias SG, Pinho DB, Miller RNG, Diagnose JC (2018) Crossopsorella, a new tropical genus of rust fungi. Phytotaxa 375, 189–202.
Crossopsorella, a new tropical genus of rust fungi.Crossref | GoogleScholarGoogle Scholar |

Su S, Higashiyama T (2018) Arabinogalactan proteins and their sugar chains: functions in plant reproduction, research methods, and biosynthesis. Plant Reproduction 31, 67–75.
Arabinogalactan proteins and their sugar chains: functions in plant reproduction, research methods, and biosynthesis.Crossref | GoogleScholarGoogle Scholar |

Sun X, Andrew IG, Harris PJ, Hoskin SO, Joblin KN, He Y (2021) Mapping pectic-polysaccharide epitopes in cell walls of forage chicory (Cichorium intybus) leaves. Frontiers in Plant Science 12, 762121
Mapping pectic-polysaccharide epitopes in cell walls of forage chicory (Cichorium intybus) leaves.Crossref | GoogleScholarGoogle Scholar |

Tan L, Mort A (2020) Extensins at the front line of plant defence. A commentary on: ‘Extensin arabinosylation is involved in root response to elicitors and limits oomycete colonization’. Annals of Botany 125, vii–viii.
Extensins at the front line of plant defence. A commentary on: ‘Extensin arabinosylation is involved in root response to elicitors and limits oomycete colonization’.Crossref | GoogleScholarGoogle Scholar |

Toome-Heller M (2016) Latest developments in the research of rust fungi and their allies (Pucciniomycotina). In ‘Biology of microfungi, fungal biology’. (Ed. DW Li) pp. 147–168. (Springer Publishing: Cham, Switzerland) https://doi.org/10.1007/978-3-319-29137-6_7

Ullah A, Rahman L, Yazdani MB, Irfa M, Khan WS, Rehman A (2021) Cell wall polysaccharides. In ‘Polysaccharides: properties and applications’, (Eds Inamuddin, MI Ahamed, R Boddula, T Altalhi) pp. 23–36. (Wiley) https://doi.org/10.1002/9781119711414.ch2

Vanden-Bosch KA, Bradley DJ, Knox JP, Perotto S, Butcher GW, Brewin NJ (1989) Common components of the infection thread matrix and the intercellular space identified by immunocytochemical analysis of pea nodules and uninfected roots. The EMBO Journal 8, 335–342.
Common components of the infection thread matrix and the intercellular space identified by immunocytochemical analysis of pea nodules and uninfected roots.Crossref | GoogleScholarGoogle Scholar |

Vazquez-Cooz I, Meyer R (2002) A differential staining method to identify lignified and unlignified tissues. Biotechnic & Histochemistry 77, 277–282.
A differential staining method to identify lignified and unlignified tissues.Crossref | GoogleScholarGoogle Scholar |

Voegele RT, Mendgen K (2003) Rust haustoria: nutrient uptake and beyond. New Phytologist 159, 93–100.
Rust haustoria: nutrient uptake and beyond.Crossref | GoogleScholarGoogle Scholar |

Weber RWS, Davoli P (2002) Autophagocytosis of carotenoid-rich lipid droplets into vacuoles during aeciospore ageing in Puccinia distincta. New Phytologist 154, 471–479.
Autophagocytosis of carotenoid-rich lipid droplets into vacuoles during aeciospore ageing in Puccinia distincta.Crossref | GoogleScholarGoogle Scholar |

Willats WGT, Knox JP (1996) A role for arabinogalactan-proteins in plant cell expansion: evidence from studies on the interaction of β-glucosyl Yariv reagent with seedlings of Arabidopsis thaliana. The Plant Journal 9, 919–925.
A role for arabinogalactan-proteins in plant cell expansion: evidence from studies on the interaction of β-glucosyl Yariv reagent with seedlings of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Willats WGT, Marcus SE, Knox JP (1998) Generation of monoclonal antibody specific to (1 → 5)-α-l-arabinan. Carbohydrate Research 308, 149–152.
Generation of monoclonal antibody specific to (1 → 5)-α-l-arabinan.Crossref | GoogleScholarGoogle Scholar |

Willats WGT, Limberg G, Buchholt HC, van Alebeek GJ, Benen J, Christensen TMIE, Visser J, Voragen A, Mikkelsen Jørn D, Knox JP (2000) Analysis of pectic epitopes recognised by hybridoma and phage display monoclonal antibodies using defined oligosaccharides, polysaccharides, and enzymatic degradation. Carbohydrate Research 327, 309–320.
Analysis of pectic epitopes recognised by hybridoma and phage display monoclonal antibodies using defined oligosaccharides, polysaccharides, and enzymatic degradation.Crossref | GoogleScholarGoogle Scholar |

Wongsuk T, Pumeesat P, Luplertlop N (2016) Fungal quorum sensing molecules: role in fungal morphogenesis and pathogenicity. Journal of Basic Microbiology 56, 440–447.
Fungal quorum sensing molecules: role in fungal morphogenesis and pathogenicity.Crossref | GoogleScholarGoogle Scholar |

Xu H, Mendgen K (2007) Targeted cell wall degradation at the penetration site of cowpea rust basidiosporelings. Molecular Plant-Microbe Interactions 10, 87–94.
Targeted cell wall degradation at the penetration site of cowpea rust basidiosporelings.Crossref | GoogleScholarGoogle Scholar |

Yates EA, Valdor JF, Haslam SM, Morris HR, Dell A, Mackie W, Knox JP (1996) Characterization of carbohydrate structural features recognized by anti-arabinogalactan-protein monoclonal antibodies. Glycobiology 6, 131–139.
Characterization of carbohydrate structural features recognized by anti-arabinogalactan-protein monoclonal antibodies.Crossref | GoogleScholarGoogle Scholar |