{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T01:45:10Z","timestamp":1760147110834,"version":"build-2065373602"},"reference-count":45,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2023,1,12]],"date-time":"2023-01-12T00:00:00Z","timestamp":1673481600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Conselho Nacional de Desenvolvimento Cient\u00edfico e Tecnol\u00f3gico (CNPq)"},{"name":"Coordena\u00e7\u00e3o de Aperfei\u00e7oamento de Pessoal de N\u00edvel Superior (CAPES)"},{"name":"Funda\u00e7\u00e3o de Amparo \u00e0 Pesquisa do Estado de Minas Gerais (FAPEMIG)"},{"name":"Programa Cooperativo sobre Prote\u00e7\u00e3o Florestal (PROTEF) do Instituto de Pesquisas e Estudos Florestais (IPEF)"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Plants"],"abstract":"<jats:p>The fungus Austropuccinia psidii infects young tissues of Eucalyptus plants until they are two years old in the nursery and field, causing Myrtaceae rust. The characteristics making older eucalypt leaves resistant to A. psidii and the reason for the low levels of this pathogen in older plants need evaluations. The aim of this study was to evaluate the morphological differences between Eucalyptus grandis leaves of different growth stages and two plant ages to propose a visual phenological scale to classify E. grandis leaves according to their maturation stages and to evaluate the time of leaf maturation for young and adult plants. A scale, based on a morphological differentiation for E. grandis leaves, was made. The color, shape and size distinguished the leaves of the first five leaf pairs. Anatomical analysis showed a higher percentage of reinforced tissue, such as sclerenchyma-like tissue and collenchyma, greater leaf blade thickness, absence of lower palisade parenchyma in the mature leaves and a higher number of cavities with essential oils than in younger ones. Changes in anatomical characteristics that could reduce the susceptibility of older E. grandis leaves to A. psidii coincide with the time of developing leaf resistance. Reduced infection of this pathogen in older plants appears to be associated with a more rapid maturation of their leaf tissues.<\/jats:p>","DOI":"10.3390\/plants12020353","type":"journal-article","created":{"date-parts":[[2023,1,12]],"date-time":"2023-01-12T03:11:02Z","timestamp":1673493062000},"page":"353","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Morphoanatomical Changes in Eucalyptus grandis Leaves Associated with Resistance to Austropuccinia psidii in Plants of Two Ages"],"prefix":"10.3390","volume":"12","author":[{"given":"Edson Luiz","family":"Furtado","sequence":"first","affiliation":[{"name":"Departamento de Prote\u00e7\u00e3o Vegetal, Faculdade de Ci\u00eancias Agron\u00f4micas, Universidade Estadual Paulista, Botucatu 18610-034, S\u00e3o Paulo, Brazil"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5505-7678","authenticated-orcid":false,"given":"Andr\u00e9 Costa da","family":"Silva","sequence":"additional","affiliation":[{"name":"Departamento de Fitossanidade, Universidade Federal do Rio Grande do Sul, Porto Alegre 91540-000, Rio Grande do Sul, Brazil"}]},{"given":"\u00c9rica Ara\u00fajo Rodrigues","family":"Silva","sequence":"additional","affiliation":[{"name":"Instituto de Pesquisas e Estudos Florestais (IPEF), Piracicaba 18618-000, S\u00e3o Paulo, Brazil"}]},{"given":"Roberto Ant\u00f4nio","family":"Rodella","sequence":"additional","affiliation":[{"name":"Departamento de Bot\u00e2nica, Instituto de Bioci\u00eancias de Botucatu, Universidade Estadual Paulista, Botucatu 18618-000, S\u00e3o Paulo, Brazil"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8725-3697","authenticated-orcid":false,"given":"Marcus Alvarenga","family":"Soares","sequence":"additional","affiliation":[{"name":"Programa de P\u00f3s-Gradua\u00e7\u00e3o em Produ\u00e7\u00e3o Vegetal, Universidade Federal dos Vales do Jequitinhonha e Mucuri, Diamantina 39100-000, Minas Gerais, Brazil"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0477-4252","authenticated-orcid":false,"given":"Jos\u00e9 Eduardo","family":"Serr\u00e3o","sequence":"additional","affiliation":[{"name":"Departamento de Biologia Geral, Universidade Federal de Vi\u00e7osa, Vi\u00e7osa 36570-900, Minas Gerais, Brazil"}]},{"given":"Cristiane","family":"de Pieri","sequence":"additional","affiliation":[{"name":"Departamento de Prote\u00e7\u00e3o Vegetal, Faculdade de Ci\u00eancias Agron\u00f4micas, Universidade Estadual Paulista, Botucatu 18610-034, S\u00e3o Paulo, Brazil"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2026-281X","authenticated-orcid":false,"given":"Jos\u00e9 Cola","family":"Zanuncio","sequence":"additional","affiliation":[{"name":"Departamento de Entomologia\/BIOAGRO, Universidade Federal de Vi\u00e7osa, Vi\u00e7osa 36570-900, Minas Gerais, Brazil"}]}],"member":"1968","published-online":{"date-parts":[[2023,1,12]]},"reference":[{"key":"ref_1","unstructured":"Alfenas, A.C., Zauza, E.A.V., Mafia, R.G., and Assis, T.F. (2009). Clonagem e Doen\u00e7as do Eucalipto, Editora UFV. [2nd ed]."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1016\/j.foreco.2012.12.030","article-title":"Integrating genetic and silvicultural strategies to minimize abiotic and biotic constraints in Brazilian eucalypt plantations","volume":"301","author":"Alvares","year":"2013","journal-title":"For. Ecol. Manag."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"920","DOI":"10.1016\/j.foreco.2007.09.085","article-title":"Production and carbon allocation in a clonal Eucalyptus plantation with water and nutrient manipulations","volume":"255","author":"Stape","year":"2008","journal-title":"For. Ecol. Manag."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/j.foreco.2013.04.002","article-title":"Selecting for rust (Puccinia psidii) resistance in Eucalyptus grandis in S\u00e3o Paulo State, Brazil","volume":"303","author":"Silva","year":"2013","journal-title":"For. Ecol. Manag."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1007\/s00122-003-1415-9","article-title":"Resistance to rust (Puccinia psidii Winter) in Eucalyptus: Mode of inheritance and mapping of a major gene with RAPD markers","volume":"108","author":"Junghans","year":"2003","journal-title":"Theor. Appl. Genet."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1111\/ppa.12097","article-title":"Screening Corymbia populations for resistance to Puccinia psidii","volume":"63","author":"Pegg","year":"2014","journal-title":"Plant Pathol."},{"key":"ref_7","unstructured":"Walker, J. (2011). New introductions\u2014Doing it right. Developing a Eucalypt Resource, University of Canterbury. Learning from Australia and elsewhere Wood Technology Research Centre."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"e420201","DOI":"10.1590\/1806-90882018000200001","article-title":"Anatomical, ultrastructural, physical and mechanical wood properties of two-year-old Eucalyptus grandis \u00d7 Eucalyptus urophylla clones","volume":"42","author":"Zanuncio","year":"2018","journal-title":"Rev. \u00c1rvore"},{"key":"ref_9","first-page":"227","article-title":"Variabilidade fisiol\u00f3gica de Puccinia psidii Winter em Eucalyptus grandis e no h\u00edbrido urograndis","volume":"31","author":"Furtado","year":"2005","journal-title":"Summa Phytopathol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"819","DOI":"10.1094\/PDIS.1998.82.7.819","article-title":"Eucalyptus Rust: A disease with the potential for serious international implications","volume":"82","author":"Coutinho","year":"1998","journal-title":"Plant Dis."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1007\/s11557-010-0698-x","article-title":"Puccinia psidii infecting cultivated Eucalyptus and native Myrtaceae in Uruguay","volume":"10","author":"Wingfield","year":"2011","journal-title":"Mycol. Prog."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1007\/s11295-012-0572-x","article-title":"Heritability for resistance to Puccinia psidii Winter rust in Eucalyptus grandis Hill ex Maiden in Southwestern Brazil","volume":"9","author":"Miranda","year":"2012","journal-title":"Tree Genet. Genomes"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1831","DOI":"10.1007\/s11738-011-0722-z","article-title":"Leaf gas exchange and chlorophyll a fluorescence of Eucalyptus urophylla in response to Puccinia psidii infection","volume":"33","author":"Alves","year":"2011","journal-title":"Acta Physiol. Plant."},{"key":"ref_14","first-page":"91","article-title":"Ferrugem do Eucalipto","volume":"7","author":"Ferreira","year":"1983","journal-title":"Rev. Arvore"},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Silva-Souza, R.R., Silva, A.C., Rodella, R.A., Serr\u00e3o, J.E., Zanuncio, J.C., and Furtado, E.L. (2017). Pre-infection stages of Austropuccinia psidii in the epidermis of Eucalyptus hybrid leaves with different resistance levels. Forests, 8.","DOI":"10.3390\/f8100362"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"318","DOI":"10.1007\/s40858-015-0043-7","article-title":"Infection process of Puccinia psidii in Eucalyptus grandis leaves of different ages","volume":"40","author":"Xavier","year":"2015","journal-title":"Trop. Plant Pathol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1071\/AP01038","article-title":"Infection of resistant and susceptible Eucalyptus grandis genotypes by urediniospores of Puccinia psidii","volume":"30","author":"Xavier","year":"2001","journal-title":"Australas. Plant Pathol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"484","DOI":"10.1111\/ppa.13145","article-title":"Symptom development and latent period of Austropuccinia psidii (myrtle rust) in relation to host species, temperature, and ontogenic resistance","volume":"69","author":"Beresford","year":"2020","journal-title":"Plant Pathol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1111\/j.1469-8137.2007.02130.x","article-title":"Resistance to pathogens and host developmental stage: A multifaceted relationship within the plant kingdom","volume":"175","author":"Galiana","year":"2007","journal-title":"New Phytol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"118","DOI":"10.1590\/S1982-56762009000200007","article-title":"Influ\u00eancia do est\u00e1dio fenol\u00f3gico e da idade dos trif\u00f3lios de soja na infec\u00e7\u00e3o de Phakopsora pachyrhizi","volume":"34","author":"Furtado","year":"2009","journal-title":"Trop. Plant Pathol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"124","DOI":"10.1590\/S1982-56762010000200009","article-title":"Atividade de quitinases e peroxidases em folhas de eucalipto em diferentes est\u00e1gios de desenvolvimento ap\u00f3s tratamento com acibenzolar-S-metil (ASM) e inocula\u00e7\u00e3o com Puccinia psidii","volume":"35","author":"Boava","year":"2010","journal-title":"Trop. Plant Pathol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"414","DOI":"10.1094\/PDIS-05-19-1002-RE","article-title":"Limonene, a chemical compound related to the resistance of Eucalyptus to Austropuccinia psidii","volume":"104","author":"Silva","year":"2020","journal-title":"Plant Dis."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"641","DOI":"10.1007\/s13313-020-00739-z","article-title":"Changes in leaf chemistry and anatomy of Corymbia citriodora subsp. variegata (Myrtaceae) in response to native and exotic pathogens","volume":"49","author":"Bonora","year":"2020","journal-title":"Australas. Plant Pathol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1002\/j.1537-2197.1973.tb10192.x","article-title":"Classification of architecture of dicotyledonous leaves","volume":"60","author":"Hickey","year":"1973","journal-title":"Am. J. Bot."},{"key":"ref_25","unstructured":"Graf, A.B. (1970). Exotical horticultural color guide. Exotica 3: Pictorial Cyclopedia of Exotic Plants, Roehrs."},{"key":"ref_26","unstructured":"Gerrits, P.O. (1991). The Application of Glycolmetacrylate in Histotechnology; Some Fundamental Principles, LeicaGmbH."},{"key":"ref_27","first-page":"367","article-title":"Polychromatic staining of plant cell walls by Toluidine Blue O","volume":"59","author":"Feder","year":"1964","journal-title":"Protoplasma"},{"key":"ref_28","unstructured":"Sneath, P.H.A.E., and Sokal, R.R. (1973). Numerical Taxonomy, W.H. Freeman."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Hall\u00e9, F., Oldeman, R.A., and Tomlinson, P.B. (1978). Tropical Trees and Forest, Springer-Verlag.","DOI":"10.1007\/978-3-642-81190-6"},{"key":"ref_30","first-page":"51","article-title":"Anatomia foliar de seringueira (Hevea spp.) e desenvolvimento da infec\u00e7\u00e3o por Microcyclus ulei","volume":"30","author":"Sambugaro","year":"2004","journal-title":"Summa Phytopathol."},{"key":"ref_31","unstructured":"Gasparotto, L., and Pereira, J.C.R. (2012). Doen\u00e7as da Seringueira No Brasil, Embrapa."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"954","DOI":"10.1139\/b05-044","article-title":"The relationships among lodging, stem anatomy, degree of lignification, and resistance to mycosphaerella blight in field pea (Pisum sativum)","volume":"83","author":"Banniza","year":"2005","journal-title":"Can. J. Bot."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1850","DOI":"10.1111\/nph.16505","article-title":"Sclerenchyma cell thickening through enhanced lignification induced by OsMYB30 prevents fungal penetration of rice leaves","volume":"226","author":"Li","year":"2020","journal-title":"New Phytol."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Crang, R., and Lyons-Sobaski, S. (2018). Parenchyma, collenchyma, and sclerenchyma. Plant Anatomy (A Concept-Based Approach to the Structure of Seed Plants), Springer-Verlag Press.","DOI":"10.1007\/978-3-319-77315-5"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"39","DOI":"10.3923\/jps.2012.39.54","article-title":"Histological mechanisms of resistance to black pod disease in cacao (Theobroma cacao L.)","volume":"7","author":"Nyadanu","year":"2012","journal-title":"J. Plant Sci."},{"key":"ref_36","first-page":"334","article-title":"Caracter\u00edsticas anat\u00f4micas quantitativas e histopatol\u00f3gica foliar de feijoeiro infectado por Glomella cingulata f. sp. phaseoli","volume":"31","author":"Jerba","year":"2005","journal-title":"Summa Phytopathol."},{"key":"ref_37","unstructured":"Metcalfe, C.R., and Chalk, L. (1979). Anatomy of Dicotyledons, Clarendon Press."},{"key":"ref_38","first-page":"24","article-title":"Studies on the leaf epidermis of rice (Oryza sativa L.)","volume":"1","author":"Sarwar","year":"2002","journal-title":"Indian J. Agric. Res."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"574","DOI":"10.1104\/pp.111.178301","article-title":"Functional characterization of evolutionarily divergent 4-coumarate: Coenzyme a ligases in rice","volume":"157","author":"Gui","year":"2011","journal-title":"Plant Physiol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1978","DOI":"10.3389\/fpls.2018.01978","article-title":"The Eucalyptus cuticular waxes contribute in preformed defense against Austropuccinia psidii","volume":"9","author":"Santos","year":"2019","journal-title":"Front. Plant Sci."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"2166","DOI":"10.1016\/j.foreco.2008.08.008","article-title":"Eucalyptus essential oil as a natural pesticide","volume":"256","author":"Batish","year":"2008","journal-title":"For. Ecol. Manag."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"392","DOI":"10.1590\/S0100-29452011000500050","article-title":"Antibacterial activity of essential oils and extracts on the development of Ralstonia solanacearum in banana seedlings","volume":"33","author":"Amorim","year":"2011","journal-title":"Rev. Bras. De Frutic."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1590\/S1413-70542011000100014","article-title":"Potential of essential oils for the control of brown eye spot in coffee plants","volume":"35","author":"Pereira","year":"2011","journal-title":"Ci\u00eancia E Agrotecnologia"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1016\/j.jspr.2008.10.006","article-title":"Activity of essential oil and its major compound, 1,8-cineole, from Eucalyptus globulus Labill., against the storage fungi Aspergillus flavus Link and Aspergillus parasiticus Speare","volume":"45","author":"Vilela","year":"2009","journal-title":"J. Stored Prod. Res."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"3415","DOI":"10.1007\/s00203-021-02324-4","article-title":"Influence of Mycosphaerella and Teratosphaeria leaf diseases on chemical composition of essential oils of Eucalyptus globulus and effect of these essential oils on ascospores germination","volume":"203","author":"Passador","year":"2021","journal-title":"Arch. Microbiol."}],"container-title":["Plants"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2223-7747\/12\/2\/353\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T18:03:44Z","timestamp":1760119424000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2223-7747\/12\/2\/353"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,1,12]]},"references-count":45,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2023,1]]}},"alternative-id":["plants12020353"],"URL":"https:\/\/doi.org\/10.3390\/plants12020353","relation":{},"ISSN":["2223-7747"],"issn-type":[{"type":"electronic","value":"2223-7747"}],"subject":[],"published":{"date-parts":[[2023,1,12]]}}}