Histopathology of <i>Thecaphora frezzii</i> Colonization: A Detailed Analysis of Its Journey Through Peanut (<i>Arachis hypogaea</i> L.) Tissues

Over the past few decades, peanut smut, caused by <i>Thecaphora frezzii</i>, has evolved from an emerging disease to a major global threat to peanut production. However, critical knowledge gaps persist regarding the anatomical pathways and host responses involved in infection, colonizati...

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Main Authors: María Florencia Romero, Sergio Sebastián Samoluk, José Guillermo Seijo, Ana María Gonzalez
Format: Article
Language:English
Published: MDPI AG 2025-04-01
Series:Plants
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Online Access:https://www.mdpi.com/2223-7747/14/7/1083
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author María Florencia Romero
Sergio Sebastián Samoluk
José Guillermo Seijo
Ana María Gonzalez
author_facet María Florencia Romero
Sergio Sebastián Samoluk
José Guillermo Seijo
Ana María Gonzalez
author_sort María Florencia Romero
collection DOAJ
description Over the past few decades, peanut smut, caused by <i>Thecaphora frezzii</i>, has evolved from an emerging disease to a major global threat to peanut production. However, critical knowledge gaps persist regarding the anatomical pathways and host responses involved in infection, colonization, and sporulation. This study examines the pathosystem and histopathology of the biotrophic phase of <i>T. frezzii</i> in the susceptible cv. Granoleico. Anatomical analyses were conducted using light microscopy, confocal laser scanning, and scanning electron microscopy. Our findings reveal that <i>T. frezzii</i> enters the host through the peg rather than the ovary tip, invading during the R2-subterranean phase. Fruit colonization occurs at the R3-stage when the mechanical layer between the mesocarp and endocarp has not yet formed. Hyphal entry into the seed takes place between the R3-medium and R3-late pod stages via the funiculus, leading to extensive seed coat colonization without penetrating the embryo. Once inside, hyperplasia and hypertrophy are triggered, coinciding with teliospore formation. Teliosporogenesis disrupts nutrient translocation, arresting embryo development. The hyphae colonize tissues intracellularly, utilizing living cells of the vascular bundles and following the peanut’s photoassimilate transport pathway. Investigating these structural responses in phenotypically contrasting peanut genotypes may provide key insights into the anatomical barriers and defense mechanisms that determine disease susceptibility and resistance, ultimately contributing to the development of resistant cultivars.
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spelling doaj-art-20d23647e9f243e893f3c7457f3387522025-08-20T03:03:25ZengMDPI AGPlants2223-77472025-04-01147108310.3390/plants14071083Histopathology of <i>Thecaphora frezzii</i> Colonization: A Detailed Analysis of Its Journey Through Peanut (<i>Arachis hypogaea</i> L.) TissuesMaría Florencia Romero0Sergio Sebastián Samoluk1José Guillermo Seijo2Ana María Gonzalez3Instituto de Botánica del Nordeste (UNNE-CONICET), Facultad de Ciencias Agrarias, Universidad Nacional del Nordeste, Corrientes 3400, ArgentinaInstituto de Botánica del Nordeste (UNNE-CONICET), Facultad de Ciencias Exactas, Naturales y Agrimensura, Universidad Nacional del Nordeste, Corrientes 3400, ArgentinaInstituto de Botánica del Nordeste (UNNE-CONICET), Facultad de Ciencias Exactas, Naturales y Agrimensura, Universidad Nacional del Nordeste, Corrientes 3400, ArgentinaInstituto de Botánica del Nordeste (UNNE-CONICET), Facultad de Ciencias Agrarias, Universidad Nacional del Nordeste, Corrientes 3400, ArgentinaOver the past few decades, peanut smut, caused by <i>Thecaphora frezzii</i>, has evolved from an emerging disease to a major global threat to peanut production. However, critical knowledge gaps persist regarding the anatomical pathways and host responses involved in infection, colonization, and sporulation. This study examines the pathosystem and histopathology of the biotrophic phase of <i>T. frezzii</i> in the susceptible cv. Granoleico. Anatomical analyses were conducted using light microscopy, confocal laser scanning, and scanning electron microscopy. Our findings reveal that <i>T. frezzii</i> enters the host through the peg rather than the ovary tip, invading during the R2-subterranean phase. Fruit colonization occurs at the R3-stage when the mechanical layer between the mesocarp and endocarp has not yet formed. Hyphal entry into the seed takes place between the R3-medium and R3-late pod stages via the funiculus, leading to extensive seed coat colonization without penetrating the embryo. Once inside, hyperplasia and hypertrophy are triggered, coinciding with teliospore formation. Teliosporogenesis disrupts nutrient translocation, arresting embryo development. The hyphae colonize tissues intracellularly, utilizing living cells of the vascular bundles and following the peanut’s photoassimilate transport pathway. Investigating these structural responses in phenotypically contrasting peanut genotypes may provide key insights into the anatomical barriers and defense mechanisms that determine disease susceptibility and resistance, ultimately contributing to the development of resistant cultivars.https://www.mdpi.com/2223-7747/14/7/1083biotrophic fungihistopathologyhost-pathogen interactionpeanut (<i>Arachis hypogaea</i>)peanut smutteliosporogenesis
spellingShingle María Florencia Romero
Sergio Sebastián Samoluk
José Guillermo Seijo
Ana María Gonzalez
Histopathology of <i>Thecaphora frezzii</i> Colonization: A Detailed Analysis of Its Journey Through Peanut (<i>Arachis hypogaea</i> L.) Tissues
Plants
biotrophic fungi
histopathology
host-pathogen interaction
peanut (<i>Arachis hypogaea</i>)
peanut smut
teliosporogenesis
title Histopathology of <i>Thecaphora frezzii</i> Colonization: A Detailed Analysis of Its Journey Through Peanut (<i>Arachis hypogaea</i> L.) Tissues
title_full Histopathology of <i>Thecaphora frezzii</i> Colonization: A Detailed Analysis of Its Journey Through Peanut (<i>Arachis hypogaea</i> L.) Tissues
title_fullStr Histopathology of <i>Thecaphora frezzii</i> Colonization: A Detailed Analysis of Its Journey Through Peanut (<i>Arachis hypogaea</i> L.) Tissues
title_full_unstemmed Histopathology of <i>Thecaphora frezzii</i> Colonization: A Detailed Analysis of Its Journey Through Peanut (<i>Arachis hypogaea</i> L.) Tissues
title_short Histopathology of <i>Thecaphora frezzii</i> Colonization: A Detailed Analysis of Its Journey Through Peanut (<i>Arachis hypogaea</i> L.) Tissues
title_sort histopathology of i thecaphora frezzii i colonization a detailed analysis of its journey through peanut i arachis hypogaea i l tissues
topic biotrophic fungi
histopathology
host-pathogen interaction
peanut (<i>Arachis hypogaea</i>)
peanut smut
teliosporogenesis
url https://www.mdpi.com/2223-7747/14/7/1083
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