Agricultural and Biological Sciences, Plant Science, Biotechnology, Molecular Biology
152
Scopus Publications
3250
Scholar Citations
33
Scholar h-index
91
Scholar i10-index
Scopus Publications
Fungal Effectors in Biotrophic, Necrotrophic and Hemibiotrophic Pathosystems: A Systematic Review Taís Araújo Santos, Darília Christiane Bomfim de Rezende, Ariana Silva Santos, Carlos Priminho Pirovani Plant Pathology, 2026 Fungal phytopathogens are responsible for numerous plant diseases that result in substantial agricultural losses worldwide. To establish successful infections, fungi secrete effector proteins that facilitate host colonisation and nutrient acquisition. This systematic review summarises the mechanisms of action of fungal effectors in biotrophic, necrotrophic and hemibiotrophic pathosystems. A total of 2979 publications were initially identified, while after screening and data extraction 184 studies were included in the analysis. All told, we compiled 222 secreted effector proteins by 50 fungal pathogens. Of these, 38% originated from biotrophic fungi, 36% from hemibiotrophs and 22% from necrotrophs. The predominant mechanism among biotrophic effectors is the suppression of plant immunity (44 effectors), particularly through the inhibition of programmed cell death and pattern‐triggered immunity (PTI) responses. In contrast, necrotrophic fungi rely on 13 effectors that promote host cell death, whereas hemibiotrophs employ a diverse array of effectors, with 20 implicated as enhancing pathogen growth and virulence. In terms of subcellular localisation, 46% of the effectors act in the apoplast and 54% in the host cytoplasm. Apoplastic effectors contribute to fungal cell wall protection and inhibit plant defence‐related enzymes such as proteases and chitinases. Cytoplasmic effectors target intracellular components, modulating defence signalling pathways. Notably, the ascomycete Magnaporthe oryzae has the highest number of functionally characterised effectors, while basidiomycete pathogens remain underexplored in this regard. This review enhances understanding of effector biology in diverse fungal lifestyles and provides a valuable foundation for future research on plant–fungal interactions and disease management strategies.
Enzymatic and proteomic changes in resistant and susceptible cacao cultivars reveal distinct response mechanisms to Phytophthora citrophthora infection Angra Paula Bomfim Rêgo, Irma Yuliana Mora-Ocampo, Elza Thaynara Cardoso de Menezes Assis, Márcia Christina da Silva Branco, Edna Dora Martins Newman Luz, et al. Frontiers in Plant Science, 2026 Black pod rot, caused by Phytophthora species, is one of the most severe diseases affecting cocoa production. Among these species, P. citrophthora is considered one of the most aggressive, yet little is known about the molecular responses of cocoa to this pathogen. This study aimed to investigate the defense mechanisms of cacao against P. citrophthora through enzymatic analyses and gel-free comparative proteomics. Seedlings obtained by rooting cuttings from one resistant and one susceptible cultivar were inoculated with the pathogen, while controls received sterile distilled water. The activities of ascorbate peroxidase (APX), guaiacol peroxidase (GPX), catalase (CAT), and superoxide dismutase (SOD) were measured at 6, 12, 18, and 24 hours after inoculation (HAI). Protein abundance was evaluated at 24 HAI using mass spectrometry. The pathogen induced GPX activity from 6 HAI in the resistant and from 12 HAI in the susceptible cultivar, while APX activity increased in both cultivars after 18 HAI. A total of 1,583 proteins were identified across treatments. In the resistant cultivar, infection was associated with reduced photosynthesis, redirection of carbohydrate metabolism, and changes in the ascorbate/dehydroascorbate ratio, suggesting an efficient activation of defense responses. Constitutively abundant proteins related to antioxidant activity may also have contributed to resistance. In contrast, the susceptible cultivar showed limited protein abundance changes, with indications of increased metabolism of small molecules and accumulation of methylglyoxal, a cytotoxic compound linked to disease susceptibility. Overall, the results demonstrate that the resistant cultivar mobilizes early antioxidant defenses and metabolic reprogramming to cope with infection, whereas the susceptible exhibits inefficient responses leading to cellular damage. These findings provide new insights into cacao- P. citrophthora interactions, offer a foundation for future transcription-level studies, and may support the development of new pre-breeding stages for cacao cultivars.
Identification of Subtle Differences in the Physiological Quality of Commercial Soybean Seed Lots Using Shotgun Proteomics During Germination Fellipe Ramos Sampaio, Irma Yuliana Mora-Ocampo, Fredy Davi Albuquerque Silva, Kevein Ruas Oliveira, Carlos Priminho Pirovani, et al. Agronomy, 2025 Soybean seeds with similar germination rates may exhibit subtle differences in physiological quality, influencing field performance and storage longevity. This study used a shotgun proteomics approach to characterize the proteomic profile of two commercial soybean seed lots (higher- and lower-quality) during germination, aiming to identify biomarkers associated with vigor and deterioration. Proteins were analyzed across three germination phases: imbibition (Phase I, 0.5 h), metabolic activation (Phase II, 20 h), and radicle protrusion (Phase III, 51 h). A total of 777 proteins were identified, and of these differentially abundant proteins (DAPs), the following totals were detected: 12 in Phase I, 17 in Phase II, and 28 in Phase III. In Phase I, ribosomal proteins were more abundant in high-quality seeds, indicating efficient translation and preparation for germination. Conversely, in Phase III, low-quality seeds showed increased levels of storage proteins and stress-response proteins, including alcohol dehydrogenase (ADH), heat shock proteins, and annexins, reflecting delayed germination and more deterioration. These findings highlight the dynamic nature of protein expression during germination and demonstrate the potential of proteomics to detect subtle differences in physiological quality. The identified biomarkers provide insights for seed quality assessment and offer practical applications for improving classification and management of commercial soybean seed lots.
Proteomic Analysis of Plants with Binding Immunoglobulin Protein Overexpression Reveals Mechanisms Related to Defense Against Moniliophthora perniciosa Grazielle da Mota Alcântara, Gláucia Carvalho Barbosa Silva, Irma Yuliana Mora Ocampo, Amanda Araújo Kroger, Rafaelle Souza de Oliveira, et al. Plants, 2025 Moniliophthora perniciosa is one of the main pathogens affecting cocoa, and controlling it generally involves planting resistant genotypes followed by phytosanitary pruning. The identification of plant genes related to defense mechanisms is crucial to unravel the molecular basis of plant–pathogen interactions. Among the candidate genes, BiP stands out as a molecular chaperone located in the endoplasmic reticulum that facilitates protein folding and is induced under stress conditions, such as pathogen attacks. In this study, the SoyBiPD gene was expressed in Solanum lycopersicum plants and the plants were challenged with M. perniciosa. The control plants exhibited severe symptoms of witches’ broom disease, whereas the transgenic lines showed no or mild symptoms. Gel-free proteomics revealed significant changes in the protein profile associated with BiP overexpression. Inoculated transgenic plants had a higher abundance of resistance-related proteins, such as PR2, PR3, and PR10, along with increased activity of antioxidant enzymes, including superoxide dismutase (SOD), catalase (CAT), guaiacol peroxidase, and fungal cell wall-degrading enzymes (glucanases). Additionally, transgenic plants accumulated less H2O2, indicating more efficient control of reactive oxygen species (ROS). The interaction network analysis highlighted the activation of defense-associated signaling and metabolic pathways, conferring a state of defensive readiness even in the absence of pathogens. These results demonstrate that BiP overexpression increases the abundance of defense proteins, enhances antioxidant capacity, and confers greater tolerance to biotic stress. This study demonstrates the biotechnological potential of the BiP gene for genetic engineering crops with increased resistance to economically important diseases, such as witches’ broom in cocoa.
The BASIDIN effector of the fungus Moniliophthora perniciosa promotes positive effects on the seed germination and seedlings development of Lactuca sativa Keilane Silva Farias, Monaliza Macêdo Ferreira, Ivina Barbosa De Oliveira, Ronaldo José Durigan Dalio, Carlos Priminho Pirovani Frontiers in Plant Science, 2025 Plant resistance inducers that activate plant defense mechanisms may be useful in reducing agrotoxic use. Lettuce is among the most economically important leafy vegetable crops in the world. Since lettuce propagates through seeds, the use of high-quality seeds is extremely important for establishing the crop. Several studies have demonstrated the potential of alternative methods of seed treatment with the aim of increasing productivity. Based on this premise, we tested the effect of the rBASIDIN effector regarding its ability to induce germination and physiological changes in lettuce seedlings through seed treatment. The seeds were treated for 30 min by soaking with 50 µg mL-1, 75 µg mL-1 and 100 µg mL-1 of the recombinant effector protein rBASIDIN. Seeds treated with distilled water and 10 mmol of Tris-HCl served as controls. The physiological parameters evaluated were germination percentage at 4 and 7 days, seedling length (aerial part and root), dry and fresh mass, electrical conductivity, and enzymatic activity. Seeds treated with 50 and 75 µg mL-1 of rBASIDIN germinated earlier than the controls. Treatment with rBASIDIN at a concentration of 50 µg mL-1 resulted in seedlings with an average root length of 1.51 cm, while the average lengths of the controls (H2O and buffer) were 0.86 and 0.70 cm respectively. Seed treatment with rBASIDIN caused an increase in the fresh and dry weight of the plants. The lowest electrolyte leakage was detected in seeds treated with the three concentrations of rBASIDIN compared to the controls. Regarding the activity of defense enzymes, seedlings treated with rBASIDIN at lower concentrations showed higher chitinase and β-glucanase activity compared to the controls. The results indicated that the rBASIDIN effector plays an important signaling role in lettuce seeds, since small doses are already sufficient to induce changes in physiological parameters to obtain more vigorous plants.
The family of glutathione peroxidase proteins and their role against biotic stress in plants: a systematic review Maria Luíza do Carmo Santos, Ariana Silva Santos, Diogo Pereira Silva de Novais, Natasha dos Santos Lopes, Carlos Priminho Pirovani, et al. Frontiers in Plant Science, 2025 IntroductionGlutathione peroxidases (GPXs) are extensively studied for their indispensable roles in eliminating reactive oxygen species by catalyzing the reduction of hydrogen peroxide or lipid peroxides to prevent cell damage. However, knowledge of GPXs in plants still has many gaps to be filled. Thus, we present the first systematic review (SR) aimed at examining the function of GPXs and their protective role against cell death in plants subjected to biotic stress.MethodsTo guide the SR and avoid bias, a protocol was developed that contained inclusion and exclusion criteria based on PRISMA guidelines. Three databases (PubMed, Science Direct, and Springer) were used to identify relevant studies for this research were selected.ResultsA total of 28 articles related to the proposed objective. The results highlight the importance of GPXs in plant defense against biotic stress, including their role in protecting against cell death, similar to the anti-apoptotic GPXs in animals. Data from gene expression and protein accumulation studies in plants under various biotic stresses reveal that GPXs can both increase resistance and susceptibility to pathogens. In addition to their antioxidant functions, GPXs act as sensors and transmitters of H2O2 signals, integrating with the ABA signaling pathway during stress.DiscussionThese findings show that GPXs delay senescence or reinforce physical barriers, thereby modulating resistance or susceptibility to pathogens. Additionally, their functions are linked to their cellular localization, which demonstrates an evolutionary relationship between the studied isoforms and their role in plant defense. This information broadens the understanding of molecular strategies involving GPX isoforms and provides a foundation for discussions and actions aimed at controlling necrotrophic and/or hemibiotrophic pathogens.
Protium heptaphyllum , a tree native to the Atlantic Forest, is a potential source of compounds against important cocoa phytopathogen CFP Bandeira, J Velasques, GB Santos, CAL Cardoso, VR Rocha, ... Scientific Reports , 2026 2026
Enzymatic and proteomic changes in resistant and susceptible cacao cultivars reveal distinct response mechanisms to Phytophthora citrophthora infection APB Rêgo, IY Mora-Ocampo, ETCM Assis, MCS Branco, EDMN Luz, ... Frontiers in Plant Science 17, 1718408 , 2026 2026
Fungal Effectors in Biotrophic, Necrotrophic and Hemibiotrophic Pathosystems: A Systematic Review TA Santos, DCB de Rezende, AS Santos, CP Pirovani Plant Pathology 75 (1), e70071 , 2026 2026 Citations: 2
Modulation of proteome profile of banana (Musa spp.) under water deficit AS Santos, AS Santos, N de Almeida Santos, MA Coelho Filho, ... 2025
Proteomic and transcriptional regulations in Theobroma cacao L., in response to Ni toxicity, reveal temporal and metabolic reprogramming JV dos Santos Silva, VC Baligar, D Ahnert, CP Pirovani, IY Mora-Ocampo, ... Journal of Hazardous Materials 495, 138971 , 2025 2025 Citations: 1
Expression of an Eucalyptus grandis Xyloglucan endoglycosylase gene in Nicotiana tabacum confers tolerance to abiotic stress ETC de Menezes Assis, MT Aguilar Quisbert, D Bispo Oliveira, ... Plant Cell, Tissue and Organ Culture (PCTOC) 162 (2), 28 , 2025 2025
Candidate effector proteins revealed by transcriptional profiling during development of Moniliophthora roreri, a fungal pathogen of Theobroma cacao KTS de Nascimento, ÍS Lopes, AS Santos, IY Mora-Ocampo, TA Santos, ... Genomics, 111083 , 2025 2025 Citations: 2
Potential effect of Wolbachia on virus restriction in the spider mite T. truncatus LYM Ferreira, JPN Santos, DGN Souza, LCB Orellana, SF de Santana, ... Frontiers in Microbiology 16, 1570606 , 2025 2025 Citations: 2
Identification of subtle differences in the physiological quality of commercial soybean seed lots using shotgun proteomics during germination FR Sampaio, IY Mora-Ocampo, FDA Silva, KR Oliveira, CP Pirovani, ... Agronomy 15 (3), 609 , 2025 2025 Citations: 3
The family of glutathione peroxidase proteins and their role against biotic stress in plants: a systematic review ML do Carmo Santos, A Silva Santos, D Pereira Silva de Novais, ... Frontiers in Plant Science 16, 1425880 , 2025 2025 Citations: 20
Proteomic Analysis of Plants with Binding Immunoglobulin Protein Overexpression Reveals Mechanisms Related to Defense Against Moniliophthora perniciosa GM Alcântara, GCB Silva, IYM Ocampo, AA Kroger, RS de Oliveira, ... Plants 14 (4), 503 , 2025 2025 Citations: 3
The BASIDIN effector of the fungus Moniliophthora perniciosa promotes positive effects on the seed germination and seedlings development of Lactuca sativa KS Farias, MM Ferreira, IB De Oliveira, RJD Dalio, CP Pirovani Frontiers in Plant Science 16, 1529096 , 2025 2025 Citations: 3
Proteomic Analyzes of Plants with BiP Overexpression Reveal Mechanisms Related to Defense Against Moniliophthora perniciosa GDM Alcântara¹, GB Silva, IYM Ocampo, AA Kroger, RS de Oliveira, ... Preprints , 2025 2025
Análise de proteínas de leucócitos polimorfonucleares de gatos domésticos GMS de Oliveira, IYM Ocampo, CP Pirovani, JLM Varjão, AD Munhoz Semina: Ciências Agrárias 45 (6), 1873-1890 , 2024 2024
Recombinant SAG2A Protein from Toxoplasma gondii Modulates Immune Profile and Induces Metabolic Changes Associated with Reduced Tachyzoite Infection in … TAR Santos, MC Oliveira, EMA Silva, UR Dos Santos, MM Ferreira, ... Microorganisms 12 (11), 2366 , 2024 2024 Citations: 1
Protein analysis of polymorphonuclear leukocytes from domestic cats GMS de Oliveira, IYM Ocampo, CP Pirovani, JLM Varjao, AD Munhoz SEMINA-CIENCIAS AGRARIAS 45 (6), 1873-1890 , 2024 2024
Cloning, heterologous expression and characterization of β-glucosidase deriving from Moniliophthora perniciosa (Stahel) Aime and Phillips Mora AB Vitor, KS Farias, GCA Ribeiro, CP Pirovani, RG Benevides, ... 3 Biotech 14 (11), 287 , 2024 2024 Citations: 1
In vitro leishmanicidal activity of Hancornia speciosa latex against Leishmania (Leishmania) amazonensis JO Castro, D de Sousa Lopes, SL Capim, PM de Souza, ... Phytomedicine Plus 4 (4), 100658 , 2024 2024 Citations: 2
Spiroplasma shows a Wolbachia-like effect in hampering virus replication in spider mite LYM Ferreira, JPN Santos, DG do Nascimento Souza, LCB Orellana, ... 2024
MOST CITED SCHOLAR PUBLICATIONS
Photosynthetic, antioxidative, molecular and ultrastructural responses of young cacao plants to Cd toxicity in the soil RP de Araújo, AAF de Almeida, LS Pereira, PAO Mangabeira, JO Souza, ... Ecotoxicology and Environmental Safety 144, 148-157 , 2017 2017 Citations: 163
Protein extraction for proteome analysis from cacao leaves and meristems, organs infected by Moniliophthora perniciosa , the causal agent of the witches' broom … CP Pirovani, HAS Carvalho, RCR Machado, DS Gomes, FC Alvim, ... Electrophoresis 29 (11), 2391-2401 , 2008 2008 Citations: 125
Comparative proteomic analysis of antimony-resistant and-susceptible Leishmania braziliensis and Leishmania infantum chagasi lines FSV Matrangolo, DB Liarte, LC Andrade, MF de Melo, JM Andrade, ... Molecular and biochemical parasitology 190 (2), 63-75 , 2013 2013 Citations: 120
Physiological and biochemical responses of Theobroma cacao L. genotypes to flooding FZ Bertolde, AAF Almeida, CP Pirovani, FP Gomes, D Ahnert, VC Baligar, ... Photosynthetica 50 (3), 447-457 , 2012 2012 Citations: 97
Molecular, Physiological and Biochemical Responses of Theobroma cacao L. Genotypes to Soil Water Deficit IC Santos, AAF Almeida, D Anhert, AS Conceição, CP Pirovani, JL Pires, ... PloS one 9 (12), e115746 , 2014 2014 Citations: 91
Hydrogen peroxide formation in cacao tissues infected by the hemibiotrophic fungus Moniliophthora perniciosa CV Dias, JS Mendes, AC Dos Santos, CP Pirovani, A da Silva Gesteira, ... Plant Physiology and Biochemistry 49 (8), 917-922 , 2011 2011 Citations: 78
Use of response surface methodology to examine chitinase regulation in the basidiomycete Moniliophthora perniciosa MA Lopes, DS Gomes, MGB Koblitz, CP Pirovani, JC de Mattos Cascardo, ... mycological research 112 (3), 399-406 , 2008 2008 Citations: 71
Thermoresistant xylanases from Trichoderma stromaticum: application in bread making and manufacturing xylo-oligosaccharides EA Carvalho, LM dos Santos Góes, APT Uetanabaro, EGP da Silva, ... Food chemistry 221, 1499-1506 , 2017 2017 Citations: 68
Morphological, biochemical, molecular and ultrastructural changes induced by Cd toxicity in seedlings of Theobroma cacao L. AV Castro, AAF de Almeida, CP Pirovani, GSM Reis, NM Almeida, ... Ecotoxicology and Environmental Safety 115, 174-186 , 2015 2015 Citations: 65
The pathogenesis-related protein PR-4b from Theobroma cacao presents RNase activity, Ca2+ and Mg2+ dependent-DNase activity and antifungal action on Moniliophthora perniciosa S Pereira Menezes, EM de Andrade Silva, E Matos Lima, ... BMC plant biology 14 (1), 161 , 2014 2014 Citations: 59
Use of SAG2A recombinant Toxoplasma gondii surface antigen as a diagnostic marker for human acute toxoplasmosis: analysis of titers and avidity of IgG and IgG1 antibodies SR Béla, DAO Silva, JP Cunha-Júnior, CP Pirovani, FA Chaves-Borges, ... Diagnostic microbiology and infectious disease 62 (3), 245-254 , 2008 2008 Citations: 59
Genetic and Biological Diversity of Trichoderma stromaticum , a Mycoparasite of the Cacao Witches'-Broom Pathogen JT de Souza, AWV Pomella, JH Bowers, CP Pirovani, LL Loguercio, ... Phytopathology 96 (1), 61-67 , 2006 2006 Citations: 54
Water stress in Musa spp.: A systematic review AS Santos, EP Amorim, CF Ferreira, CP Pirovani PLoS One 13 (12), e0208052 , 2018 2018 Citations: 53
Genome sequence and effectorome of Moniliophthora perniciosa and Moniliophthora roreri subpopulations CS Barbosa, RR Fonseca, TM Batista, MA Barreto, CS Argolo, ... BMC genomics 19 (1), 509 , 2018 2018 Citations: 53
Rootstock-induced physiological and biochemical mechanisms of drought tolerance in sweet orange LP Gonçalves, TFO Alves, CPS Martins, AO de Sousa, IC dos Santos, ... Acta Physiologiae Plantarum 38 (7), 174 , 2016 2016 Citations: 49
Physiological, biochemical and molecular responses to drought conditions in field-grown grafted and ungrafted citrus plants IC dos Santos, AAF de Almeida, CP Pirovani, MGC Costa, ... Environmental and Experimental Botany 162, 406-420 , 2019 2019 Citations: 47
Exploring the mycovirus universe: Identification, diversity, and biotechnological applications DC Villan Larios, BM Diaz Reyes, CP Pirovani, LL Loguercio, VC Santos, ... Journal of Fungi 9 (3), 361 , 2023 2023 Citations: 44
dsRNA-induced gene silencing in Moniliophthora perniciosa, the causal agent of witches’ broom disease of cacao ACC dos Santos, JAL Sena, SC Santos, CV Dias, CP Pirovani, ... Fungal Genetics and Biology 46 (11), 825-836 , 2009 2009 Citations: 42
Eutirucallin: a lectin with antitumor and antimicrobial properties JG Palharini, AC Richter, MF Silva, FB Ferreira, CP Pirovani, KSC Naves, ... Frontiers in cellular and infection microbiology 7, 136 , 2017 2017 Citations: 41
Pathogenesis-related protein 10 in resistance to biotic stress: progress in elucidating functions, regulation and modes of action NS Lopes, AS Santos, DPS De Novais, CP Pirovani, F Micheli Frontiers in Plant Science 14, 1193873 , 2023 2023 Citations: 39
