Investigation of strategies of adaptation to the pathogenic life style of fungi from the Moniliophthora genus at various levels of biological organizations: species, biotypes, and geographic lineages

• Grant number: 16/10498-4
• Support Opportunities: Research Projects - Thematic Grants
• Duration: February 01, 2017 - December 31, 2022
• Field of knowledge: Biological Sciences - Genetics - Molecular Genetics and Genetics of Microorganisms
• Principal Investigator: Antonio Vargas de Oliveira Figueira
• Grantee: Antonio Vargas de Oliveira Figueira
• Host Institution: Centro de Energia Nuclear na Agricultura (CENA). Universidade de São Paulo (USP). Piracicaba , SP, Brazil
• Pesquisadores principais: Gonçalo Amarante Guimarães Pereira
• Associated researchers: Camila Caldana ; Gonçalo Amarante Guimarães Pereira ; Lázaro Eustaquio Pereira Peres ; Marcelo Falsarella Carazzolle ; Paulo José Pereira Lima Teixeira
• Associated scholarship(s): 22/04952-5 - Comparative analysis of the genomes and transcriptomes of biotypes of the phytopathogenic fungus of cocoa, Moniliophthora perniciosa (Agaricales, Basidiomycota), BP.TT; 19/12188-0 - Evaluation of the orchestrated pathways of miR156 in the interaction between Moniliophthora perniciosa and Solanum lycopersicum: consequences for pathogenesis and susceptibility, BP.MS; 19/25326-2 - Functional analysis of the SlUACA gene potentially associated with resistance to Moniliophthora perniciosa, which causes the witches' broom disease in cacao, tomato (Solanum lycopersicum) cv. Micro Tone, BP.IC; + associated scholarships 19/22063-0 - Optimization of the genetic transformation of cacao (Theobroma cacao) to modulate the expression of receptors of pathogen molecular patterns, BP.TT; 18/18711-4 - Functional analysis of genes potentially associated with resistance to the basidiomycete Moniliophthora perniciosa in tomato (Solanum lycopersicum) cv. 'Micro-Tom', BP.DR; 19/15927-9 - Investigating the genetic elements of mating-type associated with the control of sexual reproduction in Moniliophthora perniciosa, BP.IC; 19/17927-6 - Moniliophthora perniciosa mycelia quantification in infected tomato and cacao tissues, BP.IC; 18/21036-7 - Analysis of the transcriptome and metabolome of the atypical interaction between the fruits of Theobroma cacao (cocoa) and the pathogenic fungus Moniliophthora perniciosa, which causes the witch's broom, BP.PD; 17/13319-6 - Identification of MpPR1-I protein ligands and structural and functional analyses of MpPR-1s of Moniliophthora perniciosa in vitro, BP.PD; 17/25261-2 - Transgenic line obtention of Moniliophthora perniciosa S-biotype expression of GFP, BP.IC; 17/24428-0 - Cultivation of T. cacao and M. perniciosa, RNA extraction from infected plants and routine laboratory activities support, BP.TT; 17/17000-4 - Analysis of the interaction Moniliophthora perniciosa x 'Micro-Tom' tomato: non-host type resistance, effects on the development and role of phytohormones in pathogenesis, BP.PD; 17/17676-8 - Optimization of cacao (Theobroma cacao) genetic transformation aiming at modulation of pathogens molecular patterns expression of receptors, BP.TT; 17/13015-7 - Investigation of global transcriptional alterations in the Theobroma cacao x Moniliophthora perniciosa pathosystem during the progression of Witches Broom Disease of cacao, BP.DD - associated scholarships

Abstract

The invasion of the main cacao-producing region of Brazil by the basidiomycete Moniliophthora perniciosa (causal agent of the witches' broom disease) caused the collapse of cacao production, a fundamental and unique raw material for the chocolate industry. Moniliophthora perniciosa and M. roreri are the most limiting pathogens for cacao (Theobroma cacao) cultivation in the Americas. Both species belong to the Agaricales, which are mostly saprophytic; pathogenicity has evolved in a few species of the order. Likewise, the lack of other phytopathogens closely related to M. perniciosa and M. roreri suggests that the evolution of phytopathogenicy in this genus has evolved recent changes in genes associated with the control of life styles and stages (biotrophic and necrotrophic), among others directly associated with pathogenicity. While M. roreri only attacks cacao pods, M. perniciosa is capable of infecting shoots, pods and flower buds; M. perniciosa is also classified into biotypes, which are host-specific. This large variation in life habits associated with the large genetic variability makes these fungal taxa an excelent model to investigate genomic changes associated with the evolution of phytopathogenicity. Therefore, we intend to perform comparative genomic analysis involving Agaricales species to verify species- and biotype-specific genetic differences; to evaluate evolutionary and selective rates between orthologs from species/biotypes; pathogenic lineages ancestrality; patterns of expansion and retraction of gene families; and the function divergence among gene families for each lineage. The comparison of M. perniciosa isolates and biotypes will allow the search for associations between genome structure and life styles. The genetic system that controls sexual reproduction, defined by two non-linked loci A and B, and genes associated with vegetative compatibility, genetically controlled by the vic loci (vegetative incompatibility), will be investigated as they may define gene flow in M. perniciosa. Transcriptomic analysis will be conducted to investigate factors that can lead to the success of M. perniciosa and M. roreri as pathogens. The comparison between compatible and incompatible interactions of M. perniciosa with its hosts (e.g. S-biotype x tomato and S-biotype x cacao, respectively) may indicate which are the key-factors related with infection successs or failure. Comparing shoot and pod infection by M. perniciosa with pod infection by M. roreri may help to elucidate how pathogens adopt specific infection strategies, and which are the general virulence factors related with Moniliophthora virulence. Recent reports in other pathosystems sugest that, besides effector proteins, pathogens may use small RNAs (sRNA) to directly manipulate the plant defense system, therefore expression of sRNA during infection with M. perniciosa will be evaluated. Mutants and transgenic lines in the 'Micro-Tom' (MT) background with changes in synthesis or perception of hormones will enable investigating the role of this class of compounds in the pathogenesis and defense against infection by M. perniciosa isolates from the S- and C-biotype. Additionally, we intend to develop new tools of genetic manipulation of the pathogen and hosts to assist future functional studies of this pathosystem, and develop transgenic lines of cacao and MT. The genomic information generated, together with the development of populational studies and genetic manipulations, will be applied to direct functional analysis of the pathogen essential genes. (AU)

Scientific publications

(9)

(References retrieved automatically from Web of Science and SciELO through information on FAPESP grants and their corresponding numbers as mentioned in the publications by the authors)

PASCHOAL, DANIELE; COSTA, JULIANA L.; DA SILVA, EDER M.; DA SILVA, FABIA B.; CAPELIN, DIOGO; OMETTO, VITOR; ARICETTI, JULIANA A.; CARVALHO, GABRIEL G.; PIMPINATO, RODRIGO F.; DE OLIVEIRA, RICARDO F.; et al. Infection by Moniliophthora perniciosa reprograms tomato Micro-Tom physiology, establishes a sink, and increases secondary cell wall synthesis. Journal of Experimental Botany, v. 73, n. 11, p. 20-pg., 2022-02-21. (13/04309-6, 17/17000-4, 16/10498-4, 16/10524-5, 18/18711-4)

FIORIN, GABRIEL LORENCINI; SANCHEZ-VALLET, ANDREA; DE TOLEDO THOMAZELLA, DANIELA PAULA; VITAL DO PRADO, PAULA FAVORETTI; DO NASCIMENTO, LEANDRO COSTA; DE OLIVEIRA FIGUEIRA, ANTONIO VARGAS; THOMMA, BART P. H. J.; GUIMARAES PEREIRA, GONCALO AMARANTE; PEREIRA LIMA TEIXEIRA, PAULO JOSE. Suppression of Plant Immunity by Fungal Chitinase-like Effectors. Current Biology, v. 28, n. 18, p. 3023+, SEP 24 2018. (14/06181-0, 13/09878-9, 09/50119-9, 11/23315-1, 16/10498-4)

COSTA, PAULO C. S.; BARSOTTINI, MARIO R. O.; VIEIRA, MARIA L. L.; PIRES, BARBARA A.; EVANGELISTA, JOEL S.; ZERI, ANA C. M.; NASCIMENTO, ANDREY F. Z.; SILVA, JAQUELINE S.; CARAZZOLLE, MARCELO F.; PEREIRA, GONCALO A. G.; et al. N-Phenylbenzamide derivatives as alternative oxidase inhibitors: Synthesis, molecular properties, H-1-STD NMR, and QSAR. Journal of Molecular Structure, v. 1208, MAY 15 2020. (16/10498-4, 18/03130-6, 15/09870-3, 14/15339-6)

BARSOTTINI, MARIO R. O.; COPSEY, ALICE; YOUNG, LUKE; BARONI, RENATA M.; CORDEIRO, ARTUR T.; PEREIRA, GONCALO A. G.; MOORE, ANTHONY L.. Biochemical characterization and inhibition of the alternative oxidase enzyme from the fungal phytopathogen Moniliophthora perniciosa. COMMUNICATIONS BIOLOGY, v. 3, n. 1, MAY 25 2020. (17/12852-2, 14/15339-6, 15/07653-5, 17/13319-6, 16/10498-4)

VASCONCELOS, ADRIELLE A.; JOSE, JULIANA; TOKIMATU, PAULO M.; CAMARGO, ANTONIO P.; TEIXEIRA, PAULO J. P. L.; THOMAZELLA, DANIELA P. T.; DO PRADO, V, PAULA F.; FIORIN, GABRIEL L.; COSTA, JULIANA L.; FIGUEIRA, ANTONIO; et al. Adaptive evolution of Moniliophthora PR-1 proteins towards its pathogenic lifestyle. BMC ECOLOGY AND EVOLUTION, v. 21, n. 1, MAY 14 2021. (16/10498-4, 18/04240-0, 14/06181-0, 13/09878-9, 13/08293-7, 17/13015-7, 14/00802-2, 17/13319-6, 13/05979-5, 13/04309-6, 11/23315-1)

BARSOTTINI, MARIO R. O.; PIRES, BARBARA A.; VIEIRA, MARIA L.; PEREIRA, JOSE G. C.; COSTA, PAULO C. S.; SANITA, JAQUELINE; CORADINI, ALESSANDRO; MELLO, FELLIPE; MARSCHALK, CIDNEI; SILVA, EDER M.; et al. Synthesis and testing of novel alternative oxidase (AOX) inhibitors with antifungal activity against Moniliophthora perniciosa (Stahel), the causal agent of witches' broom disease of cocoa, and other phytopathogens. Pest Management Science, v. 75, n. 5, p. 1295-1303, MAY 2019. (15/09870-3, 14/15339-6, 15/07653-5, 16/10498-4, 17/17000-4, 15/06677-8)

COSTA, PAULO C. S.; EVANGELISTA, JOEL S.; LEAL, IGOR; MIRANDA, PAULO C. M. L.. Chemical Graph Theory for Property Modeling in QSAR and QSPR-Charming QSAR & QSPR. MATHEMATICS, v. 9, n. 1, JAN 2021. (16/10498-4)

CASTRO, JOAQUIM A. M.; SERIKAVA, BRUNO K.; NACIUK, FABRICIO F.; LIGIERO, CAROLINA B. P.; MORGON, NELSON H.; MIRANDA, PAULO C. M. L.. Unique Remote Regiocontrol by an N-Oxide Group in the Synthesis of Isocaulibugulones A, B, C, and D. CHEMISTRYSELECT, v. 8, n. 17, p. 7-pg., 2023-02-24. (16/10498-4, 14/25770-6)

COSTA, JULIANA L.; PASCHOAL, DANIELE; DA SILVA, EDER M.; SILVA, JAMILLE S.; DO CARMO, RAFAEL M.; CARRERA, ESTHER; LOPEZ-DIAZ, ISABEL; ROSSI, MONICA L.; FRESCHI, LUCIANO; MIECZKOWSKI, PIOTR; et al. Moniliophthora perniciosa, the causal agent of witches' broom disease of cacao, interferes with cytokinin metabolism during infection of Micro-Tom tomato and promotes symptom development. NEW PHYTOLOGIST, v. 231, n. 1, p. 365-381, JUL 2021. (16/10524-5, 13/04309-6, 19/12188-0, 16/10498-4, 15/00060-9, 17/17000-4)