Penicillium digitatum infection mechanisms in citrus: What do we know so far?

Costa, Jonas Henrique; Bazioli, Jaqueline Moraes; Pontes, João Guilherme de Moraes; Fill, Taícia Pacheco

doi:10.1016/j.funbio.2019.05.004

Cited by 87 publications

(56 citation statements)

References 84 publications

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“…In our case, both MMD-mutants were more sensitive to H 2 O 2 than parental strains. P. digitatum is able to neutralize the ROS response that citrus fruit generate upon infection (Macarisin et al, 2007; Costa et al, 2019). In our previous study, we speculated that the high sensitivity of Δ chsVII mutant to H 2 O 2 was related to its decreased virulence (Gandía et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

“…Penicillium digitatum is the main postharvest pathogen of citrus fruit and causes the green mold disease, being responsible for significant economic losses in citriculture (Marcet-Houben et al, 2012; Palou, 2014; Costa et al, 2019). We have previously identified and analyzed the expression of chitin synthase genes in P. digitatum (Gandía et al, 2012, 2014).…”

Section: Introductionmentioning

confidence: 99%

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The Myosin Motor Domain-Containing Chitin Synthases Are Involved in Cell Wall Integrity and Sensitivity to Antifungal Proteins in Penicillium digitatum

et al. 2019

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Penicillium digitatum is the main postharvest pathogen of citrus fruit and is responsible for important economic losses in spite of the massive use of fungicides. The fungal cell wall (CW) and its specific component chitin are potential targets for the development of new antifungal molecules. Among these are the antifungal peptides and proteins that specifically interact with fungal CW. Chitin is synthesized by a complex family of chitin synthases (Chs), classified into up to eight classes within three divisions. Previously, we obtained and characterized a mutant of P. digitatum in the class VII gene (ΔchsVII), which contains a short myosin motor-like domain (MMD). In this report, we extend our previous studies to the characterization of mutants in chsII and in the gene coding for the other MMD-Chs (chsV), and study the role of chitin synthases in the sensitivity of P. digitatum to the self-antifungal protein AfpB, and to AfpA obtained from P. expansum. The ΔchsII mutant showed no significant phenotypic and virulence differences with the wild type strain, except in the production and morphology of the conidia. In contrast, mutants in chsV showed a more dramatic phenotype than the previous ΔchsVII, with reduced growth and conidial production, increased chitin content, changes in mycelial morphology and a decrease in virulence to citrus fruit. Mutants in chsVII were specifically more tolerant than the wild type to nikkomycin Z, an antifungal inhibitor of chitin biosynthesis. Treatment of P. digitatum with its own antifungal protein AfpB resulted in an overall reduction in the expression of the chitin synthase genes. The mutants corresponding to MMD chitin synthases exhibited differential sensitivity to the antifungal proteins AfpA and AfpB, ΔchsVII being more susceptible than its parental strain and ΔchsV being slightly more tolerant despite its reduced growth in liquid broth. Taking these results together, we conclude that the MMD-containing chitin synthases affect cell wall integrity and sensitivity to antifungal proteins in P. digitatum.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The Myosin Motor Domain-Containing Chitin Synthases Are Involved in Cell Wall Integrity and Sensitivity to Antifungal Proteins in Penicillium digitatum

et al. 2019

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“…The citrus industry in Brazil corresponded to US$6.5 billion in revenues in 2019 (3). Citrus fruits can be affected by different diseases, leading to up to 50% of fruit losses and causing a negative economic impact (4)(5)(6).…”

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confidence: 99%

Phytotoxic Tryptoquialanines Produced In Vivo by Penicillium digitatum Are Exported in Extracellular Vesicles

Costa

Bazioli

Barbosa

et al. 2021

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Penicillium digitatum is the most aggressive pathogen of citrus fruits. Tryptoquialanines are major indole alkaloids produced by P. digitatum. It is unknown if tryptoquialanines are involved in the damage of citrus fruits caused by P. digitatum. To investigate the pathogenic roles of tryptoquialanines, we initially asked if tryptoquialanines could affect the germination of Citrus sinensis seeds. Exposure of the citrus seeds to tryptoquialanine A resulted in a complete inhibition of germination and an altered metabolic response. Since this phytotoxic effect requires the extracellular export of tryptoquialanine A, we investigated the mechanisms of extracellular delivery of this alkaloid in P. digitatum. We detected extracellular vesicles (EVs) released by P. digitatum both in culture and during infection of citrus fruits. Compositional analysis of EVs produced during infection revealed the presence of a complex cargo, which included tryptoquialanines and the mycotoxin fungisporin. The EVs also presented phytotoxicity activity in vitro and caused damage to the tissues of citrus seeds. Through molecular networking, it was observed that the metabolites present in the P. digitatum EVs are produced in all of its possible hosts. Our results reveal a novel phytopathogenic role of P. digitatum EVs and tryptoquialanine A, implying that this alkaloid is exported in EVs during plant infection. IMPORTANCE During the postharvest period, citrus fruits can be affected by phytopathogens such as Penicillium digitatum, which causes green mold disease and is responsible for up to 90% of total citrus losses. Chemical fungicides are widely used to prevent green mold disease, leading to concerns about environmental and health risks. To develop safer alternatives to control phytopathogens, it is necessary to understand the molecular basis of infection during the host-pathogen interaction. In the P. digitatum model, the virulence strategies are poorly known. Here, we describe the production of phytotoxic extracellular vesicles (EVs) by P. digitatum during the infection of citrus fruits. We also characterized the secondary metabolites in the cargo of EVs and found in this set of molecules an inhibitor of seed germination. Since EVs and secondary metabolites have been related to virulence mechanisms in other host-pathogen interactions, our data are important for the comprehension of how P. digitatum causes damage to its primary hosts.

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“…Nevertheless, the study of fruit-pathogen interactions has gained increased interest and progress has occurred in the understanding of fungal pathogenicity and fruit resistance [2]. In the citrus fruit-Pd interaction, Pd genome sequencing and establishment of Pd genetic transformation system have been completed recently [5,22,23], which have greatly promoted the understanding of Pd pathogenicity at molecular levels [24]. The recent genome sequencing of citrus, optimization of the citrus genetic transformation system, and establishment of citrus CRISPR/Cas9 gene editing system [25][26][27][28] have promoted the study of citrus disease resistance [26,29].…”

Section: Introductionmentioning

confidence: 99%

Citrus Postharvest Green Mold: Recent Advances in Fungal Pathogenicity and Fruit Resistance

et al. 2020

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As the major postharvest disease of citrus fruit, postharvest green mold is caused by the necrotrophic fungus Penicillium digitatum (Pd), which leads to huge economic losses worldwide. Fungicides are still the main method currently used to control postharvest green mold in citrus fruit storage. Investigating molecular mechanisms of plant–pathogen interactions, including pathogenicity and plant resistance, is crucial for developing novel and safer strategies for effectively controlling plant diseases. Despite fruit–pathogen interactions remaining relatively unexplored compared with well-studied leaf–pathogen interactions, progress has occurred in the citrus fruit–Pd interaction in recent years, mainly due to their genome sequencing and establishment or optimization of their genetic transformation systems. Recent advances in Pd pathogenicity on citrus fruit and fruit resistance against Pd infection are summarized in this review.

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Penicillium digitatum infection mechanisms in citrus: What do we know so far?

Cited by 87 publications

References 84 publications

The Myosin Motor Domain-Containing Chitin Synthases Are Involved in Cell Wall Integrity and Sensitivity to Antifungal Proteins in Penicillium digitatum

The Myosin Motor Domain-Containing Chitin Synthases Are Involved in Cell Wall Integrity and Sensitivity to Antifungal Proteins in Penicillium digitatum

Phytotoxic Tryptoquialanines Produced In Vivo by Penicillium digitatum Are Exported in Extracellular Vesicles

Citrus Postharvest Green Mold: Recent Advances in Fungal Pathogenicity and Fruit Resistance

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