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29 pages, 4977 KiB

Open AccessArticle

The Molecular Docking of MAX Fungal Effectors with Plant HMA Domain-Binding Proteins

by Lina Rozano, James K. Hane and Ricardo L. Mancera

Int. J. Mol. Sci. 2023, 24(20), 15239; https://doi.org/10.3390/ijms242015239 - 16 Oct 2023

Viewed by 1163

Fungal effector proteins are important in mediating disease infections in agriculturally important crops. These secreted small proteins are known to interact with their respective host receptor binding partners in the host, either inside the cells or in the apoplastic space, depending on the [...] Read more.

Fungal effector proteins are important in mediating disease infections in agriculturally important crops. These secreted small proteins are known to interact with their respective host receptor binding partners in the host, either inside the cells or in the apoplastic space, depending on the localisation of the effector proteins. Consequently, it is important to understand the interactions between fungal effector proteins and their target host receptor binding partners, particularly since this can be used for the selection of potential plant resistance or susceptibility-related proteins that can be applied to the breeding of new cultivars with disease resistance. In this study, molecular docking simulations were used to characterise protein–protein interactions between effector and plant receptors. Benchmarking was undertaken using available experimental structures of effector–host receptor complexes to optimise simulation parameters, which were then used to predict the structures and mediating interactions of effector proteins with host receptor binding partners that have not yet been characterised experimentally. Rigid docking was applied for both the so-called bound and unbound docking of MAX effectors with plant HMA domain protein partners. All bound complexes used for benchmarking were correctly predicted, with 84% being ranked as the top docking pose using the ZDOCK scoring function. In the case of unbound complexes, a minimum of 95% of known residues were predicted to be part of the interacting interface on the host receptor binding partner, and at least 87% of known residues were predicted to be part of the interacting interface on the effector protein. Hydrophobic interactions were found to dominate the formation of effector–plant protein complexes. An optimised set of docking parameters based on the use of ZDOCK and ZRANK scoring functions were established to enable the prediction of near-native docking poses involving different binding interfaces on plant HMA domain proteins. Whilst this study was limited by the availability of the experimentally determined complexed structures of effectors and host receptor binding partners, we demonstrated the potential of molecular docking simulations to predict the likely interactions between effectors and their respective host receptor binding partners. This computational approach may accelerate the process of the discovery of putative interacting plant partners of effector proteins and contribute to effector-assisted marker discovery, thereby supporting the breeding of disease-resistant crops. Full article

(This article belongs to the Special Issue Molecular Plant–Fungal Interactions)

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29 pages, 5129 KiB

Open AccessArticle

Ab Initio Modelling of the Structure of ToxA-like and MAX Fungal Effector Proteins

by Lina Rozano, Yvonne M. Mukuka, James K. Hane and Ricardo L. Mancera

Int. J. Mol. Sci. 2023, 24(7), 6262; https://doi.org/10.3390/ijms24076262 - 26 Mar 2023

Cited by 3 | Viewed by 2372

Abstract

Pathogenic fungal diseases in crops are mediated by the release of effector proteins that facilitate infection. Characterising the structure of these fungal effectors is vital to understanding their virulence mechanisms and interactions with their hosts, which is crucial in the breeding of plant [...] Read more.

Pathogenic fungal diseases in crops are mediated by the release of effector proteins that facilitate infection. Characterising the structure of these fungal effectors is vital to understanding their virulence mechanisms and interactions with their hosts, which is crucial in the breeding of plant cultivars for disease resistance. Several effectors have been identified and validated experimentally; however, their lack of sequence conservation often impedes the identification and prediction of their structure using sequence similarity approaches. Structural similarity has, nonetheless, been observed within fungal effector protein families, creating interest in validating the use of computational methods to predict their tertiary structure from their sequence. We used Rosetta ab initio modelling to predict the structures of members of the ToxA-like and MAX effector families for which experimental structures are known to validate this method. An optimised approach was then used to predict the structures of phenotypically validated effectors lacking known structures. Rosetta was found to successfully predict the structure of fungal effectors in the ToxA-like and MAX families, as well as phenotypically validated but structurally unconfirmed effector sequences. Interestingly, potential new effector structural families were identified on the basis of comparisons with structural homologues and the identification of associated protein domains. Full article

(This article belongs to the Special Issue Molecular Plant–Fungal Interactions)

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18 pages, 3044 KiB

Open AccessArticle

Interactions of the Fungal Community in the Complex Patho-System of Esca, a Grapevine Trunk Disease

by Laura Martín, Blanca García-García and María del Mar Alguacil

Int. J. Mol. Sci. 2022, 23(23), 14726; https://doi.org/10.3390/ijms232314726 - 25 Nov 2022

Cited by 3 | Viewed by 1723

Abstract

Worldwide, Esca is a complex and devastating Grapevine Trunk Disease (GTD), characterized by inconstant foliar symptoms and internal wood degradation. A large range of fungal taxa have been reported as causal agents. We applied both culture-dependent and culture-independent methods (Illumina Technology and q-PCR) [...] Read more.

Worldwide, Esca is a complex and devastating Grapevine Trunk Disease (GTD), characterized by inconstant foliar symptoms and internal wood degradation. A large range of fungal taxa have been reported as causal agents. We applied both culture-dependent and culture-independent methods (Illumina Technology and q-PCR) to investigate this concerning disease. Woods from vines with asymptomatic leaves and vines with leaf Esca symptoms were compared. Internally, different types of wood were found, from healthy wood with black necrosis to wood with white rot. A combination of leaf and wood Esca symptoms resulted in four experimental categories. Although there was no relation with symptoms, culture-independent mycobiome composition revealed Phaeomoniella chlamydospora, a GTD pathogen, as the most abundant species (detected in 85.4% of wood samples, with 14.8% relative abundance). Using TaqMan q-PCR, P. chlamydospora DNA was detected in 60.4% of samples (far from the 18.8% of positive results in the culture-dependent approach). There was a predominance of saprotrophs, even if their abundance was not affected by Esca symptoms. Concerning pathotrophs, the white rot development within grapevines was linked to the abundance of fungi belonging to the Hymenochaetaceae family. The Botryosphaeriaceae family was identified as an indicator for expression of Esca foliar symptoms. Lastly, the Aureobasidiaceae family was found to be a potential biocontrol agent for Esca, since it was most abundant in the control asymptomatic plants. Full article

(This article belongs to the Special Issue Molecular Plant–Fungal Interactions)

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23 pages, 9078 KiB

Open AccessArticle

Integrated High-Throughput Sequencing, Microarray Hybridization and Degradome Analysis Uncovers MicroRNA-Mediated Resistance Responses of Maize to Pathogen Curvularia lunata

by Weiwei Wang, Zhen Liu, Xinyuan An, Yazhong Jin, Jumei Hou and Tong Liu

Int. J. Mol. Sci. 2022, 23(22), 14038; https://doi.org/10.3390/ijms232214038 - 14 Nov 2022

Cited by 1 | Viewed by 1388

Abstract

Curvularia lunata (Wakker) Boed, the causal agent of leaf spot in maize, is prone to mutation, making it difficult to control. RNAi technology has proven to be an important tool of genetic engineering and functional genomics aimed for crop improvement. MicroRNAs (miRNAs), which [...] Read more.

Curvularia lunata (Wakker) Boed, the causal agent of leaf spot in maize, is prone to mutation, making it difficult to control. RNAi technology has proven to be an important tool of genetic engineering and functional genomics aimed for crop improvement. MicroRNAs (miRNAs), which act as post-transcriptional regulators, often cause translational repression and gene silencing. In this article, four small RNA (sRNA) libraries were generated from two maize genotypes inoculated by C. lunata; among these, ltR1 and ltR2 were from the susceptible variety Huangzao 4 (HZ), ltR3 and ltR4, from the resistant variety Luyuan (LY), and 2286, 2145, 1556 and 2504 reads were annotated as miRNA in these four sRNA libraries, respectively. Through the combined analysis of high-throughput sequencing, microarray hybridization and degradome, 48 miRNAs were identified as being related to maize resistance to C. lunata. Among these, PC-732 and PC-169, two new maize miRNAs discovered, were predicted to cleave mRNAs of metacaspase 1 (AMC1) and thioredoxin family protein (Trx), respectively, possibly playing crucial roles in the resistance of maize to C. lunata. To further confirm the role of PC-732 in the interaction of maize and C. lunata, the miRNA was silenced through STTM (short tandem target mimic) technology, and we found that knocking down PC-732 decreased the susceptibility of maize to C. lunata. Precisely speaking, the target gene of PC-732 might inhibit the expression of disease resistance-related genes during the interaction between maize and C. lunata. Overall, the findings of this study indicated the existence of miRNAs involved in the resistance of maize to C. lunata and will contribute to rapidly clarify the resistant mechanism of maize to C. lunata. Full article

(This article belongs to the Special Issue Molecular Plant–Fungal Interactions)

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22 pages, 767 KiB

Open AccessArticle

WideEffHunter: An Algorithm to Predict Canonical and Non-Canonical Effectors in Fungi and Oomycetes

by Karla Gisel Carreón-Anguiano, Jewel Nicole Anna Todd, Bartolomé Humberto Chi-Manzanero, Osvaldo Jhosimar Couoh-Dzul, Ignacio Islas-Flores and Blondy Canto-Canché

Int. J. Mol. Sci. 2022, 23(21), 13567; https://doi.org/10.3390/ijms232113567 - 05 Nov 2022

Cited by 4 | Viewed by 1646

Abstract

Newer effectorome prediction algorithms are considering effectors that may not comply with the canonical characteristics of small, secreted, cysteine-rich proteins. The use of effector-related motifs and domains is an emerging strategy for effector identification, but its use has been limited to individual species, [...] Read more.

Newer effectorome prediction algorithms are considering effectors that may not comply with the canonical characteristics of small, secreted, cysteine-rich proteins. The use of effector-related motifs and domains is an emerging strategy for effector identification, but its use has been limited to individual species, whether oomycete or fungal, and certain domains and motifs have only been associated with one or the other. The use of these strategies is important for the identification of novel, non-canonical effectors (NCEs) which we have found to constitute approximately 90% of the effectoromes. We produced an algorithm in Bash called WideEffHunter that is founded on integrating three key characteristics: the presence of effector motifs, effector domains and homology to validated existing effectors. Interestingly, we found similar numbers of effectors with motifs and domains within two different taxonomic kingdoms: fungi and oomycetes, indicating that with respect to their effector content, the two organisms may be more similar than previously believed. WideEffHunter can identify the entire effectorome (non-canonical and canonical effectors) of oomycetes and fungi whether pathogenic or non-pathogenic, unifying effector prediction in these two kingdoms as well as the two different lifestyles. The elucidation of complete effectoromes is a crucial step towards advancing effectoromics and disease management in agriculture. Full article

(This article belongs to the Special Issue Molecular Plant–Fungal Interactions)

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12 pages, 2915 KiB

Open AccessArticle

An Amidase Contributes to Full Virulence of Sclerotinia sclerotiorum

by Wei Li, Junxing Lu, Chenghuizi Yang, Kate Arildsen, Xin Li and Shitou Xia

Int. J. Mol. Sci. 2022, 23(19), 11207; https://doi.org/10.3390/ijms231911207 - 23 Sep 2022

Cited by 3 | Viewed by 1622

Abstract

Sclerotinia sclerotiorum is one of the most notorious and ubiquitous soilborne plant pathogens, causing serious economic losses to a large number of hosts worldwide. Although virulence factors have been identified in this filamentous fungus, including various cell-wall-degrading enzymes, toxins, oxalic acids and effectors, [...] Read more.

Sclerotinia sclerotiorum is one of the most notorious and ubiquitous soilborne plant pathogens, causing serious economic losses to a large number of hosts worldwide. Although virulence factors have been identified in this filamentous fungus, including various cell-wall-degrading enzymes, toxins, oxalic acids and effectors, our understanding of its virulence strategies is far from complete. To explore novel factors contributing to disease, a new pipeline combining forward genetic screening and next-generation sequencing was utilized in this study. Analysis of a hypovirulent mutant revealed that a mutation in an amidase-encoding gene, Sscle_10g079050, resulted in reduced virulence. This is a first report on the contribution of an amidase to fungal virulence, likely through affecting oxalic acid homeostasis. Full article

(This article belongs to the Special Issue Molecular Plant–Fungal Interactions)

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22 pages, 2865 KiB

Open AccessArticle

Functional Study of Lipoxygenase-Mediated Resistance against Fusarium verticillioides and Aspergillus flavus Infection in Maize

by Mikias Damtew Guche, Stefania Pilati, Francesco Trenti, Lorenza Dalla Costa, Paola Giorni, Graziano Guella, Adriano Marocco and Alessandra Lanubile

Int. J. Mol. Sci. 2022, 23(18), 10894; https://doi.org/10.3390/ijms231810894 - 17 Sep 2022

Cited by 3 | Viewed by 1791

Abstract

Mycotoxin contamination of maize kernels by fungal pathogens like Fusarium verticillioides and Aspergillus flavus is a chronic global challenge impacting food and feed security, health, and trade. Maize lipoxygenase genes (ZmLOXs) synthetize oxylipins that play defense roles and govern host-fungal interactions. [...] Read more.

Mycotoxin contamination of maize kernels by fungal pathogens like Fusarium verticillioides and Aspergillus flavus is a chronic global challenge impacting food and feed security, health, and trade. Maize lipoxygenase genes (ZmLOXs) synthetize oxylipins that play defense roles and govern host-fungal interactions. The current study investigated the involvement of ZmLOXs in maize resistance against these two fungi. A considerable intraspecific genetic and transcript variability of the ZmLOX family was highlighted by in silico analysis comparing publicly available maize pan-genomes and pan-transcriptomes, respectively. Then, phenotyping and expression analysis of ZmLOX genes along with key genes involved in oxylipin biosynthesis were carried out in a maize mutant carrying a Mu transposon insertion in the ZmLOX4 gene (named UFMulox4) together with Tzi18, Mo17, and W22 inbred lines at 3- and 7-days post-inoculation with F. verticillioides and A. flavus. Tzi18 showed the highest resistance to the pathogens coupled with the lowest mycotoxin accumulation, while UFMulox4 was highly susceptible to both pathogens with the most elevated mycotoxin content. F. verticillioides inoculation determined a stronger induction of ZmLOXs and maize allene oxide synthase genes as compared to A. flavus. Additionally, oxylipin analysis revealed prevalent linoleic (18:2) peroxidation by 9-LOXs, the accumulation of 10-oxo-11-phytoenoic acid (10-OPEA), and triglyceride peroxidation only in F. verticillioides inoculated kernels of resistant genotypes. Full article

(This article belongs to the Special Issue Molecular Plant–Fungal Interactions)

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18 pages, 4355 KiB

Open AccessArticle

Molecular Mechanisms of Phenylpropane-Synthesis-Related Genes Regulating the Shoot Blight Resistance of Bambusa pervariabilis × Dendrocalamopsis grandis

by Fengying Luo, Peng Yan, Liling Xie, Shuying Li, Tianhui Zhu, Shan Han, Tiantian Lin and Shujiang Li

Int. J. Mol. Sci. 2022, 23(12), 6760; https://doi.org/10.3390/ijms23126760 - 17 Jun 2022

Cited by 4 | Viewed by 1389

Abstract

Bambusa pervariabilis × Dendrocalamopsis grandis shoot blight caused by Arthrinium phaeospermum is a fungal disease that has affected a large area in China in recent years. However, it is not clear which genes are responsible for the disease resistance of B. pervariabilis × [...] Read more.

Bambusa pervariabilis × Dendrocalamopsis grandis shoot blight caused by Arthrinium phaeospermum is a fungal disease that has affected a large area in China in recent years. However, it is not clear which genes are responsible for the disease resistance of B. pervariabilis × D. grandis. Based on the analysis of transcriptome and proteome data, two genes, CCoAOMT2 and CAD5, which may be involved in disease resistance, were screened. Two gene expression-interfering varieties, COF RNAi and CAD RNAi were successfully obtained using RNAi technology. Quantitative real-time fluorescence (qRT-PCR) results showed that CCoAOMT2 gene, CAD5 gene and seven related genes expression was down-regulated in the transformed varieties. After inoculating pathogen spore suspension, the incidence and disease index of cof-RNAi and cad-RNAi transformed plants increased significantly. At the same time, it was found that the content of total lignin and flavonoids in the two transformed varieties were significantly lower than that of the wild-type. The subcellular localization results showed that both CCoAOMT2 and CAD5 were localized in the nucleus and cytoplasm. The above results confirm that the CCoAOMT2 and CAD5 genes are involved in the resistance of B. pervariabilis × D.grandis to shoot blight through regulating the synthesis of lignin and flavonoids. Full article

(This article belongs to the Special Issue Molecular Plant–Fungal Interactions)

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Review

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24 pages, 1293 KiB

Open AccessReview

Characterization of Arbuscular Mycorrhizal Effector Proteins

by María V. Aparicio Chacón, Judith Van Dingenen and Sofie Goormachtig

Int. J. Mol. Sci. 2023, 24(11), 9125; https://doi.org/10.3390/ijms24119125 - 23 May 2023

Cited by 2 | Viewed by 1842

Abstract

Plants are colonized by various fungi with both pathogenic and beneficial lifestyles. One type of colonization strategy is through the secretion of effector proteins that alter the plant’s physiology to accommodate the fungus. The oldest plant symbionts, the arbuscular mycorrhizal fungi (AMF), may [...] Read more.

Plants are colonized by various fungi with both pathogenic and beneficial lifestyles. One type of colonization strategy is through the secretion of effector proteins that alter the plant’s physiology to accommodate the fungus. The oldest plant symbionts, the arbuscular mycorrhizal fungi (AMF), may exploit effectors to their benefit. Genome analysis coupled with transcriptomic studies in different AMFs has intensified research on the effector function, evolution, and diversification of AMF. However, of the current 338 predicted effector proteins from the AM fungus Rhizophagus irregularis, only five have been characterized, of which merely two have been studied in detail to understand which plant proteins they associate with to affect the host physiology. Here, we review the most recent findings in AMF effector research and discuss the techniques used for the functional characterization of effector proteins, from their in silico prediction to their mode of action, with an emphasis on high-throughput approaches for the identification of plant targets of the effectors through which they manipulate their hosts. Full article

(This article belongs to the Special Issue Molecular Plant–Fungal Interactions)

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