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Genome sequencing of Rigidoporus microporus provides insights on genes important for wood decay, latex tolerance and interspecific fungal interactions.

ABSTRACT: Fungal plant pathogens remain a serious threat to the sustainable agriculture and forestry, despite the extensive efforts undertaken to control their spread. White root rot disease is threatening rubber tree (Hevea brasiliensis) plantations throughout South and Southeast Asia and Western Africa, causing tree mortality and severe yield losses. Here, we report the complete genome sequence of the basidiomycete fungus Rigidoporus microporus, a causative agent of the disease. Our phylogenetic analysis confirmed the position of R. microporus among the members of Hymenochaetales, an understudied group of basidiomycetes. Our analysis further identified pathogen's genes with a predicted role in the decay of plant cell wall polymers, in the utilization of latex components and in interspecific interactions between the pathogen and other fungi. We also detected putative horizontal gene transfer events in the genome of R. microporus. The reported first genome sequence of a tropical rubber tree pathogen R. microporus should contribute to the better understanding of how the fungus is able to facilitate wood decay and nutrient cycling as well as tolerate latex and utilize resinous extractives.

SUBMITTER: Oghenekaro AO

PROVIDER: S-EPMC7089950 | biostudies-literature | 2020 Mar

REPOSITORIES: biostudies-literature

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Genome sequencing of Rigidoporus microporus provides insights on genes important for wood decay, latex tolerance and interspecific fungal interactions.

Oghenekaro Abbot O AO Kovalchuk Andriy A Raffaello Tommaso T Camarero Susana S Gressler Markus M Henrissat Bernard B Lee Juna J Liu Mengxia M Martínez Angel T AT Miettinen Otto O Mihaltcheva Sirma S Pangilinan Jasmyn J Ren Fei F Riley Robert R Ruiz-Dueñas Francisco Javier FJ Serrano Ana A Thon Michael R MR Wen Zilan Z Zeng Zhen Z Barry Kerrie K Grigoriev Igor V IV Martin Francis F Asiegbu Fred O FO

Scientific reports 20200323 1

Fungal plant pathogens remain a serious threat to the sustainable agriculture and forestry, despite the extensive efforts undertaken to control their spread. White root rot disease is threatening rubber tree (Hevea brasiliensis) plantations throughout South and Southeast Asia and Western Africa, causing tree mortality and severe yield losses. Here, we report the complete genome sequence of the basidiomycete fungus Rigidoporus microporus, a causative agent of the disease. Our phylogenetic analysi ...[more]

PMID: 32251355

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Project description:BackgroundThe basidiomycete Rigidoporus microporus is a fungus that causes the white rot disease of the tropical rubber tree, Hevea brasiliensis, the major source of commercial natural rubber. Besides its lifestyle as a pathogen, the fungus is known to switch to saprotrophic growth on wood with the ability to degrade both lignin and cellulose. There is almost no genomic or transcriptomic information on the saprotrophic abilities of this fungus. In this study, we present the fungal transcriptomic profiles during saprotrophic growth on rubber wood.ResultsA total of 266.6 million RNA-Seq reads were generated from six libraries of the fungus growing either on rubber wood or without wood. De novo assembly produced 34, 518 unigenes with an average length of 2179 bp. Annotation of unigenes using public databases; GenBank, Swiss-Prot, Kyoto Encyclopedia of Genes and Genomes (KEGG), Cluster of Orthologous Groups (COG) and Gene Ontology (GO) produced 25, 880 annotated unigenes. Transcriptomic profiling analysis revealed that the fungus expressed over 300 genes encoding lignocellulolytic enzymes. Among these, 175 genes were up-regulated in rubber wood. These include three members of the glycoside hydrolase family 43, as well as various glycosyl transferases, carbohydrate esterases and polysaccharide lyases. A large number of oxidoreductases which includes nine manganese peroxidases were also significantly up-regulated in rubber wood. Several genes involved in fatty acid metabolism and degradation as well as natural rubber degradation were expressed in the transcriptome. Four genes (acyl-CoA synthetase, enoyl-CoA hydratase, 3-hydroxyacyl-CoA dehydrogenase and acyl-CoA acetyltransferase) potentially involved in rubber latex degradation pathway were also induced. A number of ATP binding cassette (ABC) transporters and hydrophobin genes were significantly expressed in the transcriptome during saprotrophic growth. Some genes related to energy metabolism were also induced.ConclusionsThe analysed data gives an insight into the activation of lignocellulose breakdown machinery of R. microporus. This study also revealed genes with relevance in antibiotic metabolism (e.g. cephalosporin esterase) as well as those with potential applications in fatty acid degradation. This is the first study on the transcriptomic analysis of R. microporus on rubber wood and should serve as a pioneering resource for future studies of the fungus at the genomic or transcriptomic level.

Project description:Latex production from Hevea brasiliensis rubber tree is the second most important commodity in Malaysia, but this industry is threatened by the white root rot disease (WRD) caused by Rigidoporus microporus that leads to considerable latex yield loss and tree death. This study aimed to characterize and compare the virulence of five R. microporus isolates obtained from infected rubber trees located at different states in Malaysia. These isolates were subjected to morphological and molecular characterization for species confirmation and pathogenicity test for the determination of virulence level. BLAST search showed that the ITS sequences of all the pathogen isolates were 99% identical to R. microporus isolate SEG (accession number: MG199553) from Malaysia. The pathogenicity test of R. microporus isolates conducted in a nursery with 24 seedlings per isolate showed that isolate RL21 from Sarawak has developed the most severe above- and below-ground symptoms of WRD on the rubber clone RRIM600 as host. Six months after being infected with R. microporus, RL21 was evaluated with the highest average of disease severity index of 80.52% for above- and below-ground symptoms, followed by RL22 (68.65%), RL20 (66.04%), RL26 (54.38%), and RL25 (43.13%). The in vitro growth condition tests showed that isolate RL21 of R. microporus has optimum growth at 25-30 °C, with the preference of weakly acidic to neutral environments (pH 6-7). This study revealed that different virulence levels are possessed among different R. microporus isolates even though they were isolated from the same host species under the same climate region. Taken together, field evaluation through visual observation and laboratory assays have led to screening of the most virulent isolate. Determination of the most virulent isolate in the present study is vital and shall be taken into consideration for the selection of suitable pathogen isolate in the development of more effective control measures in combating tenacious R. microporus.

Project description:Brown rot fungi release massive amounts of carbon from forest deadwood, particularly at high latitudes. These fungi degrade wood by generating small reactive oxygen species (ROS) to loosen lignocellulose, to then selectively remove carbohydrates. The ROS mechanism has long been considered the key adaptation defining brown rot wood decomposition, but recently, we found preliminary evidence that fungal glycoside hydrolases (GHs) implicated in early cell wall loosening might have been adapted to tolerate ROS stress and to synergize with ROS to loosen woody lignocellulose. In the current study, we found more specifically that side chain hemicellulases that help in the early deconstruction of the lignocellulosic complex are significantly more tolerant of ROS in the brown rot fungus Rhodonia placenta than in a white rot fungus (Trametes versicolor) and a soft rot fungus (Trichoderma reesei). Using proteomics to understand the extent of tolerance, we found that significant oxidation of secreted R. placenta proteins exposed to ROS was less than half of the oxidation observed for T. versicolor or T. reesei. The principal oxidative modifications observed in all cases were monooxidation and dioxidation/trioxidation (mainly in methionine and tryptophan residues), some of which were critical for enzyme activity. At the peptide level, we found that GHs in R. placenta were the least ROS affected among our tested fungi. These results confirm and describe underlying mechanisms of tolerance in early-secreted brown rot fungal hemicellulases. These enzymatic adaptations may have been as important as nonenzymatic ROS pathway adaptations in brown rot fungal evolution. IMPORTANCE Brown rot fungi play a critical role in carbon recycling and are of industrial interest. These fungi typically use reactive oxygen species (ROS) to indiscriminately "loosen" wood cell walls at the outset of decay. Brown rot fungi avoid oxidative stress associated with this ROS step by delaying the expression/secretion of many carbohydrate-active enzymes, but there are exceptions, notably some side chain hemicellulases, implicated in loosening lignocellulose. In this study, we provide enzyme activity and secretomic evidence that these enzymes in the brown rot model Rhodonia placenta are more ROS tolerant than the white and soft rot isolates tested. For R. placenta, and perhaps all brown rot lineages, these ROS tolerance adaptions may have played a long-overshadowed role in enabling brown rot.

Dataset Information

Genome sequencing of Rigidoporus microporus provides insights on genes important for wood decay, latex tolerance and interspecific fungal interactions.

Publications

Genome sequencing of Rigidoporus microporus provides insights on genes important for wood decay, latex tolerance and interspecific fungal interactions.

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