Population Genetic Structure of Rhizoctonia oryzae-sativae from Rice in Latin America and Its Adaptive Potential to Emerge as a Pathogen on Urochloa Pastures
Abstract and Figures
The fungus Rhizoctonia oryzae-sativae is an important pathogen that causes the aggregated sheath spot disease on rice. In this study, we investigated the genetic structure of rice-adapted populations of R. oryzae-sativae sampled from traditional rice-cropping areas from the Paraíba Valley, São Paulo, Brazil, and from Meta, in the Colombian Llanos, in South America. We used five microsatellite loci to measure population differentiation and infer the pathogen's reproductive system. Gene flow was detected among the three populations of the R. oryzae-sativae from lowland rice in Brazil and Colombia. In contrast, a lack of gene flow was observed between the lowland and the upland rice populations of the pathogen. Evidence of sexual reproduction including low clonality, Hardy-Weinberg equilibrium within loci and gametic equilibrium between loci, indicated the predominance of a mixed reproductive system in all populations. In addition, we assessed the adaptive potential of the Brazilian populations of R. oryzae-sativae to emerge as a pathogen to Urochloa spp. (signalgrass) based on greenhouse aggressiveness assays. The Brazilian populations of R. oryzae-sativae were probably only incipiently adapted as a pathogen to Urochloa spp. Comparison between RST and QST showed the predominance of diversifying selection in the divergence between the two populations of R. oryzae-sativae from Brazil.
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... Análises experimentais do crescimento micelial sob condições de estresse de temperatura, associadas às medidas de variância genética aditiva e de evolucionabilidade deste carácter, nos permitiriam inferir sobre o potencial adaptativo de R. solani AG-1 IA à variações térmicas ambientais, de forma semelhante ao procedimento usado para determinar a adaptabilidade evolutiva do patógeno a novos hospedeiros (22,23,27). Isso porque evolucionabilidade é definida como a capacidade para a evolução adaptativa ou do potencial adaptativo de uma população, i.e., medidas de resposta à seleção (15,28,29) que, no caso de fitopatógenos, pode ser imposta por estresses ambientais (28,30) ou por variantes biológicas dos hospedeiros (22,23,27). ...
... Análises experimentais do crescimento micelial sob condições de estresse de temperatura, associadas às medidas de variância genética aditiva e de evolucionabilidade deste carácter, nos permitiriam inferir sobre o potencial adaptativo de R. solani AG-1 IA à variações térmicas ambientais, de forma semelhante ao procedimento usado para determinar a adaptabilidade evolutiva do patógeno a novos hospedeiros (22,23,27). Isso porque evolucionabilidade é definida como a capacidade para a evolução adaptativa ou do potencial adaptativo de uma população, i.e., medidas de resposta à seleção (15,28,29) que, no caso de fitopatógenos, pode ser imposta por estresses ambientais (28,30) ou por variantes biológicas dos hospedeiros (22,23,27). ...
... Uma terceira população de outra espécie de Rhizoctonia associada ao arroz (R. oryzae-sativae, classificada como Ceratobasidium oryzae-sativae em sua fase sexuada) foi incluída neste estudo para efeito comparativo. O fungo R. oryzaesativae (agente causal da mancha agregada da bainha do arroz) é adaptado a temperaturas mais elevadas, com ótimo de crescimento a 32 o C (3) e ocorre naturalmente em áreas de arroz na Colômbia (22,25). Nossa hipótese foi de que o estresse imposto pelo aumento da temperatura afetaria, de forma semelhante, o potencial adaptativo de R. solani AG-1 IA, obtido de Urochloa e de arroz. ...
A large number of widely distributed plant pathogens such as the phytopathogenic fungi of the genus Rhizoctonia are subject to extreme temperature fluctuations in their habitats. To survive such thermal fluctuations, these organisms have developed the capability of regulating their phenotypic values for specific thermal adaptations and to other specific environmental variations. The objective of this study was to determine the effects of thermal stress on the evolvability for mycelial growth in two host-distinct populations of Rhizoctonia solani AG-1 IA infecting either rice (OS6) or Urochloa (BBT1), and to compare them with a population of R. oryzae-sativae from rice (OS5), a species adapted to higher temperatures. The populations were subjected to two growth temperatures: 25°C and 35°C (optimal and stress temperatures for R. solani AG-1 IA). Based on mycelial growth, estimates of genotypic variance (IG), environmental variance (IE) and broad sense heritability (h2) were determined as measures of evolvability. The population OS5 of R. oryzae-sativae was almost not influenced by temperature stress, while at 35oC there was a reduction in h2 for the populations BBT1 and OS6 of R. solani AG-1 IA. However, the relatively high h2 values for mycelial growth at 35oC (0.63 ± 0.07) indicate that both populations BBT1 and OS6 of R. solani AG-1 IA have potential for adaptation to temperature stress.
... Source and origin of formerly identified Rhizoctonia species included in the multigene phylogenetic analyses: a Chavarro-Mesa et al. (2015); bGaino et al. (2010) andGasparotto et al. (2017); cCiampi et al. (2008); and dPereira et al. (2017). ...
... There have been no reports of this disease on Urochloa in Brazil yet. However, a recent study fromPereira et al. (2017) indicated that the populations of R. oryzae-sativae were at an early stage in the process of host shift with incipient pathogenic adaptation to Urochloa. Similar to what was detected in our study, the overall aggressiveness of these rice-adapted populations of R. oryzae-sativae on Urochloa was low, ranging from 1% diseased leaf area on U. brizantha 'Piatã' to 7% on U. brizantha 'Marandu'. ...
Leaf blight, sheath blight, and web blight are major diseases caused by Rhizoctonia species on both Fabaceae and Poaceae plant hosts in the Brazilian Amazon agroecosystem. To determine the diversity of Rhizoctonia species associated with foliar diseases on fabaceous (cowpea and soybeans) and poaceous [rice and signal grass (Urochloa brizantha)] hosts, a broad survey was conducted in Pará, Rondônia, Roraima and Mato Grosso, in the Amazon, from 2012 to 2013. We extended our survey to Cerrado areas of Mato Grosso, and the lowlands of Paraíba Valley, in São Paulo, where these Rhizoctonia foliar diseases have not been reported so far. Our findings revealed that these diseases are caused by a diversity of Rhizoctonia solani AG‐1 complex. We detected that R. solani AG‐1 IA (sexual phase Thanatephorus cucumeris) was the predominant pathogen associated with signal grass leaf blight and collar rot diseases in the Amazon, especially in Rondônia and northern Mato Grosso. In addition, a subgroup of R. solani (AG‐1 IF) not previously reported in Brazil, was associated with leaf blight on cowpea and soybean, in Roraima. Also in Roraima, another subgroup (AG‐1 ID) was detected. In Mato Grosso Cerrados we did not find any of the major Rhizoctonia foliar pathogens. Instead, R. oryzae (Waitea circinata) was the predominant species associated with a collar rot on U. brizantha. In the lowlands of São Paulo, R. oryzae‐sativae (Ceratobasidium oryzae‐sativae) was the predominant pathogen detected causing the rice sheath spot disease.
... Jamur Rhizoctonia (R. solani) diketahui sebagai penyebab penyakit hawar pelepah pada padi (Li et al., 2021). Selain itu, jamur Rhizoctonia yang lain (R. oryzae dan R. oryzae-sativae) juga dilaporkan menjadi penyebab penyakit sheath spot dan aggregate sheath spot pada tanaman padi (Pereira et al., 2017;Aye et al., 2009). Jamur R. solani juga diketahui mampu bertahan dengan baik pada benih selama di penyimpanan dari satu musim ke musim berikutnya (Sivalingam et al., 2006) dan juga mampu menghasilkan metabolit yang dapat menghambat pemanjangan kecambah benih (Xu et al., 2015). ...
Seed quality is the main factor to gain optimal yields. The presence of fungi in seeds can cause damage to seeds, decrease germination and seed vigor, and cause disease in plants. The aim of this study was to detection of fungi in four varieties of rice seeds from local seed producers in Lampung. The rice seeds of Ciherang, Ciliwung, Cilamaya Muncul, and Inpari 42 varieties were obtained from the Center for Seed Certification for Food Crops and Horticulture in Lampung Province. Fungal detection in rice seeds was carried out using three methods, namely the washing method, blotter test, and agar plate test. The results showed that on four varieties of rice seeds tested was found five genera of fungi, i.e. Fusarium, Rhizoctonia, Curvularia, Rhizopus, and Aspergillus. In the washing method, Fusarium, Curvularia, and Aspergillus fungi were found. In the Blotter test method and the agar plate, Rhizoctonia, Curvularia, Rhizopus, and Aspergillus fungi were found. All of five fungi were found in Ciherang and Ciliwung seed. Rhizopus were not found in Inpari 42 seeds. Fusarium and Curvularia was not found in Cilamaya Muncul seeds. The Inpari 42 were the seeds with the highest number of fungi found and the lowest number of normal germinating seeds. The Cilamaya Muncul were the seeds with the least number of fungi found.
... Concerning phytopathogenic populations, genetic diversity is primarily related to its evolutive potential and population structure. High-risk pathogens that impact agricultural endeavors have high levels of genetic diversity and mixed reproduction systems (sexual/asexual), allowing the emergence and permanence of "new" pathogens in the agroecosystems (Chavarro-Mesa et al., 2015;Edisson, Chavarro-Mesa; McDonald & Linde, 2002;Pereira et al., 2016;Willi et al., 2011). Moreover, this pathogen displays a highly conserved evolutive potential subject to the population structure of the fungus observed in Colombia, which could impact the management strategy and alternatives for this disease. ...
El chancro del tallo y la sarna negra de la papa son enfermedades ocasionadas por el hongo Rhizoctonia solani grupo de anastomosis tres (GA-3PT), el cual afecta raíces, tallos y tubérculos de papa y reduce el rendimiento de los cultivos. El objetivo de la presente investigación fue determinar la diversidad genética de R. solani GA-3PT presente en los departamentos colombianos de Antioquia, Boyacá y Cundinamarca. La restricción enzimática de la región ribosomal (RFLP, por sus siglas en inglés) ITS-5.8S permitió la diferenciación e identificación específica de los grupos de anastomosis GA-3PT y GA2-1 y confirmó que el GA-3PT es el principal agente causal y origen etiológico de la enfermedad en Colombia. Mediante amplificación aleatoria de marcadores microsatélites (RAMs), por sus siglas en inglés), se observaron dos agrupamientos dentro de R. solani GA-3PT; el GA-3PT (A) comparte un índice de similitud del 78 % entre sí, en comparación con el GA-3PT (B) que presenta una similitud del 79 % entre sus aislamientos. Los agrupamientos no están relacionados con su origen geográfico, sino con el grupo de anastomosis al que pertenecen. La diversidad genética de Nei [D] de 0,25 confirma una alta diversidad genética para el GA-3PT mediante análisis RAMs, relacionada con un alto potencial evolutivo al interior del grupo GA-3PT en Colombia. Finalmente, el hongo R. solani GA-3PT que se obtuvo en Cundinamarca tiene potencial adaptativo para emerger como patógeno de la papa criolla (Solanum phureja) en Colombia, posiblemente, debido a la semejanza de los patosistemas.
... Within-population components of variance for each trait were determined using genetic variance and heritability (Willi et al., 2011;Stefansson et al., 2014;Pereira et al., 2016). The variance components were determined using a statistical procedure implemented in R software using the lme4 package (Bates et al., 2015). ...
Evolution favors the emergence of locally-adapted optimum phenotypes that are likely to differ across a wide array of environmental conditions. The emergence of favorable adaptive characteristics is accelerated in agricultural pathogens due to the unique properties of agro-ecosystems. We performed a QST - FST comparison using 164 strains of Parastagonospora nodorum sampled from eight global field populations to disentangle the predominant evolutionary forces driving population divergence in a wheat pathogen. We used digital image analysis to obtain quantitative measurements of growth rate and melanization at different temperatures and under different fungicide concentrations in a common garden experiment. FST measures were based on complete genome sequences obtained for all 164 isolates. Our analyses indicated that all measured traits were under selection. Growth rates at 18°C and 24°C were under stabilizing selection (QST < FST), while diversifying selection (QST > FST) was the predominant evolutionary force affecting growth under fungicide and high temperature stress. Stabilizing selection (QST < FST) was the predominant force affecting melanization across the different environments. Melanin production increased at 30°C but was negatively correlated with higher growth rates, consistent with a trade-off under heat stress. Our results demonstrate that global populations of P. nodorum possess significant evolutionary potential to adapt to changing local conditions, including warmer temperatures and applications of fungicides.
... Rhizoctonia oryzae-sativae (teleomorph: Ceratobasidium oryzae-sativae) is a soil-borne basidiomycete fungus that causes aggregate sheath spot on rice worldwide [2,13]. Recently, a novel mitovirus has been reported to infect this fungus [1]. ...
Rhizoctonia oryzae-sativae is a soil-borne basidiomycete fungus that causes aggregate sheath spot disease on rice worldwide. Here, we report the complete genome sequence of a partitivirus designated as Rhizoctonia oryzae-sativae partitivirus 1 (RosPV1) infecting this fungus. The genome of RosPV1 consists of two double-stranded RNA (dsRNA) segments. The larger segment, designated as dsRNA-1 (1,961 bp), contains a single open reading frame (ORF) that encodes a putative polypeptide with a conserved RNA-dependent RNA polymerase (RdRp) domain. The smaller segment, dsRNA-2 (1,819 bp), also has a single ORF, which is predicted to encode the capsid protein (CP). BLAST searches and phylogenetic analyses suggested that RosPV1 is a representative member of a new species within the genus Alphapartitivirus. This is the first report of an alphapartitivirus infecting the fungus R. oryzae-sativae.
Sheath blight disease caused by Rhizoctonia solani is a severe limitation of lowland rice productivity in Thailand. Typically, confound symptoms occurring with other sheath diseases caused by Rhizoctonia and Sclerotium. To classify these pathogen species, 33 Rhizoctonia isolates were collected from lowland fields in central and northeast Thailand and identified by using morphological and molecular tools described herein. The isolates were identified as R. solani AG-1 IA, R. solani, R. oryzae-sativae (aggregate sheath spot), and S. hydrophilum (stem rot). This is the first report of S. hydrophilum associated with complex rice sheath blight diseases in Thailand. According to the pathogenicity test of the KDML105 and Pathum Thani 1 varieties, R. solani AG-1 IA isolates were found to be the most virulent strain. Each isolate revealed diverts in morphology and disease severity on rice. The H-06 (from Udon Thani) and K-12 (from Buri Ram) isolates showed the highest AUDPC (1448.24–1681.24 and 1301.84–1383.72, respectively) on tested varieties. One hundred and ninety indigenous lowland rice varieties, along with seven commercial varieties, were screened with both aggressive isolates under greenhouse conditions. Interestingly, 30 varieties appeared resistant (< 20% RLH) to tested isolates. Based on result from our study, therefore, that these varieties may provide a source of sheath blight resistance in Thailand, and prove beneficial for future rice breeding programs.
Rice aggregate sheath spot disease occurs in many countries, causing serious yield losses. In China, the disease-causing fungus Rhizoctonia oryzae-sativae was reported in 1985, and since then, it has rarely been reported in major rice-growing areas after almost 30 years. Compared with Rhizoctonia solani, R. oryzae-sativae has a significantly different physiological morphology and growth status, although both fungi affect rice leaves in very similar ways. The optimum temperature for the suitable growth of R. oryzae-sativae is 31 °C, which is consistent with previous reports. We extracted phytotoxins from R. oryzae-sativae and analyzed its biological activity via the detached leaf and radicle inhibition methods. Rhizoctonia solani and R. oryzae-sativae exhibit differences in terms of pathogenicity and toxins activity, which indicates that these fungi may produce different toxins components. Based on gas chromatography-mass spectrometry data, esters, phenols, and other components were present in the crude toxins extract of R. oryzae-sativae. Our research provides a new method for studying the phytotoxins of R. oryzae-sativae. However, further studies are needed to elucidate the pathogenic mechanisms responsible for the aggregate sheath spot disease on rice.
Cabbage, a widely used and popular vegetable, and oilseed rape, the second most valuable oilseed crop in the world, are two important species from the Brassicaceae family. Two geographically separated outbreaks of cabbage and oilseed rape root rot with estimated incidence of 15% and 20%, respectively, were recorded during 2017 in the Vojvodina region, Serbia. Twelve hyphal-tip isolates were obtained from symptomatic cabbage and oilseed rape plants and identified as Waitea circinata var. zeae based on morphological and molecular features. This indicates that W. circinata var. zeae has expanded its host range to the Brassicaceae family. Sequence analyses of ITS and LSU of the rDNA, RPB2, and β-tubulin genes revealed the highest similarity with multiple W. circinata var. zeae. Neighbor-joining analyses of ITS sequences resulted in a phylogenetic tree with one well-defined branch of W. circinata var. zeae, with two separate groups. All Serbian isolates and the majority of isolates originating from natural infection of dicotyledonous plants grouped together in Group I. Following artificial inoculation, W. circinata var. zeae isolates caused mild to medium root necrosis of seedlings of 2 monocotyledonous and 12 dicotyledonous plant species, implying a wider host range than known for W. circinata var. zeae. Additionally, this is the first occurrence of W. circinata var. zeae on dicotyledonous host plants in Europe. As cabbage and oilseed rape are important crops grown worldwide, the occurrence of this new soil-borne pathogen with a broad host range imposes the necessity for changes in routine disease control practice, particularly crop rotation.
Evolution favors the emergence of locally-adapted optimum phenotypes that are likely to differ across a wide array of environmental conditions. The emergence of favorable adaptive characteristics is accelerated in agricultural pathogens due to the unique properties of agro-ecosystems. We performed a QST - FST comparison using 164 strains of Parastagonospora nodorum sampled from eight global field populations to disentangle the predominant evolutionary forces driving population divergence in a wheat pathogen. We used digital image analysis to obtain quantitative measurements of growth rate and melanization at different temperatures and under different fungicide concentrations in a common garden experiment. FST measures were based on complete genome sequences obtained for all 164 isolates. Our analyses indicated that all measured traits were under selection. Growth rates at 18C and 24C were under stabilizing selection (QST < FST), while diversifying selection (QST > FST) was the predominant evolutionary force affecting growth under fungicide and high temperature stress. Stabilizing selection (QST < FST) was the predominant force affecting melanization across the different environments. Melanin production increased at 30C but was negatively correlated with higher growth rates, consistent with a trade-off under heat stress. Our results demonstrate that global populations of P. nodorum possess significant evolutionary potential to adapt to changing local conditions, including warmer temperatures and applications of fungicides.
Arlequin ver 3.0 is a software package integrating several basic and advanced methods for population genetics data analysis, like the computation of standard genetic diversity indices, the estimation of allele and haplotype frequencies, tests of departure from linkage equilibrium, departure from selective neutrality and demographic equilibrium, estimation or parameters from past population expansions, and thorough analyses of population subdivision under the AMOVA framework. Arlequin 3 introduces a completely new graphical interface written in C++, a more robust semantic analysis of input files, and two new methods: a Bayesian estimation of gametic phase from multi-locus genotypes, and an estimation of the parameters of an instantaneous spatial expansion from DNA sequence polymorphism. Arlequin can handle several data types like DNA sequences, microsatellite data, or standard multilocus genotypes. A Windows version of the software is freely available on http://cmpg.unibe.ch/software/arlequin3.
Foliar blight and death of signalgrass (Urochloa spp.) pastures are caused by the Rhizoctonia solani fungus. This study aimed at determining which pathogens from the Rhizoctonia species complex are associated with leaf and sheath blight in Urochloa and rice, in the Colombian Llanos. Sympatric areas of Urochloa pastures adjacent to rice cropping areas were sampled using a linear transect system. The pathogens were identified using morphological traits, molecular detection based on specific primers and sequencing of the ITS-5.8S rDNA region. R. solani AG-1 IA predominated as the pathogen associated with foliar blight in all samples from U. brizantha cv. ‘Toledo’ and hybrid Urochloa cv. ‘Mulato’. Besides R. solani AG-1 IA (18 % of the samples), Rhizoctonia oryzae-sativae (71 %) and Sclerotium hydrophilum (11 %) were also detected. In the cross-pathogenicity test, the R. solani AG-1 IA fungus was the most aggressive to Urochloa, while R. oryzae-sativae produced very mild infection symptoms. This is the first report of R. oryzae-sativae and S. hydrophilum associated with the complex of rice sheath blight diseases in Colombia.
A new measure of the extent of population subdivision as inferred from allele frequencies at microsatellite loci is proposed and tested with computer simulations. This measure, called R(ST), is analogous to Wright's F(ST) in representing the proportion of variation between populations. It differs in taking explicit account of the mutation process at microsatellite loci, for which a generalized stepwise mutation model appears appropriate. Simulations of subdivided populations were carried out to test the performance of R(ST) and F(ST). It was found that, under the generalized stepwise mutation model, R(ST) provides relatively unbiased estimates of migration rates and times of population divergence while F(ST) tends to show too much population similarity, particularly when migration rates are low or divergence times are long [corrected].
The teleomorph of Rhizoctonia oryzae-sativae is described as Ceratobasidium oryzae-sativae sp. nov. It differs from other known Ceratobasidium species because it has two sterigmata per basidium in conjunction with typically subglobose basidiospores. Ceratobasidium setariae comb. nov. (≡ Hypochnus setariae) is morphologically similar to C. oryzae-sativae. The description of the sclerotial state of C. setariae conforms to Sclerotium fumigatum and C. setariae is postulated to be the teleomorph of S. fumigatum. Sclerotium fumigatum is binucleate and is placed in the genus Rhizoctonia.
Ten GATA microsatellite DNA markers were isolated and characterized from black grouse (Tetrao tetrix) using an enrichment cloning procedure. High levels of heterozygosity (mean Ho = 0.74 ± 0.026), and a large number of alleles (range = 5-16) were resolved in 70 individuals, indicating these markers will be useful for examining parentage, inbreeding and population structure in black grouse. No evidence for linkage disequilibrium or the presence of null alleles was found.