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Light micrographs of representative sporosori of Spongospora subterranea f. sp. subterranea from powdery scab lesions on potato tubers (cv. 'Agria', New Zealand 2004), indicating their range in size and overall form. Calculated numbers of resting spores (see text) for each sporosorus are indicated. Bar: 10 μm.
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Plasmodiophorid sporosori (aggregations of resting spores) reach their most complex form in Spongospora subterranea f. sp. subterranea, the biotrophic plant pathogen which causes the economically important disease powdery scab of potato (Solanum tuberosum). Resting spores are the perennation life cycle stage of plasmodiophorids, allowing them to su...
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... of internal channelling increased with in- creasing sporosorus size. In a detailed examination of one sectioned sporosorus, large internal spaces unoc- cupied by resting spores were obvious, and 47% of the sporosorus was occupied by resting spores. Variability in sporosorus form in one collection of sporosori is in- dicated by the examples in Fig. 2. Fig. 3 illustrates general sporosorus form and sur- face ornamentation. Individual resting spores in sporo- sori ranged from circular to roughly hexagonal in cross section, and had punctate outer surfaces. They were arranged within sporosori in roughly double layers (Fig. 5). The punctate surface of each resting spore was always the ...
Citations
... Notably, sporosori possess a robust cell wall structure (Ciafardini et al. 1995;Miller et al. 1985), making 31 them resistant to degradation in soil or water environments and desiccation in dry conditions. Among the 32 Plasmodiophorids, Spongospora exhibits the most intricate sporosorus structure, generating sponge-like 33 formations that house numerous resting spores (Falloon et al. 2011). Kole 1954). ...
... It has been observed that 66 substantial accumulation of Sss sporosori occurs within brown root galls (Falloon et al. 2016). Sss 67 sporosori have a sponge-like structure characterized by holes on their outer surface, which penetrate 68 inward (Falloon et al. 2011). Their shape is variable but mostly observed as spheroids and prolate 69 spheroids (EW 2009). ...
Powdery scab disease, caused by the soilborne protist Spongospora subterranea f. sp. subterranea, poses a major constraint to potato production worldwide. Disease symptoms include damage to the tuber skin and the formation of root galls. This study aimed to investigate the potential mechanism behind the formation of sporosori, which are aggregates of resting spores, within root galls. Scanning electron microscopy analysis revealed that the early stage of gall formation, characterized by a white color, involved the accumulation of starch grains, which later disappeared as the gall matured and turned brown. The mature brown galls were found to contain fully formed sporosori. Light microscopy examination of ultramicrotome sections of the root galls showed that the high-amylopectin starches were surrounded by a plasmodium, a precursor to sporosorus. These findings suggest that starch grains contribute to the formation of a sponge-like structure within the sporosori. A significant reduction in total starch levels in both the root galls and their associated roots was observed compared to healthy roots. These findings indicate starch consumption by sporosori during the maturation of root galls. Interestingly, analysis of the transcript levels of starch-related genes showed downregulation of genes encoding starch degrading enzymes and a amylopectin-debranching enzyme, whereas genes encoding a starch synthase and a protein facilitating starch synthesis were upregulated in the root galls. Overall, our results demonstrate that starch is consumed during sporosorus formation, and the pathogen likely manipulates starch homeostasis to its advantage for sporosorus development within the root galls.
... Este patógeno sobrevive por muchos años en el suelo en forma quiescente, como quistes uninucleados o binucleados de pared gruesa, y resiste a condiciones adversas. Las esporas de resistencia miden aproximadamente 4 mm de diámetro y se agrupan en estructuras más grandes denominadas quistosoros, que individualmente dan origen a las zoosporas (Falloon et al., 2011). ...
Objetivo. Analizar histológicamente las estructuras de Spongospora subterranea (Wallr.) Lagerh f. sp subterranea Tomlinson (Sss) localizados en los tejidos radicales de plantas de papa infectadas con este patógeno en condiciones controladas de laboratorio en la Universidad Nacional de Colombia. Materiales y métodos. Se realizaron inoculaciones con quistosoros de Sss en solución Hoagland en plantas hidropónicas de papa var. Capiro, posterior a la inoculación se realizó la tinción de raíces para observar estructuras de infección típicas del patógeno bajo microscopía. Resultados. Mediante la metodología propuesta se logró observar diferentes estructuras de Sss, como plasmodios esporangiales, zoosporangios, plasmodios esporogénicos y quistosoros. Conclusión. A partir de las observaciones realizadas se logró identificar diferentes estados de infección de Spongospora subterranea f. sp subterranea y se verificó el desarrollo de cada una de las fases del ciclo de vida del patógeno en los tejidos radicales de papa var. Capiro.
... The inoculum (20 mL of sporosorus suspension in water + Tween® 20; approx. 1.75 × 10 7 resting spores; Falloon et al. 2011; was applied to the soil at the bottom of each seed tuber planting hole in each S. subterranea-amended pot before the seed tuber was planted. ...
Soils in which disease fails to develop despite pathogen presence are considered disease-suppressive. They offer sustainable, effective protection to plants against infection by soil-borne pathogens. Naturally disease-suppressive soils have been reported for diseases of a diverse range of agricultural crops worldwide yet the underlying mechanisms of disease suppression are still not completely understood. Two large greenhouse experiments, conducted during 2017/18 (Year 1) and 2018/19 (Year 2), determined that soils naturally suppressive to stem canker and black scurf of potato (caused by Rhizoctonia solani) are present in vegetable-arable cropping soils of the Auckland and Waikato regions of New Zealand. Soil was pre-treated with heat prior to inoculation with R. solani and compared with untreated and uninoculated controls to ascertain if stem canker and black scurf suppression was ‘general’, or ‘specific’ (i.e. transferable; possibly involving specific microorganisms). Rhizoctonia solani inoculation was also combined with transfer of one part test soil to nine parts of a known disease-conducive soil. Abiotic factors such as soil texture and organic matter content influenced black scurf incidence and severity. Soil microorganisms were also involved in disease suppression since black scurf incidence and severity markedly increased when they were eliminated or reduced by soil heat pre-treatment. Microbial profiling of the soils through sequencing revealed that taxa of geographically close soils of the same type had similar fungal and bacterial community structure and diversity even though they differed in their capacity to suppress black scurf. These results suggest that although the soil microbiome as a whole, was mainly responsible for soil disease suppressiveness, certain bacterial genera or species may play a role in black scurf suppression.
... Spongospora subterranea has a complex life cycle, including different zoosporic stages, plasmodium and resting spore formation. Resting spores are highly resistant to environmental stresses and can survive for decades in the soil (Falloon et al., 2011). Under favourable conditions, resting spores germinate and releases primary zoospores, which infect host roots, leading to intracellular haploid primary plasmodia (Hernandez Maldonado et al., 2013;Amponsah et al., 2021). ...
... Plasmodiophora produces individual non-aggregated resting spores, while Polymyxa, Spongospora, Sorodiscus, Tetramyxa, Octomyxa, Woronina and Ligniera all produce sporosori of variable shape and size (Sherwood, 1968;Dylewski and Miller, 1984;Devi et al., 1995;Robbins and Braselton, 1997;Tamada and Asher, 2016;Amponsah et al., 2021). Among all the known plasmodiophorids, Spongospora has the most complex sporosori with a sponge-like structure of variable size (Falloon et al., 2011). ...
... While non-dormant spores need only a favourable environment, dormant spores require an external germination stimulant which can be the host root exudate or nutrient solution (Neuhauser et al., 2010). Among the plasmodiophorids, S. subterranea has the most complex sporosori (Falloon et al., 2011). In S. ...
The obligate biotroph Spongospora subterranea is an important pathogen of potato, the world’s third most valuable food crop for human consumption. Resting spores are essential for the spread and survival of S. subterranea and can remain viable in the soil in their dormant states for decades rendering fields unsuitable for planting. In the presence of potato roots, resting spores germinate and release zoospores that subsequently infect potato roots. A better understanding of the molecular basis of resting spore germination of S. subterranea and the regulatory principles underlying Spongospora-potato interactions could be important for developing novel disease interventions. However, as a soilborne and obligate biotroph pathogen, the application of omics techniques for the detailed study of the pre- and post-infection processes in S. subterranea has been problematic.
This thesis developed a method for the partial purification of S. subterranea resting spores utilizing Ludox® gradient centrifugation. A series of preliminary experiments were then undertaken for S. subterranea protein preparation. Protein profiles between dormant and germination stimulant-treated resting spores were compared using label-free quantitative proteomics. A deep RNA sequencing approach was then employed to analyse S. subterranea resting spores' reprogramming during the transition to zoospores in an in vitro model. Further, to expand our understanding of S. subterranea biology during infection, the transcriptome and proteome of the pathogen during the invasion of roots of a susceptible and a resistant potato cultivar was characterized in planta. Later an integrated transcriptomic and proteomic dataset was employed to uncover these mechanisms underlying S. subterranea resistance in potato roots. In relation to this, the proteome and phosphoproteome of potato leaves were also profiled to explore potato resistance mechanisms to S. subterranea at the post-transcriptome levels.
Without affecting the viability of the spores, the Ludox® purification protocol produced a semi- purified and concentrated suspension of S. subterranea resting spores and improved protein identification by approximately 40%. The transcriptome and proteome analysis of S. subterranea spore germination introduced several candidate genes and proteins related to the germination of the pathogen, including those belonging to transcription and translation, transport, energy metabolic processes, stress response, and DNA repair. The in planta analysis of S. subterranea transcriptome and proteome indicated that transportation, metabolic processes and cytoskeletal processes were induced in the resistant cultivar. Enzyme activity and nucleic acid metabolism were decreased in this cultivar, suggesting a probable influence of these processes in the virulence of S. subterranea. The transcriptomic and proteomic datasets of potato roots infected by S. subterranea uncovered the critical role of glutathione metabolism and lignin metabolic process in potato resistance to S. subterranea. In addition, this experiment also confirmed that the inositol phosphate pathway might be related to the susceptibility of potato plants to the root disease by S. subterranea. The proteome and phosphoproteome analysis of potato leaves after infection by S. subterranea showed that oxidoreductase activity, electron transfer, and photosynthesis were significant processes that differentially changed in the proteome of resistant cultivar. The phosphoproteomics results indicated increased activity of signal transduction and defence response functions in resistant cultivars but not in the susceptible cultivar. In contrast, the majority of increased phosphoproteins in the susceptible cultivar were related to transporter activity and subcellular localisation.
This thesis provides a comprehensive overview of the changes in transcriptome and proteome during the germination of S. subterranea resting spores and extends our knowledge on the spore germination in plasmodiophorids. In planta study and potato defence response analysis contributes to the significant progress in our understanding of the interaction between the obligate biotrophic pathogens and their host plants. More than that, the study increased the availability of omics data in such a complex interaction and can allow the exploitation of this knowledge for the benefit of agriculture.
... The inoculum (20 mL of sporosorus suspension in water + Tween® 20; approx. 1.75 × 10 7 resting spores; Falloon et al. 2011; was applied to the soil at the bottom of each seed tuber planting hole in each S. subterranea-amended pot before the seed tuber was planted. ...
Powdery scab, caused by Spongospora subterranea, is an important potato disease. Greenhouse experiments in 2017/18 and 2018/19 on (very susceptible) ‘Agria’ seed tubers assessed if field-collected soils had different powdery scab-suppressive capabilities and identified factors involved in disease suppression. 2017/18: 12 geographically diverse soils with either S. subterranea added at planting or not added; 2018/19: six single-type soils used, to determine if powdery scab suppression was ‘general’, or ‘specific’ (transferable; possibly involving microorganisms), and if suppression was associated with soil physical, chemical, or biological factors (bacteria/fungi). For both seasons, S. subterranea soil ammendment increased scab severity on harvested tubers in all soils but one. Powdery scab severity (percent tubers with > 5% surface area covered by scabs) ranged from 0 to 39%. Soil texture, pH, soil organic matter and nutrient contents were associated with powdery scab incidence for some soils but not others. Effects of previous crop rotations on powdery scab were variable: one soil with three recent previous potato crops in rotation was disease-suppressive. All 2018/19 soils displayed some microbe-mediated disease suppression, three being more suppressive than others. Two had possible ‘specific’ Spongospora suppression (less disease when added to the conducive soil). Thus Spongospora-suppressive soils are present in New Zealand, and abiotic and biotic soil factors influenced incidence/severity of powdery scab of potato.
... However, within the resting spore population, germination stimulation did not fully exhaust the germination potential of all resting spores, even after a period of over 2 years (Balendres et al., 2017b), providing evidence for constitutive dormancy within the resting spore population. The aggregation of resting spores into sporosori, albeit permeated with a network of internal channels (Falloon et al., 2011) could prevent or limit the exposure of the innermost resting spores to germination-inducing conditions and may thus contribute to delayed germination in some spores. This confirms earlier observations (see Harrison et al., 1997) that germination of resting spores in a single sporosorus may be staggered in a coordinated manner to ensure longterm survival and increase the chances of infection occurring. ...
Attempts at management of diseases caused by protozoan plant parasitic Phytomyxea have often been ineffective. The dormant life stage is characterised by long‐lived highly robust resting spores that are largely impervious to chemical treatment and environmental stress. This review explores some life stage weaknesses and highlights possible control measures associated with resting spore germination and zoospore taxis. With phytomyxid pathogens of agricultural importance, zoospore release from resting spores is stimulated by plant root exudates. On germination, the zoospores are attracted to host roots by chemoattractant components of root exudates. Both the relatively metabolically inactive resting spore and motile zoospore need to sense the chemical environment to determine the suitability of these germination stimulants or attractants respectively, before they can initiate an appropriate response. Blocking such sensing could inhibit resting spore germination or zoospore taxis. Conversely, the short life span and the vulnerability of zoospores to the environment require them to infect their host within a few hours after release. Identifying a mechanism or conditions that could synchronise resting spore germination in the absence of host plants could lead to diminished pathogen populations in the field.
... While non-dormant spores need only a favourable environment, dormant spores require an external germination stimulant which can be the host root exudate or nutrient solution (Neuhauser et al., 2010). Among the plasmodiophorids, S. subterranea has the most complex sporosori (Falloon et al., 2011). ...
The soil‐borne and obligate plant‐associated nature of S. subterranea has hindered a detailed study of this pathogen and in particular, the regulatory pathways driving the germination of S. subterranea remain unknown. To better understand the mechanisms that control the transition from dormancy to germination, protein profiles between dormant and germination stimulant‐treated resting spores were compared using label‐free quantitative proteomics. Among the ~680 proteins identified 20 proteins were found to be differentially expressed during the germination of S. subterranea resting spores. Elongation factor Tu, histones (H2A and H15), proteasome and DJ‐1_PfpI, involved in transcription and translation, were upregulated during the germination of resting spores. Downregulation of both actin and beta‐tubulin proteins occurred in the germinating spores, indicating that the changes in the cell wall cytoskeleton may be necessary for the morphological changes during the germination of the resting spore in S. subterranea. Our findings provide new approaches for the study of these and similar recalcitrant micro‐organisms provide the first insights into the basic protein components of S. subterranea spores. A better understanding of S. subterranea biology may lead to the development of novel approaches for the management of persistent soil inoculum.
... The pathogen persists in the soil for many years in the form of agglomerations of resting spores termed sporosori, which are highly resistant to environmental stresses (Harrison et al. 1997;Merz and Falloon 2009) and also through infection cycles on alternative hosts (Falloon 2008;Tsror et al. 2019b). Sporosori are produced in potato tuber lesions and in root galls (Falloon et al. 2011;Merz 2008). Root infections have the potential to reduce plant growth and yield (Falloon et al. 2016). ...
Potato powdery scab caused by Spongospora subterranea subsp . subterranea (Sss) causes extensive damage to the quality and marketability of tubers. Disease outbreaks in potatoes grown in virgin soils in south Israel, lead us to the hypothesis that wind-driven inoculum may also be a source of new infections. Wind and ground traps (13 of each type) were positioned near contaminated commercial potato fields with a history of powdery scab in two plots during 2013–14 (‘Nave 5’ and ‘Nave 89’). Quantification of pathogen density in soil/dust was carried out by DNA extraction and qPCR analysis. In ‘Nave 5’ plot, 58 and 45% (December and January, respectively) and 75 and 50% of the ground and wind traps, respectively, were Sss-positive, with no significant differences in Sss concentrations. In ‘Nave 89’ plot, the percentage of Sss-positive traps increased from 31% and 18% in the ground and wind traps, respectively, in February, to 100% in both trap types, in April, with no significant differences. Evaluation of the dispersal distance of Sss inoculum from contaminated fields was examined in soil samples taken from the top layer of the ground in the uncultivated area adjacent to the contaminated commercial potato fields with a history of powdery scab, in two sites (‘Nave 5’ and ‘Shalom 7’) during 2016. All soil samples, taken from uncultivated areas near the infested fields in various distances of up to 750 m, were Sss positive. This study demonstrated that Sss can be dispersed by wind, particularly in an intensive potato production region where contaminated fields exist.
... Plasmodiophora produces individual non-aggregated resting spores, while Polymyxa, Spongospora, Sorodiscus, Tetramyxa, Octomyxa, Woronina and Ligniera all produce sporosori of variable shape and size [5][6][7][8][9]. Among all the known plasmodiophorids, Spongospora has the most complex sporosori with a sponge-like structure of variable size [10]. ...
Spongospora subterranea is a soil-borne plant pathogen responsible for the economically significant root and powdery scab diseases of potato. However, the obligate biotrophic nature of S. subterranea has made the detailed study of the pathogen problematic. Here, we first compared the benefits of sporosori partial purification utilizing Ludox ® gradient centrifugation. We then undertook optimization efforts for protein isolation comparing the use of a urea buffer followed by single-pot solid-phase-enhanced sample preparation (SP3) and a sodium dodecyl sulphate (SDS) buffer followed by suspension-trapping (S-Trap). Label-free, quantitative proteomics was then used to evaluate the efficiency of the sporosori purification and the protein preparation methods. The purification protocol produced a highly purified suspension of S. subterranea sporosori without affecting the viability of the spores. The results indicated that the use of a combination of SDS and STrap for sample clean-up and digestion obtained a significantly higher number of identified proteins compared to using urea and SP3, with 218 and 652 proteins identified using the SP3 and STrap methods, respectively. The analysis of proteins by mass spectrometry showed that the number of identified proteins increased by approximately 40% after the purification of spores by Ludox ®. These results suggested a potential use of the described spore purification and protein preparation methods for the proteomics study of obligate biotrophic pathogens such as S. subterranea.
... These resting spores are aggregated together in sponge-like sporosori which vary in size from 19 to 85 μm. Falloon et al. (2011) determined the mean numbers of resting spores in sporosori to be about 700. Resting spores may then persist in the soil, where they are able to survive in a dormant state in the absence of potato cultivation for many years, or on tubers. ...
This chapter discusses the major potato diseases worldwide: late blight, early blight, wart, and powdery scab. Late blight, caused by the oomycete Phytophthora infestans, continues to be the main biotic constraint of potato production. Annual losses have been estimated to be about €6.1 billion, with major consequences to food security, especially in developing countries. Symptoms of the disease can be seen in leaves (water-soaked light to dark brown spots), stems (brown spots), and tubers (slightly depressed areas with reddish-brown color). High humidity and mild temperatures are essential for disease development and, under optimal conditions, the disease can destroy a field in a few days. Phytophthora infestans evolves continuously, mainly through recombination and migration from other areas. Thus, monitoring of P. infestans populations is critical for the design of effective management strategies. Fungicides remain as the most common tactic for late blight management, but environmental considerations are increasing the pressure to use host resistance, sanitation, and other measures. New solutions being developed to manage late blight include, among others, smart phone-based decision support systems linked to portable molecular diagnostics kits that can disseminate disease information rapidly to a large number of farmers. Emerging research topics on P. infestans include the role of the pathogen–microbiota interaction in promotion or suppression of the disease, as well as the metabolism of P. infestans.
