Evolutionary bi-stability in pathogen transmission mode

Bosch, Frank van den; Fraaije, Bart A.; Berg, Femke van den; Shaw, M. W.

doi:10.1098/rspb.2009.2211

Cited by 31 publications

(22 citation statements)

References 52 publications

(77 reference statements)

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“…In other systems, transmission may also be “vertical”, that is to say the pathogen infects the host’s offspring [2]. Although many pathogens spread by a combination of horizontal and vertical transmission, these two transmission modes require specific adaptations of the pathogen that can be mutually exclusive, resulting in a trade-off between horizontal and vertical transmission [1]. While an inverse relation between aggressiveness and vertical transmission has been shown for some pathogens [3], the ability to transmit by seed may have significant advantages for pathogens, such as long-term survival, maximum opportunity for progeny infection and long distance dissemination [4,5].…”

Section: Introductionmentioning

confidence: 99%

The Arabidopsis thaliana-Alternaria brassicicola pathosystem: A model interaction for investigating seed transmission of necrotrophic fungi

et al. 2012

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BackgroundSeed transmission constitutes a major component of the parasitic cycle for several fungal pathogens. However, very little is known concerning fungal or plant genetic factors that impact seed transmission and mechanisms underlying this key biological trait have yet to be clarified. Such lack of available data could be probably explained by the absence of suitable model pathosystem to study plant-fungus interactions during the plant reproductive phase.ResultsHere we report on setting up a new pathosystem that could facilitate the study of fungal seed transmission. Reproductive organs of Arabidopsis thaliana were inoculated with Alternaria brassicicola conidia. Parameters (floral vs fruit route, seed collection date, plant and silique developmental stages) that could influence the seed transmission efficiency were tested to define optimal seed infection conditions. Microscopic observations revealed that the fungus penetrates siliques through cellular junctions, replum and stomata, and into seed coats either directly or through cracks. The ability of the osmosensitive fungal mutant nik1Δ3 to transmit to A. thaliana seeds was analyzed. A significant decrease in seed transmission rate was observed compared to the wild-type parental strain, confirming that a functional osmoregulation pathway is required for efficient seed transmission of the fungus. Similarly, to test the role of flavonoids in seed coat protection against pathogens, a transparent testa Arabidopsis mutant (tt4-1) not producing any flavonoid was used as host plant. Unexpectedly, tt4-1 seeds were infected to a significantly lower extent than wild-type seeds, possibly due to over-accumulation of other antimicrobial metabolites.ConclusionsThe Arabidopsis thaliana-Alternaria brassicicola pathosystem, that have been widely used to study plant-pathogen interactions during the vegetative phase, also proved to constitute a suitable model pathosystem for detailed analysis of plant-pathogen interactions during the reproductive phase. We demonstrated that it provides an excellent system for investigating the impact of different fungal or plant mutations on the seed transmission process and therefore paves the way towards future high-throughput screening of both Arabidopsis and fungal mutant.

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Section: Introductionmentioning

confidence: 99%

The Arabidopsis thaliana-Alternaria brassicicola pathosystem: A model interaction for investigating seed transmission of necrotrophic fungi

et al. 2012

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“…A mixed strategy, blending transmission modes, may also occur. While mixed strategies have been previously considered to be transitory in nature, with fitness trade-offs6 selecting for the evolutionarily preferred mode7, it is possible that the mixed strategy can be the more advantageous scenario particularly if the transmission modes are not exclusive of one another48. However, the adaptive features that may enable the persistence of an evolutionary favorable mixed strategy are not well understood.…”

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confidence: 99%

Hitchhiking of host biology by beneficial symbionts enhances transmission

Ott

Cruciger

Dacks

et al. 2014

Sci Rep

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Transmission plays a key role in the evolution of symbiosis. Mixed mode transmission combines horizontal and vertical mechanisms for symbiont acquisition. However, features that enable mixed transmission are poorly understood. Here, we determine the mechanistic basis for the recruitment of the beneficial bacterium, Aeromonas veronii by the leech, Hirudo verbana. We demonstrate that host mucosal secretions complement imperfect symbiont vertical transmission. First, we show that the A. veronii population within secretions originates from the host digestive tract and proliferates synchronously with shedding frequency, demonstrating the coupling of partner biology. Furthermore, leeches are attracted to these castings with oral contact proving sufficient for symbiont transmission. Leech attraction to mucus is not affected by the symbiont state of either the host or mucus, suggesting that A. veronii exploits preexisting host behavior and physiological traits. A dual transmission mode, integrating multiple layers of host contributions, may prove evolutionarily advantageous for a wide range of symbioses. Using such a strategy, host infection is ensured, while also providing access to a higher genetic diversity of symbionts. Countless host-associated microbes exhibit mixed mode transmission, supporting the use of the leech symbiosis as a model for enhancing our understanding of the specificity, establishment and persistence of microbiotas.

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“…This picture is certain to be over‐simplified, but is a clear and testable hypothesis about the main drivers of the changes in prevalence observed in the Broadbalk experiment. It ignores evolutionary changes in virulence and aggressiveness, for which there is evidence in both pathogens (Cowger & Mundt, ; van den Bosch et al ., ). Such changes are likely to proceed faster when regional disease severity is greater, because both fungi are heterothallic and require dissimilar isolates to infect adjacent tissue in order for sexual reproduction and reassortment to occur (Cowger & Brunner, ).…”

Section: Discussionmentioning

confidence: 97%

“…Changes in prevalence and severity in England and Wales during 1970–2003 were well correlated with measurements of DNA characteristic of the two species in archived wheat samples from the Broadbalk continuous wheat experiment at Rothamsted in southeast England. This series was then used to construct a record of abundance reaching back to the 1840s (Bearchell et al ., ; Shaw et al ., ; van den Bosch et al ., ). Mycosphaerella graminicola was abundant in two periods: in the mid‐19th century and since the 1980s.…”

Section: Introductionmentioning

confidence: 97%

Sulphate and sulphurous acid alter the relative susceptibility of wheat to Phaeosphaeria nodorum and Mycosphaerella graminicola

Chandramohan

Shaw

2013

Plant Pathology

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The relative abundances of DNA of Mycosphaerella graminicola and Phaeosphaeria nodorum in archived wheat samples are closely correlated with UK anthropogenic emissions of oxidized sulphur over the last 160 years. To test whether this could be a causal relationship, possible modes of action of sulphur on the two fungi were examined. Mycelial growth of the two fungi in solutions of sulphurous acid was similar. Sulphurous acid at pH 4 reduced percentage germination of P. nodorum conidia more strongly than M. graminicola conidia. In spray inoculations of wheat cv. Squarehead's Master, Cappelle Desprez and Riband with water or sulphurous acid (pH 4), the ratio of leaves infected by P. nodorum to leaves infected by M. graminicola was increased by factors of 2Á5, 2Á1 and 0Á6, respectively at pH 4. The same three cultivars of wheat were grown in sand and vermiculite and fertilized with nutrient solution containing 2Á5 or 0Á5 mM sulphate. Both pathogens infected less frequently at 2Á5 mM sulphate, by a factor of about 2. The severity of infection by M. graminicola was reduced on all three cultivars by a factor of about 4Á5 at 2Á5 mM sulphate, but severity of P. nodorum was reduced only by a factor of about 2. Both elevated free sulphate concentrations in soil and sulphite in rainwater could therefore increase the prevalence of P. nodorum relative to M. graminicola, which is consistent with the historical changes in abundance.

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Evolutionary bi-stability in pathogen transmission mode

Cited by 31 publications

References 52 publications

The Arabidopsis thaliana-Alternaria brassicicola pathosystem: A model interaction for investigating seed transmission of necrotrophic fungi

The Arabidopsis thaliana-Alternaria brassicicola pathosystem: A model interaction for investigating seed transmission of necrotrophic fungi

Hitchhiking of host biology by beneficial symbionts enhances transmission

Sulphate and sulphurous acid alter the relative susceptibility of wheat to Phaeosphaeria nodorum and Mycosphaerella graminicola

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