Seminar in Evolutionary Ecology of Infectious Diseases ... · PDF fileSeminar in Evolutionary...

Seminar in Evolutionary Ecology of Infectious Diseases

November 25th

Annie Champagne Queloz

26.11.14 Annie Champagne Queloz 1

Overview

¤  Melampsora lini (rust) in Linum marginale (wild flax)

¤  Broadly virulent pathogens ⇒ in highly resistant host populations

¤  Avirulent pathogens ⇒ in susceptible populations

¤  Experimental inoculations indicated a negative trade-off between spore production (aggressiveness) and virulence.

¤  Gene-for-Gene hypothesis


Gene for gene hypothesis

¤  Harold Harry Flor

¤  Proposed in 40’s- 50’s

¤  Rust (Melamspora lini) in flax (Linum usitatissimum)

¤  This hypothesis states that for each host dominant resistance gene (R), there is a corresponding dominant avirulence gene in the pathogen (Avr) with which it interacts.

¤  The effectors of the pathogen trigger immunity (R proteins) of host plants.

¤  This coevolutionary process is more advantageous to the pathogens than the host plants due to the shorter generation time and large population sizes. (Thrall et al. 2014. Trends Plant Sci )


Virulence

¤  Defined as the ability of a pathogen to overcome a given host resistance gene.

¤  At the population level, virulence can be thought of as the average ability of a pathogen population to overcome the diversity of resistance genes present in the corresponding host population.

¤  Avirulence genes in pathogen ⇒ Avr effectors ¤  Increase fitness on its host

¤  Avirulence ⇒ Virulence = Avr effectors = Fitness

Leach et al. 2001. Ann. Rev. Phytopathol.


Aggressiveness

¤  Pathogen fecundity ¤  the number of spores produced per pustule

¤  Pathogens have to invest significant amounts of energy in spore production. (Thrall et al. 2014. Trends Plant Sci )

Ellis et al. 2007. Annu. Rev. Phytopathol.


Objectives

Use of the Linum-Melampsora interaction to demonstrate the links among genetic diversity, host resistance, and the evolution of pathogen virulence and aggressiveness in a natural system


Linum marginale (Australian Flax)

http://plantnet.rbgsyd.nsw.gov.au/cgi-bin/NSWfl.pl?page=nswfl&lvl=sp&name=Linum~marginale http://avh.ala.org.au/occurrences/search?taxa=Linum+marginale#tab_mapView

¤  Herbaceous perennial

¤  Southern Australia


Linum marginale (Australian Flax)

¤  Kiandra Plain, Kosciuszko National Park, Australia

¤  Considerable differentiation, within and among population, in resistance to locale isolates of M. lini (Thrall et al. 2001. J. Ecol)

¤  Nonrandom spatial distribution of resistance (Thrall et al. 2001. J. Ecol.)

¤  Nearby populations share more resistant phenotypes than more distance one (Thrall et al. 2001. J. Ecol.)

Thrall et al. 2001 J. of Ecol.

Metapopulation


Melampsora lini

¤  Causing flax rust

¤  Obligate biotrophic fungus

¤  Spores are aerially dispersed

¤  Infects leaves, stems and sepals

¤  Regular sexual cycles = recombinant types

Ellis et al. 2007. Annu. Rev. Phytopathol. http://www.bioimages.org.uk/html/p5/p57288.php

Urediospores 26.11.14 Annie Champagne Queloz 9

Relationship between average host resistance and average pathogen virulence in same populations

¤  Host population (L. marginale)

¤  Experimental inoculation ¤  6 Pathotypes of M. lini: Group of pathogens having the same

virulence on a specified host.

¤  six L. marginale demes were determined by exposing 20 maternal plant lines per host population to 60 isolates of M. lini [10 isolates × 6 host populations in all pairwise combinations (20 maternal plant lines) = 7200 individual inoculation tests (any tests giving ambiguous results were repeated)

SH1 SH2 WHP1

WP2 G1 G3

SH1 SH2 WHP1

WP2 G1 G3


Fraction of hosts which could be attacked

Fraction of pathogens against which resistance was observed

The virulence of a given pathogen population increases directly with the mean resistance of plant populations


Highly virulent pathotypes don’t dominate susceptible host populations

Why??


Over prolonged periods of time, pathogen populations are highly variable and relatively mobile

Pathotype A: virulent Pathotype K: avirulent Kiandra: Resistant P1: Susceptible

A. M. Jarosz, J. J. Burdon, Evolution 45, 1618 (1991)


¤  Pathotype competition

¤  The ability to infect multiple host genotypes (greater virulence) is favored in resistant populations.

¤  There is a cost to carrying extra virulence genes

¤  Avirulence ⇒ Virulence = effector = Fitness

¤  A negative relationship between virulence and aggressiveness

Over prolonged periods of time, pathogen populations are highly variable and relatively mobile


Evaluation of the aggressiveness and the virulence

¤  Virulence essays

¤  11 lines of L. marginale

¤  6 pathotypes of M. lini: SH1, SH2, WHP1, WHP2, G1, G3

¤  Combinations of the host lines and pathotypes

¤  Susceptible or resistant

¤  Aggressiveness assays

¤  6 Pathotypes of M. lini

¤  Linum usitatissinum (universal susceptible host)

¤  4 hemocytometer counts for each of 10 pustules per pathogen isolate


More virulent pathotypes able to affect a greater proportion of resistance genes, show reduced levels of spore production

M. lini from different populations of L. marginale: Susceptible (SH1, WHP2) Intermediate (SH2, G1) Highly (WHP1, G3)

Favoured in more susceptible host populations

Favoured in more resistant host populations

of L. marginale 26.11.14 Annie Champagne Queloz 16

Evidence for a trade-off between virulence and aggressiveness

Infectivity (Virulence)

Number of overcome resistant genes in L. marginale

Average spore production (Aggressiveness)

= better fitness!


Evolutionary dynamics are highly stochastic

¤  Expectation ⇒ ¤  The pathogen with the highest reproductive rate (R0) will

eventually come to dominate

¤  In reality ⇒ ¤  A pathogen with the highest reproductive rate ≠ domination

in natural situations

¤  Frequent pathogen extinction

¤  Reinvasion by the same or different pathotypes = high variability

¤  Pathogen sexual reproduction = recombination


Trade-offs between virulence and aggressiveness play a important role in generating local adaptation in gene-for-gene system

¤  Local adaptation of pathogens to their host plants.

¤  Determined by the interaction of specific resistance and virulence genes.

¤  Prevent the emergence and evolution of highly virulent pathotypes capable of attacking all host genotypes


Evolutionary principles can be used to guide the formulation of sustainable disease management strategies


Evolutionary principles can be used to guide the formulation of sustainable disease management strategies

¤  Can minimize disease epidemics while simultaneously reducing pressure on pathogens to evolve increased infectivity and aggressiveness.

¤  Modern agriculture disrupts the coevolutionary dynamics ¤  High-intensity

¤  Multi-cropping

¤  Monoculture production


Sexual reproduction of plants serves as a compensating mechanism again pathogen infectivity

¤  Generating new genetic variation ¤  Intragenetic recombination

¤  Reshuffling of existing genes

¤  Elimination of deleterious mutation

¤  Environmental heterogeneity in natural systems


The management approaches have different effects on epidemic frequency and evolution of pathogens


The host resistance remains the best approach to control plant diseases

¤  Limits ⇒ Increase of pathogen resistance

¤  Strong selective pressure on pathogen populations = fast

evolution

¤  The repeated use of the same few resistant genes

Is not sustainable without appropriate deployment strategies


Outlooks

¤  The origin of infectivity

¤  The patterns of local adaptation in hosts and pathogens ¤  The trade-off between virulence vs aggressiveness

¤  Comparative patterns of host-pathogen interactions in natural and agricultural ecosystems

¤  Effects of agricultural practices on pathogen evolution


Questions!

Thank you for your attention


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