RESISTANCE TO PATHOGENS:

EVOLUTION, CO-EVOLUTION AND USE IN

DISEASE CONTROL
 GENETIC RESISTANCE

A major strategy for the control of pathogens

(infectious diseases) in crops

Also important for the control of pests

Scientific use since early XXth century:

Biffen, R.H. (1905) Mendel’s laws of inheritance and

wheat breeding.J.Agr.Sci. 1: 4
Advantages of resistance:

Highly efficient
Specific
Environment friendly
Unexpensive

But resistance is eroded: usually it is not durable

Durable resistance:
A resistance that remains effective while being extensively
used in agriculture for a long period (in an environment
conductive to the disease)

Johnson, R. (1981) Phytopathology 71:567

The erosion of resistance: boom and bust cycles

McDonald, APS net

The erosion of resistance: boom and bust cycles

Resistant 8
7

Susceptible
3
Brown. 2015. Annu. Rev. Phytopathol. 53:513
2
Duration of resistance

16

14

12

10
Fungi x = 6.5 years
8

6 N=27
4

0
1-3 yr 4-6 yr 7-9 yr 10-12 yr 13-15 yr > 15 yr

18

16 Viruses x = 12.5 years

14

12

10
N=21
8

2 McDonald & Linde . 2002 ARP 40:349

0 García-Arenal & McDonald. 2003.
1-3 yr 4-6 yr 7-9 yr 10-12 yr 13-15 yr > 15 yr Phytopathology 93: 941
Host-Pathogen co-evolution
Reciprocal adaptive genetic change in two or more species

Woolhouse et al. 2002. Nat. Genet. 32: 569

Flor, H. H. (1955) Host-parasite interactions in flax-its genetic and other
implications. Phytopathology 45, 680-685.

Melampsora lini x Linum usitatissimum

Models of host-pathogen co-evolution

Fraile & García-Arenal. 2010. Adv. Virus. Res. 76:1

Gene-for-Gene (GFG) model

Some resistance (infectivity) genes are intrinsically more efficient

than other, conferring protection (infection) to a larger set of
pathogen (host) genotypes

Universal infectivity occurs in pathogens

RESISTANCE

AVIRULENCE A-B- A-bb aaB- aabb

aA aB + + + +
AAaB - - + +
aAAB - + - +
AAAB - - - +
Gene-for-Gene (GFG) model
Recognition of the pathogen by the host determines resistance

Milgroom, MG. 2015. Population biology of plant pathogens. APS Press.

Gene-for-Gene (GFG) model
Recognition of the pathogen by the host determines resistance

Stukenbrock & McDonald. 2009. MPMI 22:371

 Models of host-pathogen co-evolution
Arms race

R gene frequency

Trench warfare avr gene frequency

Woolhouse et al. 2002. Nat. Genet. 32: 569

Resistance-breaking in wild ecosystems?

Senecio vulgaris Erysiphe fischeri

0,6 0,6

0,5 0,5

0,4 0,4

0,3 0,3
Plant lines / fungus isolate

0,2 0,2

0,1 0,1

6E-16 6E-16
0 1 2 3 4 5 6 7 8 9 10 11 1 2 3 4 5
-0,1
0,6 -0,1
0,6
No. R genes / line No. Avr genes / isolate
0,5 0,5

0,4 0,4

0,3 0,3

0,2 0,2

0,1 0,1

6E-16 0
R1 R2 R3 R4 R5 R6 R7 R8 R9 R10 R11 R12 R13 R14 A1 A2 A3 A4 A5 A6 A7 A8 A9 A10 A11 A12 A13 A14
-0,1
14 Resistance genes 14 Avr genes

Bevant et al (1993). Plant Pathol. 42:622

Evolution of R genes

Most Encode NB-LRR proteins

CC NB ARC LRR

TIR NB ARC LRR

 RCR3 locus of resistance to
Evolution of R genes Cladosporium fulvum in Solanum
peruvianum

R loci are hypermutagenic:

● High frequency of non-

synonymous mutations
● High frequency of
deleterious mutations
● Gene duplications
● High recombination rates

R loci are under diversifying

selection

R loci polymorphisms are

maintained by balancing
selection

Hörger et al. 2012. PLoS Genet. 8: 21002813

 RCR3 locus of resistance to
Evolution of R genes Cladisporium fulvum in Solanum
peruvianum

Hörger et al. 2012. PLoS Genet. 8: 21002813

The boom and bust cycle

Milgroom, MG. 2015. Population biology of plant pathogens. APS Press.

The boom and bust cycle: equilibria

Stable equilibra require that resistance and infectivity have fitness

costs for host and pathogen, respectively

Milgroom, MG. 2015. Population biology of plant pathogens. APS Press.

Host-Pathogen co-evolution

Woolhouse et al. 2002. Nat. Genet. 32: 569

Costs of resistance

Estimation of RPM1 resistance costs in A. thaliana TG NILS

Tian et al. 2003. Nature 423: 74

Brown. 2003. Trends Genet. 19:617
Costs of resistance Rx gene of Solanum andigena
Potato virus X

CP KR CP TK

Farnham & Baulcombe 2006. PNAS USA 103: 18828

Costs of resistance

Farnham & Baulcombe 2006. PNAS USA 103: 18828

Costs of infectivity/virulence: Xanthomonas oryzae and rice

Races 9a and 9c overcome resistance of IRBB7

Vera cruz et al. 2000. PNAS 97:13500

Costs of infectivity/virulence: Tobamoviruses and pepper

P0 overcomes L+

P12 overcomes L+, L1, L2

P123 overcomes L+, L1, L2, L3

Fraile et al. 2011. Mol Biol Evol 28:1425

 Costs of infectivity/virulence: Tobamoviruses and pepper
350
Competitive abilities: P12 <> P0 0.083
300 P123 <> P0 0.002
P123 <> P12 0.470

Number of NLL
Virus Accumulation

250
(μg virus RNA/g total RNA)

200

150

100

50

0
P0 SOIL
LEAF ROOT P12 SOIL
LEAF ROOT P123 SOIL
LEAF ROOT
SURVIVAL SURVIVAL SURVIVAL
P0 P12 P123
Pathotype
Fraile et al. 2014. Mol Biol Evol 31:928
Duration of resistance

16

14

12

10
Fungi x = 6.5 years
8

6 N=27
4

0
1-3 yr 4-6 yr 7-9 yr 10-12 yr 13-15 yr > 15 yr

18

16 Viruses x = 12.5 years

14

12

10
N=21
8

2 McDonald & Linde . 2002 ARP 40:349

0 García-Arenal & McDonald. 2003.
1-3 yr 4-6 yr 7-9 yr 10-12 yr 13-15 yr > 15 yr Phytopathology 93: 941
Pathogens and pests in wild and agricultural ecosystems

1. High species diversity versus low species

diversity.
2. Low plant density versus high plant
density.
3. Clumpy distribution of plants versus
uniform distribution of plants.
4. High genetic diversity versus low genetic
diversity among plants of the same
species.
5. Low environmental homogeneity versus
high environmental homogeneity.
6. Interconnected nearly-identical
landscapes, rare in natural ecosystems,
common in agroecosystems.

Stukenbrock and McDonald,. 2008 Ann Rev

Phytopath. 46: 75.
Population dynamics of pathogens and pests in wild and
agricultural ecosystems

Fraile & García-Arenal. 2016. Curr. Op. Virol. 17:50-56

Strategies to increase resistance durability in crops

McDonald, APS net

Mixtures and Multilines

McDonald, APS net

Mixtures and Multilines

Cumulative numbers of common maize rust pustules on susceptible plants

in pure stands and in mixtures of 25% susceptible and 75% resistant plants
(adapted from Mundt and Leonard, 1986. Phytopathology 76:590 ).
McDonald, APS net
Mixtures and Multilines

Change in scald severity in mixtures of winter barley cultivars

compared as influenced by the number of component cultivars
(adapted from Newton et al., 1997. Plant Pathol 45:930).
McDonald, APS net
References

Milgroom, MG. 2015. Population biology of plant pathogens. APS Press.

Brown, JKM & Tellier, A. 2011. Plant-parastie co-evolution: bridging the gap
between gentics and ecology. Annu. Rev. Phytopathol. 49:14.

Brown, JKM. 2015. Durable resistance of crops to disease: a Darwininan

perspective. Annu. Rev. Phytopathol. 53:513.

Karasov, TL, Horton, MW, Bergelson, J. 2014. Genomic variability as a

driver of plant pathogen coevolution?. Curr. Op. Plant Biol. 18: 24.

Fraile, A & García-Arenal, F. 2010. The coevolution of plants and viruses:

resistance and pathogenicity. Adv. Virus. Res. 76:1.

Fraile, A & García-Arenal, F. 2016. Environment and evolution modulate

plant virus pathogenesis. Corr. Op. Virol. 70:50.