To resistance mechanisms and beyond: an evolutionary approach of herbicide resistance. Christophe Délye Valérie Le Corre

Transcription

1 To resistance mechanisms and beyond: an evolutionary approach of herbicide resistance Christophe Délye Valérie Le Corre

2 What parameters drive resistance evolution?

3 What parameters drive resistance evolution? Gene(s) Genetic architecture Pleiotropic effects Resistance P(appearance) / initial frequency Appearance vs. spread

4 What parameters drive resistance evolution? Gene(s) Genetic architecture Pleiotropic effects Resistance P(appearance) / initial frequency Appearance vs. spread The whole picture Understanding resistance evolution = getting the whole picture

5 What parameters drive resistance evolution? Gene(s) Genetic architecture Pleiotropic effects Resistance P(appearance) / initial frequency Appearance vs. spread

6 The genetic architecture of resistance Monogenic resistance One gene Resistance Polygenic resistance Several genes Resistance Resistance gene Gene 1 Gene 2 Gene 3 Gene 4 A B Resistance to A & B Positive crossresistance C No change in sensitivity to C No resistance D Hypersensitivity to D Negative crossresistance Resistance pattern fully inheritable by the progeny A B C Resistance to A, B, C, D Multiple resistance Resistance pattern can be dissociated during sexual reproduction D

7 Identifying resistance genes Is necessary Monogenic vs. polygenic resistance Resistance diagnosis Is only the first step towards fully understanding resistance Evolutionary biology of resistance

8 What parameters drive resistance evolution? Gene(s) Genetic architecture Pleiotropic effects Resistance P(appearance) / initial frequency Appearance vs. spread

9 The initial frequency of resistance: a tricky question How has initial resistance frequency been assessed? Low frequencies expected Massive screening of naïve populations Theoretical expectations: 10-6 / 10-9 Jasieniuk et al., 1996, Weed Sci 44: Gressel & Levy, 2006, Proc Natl Acad Sci USA 103: Field studies: up to Amaranthus rudis & glyphosate: 2.2% resistant plants Smith & Hallett, 2006, Weed Technol 20, Lolium rigidum & diclofop (ACCase inhibitor): 0.4% resistant plants Neve & Powles, 2005, Heredity 95, Lolium rigidum & ALS inhibitors: 10-4 to 10-5 TSR plants Preston & Neve, 2002, Heredity 88, 8 13 Inconsistent + variable among species and herbicides

10 The initial frequency of resistance: two standard scenarios for resistance Scenario A: De novo mutation Herbicide use Waiting time mutation resistance time Scenario B: Pre-existing mutation mutation Herbicide use Resistance present at very low frequency resistance time Application: the case of glyphosate resistance: The initial dogma was that mutation rate was very low waiting time in scenario A would be exceedingly long scenario B was unlikely

11 Million hectares The initial frequency of resistance: Why are the standard scenarios misleading? The initial frequency of resistance does not only depend on mutation rate µ Estimate of the frequency of resistant individuals in a population: Θ = 4Nµ N = Weed population size subjected to the herbicide selective pressure (i.e., all the weeds present in all the area where the herbicide is applied) Θ > 1 resistant individuals are present and can be selected! (Messer & Petrov, 2010,TREE 28, ) The case of glyphosate: Rapid increase in the total area cultivated with GMO crops and sprayed with glyphosate Low µ but tremendous N values Unavoidable evolution of resistance (Neve et al., 2011, Weed Res 51, ) Area cultivated with GMOs Source ISAAA,

12 The initial frequency of resistance: evolution of monogenic versus polygenic resistance Monogenic resistance One gene Field rate Polygenic resistance Several genes, a variety of combinations Field Field rate rate % plants % plants Θ 0 Sensitivity R plants Resistance evolution Θ 0 R plants Sensitivity Resistance evolution Θ = f(efficacy) (dose) May explain inconsistencies in the literature

13 Is assessing initial frequency of resistance to new herbicides still of importance? Probably NO in the case of major weeds which have already evolved resistance: Lack of new modes of action Where to find naïve populations? More relevant to screen populations where resistance to other herbicides has already evolved (possible pre-selection of NTSR)? Population size matters as much as mutation rate Genes for polygenic resistance likely already present in populations Crucial point: efficacy security of the field rate Field rate - Not allowing resistance expression % survivors - Compatible with regulations Efficacy security Field rate Baseline sensitivity of populations via dose-response experiments Regular baseline updates Adjustable field rate? (regionally?) 0 Herbicide rate

14 What parameters drive resistance evolution? Gene(s) Genetic architecture Pleiotropic effects Resistance P(appearance) / initial frequency Appearance vs. spread

15 Resistance appearance vs. spread Does resistance evolve globally or locally? Globally spread = predominant Locally appearance = predominant Different consequences in terms of management

16 Multiple, independent and redundant appearances of resistance seems the rule at a broad scale Multiple, independent appearances of resistance to glyphosate in the selfing broadleaf Conyza canadensis S R Genetic groups

17 Multiple, independent and redundant appearances of resistance seems the rule at a broad scale Multiple, independent appearances of mutant ACCase alleles in the cross-pollinated, windpollinated ALOMY

18 but spread exists from local origins of resistance ALOMY Mutant ACCase allele Leu Délye et al., 2010, Basic Appl Ecol 11: Organic Conventional Independent appearances Gene flow mostly via pollen 1 km

19 Why multiple appearances? Multiple appearances are likely when: Ralph & Coop (2010) Genetics 186, Θ = 4Nµ is high (>> 1) Dispersal distance of genes (σ) << area sprayed (A) Selection is strong Mutation frequency Time

20 Resistance appearance vs. spread Multiple, independent appearances of resistance seem the rule at a broad scale Resistance spread occurs from local origins What scale is local? Crucial for resistance management - Weed biology and population genetics Local resistance management Concerted weed control How can concerted weed control be implemented / promoted? Need for landscape genetics approaches: gene flow (intensity, range) and connectivity among populations across agricultural landscapes

21 What parameters drive resistance evolution? Gene(s) Genetic architecture Pleiotropic effects Resistance P(appearance) / initial frequency Appearance vs. spread

22 Pleiotropic effects of resistance = Collateral effects of resistance (e.g., fitness cost ) Dogicide-resistant Dogicide-sensitive Lower biomass output Lower reproductive output Lower hair production Comparison NOT relevant SAME species but DIFFERENT genetic backgrounds Most differences NOT related to resistance

23 Pleiotropic effects of resistance Genetic background control is one key point

24 Pleiotropic effects of resistance: TSR to ACCase inhibitors in A. myosuroides - Genetic background controlled (F1 segregating populations) - Field conditions (2 years) - Three identified ACCase mutant alleles - Most of A. myosuroides life cycle considered

25 Pleiotropic effects of resistance: TSR to ACCase inhibitors in A. myosuroides Seed production 3200 Leu Asn Gly a a a 2700 a a a 2700 a ab b 1700 SS RS RR No fitness cost Advantage?? 1700 SS RS RR No fitness cost? 1700 SS RS RR Fitness cost (recessive) Menchari et al., 2008, J Appl Ecol 45: Variable among alleles

26 Pleiotropic effects of resistance: TSR to ACCase inhibitors in A. myosuroides Seed production Gly-2078 ACCase A A 2 populations B B B B A A AB A B A 0 SS RS RR 0 SS RS RR Fitness cost varies: - With the mutant allele - With the environment - With the genetic background Menchari et al., 2008, J Appl Ecol 45:

27 Pleiotropic effects of resistance: TSR to ACCase inhibitors in A. myosuroides Germination P(germination) P(germination) P(germination) 1 Leu Asn Gly2078 0,8 0,8 0,8 0,6 0,6 0,6 0,4 0, Days Delayed germination (T et +8 days) RR SS RS 0,4 0,2 RS SS Days No visible effect RR 0,4 0,2 RR SS Days Accelerated germination (T50-8 et -4 days) RS Resistance + presowing practices Délye et al., 2013, Ann Bot 111: Resistance COST or ADVANTAGE varies with the allele Resistance but pre-sowing practices

28 Pleiotropic effects of resistance: TSR to ACCase inhibitors in A. myosuroides Least costly (beneficial?) most frequent & widespread Intermediate Most costly least frequent & widespread

29 What parameters drive resistance evolution? Gene(s) Genetic architecture Pleiotropic effects Resistance P(appearance) / initial frequency Appearance vs. spread The whole picture Evolution of TSR to ACCase inhibitors (3 alleles)

30 Evolution of TSR to ACCase inhibitors in A. myosuroides Multiple, redundant appearances Short-range natural spread (pollen) Rare, random humanmediated spread (seeds) Leu1781 = best TSR allele Pleiotropic effects characterised over the whole life-cycle of a weed for only three TSR alleles

31 A need for more studies on pleiotropic effects of resistance Few relevant studies: - Genetic background not controlled - Resistance genes not identified Most TSR alleles / NTSR genes remain to be studied What about the pleiotropic effects of combined genes?

32 Then what? Gene(s) Genetic architecture Pleiotropic effects Resistance P(appearance) / initial frequency Appearance vs. spread The whole picture Modelling Time to resistance Weed control strategies: Non-chemical weed control, dose effect, herbicide rotation vs. mixture

33 Modelling resistance evolution A meta-model that enables the unraveling and evaluation of the effects of the numerous, diverse factors involved, but is also capable of integrating all aspects of resistance evolution, is essential for understanding the adaptive process, designing resistance management strategies, and ultimately ensuring the long-term security of our food supply. This model remains to be built. Thanks for listening!