Population Biology of Plant Pathogens: Genetics, Ecology, and Evolution

417 Pages·2015·144.28 MB·English

by  Michael G. Milgroom

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ISBN978-0-89054-450-1
“1 > " I 1 MICHAEL G. MILGROOM
9 780890 5445
Formation
of Want Pathogens
GENETICS, ECOLOGY, AND EVOLUTION
Michael G. Milgroom
Cornell University
Ithaca, New York
!APSi
PRESS
The American PhytOpathological Society
St. Paul, Minnesota U.S.A.
To the giants on whose shoulders
I would like to stand
Photo Credits
Frontandbackcovers: PhotographsbyH. DavidThurston.
ReproducedcourtesyCornellPlantPathologyHerbarium.
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Preface
”Nothing makes sense in biology except in the light of evolution.”
Theodosius Dobzhansky
AsDobzhansky(1964) expressedsosuccinctlyinresponse This book is intended as an interpretative guide for
to the reductionism in molecular biology in the 19605, plant pathologists to understand the evolution of plant
evolution is the central paradigm in which to understand pathogens and how concepts ofpopulation genetics can
biology, and the biology ofplant pathogens is no excep- be applied in plant pathology. It is aimed at graduate
tion. The evolution—or more precisely, microevolution— students in plant pathology and assumes the reader has
ofplant pathogens has profound applied implications in a basic knowledge of plant diseases and the biology of
thepresenttime,fromtheemergenceofnewpathogensto plantpathogens.Althoughitintroducesbasicconceptsof
themanagementofoldones. These implications areespe- population genetics, it is not a comprehensive textbook;
ciallyrelevantforbreedinganddeployingdisease-resistant readers are encouraged to consult other sources to sup-
cropsandthechallengesofchemicalcontrolinthefaceof plement the population genetics theory presented here.
fungicide resistance. Every time a new disease-resistance Thisbookattemptstointroduceabroadrangeofconcepts
gene or defense mechanism is discovered in plants, there thatapplytoplantpathogens,butitisbynomeansanex-
are some who claim they have found the silver bullet, haustive reviewofthefield; it clearlylacks depth in some
forgetting that pathogens are “shifty enemies,” as E. C. areas,butinterestedreadersshouldfindreferencestopro-
Stakman (1947) pointed out in the 19405. Genomics and vide an entryto the literature in most areas formore ad—
genetic engineering may improve the technology for cre- vanced reading. All the major groups ofplant pathogens
atingresistantvarieties,butplantpathologistsmustnever (fungi, oomycetes, viruses, bacteria, and nematodes) are
forget the capacity ofpathogens to evolve means ofcir- addressed to some degree, although not equally. I admit
cumventingtheirbestefforts. havingabiastofungiandoomycetes,butthismayalsore-
The aim ofthis book is to introduce the basic con- flecttheirrelative importance asplantpathogens andthe
cepts ofpopulation biology'as a framework in which to availability ofstudies ofpopulation biology from which
understandevolutionaryphenomena in plantpathogens. to drawexamples. Finally, I liberallyused examples from
Inthiscontext, populationbiologyrepresentsthe synthe— my own research and from that ofcollaborators, mostly
sisofpopulationgeneticsandplantdiseaseepidemiology. becausethesearetheexamplesIknowbest. Iapologizeto
Populationgeneticsisadisciplinethataimstounderstand thosewhoseexcellentworkIhavenotincluded.
theprocessesthatgenerateandmaintaingeneticvariation. Readers with a sound knowledge of evolutionary
Epidemiology aims to understand the temporal and spa— biology may want to skim through parts of Chapters
tial dynamics ofdisease and pathogen populations. With 1 through 6 on basic population genetics and begin
emphases on evolution and ecologyofpathogen popula- with Chapters 7 and 8 on recombination and clonality
tions, respectively, these two disciplines are naturallyand in plant pathogens. Chapters 9 and 10 focus on evolu-
inextricablyinterlinked. However, forthe mostpart, they tion in gene-for-gene (GFG) systems and the durabili-
diverged25 years ago anddevelopedindependently. This ty ofdisease resistance. Chapter 11 addresses emerging
bookisanattempttobringthetwodisciplinesastepcloser plantdiseases, andChapter 12 aimsto showsome ofthe
togetheragain, althoughthebalanceistiltedtowardpop- applications ofpopulation biology to epidemiology and
ulationgeneticstocomplementthewealthofbackground applied agriculture. Many key terms (indicated in bold
alreadyavailableinepidemiology. whenfirstused) are foundin theglossary.
iv PREFACE
POpulation biology is a fast—moving field, and some I am especially indebted to my sabbatical host, Rafael
parts ofthisbookwill alreadybe outdatedbythe time it Jiménez-Diaz, and to Pablo Castillo, Blanca Landa, and
isprinted. Genotyping technologies and analytical meth- JuanNavas—Cortés in the plantpathologyunit at IAS for
ods are rapidly changing; their costs are coming down, innumerablestimulatingconversationsandforproviding
and theyare becomingaccessible to researchers working an environment conducive to scholarly writing. Many
on nonmodel systems. We will soon be inundated by an others have contributedby commentingon parts ofear—
avalanche ofgenomic data, in which whole—genome se— lier drafts and/or providing helpful, stimulating, and
quences will be the expected standard for genotyping. encouraging discussion. 'Ihanks go to the spring 2013
Population genomics studies of plant pathogens are in students and my co-teacher, Keith Perry, ofthe Cornell
progress in many labs, but few have been published yet. University course Biology ofPlant Pathogens, who were
This next technological/analytical wave is building and “guineapigs” subjectedto earlydraftsofseveral chapters
willbeginsweepingthrough plantpathologyasthisbook asclassassignments.
comes outbutnotin time to include here. Similarly, soft- Many thanks go to colleagues who reviewed parts
wareprogramsforanalyzingpopulationgeneticsdataare of the book or provided other substantive suggestions:
changing quickly; I have not attempted to review them Pablo Castillo, Alan Collmer, Omer Frenkel, Bill Fry,
because new and improved programs no doubt will be NikGriinwald, Iago Hale, KathieHodge, RafaelIiménez-
coming soon. Excellent reviews ofthis subject are pub— Diaz, and Robert Park. I am especially grateful to those
lishedperiodically(e.g., ExcoffierandHeckel, 2006). who provided detailed reviews ofone or more chapters:
Jim Anderson, James K. M. Brown, Fernando Garcia-
Arenal, RichardHamelin, LindaKohn, Anna—LiisaLaine,
Acknowledgments
Chris Mundt, and Aurélien Tellier. I am grateful forall
I could not have written this book without help from the help I have received, large and small, but I take full
many people. Much of the organization and first draft responsibilityforanyerrors.IalsothankTornGordon,my
was done while I was on sabbatical in Cérdoba, Spain, dedicated editor, and the production staffat APS PRESS
at the Institute of Sustainable Agriculture (IAS, CSIC) for their enthusiastic support. Special thanks for review-
and the University of Cordoba. I am grateful to the ing go to my PhD student, Mickey Drott, for reading
University of Gordoba for an appointment as visiting every word ofthis book in draft form and for the 1,001
professorandforfinancial supportfromtheUniversidad meetings we had to discuss everything from semicolons
ProgramaPropio. I amalsogratefulforfinancial support tothephilosophyofscienceflweboth survived. Finally, I
from the Regional Government of Andalusia, General couldnothavewrittenthisbookwithoutthepatience and
SecretaryforUniversities, ResearchandTechnologypro- understandingofmyfamily,who supportedmethrough-
gram for enhancing exchange ofinternational scientists. outthisproject.
M. G. M
Ithaca, NY
Contents
fl Introduction to Population Biology and Evolution 1
Population Genetics 3
Introduction to Evolutionary Processes 5
Natural Selection 6
Mutation 6
Random Genetic Drift 6
Migration 7
Recombination 7
Interactions among Evolutionary Processes 8
Challenges in Studying the Population Biology of Plant Pathogens 8
Hypothesis Testing and Interpretations of Data in Population Biology 9
The Relevance of Population Biology in Plant Pathology 10
Summary of Key Concepts 11
Recommended Reading 11
a Genetic Markers for Population Genetics 13
Characteristics of Ideal Genetic Markers 14
Selective Neutrality 15
Polymorphisms 16
Locus Specificity 16
Minimal Homoplasy 17
Independent, Unlinked Loci 1 7
Codominance 17
Repeatable, Unambiguous Scoring 17
Historical Perspectives on Genetic Markers in Plant Pathogens 17
Phenotypic Markers in Plant Pathogens 18
Molecular Markers Before theAdvent of PCR 19
Advances in Genetic Markers Because ofthe Invention of PCR 20
PCR-Based Markers ThatAre Not Locus-Specific 20
vi CONTENTS
Amplified Fragment Length Polymorphisms 21
Microsatellites 21
Discoveryof Microsatellite Loci 25
Development and Scoring of Microsatellite Markers 26
Single Nucleotide Polymorphisms 27
Multilocus Sequencing and Small-Scale SNP Genotyping 28
High-Throughput SNP Genotyping with Hybridization Arrays 29
SNP Discovery and Genotyping Using Next-Generation Sequencing 29
Ascertainment Bias 33
Quantitative-Trait Loci and Genome—Wide Association Studies 33
A Simple Guide for Choosing Genetic Markers 35
Summary of Key Concepts 35
Recommended Reading 36
Sampling and the Estimation of Genetic Diversity 37
Defining Populations and Individuals 38
Random Sampling under Ideal Conditions 38
Defining a Target Population 38
Random Sampling from POpulations of Plant Pathogens 41
Spatial Scale of Sampling 42
Temporal Considerations 42
Sample Sizes and Replication 43
Sampling in Practice 43
Sporadic Occurrence of Some Organisms 43
Independence of Sampling Units 44
Accounting for Underlying Genetic Structure 44
Genotyping 4S
Allele Frequencies and Diversity at Single Loci 46
Allele Frequencies 46
Gene Diversity 46
Genotypic Diversity 48
Genotypic Richness 48
Commonly Used Diversity lndices 50
Genotypic Evenness 51
Comparing Genotypic Diversity Between Populations 52
Diversity Estimated from Relatedness of Multilocus Genotypes 52
Nucleotide Sequence Diversity 54
CONTENTS vii
Evolutionary Processes That Increase or Decrease Genetic Diversity 55
Diversity in Populations of the Late Blight Pathogen, Phytophthora infestans 55
Summary of Key Concepts 57
Recommended Reading 57
" Mutation and Random Genetic Drift 59
Mutation 59
Types of Mutation 59
Estimating Mutation Rates in Bacteria 62
Estimating Mutation Rates in Eukaryotes 64
Mutation Rates in RNA Viruses 65
Random Genetic Drift 68
Bottlenecks in PlantVirus Populations 70
Effective Population Size 72
Mutation and Drift: Muller's Ratchet and Mutational Meltdown 74
Mutation and Drift: The Neutral Theory of Evolution 75
The infinite—Alleles Model 75
The Infinite-Sites Model 76
Gene Genealogies and the Coalescent 77
" Applications ofthe Coalescent Model 82
Summary of Key Concepts 85
Recommended Reading 86
Natural Selection 87
Fitness 87
Predicted Fitness: Single—Generation Components of Fitness 88
Realized Fitness: Population Growth Rates 94
Realized Fitness: Estimation of Relative Fitness in Serial-Passage Competition Experiments 95
Realized Fitness: Continuous Population Growth Models 98
Practical Considerations for Conducting Selection Experiments 102
Selection Acting on Single Genes: Experimental Approaches 103
Comparison of lsogenic Isolates 103
Randomizing Alleles to Genetic Backgrounds 104
Types of Selection 104
Selection Acting on Quantitative Phenotypes 105
Selection Acting on Single Genes: Negative, Positive, and Balancing Selection 107
vm CONTENTS
Density-Dependent Selection 108
Hitchhiking Selection 108
Epistatic Selection 109
Detecting Selection Using Molecular Genetic Markers 109
Detecting Selection from Within—Population Polymorphisms: Tajima’s D Revisited 109
Detecting Selection from Divergence among Species: dN/ds Ratios 110
Trans-Species Polymorphisms and Balancing Selection 111
Selection for Fungicide Resistance 112
Genetics of Fungicide Resistance and the Strength of Selection 113
Estimating Baseline Frequencies of Resistance 114
Fitness Costs Associated with Fungicide Resistance 115 .
Epidemiology and Management of Fungicide Resistance 116
Summary of Key Concepts 117
Recommended Reading 118
Migration and Population Structure 119
Direct Estimates of Migration on an Ecological Timescale: Tracking Genotypes 120
Indirect Estimates of Migration on an Evolutionary Timescale: P0pulation Structure 121
Fixation Index and Gene DiversityAnalysis 123
Additional Methods for Estimating FST 128
Estimating the Number of Migrants from FST 129
Private Alleles and Nearest-Neighbor Methods 130
Caveats for Interpreting FST and Estimates of Migration Rates 1 30
Historical Versus Current Migration and Nonequilibrium Populations 131
Isolation by Distance 132
Clustering Methods to Assess Population Structure 134
Distance-Based Trees 134
Model-Based Bayesian Clustering Methods 137
Principal ComponentsAnalysis 1 38
Estimating Migration Using Coalescent Models 140
Populations Structured by Selection: Adaptation to Local Environments 142
Differentiation in Neutral Markers and Phenotypes under Selection 142
Differentiation of Pathogen Populations on Host Species: Evidence of Host Specialization 143
Metapopulation Structure 145
Summary of Key Concepts 146
Recommended Reading 146
CONTENTS ix
Recombination and Randomly Mating Populations 147
Evolutionary and Ecological Significance of Sex and Recombination 147
Ecological Implications of Sexual Reproduction in Eukaryotic Plant Pathogens 149
Sexual Reproduction and Mating Systems in Eukaryotic Plant Pathogens 150
Mating Systems in Fungi and Oomycetes 152
Nematode Mating Systems 153
Mixed Modes of Reproduction 156
Nonmeiotic Mechanisms of Recombination in Eukaryotes 156
Gene Conversion 157
Mitotic Crossing Over 158
Parasexuality 158
Recombination in Bacteria 160
Mechanisms of Bacterial Recombination 160
Recombination and Reassortment in PlantViruses 162
Viral Recombination 162
Reassortment of Segmented Viral Genomes 162
Effects of Sex and Recombination on Genotypic Diversity 163
Random Mating in Diploid P0pulations 166
What Is Random Mating? 166
Hardy—Weinberg Equilibrium 166
Inbreeding 168
LinkageDisequilibrium and Tests for Random Mating in Haploid Populations 169
Causes of Linkage Disequilibrium 171
Selection 172
Linkage 173
Migration and Population Admixture 174
Random Genetic Drift 174
Statistical Analysis of Linkage Disequilibrium 175
Multilocus Estimation of Linkage Disequilibrium: The Index ofAssociation 176
Clone Correctionsfor Estimating Linkage Disequilibrium 176
Additional Tests of Random Mating 177
ParsimonyTree-Length Permutation Test 177
Mating-Type Ratios 178
Genotypic Diversity 178
Frequency of Sex When Populations Appearto Be Randomly Mating 179
Estimating the Frequency of Sex Experimentally 179
Changes in Linkage Disequilibrium to Estimate the Contribution of Sexual Inoculum 179
Mark-Release-Recapture Experiments to Estimate Recombination 181