How did plants evolve under domestication? Fate of genetic diversity

Or: Why are the British tea drinkers? Why is the basketball team in Boston called the Celtics?

© Paul Gepts 2011


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PLB143: Readings - Lecture 15

  • Required:
  • Additional readings:
    • Buckler E, Thornsberry J and Kresovich S (2001) Molecular diversity, structure, and domestication of grasses. Genetical Research 77:213-218
    • Crow JF, Kimura M (1970) An introduction to population genetics theory. Harper & Row, NY
    • Duvick DN (1984) Genetic diversity in major farm crops on the farm and in reserve. Econ. Bot. 38: 161-178
    • Hargrove TR, Coffman WR, Cabanilla VL (1979) Genetic interrelationships of improved rice varieties in Asia. IRRI Reseach Paper Series No. 23
    • Hobhouse H (1986) Seeds of change. Harper & Row, NY
    • Hoyt E (1988) Conserving the wild relatives of crops. International Board Plant Genet. Res., Rome
    • Saghai Maroof MA, Soliman, KM, Jorgensen RA, Allard RW (1984) Ribosomal DNA spacer-length polymorphisms in barley, Mendelian inheritance, chromosomal location, and population dynamics. Proc. Nat. Acad. Sci. 81: 8014-8018
    • Ford-Lloyd BV, Brar D, Khush GS, Jackson MT, Virk PS (2009) Genetic erosion over time of rice landrace agrobiodiversity. Plant Genetic Resources 7:163-168
    • Smale M, Reynolds MP, Warburton M, Skovmand B, Trethowan R, Singh RP, Ortiz-Monasterio I, Crossa J (2002) Dimensions of diversity in modern spring bread wheat in developing countries from 1965. Crop Sci 42:1766-1779
    • Reif JC, Zhang P, Dreisigacker S, Warburton ML, van Ginkel M, Hoisington D, Bohn M, Melchinger AE (2005) Wheat genetic diversity trends during domestication and breeding. TAG Theoretical and Applied Genetics 110:859-864
    • Keesing F, Belden LK, Daszak P, Dobson A, Harvell CD, Holt RD, Hudson P, Jolles A, Jones KE, Mitchell CE, Myers SS, Bogich T, Ostfeld RS (2010) Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468:647-652
  • Presentation slides

Lecture 15 Plan

  • Major directions in crop evolution research
  • What is genetic diversity and how do we measure it?
  • Uncoupling of trends in genetic diversity at the molecular and phenotypic levels. How do we explain that?
  • Why is genetic diversity important? The case of disease resistance
  • How diverse or uniform are our crops?


Two major directions in crop evolution research

  • Search for the ancestor
    • First part of the course
    • Traditional goal of crop evolution studies
  • Evolution under domestication
    • Compare wild progenitor and cultivated descendant
    • This lecture and the 2 following ones will deal with differences that have appeared under domestication: genetic diversity, phenotype differences and their genetic control, and physiological and ecological differences.

Search for the ancestor

  • Agriculture is a prerequisite for the development of civilizations
  • Multiple origins of agriculture
  • Conditions promoting switch to agriculture
  • Centers of domestication
  • Each center with its own assemblage of crops
  • Fully domesticated crops cannot survive in the wild
  • Domestication syndrome
  • Some have characteristics of weeds
  • Role of hybridization
  • Humans were not the first ones!
  • Multidisciplinary approach


The domestication process

  • Definition:
    • Selection process for adaptation to the human (cultivated) environment (farmers and consumers)
  • Stages:
    • initial domestication
    • dispersal within the region of domestication
    • long-range dispersal
  • Effects on genetic diversity?


What is genetic diversity?

  • Types of traits
    • growth habit
    • disease and pest resistances
    • tolerance to abiotic stresses
    • quality
    • harvest index and yield
  • Types of plant materials
    • Gene pools: I, II, III, IV (see Lecture 5 )
    • Primary gene pool
    • wild progenitor, landraces, obsolete cultivars, advanced breeding lines, modern cultivars


How do we measure genetic diversity?

  • Morphological (phenotypic) traits
    • usually of agronomic importance:
      • growth habit, seed size and shape
      • phenology
    • problem: gene expression
  • Molecular markers
    • see Lecture 5: RFLP, RAPD
    • problem: more cumbersome
  • Contrasting results

Experiments to measure evolution of genetic diversity at the molecular level

  1. Chloroplast DNA in various species (Doebley 1992)
  2. Cereal diversity (Buckler et al. 2001)
  3. M13-homologous sequences in common-bean (Sonnante et al. 1994)

  • Chloroplast DNA
    cpDNA
  • Cereal nuclear sequence diversity
    Pdf file

  • RFLPs for M13-related sequences
    M13


Relative genetic uniformity of major U.S. crops

(National Research Council 1972)

Crop Acreage
(millions)
Value
(millions)
Total no. var. Major var. Acreage (%)
Beans, dry 1.4 143 25 2 60
Beans, snap 0.3 99 70 3 76
Cotton 11.2 120 50 3 53
Maize 66.3 5200 197 6 71
Peanut 1.4 312 15 9 95
Soybean 42.4 2500 62 6 56
Wheat 44.3 1800 269 9 50








Interpretation of the uncoupling in genetic diversity trends

  • What do we expect?
    • Evolutionary factors
    • Domestication in a limited area
  • What is an important difference between mutations with a phenotypic advantage/disadvantage and neutral mutations?
    • Probability of survival of mutant genes in large populations
    • Different evolutionary factors involved




Evolutionary factors

  • Selection: effect on genetic diversity:
    • Initial domestication
    • Later dispersal
    • Modern plant breeding, but…
  • Genetic drift: effect on genetic diversity:
    • Sampling during domestication
    • Later dispersal
    Mutation: effect on genetic diversity: ↑ or
    • Selection of novelties

    Migration/hybridization: effect on genetic diversity: or

 

Other causes of genetic erosion







Potential effect of lack of diversity on crop disease status

Three examples

Example 1: A recent wake-up call: Southern corn leaf blight (Helminthosporium maydis) epidemic (1970)
  • In 1970, country-wide epidemic leading to a loss of 15% of corn production
    • Started in Florida and moved northwards
    • Leaf disease caused by a fungus, Helmintosporium maydis
      • Known to exist before the epidemic
    • Only maize with T cytoplasm
  • Southern corn leaf blight epidemic (1970)


    • What is the T cytoplasm?
      • Maize varieties = hybrid varieties to use heterosis:
        A (female) x B (male)--> F1 with yield >>  A or B
      • To get high levels of hybrid seeds:
        • traditional way: "detasselling"
        • novel way: cytoplasmic sterility: gene in mtDNA leads to male sterility --> no need to detassel; requires male fertility restorer gene in B to restore fertility in F1!
      • New strain of H. maydis in 1969-1970:
        • More virulent on maize lines with T cytoplasm
        • Because utilization of T cytoplasm had become widespread --> epidemic affecting most of U.S. corn belt


Example 2: The rust (Hemileia vastatrix) epidemic in coffee
  • Coffea arabica originated in Ethiopia (mountainous area!) but coffee growing and brewing may have started in Ethiopia or Arabia. When?
    • First historical records: Yemen (14th century) --> export via port of Mocha (limited to Yemen until 1700)
    • First European coffee house: Venice (1615)
  • Introduction of coffee elsewhere: live plants (non-dormant seeds); Dutch: to India, Ceylon, and Java; French: to island of Bourbon (Reunion) --> S. America (Colombia) 
  • Java --> Amsterdam --> Hawaii: Kona or Surinam --> Brazil or Paris --> Martinique, Jamaica (Blue Mountain), etc.
  • In 1868, Ceylon was the leading coffee producer (export of 100 million lbs); by 1885, no coffee could be exported
    • leaf disease caused by a fungus, Hemileia vastatrix
    • Java 1876; East Africa 1894; Brazil 1970
    • made worse by limited diversity; highly variable pathogen
    • controlled by fungicides --> uneconomical in many regions except where optimal climate
    • genetic resistance: C.canephora (Robusta); lower quality: cheap blends and instant coffee
    • replace by other crops: e.g., tea


  • Coffee leaves, flowers, berries

  • Coffee bushes

  • Coffee-growing region in Colombia




Example 3:

Late blight in potato
  • Introduced into Europe (Isle of Wight) in 1845 from Americas
  • Quick dispersal in the British islands and the continent; in Ireland, major epidemics in 1845-46: island-wide potato failure
  • Control measures known at that time: plant only every 6th year, use clean seed tubers not connected to diseased field; do not feed diseased tubers to stock w/o boiling
  • Ireland = agricultural colony of Great Britain
    • absentee (foreign) landlords - Irish serfs
    • potato = major staple; wheat = export crop
    • no major industries: elimination of competition with GB; high unemployment
    • 9 million people before epidemic; 1 million deaths: starvation, diseases (cholera, typhus, etc.)
    • 1.5 million emigrants after epidemic; 5.5 million emigrants until WWI, many to U.S. East Coast (Boston!)





How is uniformity of our crops evolving (Duvick 1984)?



Lecture 13 Main Findings

  • Major directions in crop evolution research:
    • Identification of wild ancestor
    • Comparison of wild ancestor and cultivated descendant
  • What is genetic diversity and how do we measure it?
    • Useful (phenotypic) traits: farmer, consumer
    • Molecular markers: RAPDs, RFLPs, etc.
  • Uncoupling of trends in genetic diversity at the molecular and phenotypic levels. How do we explain that?
    • Phenotypic traits: increase in diversity; molecular markers: decrease in diversity
    • Inevitable reduction in genetic diversity:
      • domestication: selection, dispersal
      • economic and cultural pressures
    • Major difference between the two types of traits: probability of survival in cultivated environment: favors survival of phenotypic traits with major, "favorable" effect
  • Why is genetic diversity important?
    • The case of disease resistance: lack of diversity leads to genetic vulnerability, i.e. development of large-scale disease epidemics
    • Limited progress from selection in breeding programs to improve crops
  • How diverse or uniform are our crops?
    • Our crops are generally very uniform; however, there is a reversal in longtime trend towards increased diversification, both in space and time

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