Wheat by Thomas Hart Benton (1967), from The Emergence of Agriculture, B. Smith

1. Molecular Data and Crop EvolutionGraduate Seminar Wrap-up and summary Wheat by Thomas Hart Benton (1967), from The Emergence of Agriculture, B. Smith

2. Plant Breeding is Just the Current Phase of Crop Evolution -N.W. Simmonds

3. 2 Crop Domestication and Evolution • Domestication • Alteration from wild state to cultivated state • Process renders inability to survive in the wild • Results in large changes from wild populations • Three centuries enough to domesticate certain grasses • Continuously occurring • Earliest cases are approximately 10,000 years ago • Wheat, lentil, Cucurbits, Phaseolus older crops • Rice, sorghum, sugarcane, soybean ca. 5,000 years ago • Sugarbeet, oil palm, rubber, forage grasses very recent

4. 3 Early Agriculture in the Americas • When did farming begin? • Prevailing view has been the transition from hunter-gatherer to agriculturist happened ca. 3500 years ago • Several millennia behind Near East and Asia • Time from domestication until ag economy is ca. 1000 years • However, data from Smith (1997) suggest much older agriculture in the Americas- perhaps 10,000 years ago • New AMS technique revealed date of squash fragments • Transition to farming may have been >6,000 years • No clear distinction between the two phases, suggesting overlap and cultivation of crops while hunting/gathering

5. 4 Ecogeographical Considerations • Centers of Origin • De Candolle (1886) recognized crop origins • N. Vavilov developed center of origin concept, proposed 12 centers • Harlan modified and broadened these views in the 1970s, suggested multiple centers due to dynamic nature of crop evolution 1 China 2 India 2a Indo-Ma 3 C. Asia 4 Near East 5 Medit. 6 Ethiopia 7 Mexico 8 S. Amer. 8a Chile 8b Brazil 1 3 2 2a 7 8 8a 8b 5 4 6

6. 5 Ecogeographical Considerations • Centers of Origin and Centers of Diversity • In practice, most crops have multiple centers or ‘non-centers’ • Centers remain critically important for crop collections • Centers and non-centers as depicted by Harlan (1975) • Domestication occurs in centers and non-centers • Non-centers: multiple domestications possible Centers Non-centers Near East (oat, cabbage) Africa (sorghum, oil palm) China (rice, cucumber) Southeast Asia (sugarcane, banana) Mesoamerica (maize, squash) South America (peanut, tobacco)

7. 6 Features of Crop Evolution • Morphology and Physiology • Non-shattering habit • Reduced seed dormancy • Reduced plant size, determinate growth habit • Shorter life cycles • Less branching, fewer flowers • Altered photoperiodic or vernalization requirements • Reductions in defense mechanisms and defense compounds • Changes in flower, seed, and fruit color • Multiple uses

8. 7 Domesticated and wild Chenopods Wild and domesticated March elder (top) Sunflower (middle) Squash (bottom) Two row and six row barley Source: B. Smith The Emergence of Agriculture

9. 8 Features of Crop Evolution • Genetic Changes • Autopolyploidy where fertility is relatively unimportant • Allopolyploidy where fertility is important • Clonal propagation • Inbreeding tolerance • Hybridization with weedy or wild relatives • Speciation within cultivated germplasm • Sex expression, apomixis • Mating System • Derivation of inbreeders from outbreeders

10. 9 Concepts in Crop Evolution • Convergent Domestication • Poaceae family contains the cereals • Domesticated between 7,000 and 12,000 years ago • Despite independent domestication of the four major complexes: • Rice (Asia), Wheat/Oats (Near East), Corn (America), Sorghum (Africa) • All were converted from small-seeded shattering grasses to large-seeded grasses with non-shattering habit • Paterson et al. (1995) studied shattering, seed mass, daylength-insensitive flowering time in sorghum, rice, and corn • Conservation of gene order is well known, however • Conservation of genes affecting these traits was unexpected

11. 10 Concepts in Crop Evolution • Implications of Convergent Domestication • Unity of cereal crop genomes now recognized • Paterson et al. (1995) study shows correspondence (map position) of genes associated with independent domestication events • “Correspondence of these (genes) transcends 65 million years of reproductive isolation” • Few genes with large effects involved in major steps in domestication • Genes may be identical in the various species • Suggests rapidity of cereal domestication- major gene changes were very important

12. 11 Case Studies in Crop Evolution • The Maize-Teosinte Story (J. Doebley and colleagues) • Modern corn (maize) was derived from the wild Mexican grass known as teosinte (Zea mays ssp. Parviglumis) • Mangelsdorf of Harvard debated Beadle of Chicago regarding maize origins; Beadle supported teosinte as maize ancestor, Mangelsdorf suggested small ears from Tehuacan Valley were primitive maize • In recent years, research by Doebley has shown maize evolved from teosinte by few major modifications, each involving a major gene • Maize is also a model for genome-size evolution in crop plants • Recent work by Bennetzen and Wessler reveals causes of genome increase

13. 12 Case Studies in Crop Evolution • Genome size evolution in maize • The maize genome is highly duplicated (up to 72% of genome) • Single genes exist in a ‘sea’ of repetitive DNA • Much of this repetitive DNA is from transposable elements • Copy number of elements ranges from 600 to 54,000 per haploid • Many are the LTR retrotransposon, in copies up to 30,000 • Other classes of repetitive DNA are the elements Tourist, Stowaway • Increase in size also due to segmental allopolyploidization • Two diploid ancestors diverged ca. 20.5 M years ago • Maize evolution driven by polyploidy, transposable elements, and major regulatory genes controlling key morphological traits

14. 13 Case Studies in Crop Evolution Two genes from maize (White and Doebley, TIG, 1998 • Teosinte has hard fruitcase, Teosinte Glume Architecture (Tga1) contributes to silica deposition in epidermal cells, causing shiny hard surface • tga1reduces lignification, slower glume/rachis growth rates- suggests regulatory gene • Unlike maize, teosinte has lateral branches with terminal tassels (male) • Maize has very short lateral branches with terminal ears (female) • Teosinte-branched (tba1) represses growth of lateral branches and selection for increased apical dominance • 2x RNA levels in ear primordia of maize compared to teosinte- suggests regulatory gene Teosinte Maize Teosinte Maize

15. 14 Case Studies in Crop Evolution • The Maize-Teosinte Story (J. Doebley and colleagues) • Doebley and Stec (1991 and others) have demonstrated five major genomic regions (QTLs) explain the genetic difference between maize and teosinte • These major regions control inflorescence development and structure and plant branching patters • Two of these regions contain tb1 and tga1 • Single mutations selected over time in incremental steps or major mutations followed by selection of modifying genes?

16. 15 Case Studies in Crop Evolution • The Gossypium Story (J. Wendel and colleagues) • Polyploidy key in cotton, wheat, coffee, oat, soybean evolution • Tetraploid cotton formed 1-2 M years ago in the New World when the Old World ‘A’ genome hybridized with the New World ‘D’ genome • Wild ‘A’ diploids and cultivated ‘AD’ tetraploid cottons produce spinnable fibers, a fact likely involved in their domestication • Both G. hirsutum and G. barbadense are AD cultivated tetraploids • The former has been selected for yield, the latter for fiber length, strength, and fineness (extra long-staple cottons) • QTLs generally do not correspond in the A and D genomes, in contrast to reported cereal domestication-QTL correspondence

17. 16 Case Studies in Crop Evolution • The Gossypium Story (J. Wendel and colleagues) • Most QTLs influencing fiber quality and yield are from the D genome • Recall that the D genome does not produce spinnable fibers • AD cultivars are superior to A cultivars, likely because of D genome • “Merger of two genomes with different evolutionary histories in a common nucleus offers unique avenues for response to selection” • May compensate for corresponding reduction in quantitative variation associated with polyploid formation (due to founder effect) • Contribution of non-cultivated genome (D) to improvements in agricultural productivity via polyploid formation

18. 17 New World England Boston 510 410 London L D Dorchester

19. 18 Daylength and Onion Adaptation Source: Magruder, 1937, J. Agr. Res. 54:719 Variety Native Latitude Tops Down & Dry Foliage 12hr 14 16 18 Wolska 52o 0 0 25 60 Yellow Rijnsburg 52o 0 0 53 55 Yellow Zittau 51o 0 12 33 42

20. 19 Origin of Yellow Storage Germplasm White Portugal / Silverskin, common yellow Yellow Globe Danvers Extra Early Yellow Mountain Danvers Downing YG Southport YG Roch. Bronze MSU Inbreds Brigham YG W Series Inbreds B Series IYG Early Hybrids IA/ MSU Early YG B Series Inbreds Early Hybrids MSU4535 B2215C W202 B2108 Bonanza IA736 Pioneer

21. 20 Concepts in Crop Evolution • Population Bottlenecks • Hilton and Gaut (1998, Genetics 150:863-872) showed modern maize contains 60% of the level of genetic diversity of its progenitor based on data from the globulin-1 gene • Eyre-Walker et al. (1998, PNAS 95:4441-4446) showed modern maize had 75% of sequence diversity at Adh1 compared to its wild progenitor • Modeling studies revealed very few Z. mays parviglumis individuals (ca. 20 for 10 gens) could be responsible for founding modern maize • Based on duration of wheat domestication (300 years), 586 individuals could explain sequence diversity found at maize Adh1

22. 21 Concepts in Crop Evolution • Population Bottlenecks and Wild Species • Only a small portion of the genetic variation present in native plant populations is captured during domestication • This ‘bottleneck’ can substantially reduce genetic variation • Similar to founder effect in nature • Paradigm: wild species thought useful only for few well-chosen traits • Xiao et al. (1996, Nature, 384:223-224 and Genetics 150:899-909) showed genes from wild rice could increase yield of cultivated rice • This wild rice species had never been tapped for useful genes • O. rufipogon was used in a backcross strategy to introduce chromosome segments influencing yield of a high-yielding variety

23. 22 Case Studies in Crop Evolution • Carrot (Daucus carota) • Wild carrot (Queen Anne’s lace) ubiquitous weed • Origin of Eastern or Anthocyanin carrot is Afghanistan • Mostly purple with some yellow coloration in root • Moved to Turkey, North Africa, and Europe by 13th century • Carotenoids can confer orange, red, yellow • Gave rise to carotene (Western) carrot, likely via mutations selected in 17th century in Netherlands • Orange carrot selected in Netherlands: several populations developed • All orange carrot traces to Late Half Long, Early Half Long, Early Scarlet Horn (Banga)

24. 23 Case Studies in Crop Evolution • Wheat (Triticum aestivum) Triticum monococcum X Unknown 2n=2x=14 2n=2x=14 AA BB AB Doubled AABB 2n=4x=48 Triticum turgidum X Triticum tauschii 2n=2x=14 DD ABD Doubled AABBDD Triticum aestivum 2n=6x=42

25. 24 Case Studies in Crop Evolution • Lowman and Purugganan, 1999. J. Hered. 90:514-520 • Cauliflower phenotype (Brassica oleracea) • Protein that causes phenotype is truncated by an insertion • The wild-type allele lacks the insertion • These alleles are likely impaired in their ability to handle • floral meristem activity • Cauliflower curd has a dense mass of arrested infloresence meristems • It is likely that the these alleles are responsible, at least in part, for • domesticated cauliflower

26. 25 Case Studies in Crop Evolution • Turnip (Brassica campestris) AA Genome, wild Selection for seed nigra (BB) Biennial habit, bulbing Annual oil seed Turnip juncea (AABB) Raph. Sativus (RR) chinensis pekinensis Selection for leafiness napus (AACC) Brassicoraphanus (AARR) napocampestris (AAAACC)

27. 26 Case Studies in Crop Evolution • Potato (Solanum tuberosum) Wild diploids 2n=24 Selection for low alkaloids in tubers Cultivated Autotetraploids 2n=48 Cultivated diploids Used in breeding Cultivated triploids Wild allopolyploids Moved to Europe Tuberosum group Tetraploids

28. 27 (from Ford-Lloyd) Beta section Southern Europe Turkey, Near East B. cicla B. maritima B. vulgaris Medicinal plant and herb use during Greek and Roman periods Selection for foliage in Europe Selection for swollen roots Leaf beet, chard Red-rooted ‘garden’ beet Mangolds Early Fodder Beet Flat, globe shapes selected Fodder Beet Swiss Chard Sugarbeet Red beet