POLICY FORUM SCIENCE GALLEY

OVERLINE

1 Insert Deck Here 2 Genome plasticity a key 3 4 factor in the success of 5 6 polyploid wheat under 7 8 9 domestication 10 Jorge Dubcovsky†, Jan Dvorak 11 Wheat was domesticated approxi- Wheat domestication and southeastern Turkey revealed a gradual 12 mately 10,000 years ago and has since The transition from hunting and gathering increase of non-shattering einkorn spikes 13 spread worldwide to become one of the to agrarian lifestyles in western Asia was a from 9250 to 6500 years BP, a discovery in- 14 major crops. Its adaptability to diverse threshold in the evolution of human societies. terpreted as evidence of a prolonged domes- 15 environments and end-uses is surprising Domestication of three cereals – einkorn, tication period of cereals (13). The chromo- 16 given the diversity bottlenecks expected emmer, and barley – marked the beginning some locations of the genes controlling 17 from recent domestication and polyploid of that process (6). Genetic relationships be- shattering in einkorn are unknown, but in 18 speciation events. Wheat compensates for tween wild and domesticated einkorn and emmer wheat it is determined by the Br (brit- 19 these bottlenecks by capturing part of the emmer suggest that the region west of Diyar- tle rachis) loci on chromosomes 3A and 3B 20 genetic diversity of its progenitors and by bakir in southeastern Turkey is the most (14) (Fig. 1). 21 generating new diversity at a relatively likely site of their domestication (Fig. 2) (7- Another important trait for wheat domes- 22 fast pace. Frequent gene deletions and dis- 9). From this area, the expansion of agricul- tication was the loss of tough glumes, con- 23 ruptions generated by a fast replacement ture lead to the dissemination of domesti- verting hulled wheat into free-threshing 24 rate of repetitive sequences are buffered cated einkorn (T. monococcum, genomes wheat (Fig. 1). The primary genetic determi- 25 by the polyploid nature of wheat, resulting AmAm) and domesticated emmer (T. tur- nants of the free-threshing habit are recessive 26 in subtle dosage effects on which selection gidum ssp. dicoccon, genomes BBAA) mutations at the Tg (tenacious glume) loci 27 can operate. across Asia, Europe, and Africa. Southwest- (15), accompanied by modifying effects of 28 ern expansion of domesticated emmer culti- the dominant mutation at the Q locus and 29 With 620 million tons produced annually vation resulted in sympatry with the southern mutations at several other loci (15). The re- 30 worldwide, wheat provides approximately subpopulation of wild emmer (T. turgidum cent cloning of Q, which also controls the 31 one fifth of the calories consumed by hu- ssp. dicoccoides, genomes BBAA). Gene ex- square spike phenotype in common wheat, 32 mans (1). Roughly 95% of the wheat crop is changes between the northern domesticated showed that it encodes an AP2-like transcrip- 33 common wheat, used for making bread, emmer with southern wild emmer popula- tion factor. The mutation that gave rise to the 34 cookies, and pastries, whereas the remaining tions or with emmer domesticated in the Q allele is the same in tetraploid and hexap- 35 5% is durum wheat, used for making pasta southern region resulted in the formation of a loid free-threshing wheats suggesting that it 36 and other semolina products. Einkorn wheat center of emmer diversity in Southern Levant occurred only once (16). 37 and other hulled wheats, namely emmer and (Fig. 2) (9). The consequence was a subdivi- Seeds of free-threshing wheat began to 38 spelt, are today relic crops of minor eco- sion of domesticated emmer into northern appear in archeological sites about 10,000 39 nomic significance (2, 3). and southern subpopulations with an increase years before present (BP) (17). The tetraploid 40 While einkorn is a diploid species, durum in gene diversity in the latter (9). Northeast forms of these Neolithic free-threshing wheat 41 and common wheat are polyploid species expansion of domesticated emmer cultivation may be the ancestor of the modern large- 42 that originated by interspecific hybridization resulted in sympatry with Aegilops tauschii seeded, free-threshing durum (Fig. 1), which 43 of two and three different diploid species, re- (genomes DD) and the emergence of hexap- is genetically most closely related to the 44 spectively (Fig. 1). The success of these do- loid common wheat (T. aestivum, genomes Mediterranean and Ethiopian subpopulations 45 mesticated polyploid species parallels the BBAADD) (10) within the corridor stretch- of domesticated emmer (Fig. 2) (9). The first 46 success of natural polyploid species, which ing from Armenia to the southwestern archeological records of durum appeared in 47 represent more than 70% of the plant species coastal area of the Caspian Sea (11) (Fig. 2). Egypt during the Greco-Roman times (re- 48 (reviewed in (4)), and tend to have a more The genetic changes responsible for the viewed in (2)). 49 extended geographic distribution than their suite of traits that differentiate domesticated Other traits of the wheat domestication 50 close diploid relatives (5). Consequently, re- plants from their wild ancestors are referred syndrome shared by all domesticated wheats 51 cent advances in wheat genomics may shed to as the “domestication syndrome” (12). In are increased seed size (Fig. 1A-B), reduced 52 light on the genetic causes of the broad wheat, as in other cereals, a primary compo- number of tillers, more erect growth, and re- 53 adaptability of natural polyploid plant spe- nent of this syndrome was the loss of spike duced seed dormancy. One gene affecting 54 cies. shattering, preventing the grains to be scat- seed size is GPC-B1, an early regulator of 55 tered by the wind and facilitating harvesting senescence with pleiotropic effects on grain 56 (Fig. 1). Abscission scars of einkorn remains nutrient content (18). In some genotypes and 57 Department of Plant Sciences, University of California, One Shields Avenue, Davis, CA 95616, from archeological sites in northern Syria environments the accelerated grain maturity 58 USA. To whom correspondence should be addressed 59

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conferred by the functional GPC-B1 allele is the AB genomes from tetraploid wheat. mestication (13), even a slow rate of gene associated with smaller seeds (19). There- Compared to tetraploid wheat, hexaploid T. flow would probably be sufficient for domes- fore, indirect selection for large seeds may aestivum has broader adaptability to different ticated emmer to capture a significant pro- explain the fixation of the nonfunctional photoperiod and vernalization requirements, portion of the genetic diversity of its wild GPC-B1 allele in both durum and T. aesti- improved tolerance to salt, low pH, alumi- relative. vum (18). Except for Q and GPC-B1, no num, and frost, better resistance to several Additional diversity bottlenecks occurred other genes relevant to the wheat domestica- pests and diseases, and extended potential to during the transition from hulled to free- tion syndrome have been isolated so far, and make different food products (Table S2). threshing wheat (Fig. 1) and during the poly- a systematic effort to do so is long overdue. This does not mean, however, that gene ploid speciation of T. aestivum. A study Not only is this knowledge critical for under- expression in an allopolyploid is the summa- based on 27 RFLP loci showed that diversity standing the genetic and molecular mecha- tion of gene expression in its diploid ances- values in T. aestivum D genome are less than nisms of domestication, it is also possible tors. Non-additive gene expression has been 15% of those present in populations of Ae. that genetic variation at these same loci plays reported in numerous artificial allopolyploids tauschii from Transcaucasia, reflecting the an important role in the success of wheat as a (reviewed in (4, 21)). Rapid and stochastic severity of the initial polyploidy bottleneck modern crop. processes of differential gene expression (22) (11). However, in the A and B genomes of T. provide an additional source of genetic varia- aestivum, the average diversity at the nucleo- Success of wheat as a crop tion which could be important for the suc- tide level was found to be 30% of that pre- Domesticated wheat exemplifies the posi- cessful adaptation of new allopolyploids. sent in wild emmer (28). This result suggests tive correlation between ploidy and success There are detrimental aspects to poly- that difference in ploidy has presented only a as a crop. In almost all areas where domesti- ploidy as well. Polyploid speciation is ac- weak barrier to gene flow from tetraploid cated einkorn and domesticated emmer were companied by a “polyploidy bottleneck” (5), wheat, including wild emmer, to hexaploid cultivated together, it was domesticated em- in which the small number of plants contrib- wheat (29), a result also supported by the mer that became the primary cereal (2). Em- uting to the formation of a new polyploid discovery of hybrid swarms between wild mer remained the most important crop in the species constrains its initial gene diversity. emmer and common wheat (30). In sum- Fertile Crescent until the early Bronze Age, As only a few Ae. tauschii genotypes partici- mary, hexaploid wheat has captured a larger when it was replaced by free-threshing wheat pated in the origin of T. aestivum (23, 24), its portion of the natural gene diversity present (2). Even though a free-threshing form of D-genome diversity is expected to be limited. in its tetraploid ancestor than in its diploid einkorn has been identified, it is not widely Recent advances in the understanding of ancestor. cultivated because of the association between the dynamics of gene diversity during do- The proportion of diversity captured by T. soft glumes and reduced ear length in this mestication and the subsequent evolution of aestivum from both ancestors is likely to in- diploid species (17). polyploid wheat are reviewed in the follow- crease in the future as modern wheat breed- The story repeated itself with hexaploid ing sections to reconcile these opposing ef- ers, realizing the importance of expanding T. aestivum expanding further than durum. fects of polyploidy and shed light on the diversity for successful crop improvement, Today, hexaploid T. aestivum accounts for mechanisms by which T. aestivum come to are starting to use synthetic wheats in their most of the global wheat crop and is grown be one of humankind’s most important crops breeding programs (31). Synthetic wheats are from Norway and Russia at 65° N to Argen- (Fig. 2). produced by hybridizing different tetraploid tina at 45° S (Fig. 2) (20). However, in tropi- wheats and Ae. tauschii genotypes and then cal and subtropical regions wheat is restricted The capture of pre-existing diversity doubling the genomes by colchicine. to higher elevations. Although the domi- Domestication is accompanied by “do- nance of tetraploid wheat over diploid wheat mestication bottlenecks” resulting in reduced New sources of diversity potentially could be attributed to the greater gene diversity (reviewed by (25)). A study J. Doebley (32) analyzed mutations in robustness of tetraploid wheat, this does not utilizing 131 RFLP loci showed that gene di- plant genes contributing to domestication. He explain the dominance of T. aestivum over versity values in cultivated emmer were 58% pointed out that none of the mutations were durum. Durum often has larger seeds than of those observed in wild emmer across its null alleles and suggested that domestication hexaploid wheat (Fig. 1C-D) and similar entire geographic distribution (9). For com- was achieved mostly through “tinkering” yield potential as hexaploid wheat under op- parison, gene diversity values in domesti- rather than “disassembling” or “crippling” timum growth conditions (Table S1). cated maize and pearl millet are 57% (26) wild relatives. Although this is a valid con- The vast majority of polyploid plants, in- and 67% (27), respectively, of those present clusion for the diploid and ancient polyploid cluding wheat, originated by hybridization in their wild progenitors. It is surprising that species (maize) included in his study, null between different species (allopolyploidy). self-pollinating emmer has an approximately mutations that are lethal or have strong ef- Allopolyploidy results in the convergence in equivalent proportion of the genetic diversity fects in diploid species may have only subtle a single organism of genomes previously of its wild ancestor as cross-pollinating dosage effects in young polyploid species adapted to different environments, thus creat- maize and pearl millet. Several lines of evi- like wheat, hence appearing as “tinkering” ing the potential for the adaptation of the new dence indicate that gene flow between wild mutations with a potential to generate adap- allopolyploid species to a wider range of en- and domesticated emmer occurred in all tive variation. vironmental conditions. This has clearly been places where the two were sympatric (9). A null mutation of the GPC-B1 gene in the case for hexaploid wheat, which com- Additionally, if the emmer domestication the B genome of polyploid wheat illustrates bines the D genome from Ae. tauschii with process took as long as that of einkorn do- this point. In tetraploid wheat, the GPC-B1

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mutation caused a few days difference in ma- nalization genes as well as four large inde- Repetitive DNA can also facilitate gene turity, while in diploid rice, RNAi of the rice pendent deletions within the VRN1 first in- duplication. A study tracing the evolution of GPC gene brings about almost complete seed tron have been associated with the a dispersed multigene family in wheat sterility (supporting online text). Mutations in elimination of the vernalization requirement showed that duplication of a gene into the in- one of the three functional copies of a gene in (44-47). A deletion upstream of the PPD-D1 tergenic space accelerated its subsequent du- hexaploid wheat are expected to have more photoperiod gene is associated with the plication rate 20-fold (55). Additionally, a subtle effects than in tetraploid wheat. This widely distributed photoperiod insensitive al- promoter supplied by a neighboring mobile fact is illustrated by the higher tolerance of lele (48). Such diversity in genes regulating sequence facilitated the expression of one of hexaploid wheat to induced mutations than flowering time is particularly relevant due to the duplicated gene copies as well as the tetraploid wheat (33). The fact that most of its large impact on wheat adaptability to dif- generation of a new gene (55). This study the 21 T. aestivum chromosomes can be re- ferent environments. Deletions have also suggests that wheat intergenic DNA facili- moved to produce nullisomic plants exhibit- provided increased diversity in wheat prod- tates both gene duplication and novel expres- ing only minor phenotypic effects leaves no ucts. Puroindoline A and B gene deletions, sion of duplicated genes. Studies in rice and doubt of the buffering effect of polyploidy on which have become fixed in the A and B ge- maize provide extreme examples of mobile gene deletions. This buffering effect is nomes, are responsible for the hard grain tex- repetitive elements duplicating gene frag- eroded in ancient polyploid species (support- ture of pasta wheat. A polymorphism for a ments and, occasionally, complete genes ing online text). Puroindoline A deletion (or for a point muta- across the genome (reviewed by (56)). The The abundance of repetitive elements in tion in Puroindoline B) in the hexaploid importance of gene duplication in wheat is the wheat genomes (approximately 83% re- wheat D genome dramatically affects grain exemplified by the recently isolated wheat petitive) (34)) greatly facilitates the genera- hardness, dividing wheat into those used for VRN2 and GPC1 genes, both of which likely tion of null mutations either by insertion of bread (hard texture) or for cookies and pas- originated as dispersed duplications after the repetitive elements into genes (35) or by gene tries (soft texture) (49). wheat-rice divergence (18, 57). deletions (36, 37). As in maize, genes in The example in Fig. 3 shows two genes Although more research is needed to re- wheat are embedded within long stretches of affected by deletions within a small genomic fine our understanding of the specific nested retroelements and other mobile se- region, providing an additional example of mechanisms by which repetitive sequences quences (Fig. 3). Studies of microsynteny the high frequency of gene deletions. Such affect gene content in wheat, evidence al- among orthologous chromosomal regions deletions are fixed in polyploid wheat with ready available indicates that the dynamic across the tribe Triticeae showed that the in- an initial rate of 1.8 x 10-2 locus-1 MY-1, ten nature of wheat repetitive sequences readily tergenic space is subject to an exceedingly times faster than in wheat’s diploid ancestors generate new genetic variation which may high rate of turnover (38). For example, 69% (50). However, most deletions are still poly- facilitate the success of polyploid wheat as a of the intergenic space within orthologous morphic and represent, together with point crop. VRN2 regions from T. monococcum and the mutations, an important component of ge- A genome of tetraploid wheat (Fig. 3) has netic diversity in polyploid wheat (51). Concluding remarks been replaced over the course of the last 1.1 Evidence is accumulating that the crea- Polyploid wheat has been able to com- MYA (supporting online text). tion of artificial allopolyploids can be imme- pensate for diversity bottlenecks caused by These data, along with a comparison of diately followed by reactivation of mobile domestication and polyploidy by capturing a orthologous regions in T. urartu and the A elements (52, 53). In one Arabidopsis al- relatively large proportion of the variability genome of tetraploid wheat (29) yield an av- lotetraploid, these changes were associated of its tetraploid wild progenitor. In addition, erage replacement of 62% ± 3% of the inter- with genomic rearrangements, chromosomal new variation is rapidly generated in the dy- genic regions during the first million years of abnormalities, DNA deletions (1% of the ge- namic wheat genomes through gene dele- divergence (Fig. 4, and supporting online nome), and pollen sterility (52). A higher tions and insertions of repetitive elements text). The model in Fig. 4 predicts correctly level of DNA deletions (12-14%) was found into coding and regulatory gene regions. the very low levels of conservation observed in two wheat artificial allotetraploids involv- These mutations can then be expressed as among orthologous intergenic regions in the ing different diploid species than the ones quantitative gene dosage differences due to A, B and D genomes of wheat (29, 39) and that originated tetraploid wheat (54). An as- the polyploid nature of wheat. Synergy be- the complete divergence observed in com- sociation of these deletions with chromoso- tween the high mutation rates and the buffer- parisons of orthologous regions between mal abnormalities would limit the chances of ing effects of polyploidy makes it possible wheat and barley (40, 41) (Fig. 4). To put the these diploid combinations to generate new for polyploid wheat to capitalize on the di- magnitude of this rate into perspective, indel successful allopolyploid species. Examina- versity generated by its dynamic genomes. polymorphisms from both chimpanzee and tion of polymorphisms for gene deletions in human genomes (6 to 7 MYA divergence the D genome of T. aestivum showed that References and Notes 1.FAO, Statistical Yearbook 2005-2006. WEB Edition. time) equal less than 4% of the intergenic re- only 0.17% of the D genome has been de- United Nations (2006). gions from these genomes (42, 43). leted during the last 8000 years and that dele- 2.M. Nesbitt, D. Samuel, From staple crop to extinction? Studies documenting the impact of this tions are present at low frequencies, suggest- The archaeology and history of hulled wheats., S. Pa- st remarkably high rate of DNA replacement on ing a gradual accumulation of gene deletions dulosi, K. Hammer, J. Heller, Eds., Proc. 1 Int. Workshop on hulled wheats., Castelvecchio, Pacoli, wheat genes are starting to accumulate. Inser- rather than a burst of deletions immediately Italy. (Int. Plant Genet. Res. Inst., Rome, Italy, 1996). tions of repetitive elements within regulatory following the hexaploid what polyploidiza- 3.D. Zohary, M. Hopf, Domestication of plants in the Old regions of the wheat VRN1 and VRN3 ver- tion event (51). World (Oxford University Press, Oxford, Oxford, 3rd ed. 2000).

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4. J. F. Wendel, Plant Mol. Biol. 42, 225 (2000). 49.M. J. Giroux, C. F. Morris, Proc. Natl. Acad. Sci. ture: red = orthologous, blue = insertions after 5.G. L. Stebbins, Variation and Evolution in Plants (Co- U.S.A. 95, 6262 (1998). divergence, green = deletion in the opposite ge- lumbia University Press, New York, 1950). 50.J. Dvorak, E. D. Akhunov, Genetics 171, 323 (2005). nome (yellow region), black = not determined. 6. J. R. Harlan, D. Zohary, Science 153, 1074 (1966). 51.J. Dvorak, Z. L. Yang, F. M. You, M. C. Luo, Genetics 7.M. Heun et al., Science 278, 1312 (1997). 168, 1665 (2004). Only 31% of the orthologous intergenic regions 8.H. Ozkan et al., Theor. Appl. Genet. 110, 1052 (2005). 52.A. Madlung et al., Plant J. 41, 221 (2005). have not been replaced. See supporting online 9.M.-C. Luo et al., Theor. Appl. Genet. 114, 947 (2007). 53.K. Kashkush, M. Feldman, A. A. Levy, Nat. Genet. 33, text for details. 10.H. Kihara, Agric. and Hort. (Tokyo) 19, 13 (1944). 102 (2003). Fig. 4. Decay of the proportion of conserved 11.J. Dvorak, M. C. Luo, Z. L. Yang, H. B. Zhang, Theor. 54.H. Shaked, K. Kashkush, H. Ozkan, M. Feldman, A. A. sequences (C(t)) in orthologous intergenic re- Appl. Genet. 97, 657 (1998). Levy, Plant Cell 13, 1749 (2001). gions with divergence time. The upper and 12.K. Hammer, Kulturpflanze 32, 11 (1984). 55.E. D. Akhunov, A. R. Akhunova, J. Dvorak, Mol. Biol. 13.K. Tanno, G. Willcox, Science 311, 1886 (2006). Evol. 24, 539 (2007). lower red curves were calculated using two in- 14.V. J. Nalam, M. I. Vales, C. J. W. Watson, S. F. 56.M. Morgante, Curr. Opin. Biotech. 17, 168 (2006). dependent decay rate constants (K1 and K2), and Kianian, O. Riera-Lizarazu, Theor. Appl. Genet. 112, 57.L. Yan et al., Science 303, 1640 (2004). the blue curve using an average rate constant. 373 (2006). 58.X. Y. Kong, Y. Q. Gu, F. M. You, J. Dubcovsky, O. D. A) The blue circle represents identical se- 15.C. Jantasuriyarat, M. I. Vales, C. J. W. Watson, O. Ri- Anderson, Plant Mol. Biol. 54, 55 (2004). quences at the initial time of divergence. B) era-Lizarazu, Theor. Appl. Genet. 108, 261 (2004). 59. We thank Drs. L. Yan, W. Ramakrishna, P. SanMiguel 16.K. J. Simons et al., Genetics 172, 547 (2006). and J. Bennetzen for their help to sequence the VRN2 The comparison between T. urartu and durum 17.F. Salamini, H. Ozkan, A. Brandolini, R. Schafer- region. We also thank M. Feldman, A. Levy, P. Mo- A genome PSR920 regions was used to estimate Pregl, W. Martin, Nat. Rev. Genet. 3, 429 (2002). rell, P. McGuire, M. Nesbitt, C. Uauy, E. Akhunov, K1 (upper red curve) (29). C) The comparison 18.C. Uauy, A. Distelfeld, T. Fahima, A. Blechl, J. Dub- and I. Lowe for their valuable suggestions. This re- between einkorn and durum A genome VRN2 covsky, Science 314, 1298 (2006). search was supported by NRI USDA-CSREES Grants regions was used to estimate K2 (lower red 19.C. Uauy, J. C. Brevis, J. Dubcovsky, J. Exp. Bot. 57, No. 2007-35301-17737 and 2006-55606-16629 and curve). D) Comparison of orthologous inter- 2785 (2006). by NSF Grant No. DBI-0321757. 20.M. A. Lantican, H. J. Dubin, M. L. Morris, “Impacts of genic regions between wheat B genome international wheat breeding research in the Develop- Supporting Online Material (AY368673) and D genome (AF497474) GLU1 ing World, 1988-2002.” CIMMYT, (2005). www.sciencemag.org regions (58). E) Comparison of orthologous in- 21.Z. J. Chen, Z. F. Ni, Bioessays 28, 240 (2006). Materials and Methods tergenic regions between wheat (AF459639) 22.J. L. Wang et al., Genetics 167, 1961 (2004). Table S1, S2 and barley (AY013246) VRN1 regions (40, 41). 23.J. Dvorak, M. C. Luo, Z. L. Yang, in The origins of ag- References riculture and crop domestication A. B. Damania, J. See supporting online text for details. Valkoun, G. Willcox, C. O. Qualset, Eds. (ICARDA, Aleppo, Syria, 1998) pp. 235. FIGURE LEGENDS 24.L. E. Talbert, L. Y. Smith, M. K. Blake, Genome 41, Fig. 1. Wheat spikes showing A) brittle rachis, 402 (1998). B-D) non-brittle rachis, A-B) hulled grain, C-D) 25.E. S. Buckler, J. M. Thornsberry, S. Kresovich, Genet. naked grain. A) wild emmer wheat (T. turgidum Res. 77, 213 (2001). ssp. dicoccoides), B) domesticated emmer (T. 26.S. I. Wright et al., Science 308, 1310 (2005). 27.B. S. Gaut, M. T. Clegg, Genetics 135, 1091 (1993). turgidum ssp. dicoccon), C) durum (T. turgidum 28.A. Haudry et al., Mol. Biol. Evol. ssp. durum), and D) common wheat (T. aesti- doi:10.1093/molbev/msm077, (2007). vum). White bars represent 1 cm. Letters at the 29.J. Dvorak, E. D. Akhunov, A. R. Akhunov, K. R. Deal, lower right corner indicate the genome formula M. C. Luo, Mol. Biol. Evol. 23, 1386 (2006). of each type of wheat. Gene symbols: Br = brit- 30.D. Zohary, Z. Brick, Wheat Inf. Service 13, 6 (1961). tle rachis, Tg = tenacious glumes, and Q = 31.M. L. Warburton et al., Euphytica 149, 289 (2006). 32.J. Doebley, Science 312, 1318 (2006). square head. Photos by C. Uauy. 33.A. Slade, S. Fuerstenberg, D. Loeffler, M. Steine, D. Fig. 2. The origin and current distribution of Facciotti, Nat. Biotechnol. 23, 75 (2005). wheat. The wheat production map was provided 34.R. B. Flavell, M. D. Bennett, J. B. Smith, D. B. Smith, by Dave Hodson, CIMMYT (20). The solid line Biochem. Genet. 12, 257 (1974). ovals in the inset indicate the geographic re- 35.N. P. Harberd, R. B. Flavell, R. D. Thompson, Mol. Gen. Genet. 209, 326 (1987). gions of origin of the cultivated forms, while 36.N. Chantret et al., Plant Cell 17, 1033 (2005). the dotted red line indicates a southern center of 37.M. G. Kidwell, D. Lisch, Proc. Natl. Acad. Sci. U.S.A. emmer diversity. The approximate distributions 94, 7704 (1997). of wild emmer and Ae. tauschii are indicated by 38.T. Wicker et al., Plant Cell 15, 1186 (2003). dots and that of wild einkorn by yellow shading 39.Y. Q. Gu et al., Genetics 174, 1493 (2006). (3). Numbers indicate archeological sites where 40.P. SanMiguel, W. Ramakrishna, J. L. Bennetzen, C. S. Busso, J. Dubcovsky, Funct. Integr. Genomics 2, 70 remains of domesticated cereals dating back (2002). more than 9000 years BP were found: 1) Tell 41.W. Ramakrishna et al., Genetics 162, 1389 (2002). Aswad, 2) Abu Hureyra, 3) Cafer Höyük, 4) 42.T. S. Mikkelsen et al., Nature 437, 69 (2005). Jericho, 5) Cayönü, 6) Nahal Hemar, 7) Nevali 43.It would be interesting to compare mammalian ge- Cori (from (2)). nomes from species with more similar generation Fig. 3. DNA insertions and deletions in times to those of annual cereals, to determine the ef- m fect of generation time on these differences. orthologous VRN2 regions from the A genome 44.L. Yan et al., Theor. Appl. Genet. 109, 1677 (2004). of T. monococcum (AY485644) and the A ge- 45.A. Loukoianov, L. Yan, A. Blechl, A. Sanchez, J. Dub- nome of durum wheat variety Langdon (new covsky, Plant Physiol. 138, 2364 (2005). sequence EF540321), which diverged 1.1 ± 0.1 46.L. Yan et al., Proc. Natl. Acad. Sci. U.S.A. 103, 19581 MYA. The red lines connect orthologous re- (2006). 47.D. Fu et al., Mol. Gen. Genomics 273, 54 (2005). gions (>96% identical). Arrows represent 48.S. Faure, A. Turner, J. Beales, J. Higgins, D. A. Laurie, genes: red = orthologous, blue = ortholog ab- Photoperiodic control of flowering time in barley and sent, violet = pseudogene. Rectangles represent wheat., Plant & Animal Genome XV, San Diego, CA, repetitive elements in their actual nested struc- January 2007 (2007).

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Figure 1

Wild emmer Durum wheat Common wheat Domesticated emmer A B C D

BBAA BBAA BBAA BBAADD

Brittle rachis (Br) Non-brittle rachis (br)

Hulled grain (q, Tg) Naked grain (Q, tg) Wild forms Emmer A. tauschii 3 5 Einkorn 7

20,000 tons production 2 1

4 6 0 100 200 km

Origin of cultivated forms Secondary center Einkorn Emmer Emmer Common Durum Figure 3

Einkorn 20 kb

Durum

Figure 4

C(t) Decay of synteny in intergenic regions 1.0 A

0.8

0.6 B

0.4 C 0.2

0.0 D E 0 2 4 6 8 10 12 Million years since divergence