- Email: [email protected]
Crop Domestication: A Sneak-Peek into the Midpoint of Maize Evolution
Current Biology
Dispatches history. What other molecular paths lead to limblessness? Kvon et al. found that, contrary to the python ZRS, the boa constrictor ZRS drives proper Shh expression in transgenic mice enhancer assays. These data suggest that these boa sequences may support mouse limb development in a CRIPSR/Cas9mediated replacement, implying a divergence between pythons and boas. In a different taxonomic class, cetaceans lost their hindlimbs about 34 million years ago. The dolphin ZRS appears to be functional in the mouse [5]. Nevertheless, in the dolphin hindlimb bud Shh expression is absent because of a lack of HAND2 activity [20], which one can imagine is also due to loss in enhancer function. Thus, cis-acting regulatory sequences are at the center of much of the diversity in animal body plans. REFERENCES
10. Lettice, L.A., Horikoshi, T., Heaney, S.J., van Baren, M.J., van der Linde, H.C., Breedveld, G.J., Joosse, M., Akarsu, N., Oostra, B.A., Endo, N., et al. (2002). Disruption of a longrange cis-acting regulator for Shh causes preaxial polydactyly. Proc. Natl. Acad. Sci. USA 99, 7548–7553.
15. Houssaye, A., Xu, F., Helfen, L., De Buffrenil, V., Baumbach, T., and Tafforeau, P. (2011). Three-dimensional pelvis and limb anatomy of the Cenomanian hind-limbed snake Eupodophis descouensi (Squamata, Ophidia) revealed by synchrotron-radiation computed laminography. J. Vertebr. Paleontol. 31, 2–7.
11. Sagai, T., Hosoya, M., Mizushina, Y., Tamura, M., and Shiroishi, T. (2005). Elimination of a long-range cis-regulatory module causes complete loss of limb-specific Shh expression and truncation of the mouse limb. Development 132, 797–803.
16. Tchernov, E., Rieppel, O., Zaher, H., Polcyn, M.J., and Jacobs, L.L. (2000). A fossil snake with limbs. Science 287, 2010–2012.
12. Lettice, L.A., Williamson, I., Wiltshire, J.H., Peluso, S., Devenney, P.S., Hill, A.E., Essafi, A., Hagman, J., Mort, R., Grimes, G., et al. (2012). Opposing functions of the ETS factor family define Shh spatial expression in limb buds and underlie polydactyly. Dev. Cell 22, 459–467. 13. Infante, C.R., Mihala, A.G., Park, S., Wang, J.S., Johnson, K.K., Lauderdale, J.D., and Menke, D.B. (2015). Shared enhancer activity in the limbs and phallus and functional divergence of a limb-genital cis-regulatory element in snakes. Dev. Cell 35, 107–119. 14. Caldwell, M.W., and Lee, M.S.Y. (1997). A snake with legs from the marine Cretaceous of the Middle East. Nature 386, 705–709.
17. Rage, J.C., and Escuillie, F. (2003). The Cenomanian: stage of hindlimbed snakes. ologie 2002, 1–11. Carnets de Ge 18. Reeder, T.W., Townsend, T.M., Mulcahy, D.G., Noonan, B.P., Wood, P.L., Jr., Sites, J.W., Jr., and Wiens, J.J. (2015). Integrated analyses resolve conflicts over squamate reptile phylogeny and reveal unexpected placements for fossil taxa. PLoS One 10, e0118199. 19. Evans, S. (2015). PALEONTOLOGY. Four legs too many? Science 349, 374–375. 20. Thewissen, J.G., Cohn, M.J., Stevens, L.S., Bajpai, S., Heyning, J., and Horton, W.E., Jr. (2006). Developmental basis for hind-limb loss in dolphins and origin of the cetacean bodyplan. Proc. Natl. Acad. Sci. USA 103, 8414–8418.
1. Schneider, I., and Shubin, N.H. (2013). The origin of the tetrapod limb: from expeditions to enhancers. Trends Genet. 29, 419–426. 2. Zuniga, A. (2015). Next generation limb development and evolution: old questions, new perspectives. Development 142, 3810– 3820. 3. Pyron, R.A., Burbrink, F.T., and Wiens, J.J. (2013). A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evol. Biol. 13, 93.
Crop Domestication: A Sneak-Peek into the Midpoint of Maize Evolution
4. Leal, F., and Cohn, M.J. (2016). Loss and re-emergence of legs in snakes by modular evolution of Sonic hedgehog and Hoxd enhancers. Curr. Biol. 26, 2966–2973.
Garrett M. Janzen and Matthew B. Hufford*
5. Kvon, E.Z., Kamneva, O.K., Melo, U.S., Barozzi, I., Osterwalder, M., Mannion, B.J., Tissie`res, V., Pickle, C.S., Plajzer-Frick, I., Lee, E.A., et al. (2016). Progressive loss of function in a limb enhancer during snake evolution. Cell 167, 633–642. 6. Cohn, M.J., and Tickle, C. (1999). Developmental basis of limblessness and axial patterning in snakes. Nature 399, 474–479. 7. Chiang, C., Litingtung, Y., Harris, M.P., Simandl, B.K., Li, Y., Beachy, P.A., and Fallon, J.F. (2001). Manifestation of the limb prepattern: limb development in the absence of sonic hedgehog function. Dev. Biol. 236, 421–435. 8. Galli, A., Robay, D., Osterwalder, M., Bao, X., Benazet, J.D., Tariq, M., Paro, R., Mackem, S., and Zeller, R. (2010). Distinct roles of Hand2 in initiating polarity and posterior Shh expression during the onset of mouse limb bud development. PLoS Genet. 6, e1000901. 9. Riddle, R.D., Johnson, R.L., Laufer, E., and Tabin, C. (1993). Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75, 1401–1416.
Department of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, Iowa, USA *Correspondence: [email protected] http://dx.doi.org/10.1016/j.cub.2016.10.045
In a new study, DNA from a 5,310-year-old corn cob found in the Tehuaca´n Valley in Mexico was sequenced and compared to modern maize and its wild progenitor grasses. The sample was found to be an intermediate between modern maize and its wild relatives, suggesting a gradual, protracted domestication process. Maize (Zea mays subsp. mays L.) was domesticated in the Balsas River Valley of southern Mexico from a wild grass called Balsas teosinte (Zea mays subsp. parviglumis; hereafter, parviglumis) approximately 9,000 years ago [1]. When an organism is domesticated, it undergoes a suite of phenotypic changes that are collectively called the ‘domestication syndrome’ [2]. In plants, the domestication syndrome often
R1240 Current Biology 26, R1226–R1245, December 5, 2016 ª 2016 Elsevier Ltd.
includes gigantism in the harvested part(s) as well as alterations to such traits as plant size, body architecture, and seed dispersal mechanism [2,3]. The rate and sequence in which domestication traits are acquired are unique elements of a crop’s history. The genetic foundations of this process are of particular interest to researchers as they endeavor to understand and improve a crop.
Current Biology
Dispatches To study the domestication process, researchers often make genetic and morphological comparisons between a crop species and its extant wild relatives [4]. However, the use of present-day specimens to make inferences about a process stretching back thousands of years has certain limitations. For example, modern samples provide little resolution regarding the order in which domestication syndrome traits appeared and the timing of selection on genetic loci underlying these traits. Recent developments in ancient DNA (aDNA) sequencing technology are now allowing researchers to sequence archaeological specimens from multiple, ancient time points to answer questions that were once inaccessible. A new study by Jazmı´n Ramos-Madrigal and colleagues, published in this issue of Current Biology, uses a single-strand approach to generate genome-wide sequence data from a 5,310-year-old cob from the Tehuaca´n Valley in Mexico, providing a detailed look into the midpoint of maize evolution (Figure 1) [5]. The first step in any aDNA study is to find a well-preserved archaeological specimen. In the mid-1960s, renowned archaeologist Richard MacNeish identified a series of caves in the Tehuaca´n Valley in Puebla, Mexico, that had been continuously occupied for thousands of years by Native Americans. MacNeish excavated the six driest and best-preserved caves. Dry caves are an ideal location to search for preserved archaeological artifacts, as moisture accelerates decomposition rates. In these caves, MacNeish uncovered some of the oldest maize specimens yet discovered [6]. Many of these specimens were later exhibited at the Robert S. Peabody Museum of Archaeology in Andover, Massachusetts, and it was from this exhibit that Ramos-Madrigal and colleagues found their well-preserved sample, dubbed ‘Tehuaca´n162’. The authors utilized a single-stranded DNA library preparation technique [7] to prepare the specimen’s aDNA for sequencing. This method is optimized for the unique and challenging properties of aDNA. Over time, DNA in archaeological samples degrades and the amount that can be recovered diminishes. The single-stranded method minimizes further DNA loss by
Figure 1. Ancient maize from the Tehuaca´n Valley. A 5,310-year-old maize ear known as Tehuaca´n162 that was collected in an expedition led by Richard MacNeish in the 1960s, curated by the Robert S. Peabody Museum of Archaeology, and ultimately sequenced by Ramos-Madrigal and colleagues.
cutting out the DNA purification step required by double-stranded DNA methods. Use of this method generated DNA sequence from Tehuaca´n162 at an average depth of coverage of 1.7x. Population genomic analyses revealed that Tehuaca´n162 is more related to modern maize than to its wild progenitor, parviglumis, suggesting the domestication process was well on its way by 5,310 BP. Tehuaca´n162 was also shown to be similarly related to each of a panel of extant landraces. Taken together, these analyses support the idea that Tehuaca´n162 represents an intermediate step in the evolution of modern maize. Tehuaca´n162’s placement at the midpoint of maize evolution was further established at the level of individual genes. Within a set of key genes that distinguish modern maize from parviglumis, Tehuaca´n162 contains the maize allele for some genes (td1, zmgl, bt2, ba1, and tga1) and the parviglumis allele for others (zagl1, su1, and wx1). Several of these loci have been clearly linked to phenotypic changes associated with the domestication syndrome of maize [4,8]. The fact that Tehuaca´n162 shows a combination of parviglumis and modern maize alleles at domestication loci further illustrates the incomplete domestication of this specimen. Analysis of Tehuaca´n162 was particularly informative with regards to evolution of a non-shattering maize phenotype. Shattering is known to be one of the primary wild traits selected
against during plant domestication [9] and one of the five key differences between parviglumis and maize [10]. During the early stages of domestication, gatherers would have had more success collecting from plants that retained their seeds than from plants with a shattering phenotype. Weber and colleagues [11] showed that zagl1 in teosinte was associated with the shattering trait, and Vigouroux and colleagues [12] demonstrated that this gene experienced a selective sweep during domestication. However, the work of Ramos-Madrigal and colleagues shows that this sweep must have completed in the last 5,310 years, as Tehuaca´n162 has the parviglumis-like shattering allele. This finding suggests, as previously described by [8], that genes other than zagl1 (e.g., loci described in [13]) may have been more important during early selection for non-shattering. Another possible interpretation is that shattering simply was not strongly selected against prior to 5,310 BP. This interpretation seems unlikely given both the nonshattering phenotype of Tehuaca´n162 and our understanding of the domestication process. When studying domestication (or evolution in general), most genetic research uses DNA sequences from contemporary samples to make inferences regarding the evolutionary process. In contrast, the use of aDNA allows for direct observations of changes in genetic composition. Analysis of aDNA has been used to address questions including the evolution of archaic human
Current Biology 26, R1226–R1245, December 5, 2016 R1241
Current Biology
Dispatches groups such as the Denisovans [14] and the patterns of human migration associated with the onset of agriculture [15]. Previous studies have also used aDNA to address early selection and the evolution of maize in the American Southwest [16,17]. However, RamosMadrigal and co-authors provide the first study employing a whole-genome aDNA approach to explicitly address the sequence and tempo of maize domestication. As we begin to uncover the sequential order in which the ‘symptoms’ of the domestication syndrome arose in maize, we can ask if this order is also found in other domesticated plants, or if the story of domestication for each crop species is unique. Similarly, for crops that arose through multiple domestication events, aDNA analysis can help determine whether domestication is a repeatable process. The chronology of domestication events identified by Ramos-Madrigal and co-authors refines our understanding of the history of maize and reveals that domestication was a complex, protracted process. As valuable as this snapshot into the process of domestication is, it is only one snapshot. To achieve a more comprehensive vision of maize domestication, further research is necessary. In particular, additional studies should target archaeological maize samples from a broad range of time points to improve our understanding of the trajectory of domestication. The work of Ramos-Madrigal and colleagues, however, is an important step forward as we strive to understand the historical relationship between crops and humankind.
5. Ramos-Madrigal, J., Smith, B.D., Moreno-Mayar, J.V., Gopalakrishnan, S., Ross-Ibarra, J., Gilbert, M.T.P., and Wales, N. (2016). Genome sequence of a 5,310-year-old maize cob provides insights into the early stages of maize domestication. Curr. Biol. 26, 3195–3201.
12. Vigouroux, Y., McMullen, M., Hittinger, C., Houchins, K., Schulz, L., Kresovich, S., Matsuoka, Y., and Doebley, J. (2002). Identifying genes of agronomic importance in maize by screening microsatellites for evidence of selection during domestication. Proc. Nat. Acad. Sci. USA 99, 9650–9655.
6. Smith, B.D. (2005). Reassessing Coxcatla´n cave and the early history of domesticated plants in Mesoamerica. Proc. Nat. Acad. Sci. USA 102, 9438–9445.
13. Lin, Z., Li, X., Shannon, L.M., Yeh, C.-T., Wang, M.L., Bai, G., Peng, Z., Li, J., Trick, H.N., Clemente, T.E., et al. (2012). Parallel domestication of the shattering1 genes in cereals. Nat. Genet. 44, 720–724.
7. Gansauge, M.-T., and Meyer, M. (2013). Single-stranded DNA library preparation for the sequencing of ancient or damaged DNA. Nat. Methods 8, 737–748. 8. Meyer, R.S., and Purugganan, M.D. (2013). Evolution of crop species: genetics of domestication and diversification. Nat. Rev. Genet. 14, 40–852. 9. Fuller, D.Q., and Allaby, R. (2009). Seed Dispersal and Crop Domestication: Shattering, Germination and Seasonality in Evolution under Cultivation (Wiley-Blackwell), pp. 238–295. 10. Doebley, J. (2001). George Beadle’s other hypothesis: one-gene, one-trait. Genetics 158, 487–493. 11. Weber, A.L., Briggs, W.H., Rucker, J., Baltazar, B.M., de Jesu´s Sa´nchez-Gonzalez, J., Feng, P., Buckler, E.S., and Doebley, J. (2008). The genetic architecture of complex traits in teosinte (Zea mays ssp. parviglumis): new evidence from association mapping. Genetics 180, 1221–1232.
14. Meyer, M., Kircher, M., Gansauge, M.-T., Li, H., Racimo, F., Mallick, S., Schraiber, J.G., Jay, F., Pru¨fer, K., De Filippo, C., et al. (2012). A high-coverage genome sequence from an archaic Denisovan individual. Science 338, 222–226. 15. Lazaridis, I., Nadel, D., Rollefson, G., Merrett, D.C., Rohland, N., Mallick, S., Fernandes, D., Novak, M., Gamarra, B., Sirak, K., et al. (2016). Genomic insights into the origin of farming in the ancient near east. Nature 536, 419–424. 16. Jaenicke-Despres, V., Buckler, E.S., Smith, B.D., Gilbert, M.T.P., Cooper, A., Doebley, J., €a €bo, S. (2003). Early allelic selection in and Pa maize as revealed by ancient DNA. Science 302, 1206–1208. 17. da Fonseca, R.R., Smith, B.D., Wales, N., Cappellini, E., Skoglund, P., Fumagalli, M., Samaniego, J., Carøe, C., A´vila-Arcos, M.C., Hufnagel, D.E., et al. (2015). The origin and evolution of maize in the southwestern united states. Nat. Plants 1, 14003, EP–01.
Chromosome Segregation: Reconstituting the Kinetochore Frederick G. Westhorpe and Aaron F. Straight* Department of Biochemistry, Stanford Medical School, Stanford, CA, USA *Correspondence: [email protected] http://dx.doi.org/10.1016/j.cub.2016.09.051
REFERENCES 1. Matsuoka, Y., Vigouroux, Y., Goodman, M.M., Sanchez, J., Buckler, E., and Doebley, J. (2002). A single domestication for maize shown by multilocus microsatellite genotyping. Proc. Natl. Acad. Sci. USA 99, 6080–6084. 2. Gepts, P. (2010). Crop domestication as a long-term selection experiment. Plant Breed. Rev. 24, 1–44. 3. Koinange, E.M., Singh, S.P., and Gepts, P. (1996). Genetic control of the domestication syndrome in common bean. Crop Sci. 36, 1037–1045. 4. Doebley, J.F., Gaut, B.S., and Smith, B.D. (2006). The molecular genetics of crop domestication. Cell 127, 1309–1321.
Faithful chromosome segregation is accomplished by attachment of chromosomes to spindle microtubules using the kinetochore. In a major step forward in understanding the functional and structural complexity of kinetochores, a 21-subunit human centromere – kinetochore complex has been reconstituted entirely from purified components, recreating the connection between DNA and microtubule. To survive, all organisms must accurately replicate a copy of their genome and distribute it to newly forming daughter cells. Eukaryotic cells segregate their chromosomes during mitosis, first by attaching their duplicated chromosomes
R1242 Current Biology 26, R1226–R1245, December 5, 2016 ª 2016 Elsevier Ltd.
to the microtubules of the mitotic spindle, then by aligning them at the cell equator, before finally transporting one chromosome copy to each daughter cell. When chromosome segregation fails, chromosomal aneuploidies result,
Dispatches history. What other molecular paths lead to limblessness? Kvon et al. found that, contrary to the python ZRS, the boa constrictor ZRS drives proper Shh expression in transgenic mice enhancer assays. These data suggest that these boa sequences may support mouse limb development in a CRIPSR/Cas9mediated replacement, implying a divergence between pythons and boas. In a different taxonomic class, cetaceans lost their hindlimbs about 34 million years ago. The dolphin ZRS appears to be functional in the mouse [5]. Nevertheless, in the dolphin hindlimb bud Shh expression is absent because of a lack of HAND2 activity [20], which one can imagine is also due to loss in enhancer function. Thus, cis-acting regulatory sequences are at the center of much of the diversity in animal body plans. REFERENCES
10. Lettice, L.A., Horikoshi, T., Heaney, S.J., van Baren, M.J., van der Linde, H.C., Breedveld, G.J., Joosse, M., Akarsu, N., Oostra, B.A., Endo, N., et al. (2002). Disruption of a longrange cis-acting regulator for Shh causes preaxial polydactyly. Proc. Natl. Acad. Sci. USA 99, 7548–7553.
15. Houssaye, A., Xu, F., Helfen, L., De Buffrenil, V., Baumbach, T., and Tafforeau, P. (2011). Three-dimensional pelvis and limb anatomy of the Cenomanian hind-limbed snake Eupodophis descouensi (Squamata, Ophidia) revealed by synchrotron-radiation computed laminography. J. Vertebr. Paleontol. 31, 2–7.
11. Sagai, T., Hosoya, M., Mizushina, Y., Tamura, M., and Shiroishi, T. (2005). Elimination of a long-range cis-regulatory module causes complete loss of limb-specific Shh expression and truncation of the mouse limb. Development 132, 797–803.
16. Tchernov, E., Rieppel, O., Zaher, H., Polcyn, M.J., and Jacobs, L.L. (2000). A fossil snake with limbs. Science 287, 2010–2012.
12. Lettice, L.A., Williamson, I., Wiltshire, J.H., Peluso, S., Devenney, P.S., Hill, A.E., Essafi, A., Hagman, J., Mort, R., Grimes, G., et al. (2012). Opposing functions of the ETS factor family define Shh spatial expression in limb buds and underlie polydactyly. Dev. Cell 22, 459–467. 13. Infante, C.R., Mihala, A.G., Park, S., Wang, J.S., Johnson, K.K., Lauderdale, J.D., and Menke, D.B. (2015). Shared enhancer activity in the limbs and phallus and functional divergence of a limb-genital cis-regulatory element in snakes. Dev. Cell 35, 107–119. 14. Caldwell, M.W., and Lee, M.S.Y. (1997). A snake with legs from the marine Cretaceous of the Middle East. Nature 386, 705–709.
17. Rage, J.C., and Escuillie, F. (2003). The Cenomanian: stage of hindlimbed snakes. ologie 2002, 1–11. Carnets de Ge 18. Reeder, T.W., Townsend, T.M., Mulcahy, D.G., Noonan, B.P., Wood, P.L., Jr., Sites, J.W., Jr., and Wiens, J.J. (2015). Integrated analyses resolve conflicts over squamate reptile phylogeny and reveal unexpected placements for fossil taxa. PLoS One 10, e0118199. 19. Evans, S. (2015). PALEONTOLOGY. Four legs too many? Science 349, 374–375. 20. Thewissen, J.G., Cohn, M.J., Stevens, L.S., Bajpai, S., Heyning, J., and Horton, W.E., Jr. (2006). Developmental basis for hind-limb loss in dolphins and origin of the cetacean bodyplan. Proc. Natl. Acad. Sci. USA 103, 8414–8418.
1. Schneider, I., and Shubin, N.H. (2013). The origin of the tetrapod limb: from expeditions to enhancers. Trends Genet. 29, 419–426. 2. Zuniga, A. (2015). Next generation limb development and evolution: old questions, new perspectives. Development 142, 3810– 3820. 3. Pyron, R.A., Burbrink, F.T., and Wiens, J.J. (2013). A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evol. Biol. 13, 93.
Crop Domestication: A Sneak-Peek into the Midpoint of Maize Evolution
4. Leal, F., and Cohn, M.J. (2016). Loss and re-emergence of legs in snakes by modular evolution of Sonic hedgehog and Hoxd enhancers. Curr. Biol. 26, 2966–2973.
Garrett M. Janzen and Matthew B. Hufford*
5. Kvon, E.Z., Kamneva, O.K., Melo, U.S., Barozzi, I., Osterwalder, M., Mannion, B.J., Tissie`res, V., Pickle, C.S., Plajzer-Frick, I., Lee, E.A., et al. (2016). Progressive loss of function in a limb enhancer during snake evolution. Cell 167, 633–642. 6. Cohn, M.J., and Tickle, C. (1999). Developmental basis of limblessness and axial patterning in snakes. Nature 399, 474–479. 7. Chiang, C., Litingtung, Y., Harris, M.P., Simandl, B.K., Li, Y., Beachy, P.A., and Fallon, J.F. (2001). Manifestation of the limb prepattern: limb development in the absence of sonic hedgehog function. Dev. Biol. 236, 421–435. 8. Galli, A., Robay, D., Osterwalder, M., Bao, X., Benazet, J.D., Tariq, M., Paro, R., Mackem, S., and Zeller, R. (2010). Distinct roles of Hand2 in initiating polarity and posterior Shh expression during the onset of mouse limb bud development. PLoS Genet. 6, e1000901. 9. Riddle, R.D., Johnson, R.L., Laufer, E., and Tabin, C. (1993). Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75, 1401–1416.
Department of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, Iowa, USA *Correspondence: [email protected] http://dx.doi.org/10.1016/j.cub.2016.10.045
In a new study, DNA from a 5,310-year-old corn cob found in the Tehuaca´n Valley in Mexico was sequenced and compared to modern maize and its wild progenitor grasses. The sample was found to be an intermediate between modern maize and its wild relatives, suggesting a gradual, protracted domestication process. Maize (Zea mays subsp. mays L.) was domesticated in the Balsas River Valley of southern Mexico from a wild grass called Balsas teosinte (Zea mays subsp. parviglumis; hereafter, parviglumis) approximately 9,000 years ago [1]. When an organism is domesticated, it undergoes a suite of phenotypic changes that are collectively called the ‘domestication syndrome’ [2]. In plants, the domestication syndrome often
R1240 Current Biology 26, R1226–R1245, December 5, 2016 ª 2016 Elsevier Ltd.
includes gigantism in the harvested part(s) as well as alterations to such traits as plant size, body architecture, and seed dispersal mechanism [2,3]. The rate and sequence in which domestication traits are acquired are unique elements of a crop’s history. The genetic foundations of this process are of particular interest to researchers as they endeavor to understand and improve a crop.
Current Biology
Dispatches To study the domestication process, researchers often make genetic and morphological comparisons between a crop species and its extant wild relatives [4]. However, the use of present-day specimens to make inferences about a process stretching back thousands of years has certain limitations. For example, modern samples provide little resolution regarding the order in which domestication syndrome traits appeared and the timing of selection on genetic loci underlying these traits. Recent developments in ancient DNA (aDNA) sequencing technology are now allowing researchers to sequence archaeological specimens from multiple, ancient time points to answer questions that were once inaccessible. A new study by Jazmı´n Ramos-Madrigal and colleagues, published in this issue of Current Biology, uses a single-strand approach to generate genome-wide sequence data from a 5,310-year-old cob from the Tehuaca´n Valley in Mexico, providing a detailed look into the midpoint of maize evolution (Figure 1) [5]. The first step in any aDNA study is to find a well-preserved archaeological specimen. In the mid-1960s, renowned archaeologist Richard MacNeish identified a series of caves in the Tehuaca´n Valley in Puebla, Mexico, that had been continuously occupied for thousands of years by Native Americans. MacNeish excavated the six driest and best-preserved caves. Dry caves are an ideal location to search for preserved archaeological artifacts, as moisture accelerates decomposition rates. In these caves, MacNeish uncovered some of the oldest maize specimens yet discovered [6]. Many of these specimens were later exhibited at the Robert S. Peabody Museum of Archaeology in Andover, Massachusetts, and it was from this exhibit that Ramos-Madrigal and colleagues found their well-preserved sample, dubbed ‘Tehuaca´n162’. The authors utilized a single-stranded DNA library preparation technique [7] to prepare the specimen’s aDNA for sequencing. This method is optimized for the unique and challenging properties of aDNA. Over time, DNA in archaeological samples degrades and the amount that can be recovered diminishes. The single-stranded method minimizes further DNA loss by
Figure 1. Ancient maize from the Tehuaca´n Valley. A 5,310-year-old maize ear known as Tehuaca´n162 that was collected in an expedition led by Richard MacNeish in the 1960s, curated by the Robert S. Peabody Museum of Archaeology, and ultimately sequenced by Ramos-Madrigal and colleagues.
cutting out the DNA purification step required by double-stranded DNA methods. Use of this method generated DNA sequence from Tehuaca´n162 at an average depth of coverage of 1.7x. Population genomic analyses revealed that Tehuaca´n162 is more related to modern maize than to its wild progenitor, parviglumis, suggesting the domestication process was well on its way by 5,310 BP. Tehuaca´n162 was also shown to be similarly related to each of a panel of extant landraces. Taken together, these analyses support the idea that Tehuaca´n162 represents an intermediate step in the evolution of modern maize. Tehuaca´n162’s placement at the midpoint of maize evolution was further established at the level of individual genes. Within a set of key genes that distinguish modern maize from parviglumis, Tehuaca´n162 contains the maize allele for some genes (td1, zmgl, bt2, ba1, and tga1) and the parviglumis allele for others (zagl1, su1, and wx1). Several of these loci have been clearly linked to phenotypic changes associated with the domestication syndrome of maize [4,8]. The fact that Tehuaca´n162 shows a combination of parviglumis and modern maize alleles at domestication loci further illustrates the incomplete domestication of this specimen. Analysis of Tehuaca´n162 was particularly informative with regards to evolution of a non-shattering maize phenotype. Shattering is known to be one of the primary wild traits selected
against during plant domestication [9] and one of the five key differences between parviglumis and maize [10]. During the early stages of domestication, gatherers would have had more success collecting from plants that retained their seeds than from plants with a shattering phenotype. Weber and colleagues [11] showed that zagl1 in teosinte was associated with the shattering trait, and Vigouroux and colleagues [12] demonstrated that this gene experienced a selective sweep during domestication. However, the work of Ramos-Madrigal and colleagues shows that this sweep must have completed in the last 5,310 years, as Tehuaca´n162 has the parviglumis-like shattering allele. This finding suggests, as previously described by [8], that genes other than zagl1 (e.g., loci described in [13]) may have been more important during early selection for non-shattering. Another possible interpretation is that shattering simply was not strongly selected against prior to 5,310 BP. This interpretation seems unlikely given both the nonshattering phenotype of Tehuaca´n162 and our understanding of the domestication process. When studying domestication (or evolution in general), most genetic research uses DNA sequences from contemporary samples to make inferences regarding the evolutionary process. In contrast, the use of aDNA allows for direct observations of changes in genetic composition. Analysis of aDNA has been used to address questions including the evolution of archaic human
Current Biology 26, R1226–R1245, December 5, 2016 R1241
Current Biology
Dispatches groups such as the Denisovans [14] and the patterns of human migration associated with the onset of agriculture [15]. Previous studies have also used aDNA to address early selection and the evolution of maize in the American Southwest [16,17]. However, RamosMadrigal and co-authors provide the first study employing a whole-genome aDNA approach to explicitly address the sequence and tempo of maize domestication. As we begin to uncover the sequential order in which the ‘symptoms’ of the domestication syndrome arose in maize, we can ask if this order is also found in other domesticated plants, or if the story of domestication for each crop species is unique. Similarly, for crops that arose through multiple domestication events, aDNA analysis can help determine whether domestication is a repeatable process. The chronology of domestication events identified by Ramos-Madrigal and co-authors refines our understanding of the history of maize and reveals that domestication was a complex, protracted process. As valuable as this snapshot into the process of domestication is, it is only one snapshot. To achieve a more comprehensive vision of maize domestication, further research is necessary. In particular, additional studies should target archaeological maize samples from a broad range of time points to improve our understanding of the trajectory of domestication. The work of Ramos-Madrigal and colleagues, however, is an important step forward as we strive to understand the historical relationship between crops and humankind.
5. Ramos-Madrigal, J., Smith, B.D., Moreno-Mayar, J.V., Gopalakrishnan, S., Ross-Ibarra, J., Gilbert, M.T.P., and Wales, N. (2016). Genome sequence of a 5,310-year-old maize cob provides insights into the early stages of maize domestication. Curr. Biol. 26, 3195–3201.
12. Vigouroux, Y., McMullen, M., Hittinger, C., Houchins, K., Schulz, L., Kresovich, S., Matsuoka, Y., and Doebley, J. (2002). Identifying genes of agronomic importance in maize by screening microsatellites for evidence of selection during domestication. Proc. Nat. Acad. Sci. USA 99, 9650–9655.
6. Smith, B.D. (2005). Reassessing Coxcatla´n cave and the early history of domesticated plants in Mesoamerica. Proc. Nat. Acad. Sci. USA 102, 9438–9445.
13. Lin, Z., Li, X., Shannon, L.M., Yeh, C.-T., Wang, M.L., Bai, G., Peng, Z., Li, J., Trick, H.N., Clemente, T.E., et al. (2012). Parallel domestication of the shattering1 genes in cereals. Nat. Genet. 44, 720–724.
7. Gansauge, M.-T., and Meyer, M. (2013). Single-stranded DNA library preparation for the sequencing of ancient or damaged DNA. Nat. Methods 8, 737–748. 8. Meyer, R.S., and Purugganan, M.D. (2013). Evolution of crop species: genetics of domestication and diversification. Nat. Rev. Genet. 14, 40–852. 9. Fuller, D.Q., and Allaby, R. (2009). Seed Dispersal and Crop Domestication: Shattering, Germination and Seasonality in Evolution under Cultivation (Wiley-Blackwell), pp. 238–295. 10. Doebley, J. (2001). George Beadle’s other hypothesis: one-gene, one-trait. Genetics 158, 487–493. 11. Weber, A.L., Briggs, W.H., Rucker, J., Baltazar, B.M., de Jesu´s Sa´nchez-Gonzalez, J., Feng, P., Buckler, E.S., and Doebley, J. (2008). The genetic architecture of complex traits in teosinte (Zea mays ssp. parviglumis): new evidence from association mapping. Genetics 180, 1221–1232.
14. Meyer, M., Kircher, M., Gansauge, M.-T., Li, H., Racimo, F., Mallick, S., Schraiber, J.G., Jay, F., Pru¨fer, K., De Filippo, C., et al. (2012). A high-coverage genome sequence from an archaic Denisovan individual. Science 338, 222–226. 15. Lazaridis, I., Nadel, D., Rollefson, G., Merrett, D.C., Rohland, N., Mallick, S., Fernandes, D., Novak, M., Gamarra, B., Sirak, K., et al. (2016). Genomic insights into the origin of farming in the ancient near east. Nature 536, 419–424. 16. Jaenicke-Despres, V., Buckler, E.S., Smith, B.D., Gilbert, M.T.P., Cooper, A., Doebley, J., €a €bo, S. (2003). Early allelic selection in and Pa maize as revealed by ancient DNA. Science 302, 1206–1208. 17. da Fonseca, R.R., Smith, B.D., Wales, N., Cappellini, E., Skoglund, P., Fumagalli, M., Samaniego, J., Carøe, C., A´vila-Arcos, M.C., Hufnagel, D.E., et al. (2015). The origin and evolution of maize in the southwestern united states. Nat. Plants 1, 14003, EP–01.
Chromosome Segregation: Reconstituting the Kinetochore Frederick G. Westhorpe and Aaron F. Straight* Department of Biochemistry, Stanford Medical School, Stanford, CA, USA *Correspondence: [email protected] http://dx.doi.org/10.1016/j.cub.2016.09.051
REFERENCES 1. Matsuoka, Y., Vigouroux, Y., Goodman, M.M., Sanchez, J., Buckler, E., and Doebley, J. (2002). A single domestication for maize shown by multilocus microsatellite genotyping. Proc. Natl. Acad. Sci. USA 99, 6080–6084. 2. Gepts, P. (2010). Crop domestication as a long-term selection experiment. Plant Breed. Rev. 24, 1–44. 3. Koinange, E.M., Singh, S.P., and Gepts, P. (1996). Genetic control of the domestication syndrome in common bean. Crop Sci. 36, 1037–1045. 4. Doebley, J.F., Gaut, B.S., and Smith, B.D. (2006). The molecular genetics of crop domestication. Cell 127, 1309–1321.
Faithful chromosome segregation is accomplished by attachment of chromosomes to spindle microtubules using the kinetochore. In a major step forward in understanding the functional and structural complexity of kinetochores, a 21-subunit human centromere – kinetochore complex has been reconstituted entirely from purified components, recreating the connection between DNA and microtubule. To survive, all organisms must accurately replicate a copy of their genome and distribute it to newly forming daughter cells. Eukaryotic cells segregate their chromosomes during mitosis, first by attaching their duplicated chromosomes
R1242 Current Biology 26, R1226–R1245, December 5, 2016 ª 2016 Elsevier Ltd.
to the microtubules of the mitotic spindle, then by aligning them at the cell equator, before finally transporting one chromosome copy to each daughter cell. When chromosome segregation fails, chromosomal aneuploidies result,