Evolution of the Grain Dispersal System in Barley

Mohammad Pourkheirandish; Goetz Hensel; Benjamin Kilian; Natesan Senthil; Guoxiong Chen; Mohammad Sameri; Perumal Azhaguvel; Shun Sakuma; Sidram Dhanagond; Rajiv Sharma; Martin Mascher; Axel Himmelbach; Sven Gottwald; Sudha K. Nair; Akemi Tagiri; Fumiko Yukuhiro; Yoshiaki Nagamura; Hiroyuki Kanamori; Takashi Matsumoto; George Willcox; Christopher P. Middleton; Thomas Wicker; Alexander Walther; Robbie Waugh; Geoffrey B. Fincher; Nils Stein; Jochen Kumlehn; Kazuhiro Sato; Takao Komatsuda

doi:10.1016/j.cell.2015.07.002

Evolution of the Grain Dispersal System in Barley

Mohammad Pourkheirandish, Goetz Hensel, Benjamin Kilian, Natesan Senthil, Guoxiong Chen, Mohammad Sameri, Perumal Azhaguvel, Shun Sakuma, Sidram Dhanagond, Rajiv Sharma, Martin Mascher, Axel Himmelbach, Sven Gottwald, Sudha K. Nair, Akemi Tagiri, Fumiko Yukuhiro, Yoshiaki Nagamura, Hiroyuki Kanamori, Takashi Matsumoto, George WillcoxChristopher P. Middleton, Thomas Wicker, Alexander Walther, Robbie Waugh, Geoffrey B. Fincher, Nils Stein, Jochen Kumlehn, Kazuhiro Sato, Takao Komatsuda

Institute of Plant Science and Resources

Research output: Contribution to journal › Article › peer-review

104 Citations (Scopus)

Abstract

About 12,000 years ago in the Near East, humans began the transition from hunter-gathering to agriculture-based societies. Barley was a founder crop in this process, and the most important steps in its domestication were mutations in two adjacent, dominant, and complementary genes, through which grains were retained on the inflorescence at maturity, enabling effective harvesting. Independent recessive mutations in each of these genes caused cell wall thickening in a highly specific grain "disarticulation zone," converting the brittle floral axis (the rachis) of the wild-type into a tough, non-brittle form that promoted grain retention. By tracing the evolutionary history of allelic variation in both genes, we conclude that spatially and temporally independent selections of germplasm with a non-brittle rachis were made during the domestication of barley by farmers in the southern and northern regions of the Levant, actions that made a major contribution to the emergence of early agrarian societies.

Original language	English
Pages (from-to)	527-539
Number of pages	13
Journal	Cell
Volume	162
Issue number	3
DOIs	https://doi.org/10.1016/j.cell.2015.07.002
Publication status	Published - Aug 1 2015

ASJC Scopus subject areas

Biochemistry, Genetics and Molecular Biology(all)

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Pourkheirandish, M., Hensel, G., Kilian, B., Senthil, N., Chen, G., Sameri, M., Azhaguvel, P., Sakuma, S., Dhanagond, S., Sharma, R., Mascher, M., Himmelbach, A., Gottwald, S., Nair, S. K., Tagiri, A., Yukuhiro, F., Nagamura, Y., Kanamori, H., Matsumoto, T., ... Komatsuda, T. (2015). Evolution of the Grain Dispersal System in Barley. Cell, 162(3), 527-539. https://doi.org/10.1016/j.cell.2015.07.002

Evolution of the Grain Dispersal System in Barley. / Pourkheirandish, Mohammad; Hensel, Goetz; Kilian, Benjamin; Senthil, Natesan; Chen, Guoxiong; Sameri, Mohammad; Azhaguvel, Perumal; Sakuma, Shun; Dhanagond, Sidram; Sharma, Rajiv; Mascher, Martin; Himmelbach, Axel; Gottwald, Sven; Nair, Sudha K.; Tagiri, Akemi; Yukuhiro, Fumiko; Nagamura, Yoshiaki; Kanamori, Hiroyuki; Matsumoto, Takashi; Willcox, George; Middleton, Christopher P.; Wicker, Thomas; Walther, Alexander; Waugh, Robbie; Fincher, Geoffrey B.; Stein, Nils; Kumlehn, Jochen; Sato, Kazuhiro; Komatsuda, Takao.

In: Cell, Vol. 162, No. 3, 01.08.2015, p. 527-539.

Research output: Contribution to journal › Article › peer-review

Pourkheirandish, M, Hensel, G, Kilian, B, Senthil, N, Chen, G, Sameri, M, Azhaguvel, P, Sakuma, S, Dhanagond, S, Sharma, R, Mascher, M, Himmelbach, A, Gottwald, S, Nair, SK, Tagiri, A, Yukuhiro, F, Nagamura, Y, Kanamori, H, Matsumoto, T, Willcox, G, Middleton, CP, Wicker, T, Walther, A, Waugh, R, Fincher, GB, Stein, N, Kumlehn, J, Sato, K & Komatsuda, T 2015, 'Evolution of the Grain Dispersal System in Barley', Cell, vol. 162, no. 3, pp. 527-539. https://doi.org/10.1016/j.cell.2015.07.002

Pourkheirandish, Mohammad ; Hensel, Goetz ; Kilian, Benjamin ; Senthil, Natesan ; Chen, Guoxiong ; Sameri, Mohammad ; Azhaguvel, Perumal ; Sakuma, Shun ; Dhanagond, Sidram ; Sharma, Rajiv ; Mascher, Martin ; Himmelbach, Axel ; Gottwald, Sven ; Nair, Sudha K. ; Tagiri, Akemi ; Yukuhiro, Fumiko ; Nagamura, Yoshiaki ; Kanamori, Hiroyuki ; Matsumoto, Takashi ; Willcox, George ; Middleton, Christopher P. ; Wicker, Thomas ; Walther, Alexander ; Waugh, Robbie ; Fincher, Geoffrey B. ; Stein, Nils ; Kumlehn, Jochen ; Sato, Kazuhiro ; Komatsuda, Takao. / Evolution of the Grain Dispersal System in Barley. In: Cell. 2015 ; Vol. 162, No. 3. pp. 527-539.

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title = "Evolution of the Grain Dispersal System in Barley",

abstract = "About 12,000 years ago in the Near East, humans began the transition from hunter-gathering to agriculture-based societies. Barley was a founder crop in this process, and the most important steps in its domestication were mutations in two adjacent, dominant, and complementary genes, through which grains were retained on the inflorescence at maturity, enabling effective harvesting. Independent recessive mutations in each of these genes caused cell wall thickening in a highly specific grain {"}disarticulation zone,{"} converting the brittle floral axis (the rachis) of the wild-type into a tough, non-brittle form that promoted grain retention. By tracing the evolutionary history of allelic variation in both genes, we conclude that spatially and temporally independent selections of germplasm with a non-brittle rachis were made during the domestication of barley by farmers in the southern and northern regions of the Levant, actions that made a major contribution to the emergence of early agrarian societies.",

author = "Mohammad Pourkheirandish and Goetz Hensel and Benjamin Kilian and Natesan Senthil and Guoxiong Chen and Mohammad Sameri and Perumal Azhaguvel and Shun Sakuma and Sidram Dhanagond and Rajiv Sharma and Martin Mascher and Axel Himmelbach and Sven Gottwald and Nair, {Sudha K.} and Akemi Tagiri and Fumiko Yukuhiro and Yoshiaki Nagamura and Hiroyuki Kanamori and Takashi Matsumoto and George Willcox and Middleton, {Christopher P.} and Thomas Wicker and Alexander Walther and Robbie Waugh and Fincher, {Geoffrey B.} and Nils Stein and Jochen Kumlehn and Kazuhiro Sato and Takao Komatsuda",

note = "Funding Information: We thank M. Ashikari, T. Izawa, M. Yano, J.F. Ma, and Y. Mano for reading the manuscript, T.R. Endo, A. Graner, R.v. Bothmer, F.R. Blattner, N. Sentoku, N. Wang, and A. Fukuda for helpful discussions, K. Mayer and M. Pfeifer for investigating synteny in model grass genomes. We wish to thank R. Burton, M. Henderson, Hweit-Ting Tan, and N. Hara for their skilled technical assistance with the microscopy, H. Koyama and J. Keilwagen for their assistance in sequence alignment, W. Weissgerber and all technicians, field staff, and students for their excellent technical assistance. We thank J. Russell and I.K. Dawson for manually curating geographic coordinates of barley accessions and D. Stengel for sequence data submission. We are grateful to K. Takeda, J. Valkoun, H. {\"O}zkan, E. Fridman, S. H{\"u}bner, S. Jakob, S. Shaaf, B. Steffenson, H. Hirabayashi, the German Federal ex situ Genebank at Gatersleben, the National BioResource Project of Japan, the USDA National Plant Germplasm System and Agricultural Research Service, the International Center for Agricultural Research in Dry Areas (ICARDA), and the Max Planck Institute for Plant Breeding Research Cologne, for providing grain/DNA/information related to the barley accessions. The authors acknowledge financial support given by the Japan Science and Technology Agency (CREST) to K.S. and T.K., by the Japanese Society for Promotion of Science to M.P., C.G., S.K.N., P.A., N. Senthil, and T.K., by the German Science Foundation Priority Programme SPP1530 to B.K., by the Australian Research Council for its long term support of our cell wall research programs to G.B.F., and by NIAS Tsukuba and IPK Gatersleben. R.W. acknowledges support from The University of Dundee and the James Hutton Institute . ",

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T1 - Evolution of the Grain Dispersal System in Barley

AU - Pourkheirandish, Mohammad

AU - Hensel, Goetz

AU - Kilian, Benjamin

AU - Senthil, Natesan

AU - Chen, Guoxiong

AU - Sameri, Mohammad

AU - Azhaguvel, Perumal

AU - Sakuma, Shun

AU - Dhanagond, Sidram

AU - Sharma, Rajiv

AU - Mascher, Martin

AU - Himmelbach, Axel

AU - Gottwald, Sven

AU - Nair, Sudha K.

AU - Tagiri, Akemi

AU - Yukuhiro, Fumiko

AU - Nagamura, Yoshiaki

AU - Kanamori, Hiroyuki

AU - Matsumoto, Takashi

AU - Willcox, George

AU - Middleton, Christopher P.

AU - Wicker, Thomas

AU - Walther, Alexander

AU - Waugh, Robbie

AU - Fincher, Geoffrey B.

AU - Stein, Nils

AU - Kumlehn, Jochen

AU - Sato, Kazuhiro

AU - Komatsuda, Takao

N1 - Funding Information: We thank M. Ashikari, T. Izawa, M. Yano, J.F. Ma, and Y. Mano for reading the manuscript, T.R. Endo, A. Graner, R.v. Bothmer, F.R. Blattner, N. Sentoku, N. Wang, and A. Fukuda for helpful discussions, K. Mayer and M. Pfeifer for investigating synteny in model grass genomes. We wish to thank R. Burton, M. Henderson, Hweit-Ting Tan, and N. Hara for their skilled technical assistance with the microscopy, H. Koyama and J. Keilwagen for their assistance in sequence alignment, W. Weissgerber and all technicians, field staff, and students for their excellent technical assistance. We thank J. Russell and I.K. Dawson for manually curating geographic coordinates of barley accessions and D. Stengel for sequence data submission. We are grateful to K. Takeda, J. Valkoun, H. Özkan, E. Fridman, S. Hübner, S. Jakob, S. Shaaf, B. Steffenson, H. Hirabayashi, the German Federal ex situ Genebank at Gatersleben, the National BioResource Project of Japan, the USDA National Plant Germplasm System and Agricultural Research Service, the International Center for Agricultural Research in Dry Areas (ICARDA), and the Max Planck Institute for Plant Breeding Research Cologne, for providing grain/DNA/information related to the barley accessions. The authors acknowledge financial support given by the Japan Science and Technology Agency (CREST) to K.S. and T.K., by the Japanese Society for Promotion of Science to M.P., C.G., S.K.N., P.A., N. Senthil, and T.K., by the German Science Foundation Priority Programme SPP1530 to B.K., by the Australian Research Council for its long term support of our cell wall research programs to G.B.F., and by NIAS Tsukuba and IPK Gatersleben. R.W. acknowledges support from The University of Dundee and the James Hutton Institute .

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Y1 - 2015/8/1

N2 - About 12,000 years ago in the Near East, humans began the transition from hunter-gathering to agriculture-based societies. Barley was a founder crop in this process, and the most important steps in its domestication were mutations in two adjacent, dominant, and complementary genes, through which grains were retained on the inflorescence at maturity, enabling effective harvesting. Independent recessive mutations in each of these genes caused cell wall thickening in a highly specific grain "disarticulation zone," converting the brittle floral axis (the rachis) of the wild-type into a tough, non-brittle form that promoted grain retention. By tracing the evolutionary history of allelic variation in both genes, we conclude that spatially and temporally independent selections of germplasm with a non-brittle rachis were made during the domestication of barley by farmers in the southern and northern regions of the Levant, actions that made a major contribution to the emergence of early agrarian societies.

AB - About 12,000 years ago in the Near East, humans began the transition from hunter-gathering to agriculture-based societies. Barley was a founder crop in this process, and the most important steps in its domestication were mutations in two adjacent, dominant, and complementary genes, through which grains were retained on the inflorescence at maturity, enabling effective harvesting. Independent recessive mutations in each of these genes caused cell wall thickening in a highly specific grain "disarticulation zone," converting the brittle floral axis (the rachis) of the wild-type into a tough, non-brittle form that promoted grain retention. By tracing the evolutionary history of allelic variation in both genes, we conclude that spatially and temporally independent selections of germplasm with a non-brittle rachis were made during the domestication of barley by farmers in the southern and northern regions of the Levant, actions that made a major contribution to the emergence of early agrarian societies.

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