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Awn Reduction and the Domestication of Asian Rice: A Syndrome or Crop Improvement Trait?

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Awn Reduction and the Domestication of Asian Rice: A Syndrome or Crop Improvement Trait? Although wild progenitors of Asian cultivated rice have long awns, they are shorter or absent in domesticated landraces and cultivars. Thus, one may wonder when and why such transition from awned to awnless has occurred, i.e., is the reduction of awns a domestication syndrome trait or a trait that emerged during crop improvement? The proponents of an evolutionary model of rice domestication consider the loss/reduction of seed dispersal aids as a key domestication syndrome trait, apart from the fixation of seed retention. We challenge this view by showing that early cultivators had incentives for selecting long awns before and even after the fixation of the non-shattering trait. This is because long awns prevented seed predation by animals and facilitated harvest by means of the basket-beating method, which implies that their presence improved yield and labor efficiency. Our arguments also reveal that awns perhaps have persisted long after domestication and even after the introduction of sickles. Taken together, the reduction of awns may not fit into a domestication syndrome trait, but it can most plausibly be considered as a crop improvement trait.

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Literature Cited

  • Abbo, S. and A. Gopher. 2017. Near Eastern plant domestication: A history of thought. Trends in Plant Science 226: 491–511.

    Article  CAS  Google Scholar 

  • ———, S. Lev–Yadun, and A. Gopher. 2014a. The ‘human mind’ as a common denominator in plant domestication. Journal of Experimental Botany 65:1917–1920.

    Article  CAS  PubMed  Google Scholar 

  • ———, R. Pinhasi van–Oss, A. Gopher, Y. Saranga, I. Ofner, and Z. Peleg. 2014b. Plant domestication versus crop evolution: A conceptual framework for cereals and grain legumes. Trends in Plant Science 19:351–360.

    Article  CAS  PubMed  Google Scholar 

  • Allaby, R. G. 2010. Integrating the processes in the evolutionary system of domestication. Journal of Experimental Botany 614:935–944.

    Article  CAS  Google Scholar 

  • Asouti, E. and D. Fuller. 2013. A contextual approach to the emergence of agriculture in Southwest Asia: Reconstructing Early Neolithic plant–food production. Current Anthropology 543:299–345.

    Article  Google Scholar 

  • Bessho–Uehara, K., D. R. Wang, T. Furuta, A. Minami, K. Nagai, R. Gamuyao, K. Asano, R. B. Angeles–Shim, Y. Shimizu, M. Ayano, and N. Komeda. 2016. Loss of function at RAE2, a previously unidentified EPFL, is required for awnlessness in cultivated Asian rice. Proceedings of the National Academy of Sciences of the United States of America 113: 8969–8974.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Brown, T. A., M. K. Jones, W. Powell, and R. G. Allaby. 2009. The complex origins of domesticated crops in the Fertile Crescent. Trends in Ecology & Evolution 24(2):103–109.

    Article  Google Scholar 

  • Deb, D., E. Bhattacharya, K. K. Jana, R. Mahato, R. Pramanik, A. Ram, and S. Sinha. 2005. Seeds of tradition, seeds of future: Folk rice varieties of Eastern India, first edition. New Delhi: Research Foundation for Science Technology and Ecology.

    Google Scholar 

  • Doebley, J. F., B. S. Gaut, and B. D. Smith. 2006. The molecular genetics of crop domestication. Cell 1277:1309–21.

    Article  CAS  Google Scholar 

  • Elbaum, R., L. Zaltzman, I. Burgert, and P. Fratzl. 2007. The role of wheat awns in the seed dispersal unit. Science 316:884–886.

    Article  CAS  PubMed  Google Scholar 

  • Fuller, D. Q. 2007. Contrasting patterns in crop domestication and domestication rates: Recent archaeological insights from the Old World. Annals of Botany 100:903–924.

    Article  PubMed  PubMed Central  Google Scholar 

  • ——— (2010) An emerging paradigm shift in the origins of agriculture. General Anthropology, Bulletin of the General Anthropology Division 17(2):1–12.

    Article  Google Scholar 

  • ——— and R. Allaby. 2009. Seed dispersal and crop domestication: Shattering, germination and seasonality in evolution under cultivation. Annual Plant Reviews: Fruit Development and Seed Dispersal 38:238–295.

  • ———, E. Harvey, and L. Qin. 2007. Presumed domestication? Evidence for wild rice cultivation and domestication in the fifth millennium BC of the Lower Yangtze region. Antiquity 81(312):316–331.

    Article  Google Scholar 

  • ———, L. Qin, and E. Harvey. 2008. Evidence for a late onset of agriculture in the Lower Yangtze region and challenges for an archaeobotany of rice. In: Past human migrations in East Asia: Matching archaeology, linguistics and genetics, eds., A. Sanchez–Mazas, R. Blench, M. D. Ross, I. Peiros, and M. Lin, 40–83. London and New York: Routledge.

  • ———, ———, Y. Zheng, Z. Zhao, X. Chen, L. A. Hosoya, and G. P. Sun. 2009. The domestication process and domestication rate in rice: Spikelet bases from the Lower Yangtze. Science 323(5921):1607–1610.

    Article  CAS  PubMed  Google Scholar 

  • ———, R. G. Allaby, and C. Stevens. 2010. Domestication as innovation: The entanglement of techniques, technology and chance in the domestication of cereal crops. World Archaeology 42:13–28.

    Article  Google Scholar 

  • ———, T. Denham, M. Arroyo–Kalin, L. Lucas, C. J. Stevens, L. Qin, R. G. Allaby, and M. D. Purugganan. 2014. Convergent evolution and parallelism in plant domestication revealed by an expanding archaeological record. Proceedings of the National Academy of Sciences USA 111: 6147–6152.

    Article  CAS  Google Scholar 

  • ———, C. Stevens, L. Lucas, C. Murphy, and L. Qin. 2016. Entanglements and entrapment on the pathway toward domestication. In: Archaeology of entanglement, eds., L. Der, and F. Fernandi, 151–172. Los Angeles: Left Coast Press.

  • Gepts, P. 2004. Crop domestication as a long–term selection experiment. Plant Breeding Review 24:1–44.

    Google Scholar 

  • Gu, B., T. Zhou J. Luo, B. Gu, T. Zhou, J. Luo, H. Liu, Y. Wang, Y. Shangguan, J. Zhu, Y. Li, T. Sang, Z. Wang, and B. Han. 2015. An–2 encodes a cytokinin synthesis enzyme that regulates awn length and grain production in rice. Molecular Plant 8:1635–1650.

    Article  CAS  PubMed  Google Scholar 

  • Guo, Z. and T. Schnurbusch. 2016. Costs and benefits of awns. Journal of Experimental Botany 67(9):2533–2535.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hammer, K. 1984. Das Domestikations syndrom. Die Kulturpflanze 32:11–34.

    Article  Google Scholar 

  • Harlan, J. R., J. Wet, and E. G. Price. 1973. Comparative evolution of cereals. Evolution 27:311–325, https://doi.org/10.2307/2406971.

    Article  PubMed  Google Scholar 

  • Harris, D. R. 1989. An evolutionary continuum of people–plant interaction. In: Foraging and farming: The evolution of plant exploitation, D. R. Harris and G. C. Hillman, eds., 11–26. London: Routledge.

    Google Scholar 

  • Helbaek, H. 1959. Domestication of food plants in the Old World: Joint efforts by botanists and archeologists illuminate the obscure history of plant domestication. Science 130(3372):365–72.

    Article  Google Scholar 

  • Hu, G., D. Zhang, H. Pan, B. Li, J. Wu, X. Zhou, Q. Zhang, L. Zhou, G. Yao, J. Li, J. Li, H. Zhang, and Z. Li. 2011. Fine mapping of the awn gene on chromosome 4 in rice by association and linkage analyses. Chinese Science Bulletin 56(9): 835–839.

    Article  CAS  Google Scholar 

  • Hua, L., D. R. Wang, L. Tan, Y. Fu, F. Liu, L. Xiao, Z. Zhu, Q. Fu, X. Sun, P. Gu, and H. Cai. 2015. LABA1, a domestication gene associated with long, barbed awns in wild rice. The Plant Cell 27:1875–1888.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ikemoto, M., M. Otsuka, P. T. Thanh, P. D. T. Phan, R. Ishikawa, and T. Ishii. 2017. Gene interaction at seed–awning loci in the genetic background of wild rice. Genes & Genetic Systems 92(1):21–26.

    Article  Google Scholar 

  • Ishii, T. and R. Ishikawa. 2018. Domestication loci controlling panicle shape, seed shattering, and seed awning. In: Rice genomics, genetics and breeding, T. Sasaki and M. Ashikari, eds., 207–221. Singapore: Springer, https://doi.org/10.1007/978-981-10-7461-5_12.

    Chapter  Google Scholar 

  • ———, K. Numaguchi, K. Miura, K. Yoshida, P. T. Thanh, T. M. Htun, M. Yamasaki, N. Komeda, T. Matsumoto, R. Terauchi, and R. Ishikawa. 2013. OsLG1 regulates a closed panicle trait in domesticated rice. Nature Genetics 45(4): 462–465.

    Article  CAS  PubMed  Google Scholar 

  • Ishikawa, R., P. T. Thanh, N. Nimura, T. M. Htun, M. Yamasaki, and T. Ishii. 2010. Allelic interaction at seed–shattering loci in the genetic backgrounds of wild and cultivated rice species. Genes & Genetic Systems. 85:265–271.

    Article  Google Scholar 

  • Jin, J., L. Hua, Z. Zhu, L. Tan, X. Zhao, W. Zhang, F. Liu, Y. Fu, H. Cai, X. Sun, and P. Gu. 2016. GAD1 encodes a secreted peptide that regulates grain number, grain length and awn development in rice domestication. Plant Cell 28:2453–2463.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Konishi, S., T. Izawa, S. Y. Lin, K. Ebana, Y. Fukuta, T. Sasaki, and M. Yano. 2006. An SNP caused loss of seed shattering during rice domestication. Science 312(5778):1392–1396.

    Article  CAS  PubMed  Google Scholar 

  • Larson, G., D. R. Piperno, R. G. Allaby, M. D. Purugganan, L. Andersson, M. Arroyo–Kalin, L. Barton, C. C. Vigueira, T. Denham, K. Dobney, and A. N. Doust. 2014. Current perspectives and the future of domestication studies. Proceedings of the National Academy of Sciences of the United States of America 111(17): 6139–6146.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li C., A. Zhou, and T. Sang. 2006. Rice domestication by reducing shattering. Science 311:1936–1939.

    Article  CAS  PubMed  Google Scholar 

  • Luo, J., H. Liu, T. Zhou, B. Gu, X. Huang, Y. Shangguan, J. Zhu, Y. Li, Y. Zhao, Y. Wang, and Q. Zhao. 2013. An–1 encodes a basic helix–loop–helix protein that regulates awn development, grain size, and grain number in riceThe Plant Cell 25:3360–3376.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maeda, O., L. Lucas, F. Silva, K. I. Tanno, and D. Q. Fuller. 2016. Narrowing the harvest: Increasing sickle investment and the rise of domesticated cereal agriculture in the Fertile Crescent. Quaternary Science Reviews 145:226–237.

    Article  Google Scholar 

  • Magwa, R. A., H. Zhao, W. Yao, W. Xie, L. Yang, Y. Xing, and X. Bai. 2016. Genomewide association analysis for awn length linked to the seed shattering gene qSH1 in rice. Journal of Genetics 95(3):639–646.

    Article  CAS  PubMed  Google Scholar 

  • Meyer, R. S. and M. D. Purugganan. 2013. Evolution of crop species: Genetics of domestication and diversification. Genetics 14:840–852.

    CAS  PubMed  Google Scholar 

  • Olsen, K. M. and J. F. Wendel. 2013. A bountiful harvest: Genomic insights into crop domestication phenotypes. Annual Review of Plant Biology 64:47–70.

    Article  CAS  PubMed  Google Scholar 

  • Pingali, P. L. 2012. Green revolution: Impacts, limits, and the path ahead. Proceedings of the National Academy of Sciences of the United States of America 109(31): 12302–12308.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Purugganan, M. D. and D. Q. Fuller. 2011. Archaeological data reveal slow rates of evolution during plant domestication. Evolution 65:171–183.

    Article  PubMed  Google Scholar 

  • Ray, A. and D. Chakraborty. 2018. Shattering or not shattering: That is the question in domestication of rice (Oryza sativa L.). Genetic Resource and Crop Evolution 65(2):391–395.

    Article  Google Scholar 

  • Singh, S., T. N. Singh, and J. S. Chauhan. 2009. Architectural engineering of rice panicle for increased productivity: A powerful biological tool for combating agricultural water crisis. Journal of Crop improvement 23(4):451–66.

    Article  CAS  Google Scholar 

  • Svizzero, S. 2018. Plant domestication more rapid under optimizing behavior. Journal of Bioeconomics 20(3): 287–308. https://doi.org/10.1007/s10818-018-9272-4.

    Article  Google Scholar 

  • Tanno, K. I. and G. Willcox. 2006. How fast was wild wheat domesticated? Science 311:1886.

    Article  CAS  PubMed  Google Scholar 

  • Toriba T. and H.–Y. Hirano.2014. The DROOPING LEAF and OsETTIN2 genes promote awn development in rice. Plant Journal 77:616–626.

    Article  CAS  Google Scholar 

  • ———, T. Suzaki, T. Yamaguchi, Y. Ohmori, H. Tsukaya, and H.–Y. Hirano. 2010. Distinct regulation of adaxial–abaxial polarity in anther patterning in rice. Plant Cell 22:1452–1462.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tzarfati, R., Y. Saranga, V. Barak, A. Gopher, A. B. Korol, and S. Abbo. 2013. Threshing efficiency as an incentive for rapid domestication of emmer wheat. Annals of Botany 112:829–837.

    Article  PubMed  PubMed Central  Google Scholar 

  • Winterhalder, B. and D. J. Kennett. 2006. Behavioral ecology and the transition from hunting and gathering to agriculture. In: Behavioral ecology and the transition to agriculture, eds., D. J. Kennett and B. Winterhalder, 1–21. Berkeley: University of California Press.

    Google Scholar 

  • Zhang, L. B., Q. Zhu, Z. Q. Wu, J. Ross-Ibarra, B. S. Gaut, S. Ge, and T. Sang. 2009. Selection on grain shattering genes and rates of rice domestication. New Phytologist 184(3): 708–720.

    Article  CAS  PubMed  Google Scholar 

  • Zohary, D. 2004. Unconscious selection and the evolution of domesticated plants. Economic Botany 58(1):5–10.

    Article  Google Scholar 

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Acknowledgments

The authors thank two anonymous referees. They also acknowledge the constructive criticisms by Utpal Basu, Department of Molecular Biology and Biotechnology, University of Kalyani. The authors would like to thank Abhra Chakraborty for providing the photographs of the landraces with awns. The usual caveat applies.

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Correspondence to Avik Ray.

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Svizzero, S., Ray, A. & Chakraborty, D. Awn Reduction and the Domestication of Asian Rice: A Syndrome or Crop Improvement Trait?. Econ Bot 73, 477–488 (2019). https://doi.org/10.1007/s12231-019-09465-0

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