Classification of archaic rice grains excavated at the Mojiaoshan site within the Liangzhu site complex reveals an Indica and Japonica chloroplast complex

Food Production, Processing and Nutrition - Tập 2 Số 1 - 2020
Katsunori Tanaka1, Chao Zhao2, Ningyuan Wang3, Shinji Kubota4, Masaaki Kanehara5, Nobuhiko Kamijō1, Ryuji Ishikawa1, Hiroyuki Tasaki6, Minako Kanehara5, Bin Liu3, Ming‐Hui Chen3, Shinichi Nakamura4, Tetsuro Udatsu7, Cailin Wang2
1Faculty of Agriculture and Life Science, Hirosaki University, 3 Bunkyo, Hirosaki, Aomori 036-8561, Japan
2Institute of Food Crops, Jiangsu Academy of Agricultural Sciences, Xiaolingwei, Nanjing, 210014, Jiangsu Province, China
3Zhejiang Provincial Institute of Cultural Relics and Archaeology, Gongshuqu Jiashanxincun26, Hangzhou, 310014, Zhejiang Province, China
4Center for Cultural Resource Studies Kanazawa University, Kanazawa University, Kakuma, Kanazawa, Ishikawa, 920-1192, Japan
5Department of Teacher Training and School Education, Nara University of Education, Takahata, Nara, Nara, 630-8528, Japan
6Archaeological Research Center, Ehime University, 10-13 Dogo-hi-mata, Matsuyama, Ehime, 790-8577, Japan
7Agricultural Museum, Faculty of Agriculture, Miyazaki University, 1-1 Gakuen-Kibana-dai-Nishi, Miyazaki, Miyazaki, 889-2192, Japan

Tóm tắt

AbstractTo understand rice types that were utilized during postdomestication and in the modern age and the potential of genetic research in aged rice materials, archaeogenetic analysis was conducted for two populations of archaic rice grains from the Mojiaoshan site during the Liangzhu Period in China (2940 to 2840 BC). Sequencing after the PCR amplification of three regions of the chloroplast genome and one region of the nuclear genome showed recovery rates that were comparable to those in previous studies except for one chloroplast genome region, suggesting that the materials used in this work were appropriate for recovering genetic information related to domestication traits by using advanced technology. Classification after sequencing in these regions proved the existence ofJaponicaandIndicachloroplasts in archaic grains from the west trench, which were subsequently classified into eight plastid groups (type I–VIII), and indicated that these rice grains derived from different maternal lineages were stored together in storage houses at the Mojiaohsan site. Among these plastid groups, type V exhibited the same sequences as two modernIndicaaccessions that are utilized in basic studies and rice breeding. It was inferred that part of the chloroplast genome of archaic rice has been preserved in modern genetic resources in these two modernIndicaaccessions, and the results indicated that rice related to their maternal ancestor was present at the Mojiaoshan site during the Liangzhu Period in China. The usefulness of archaeogenetic analysis can be demonstrated by our research data as well as previous studies, providing encouragement for the possibility that archaeogenetic analysis can be applied to older rice materials that were utilized in the rice-domesticated period.Graphical abstract

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Tài liệu tham khảo

Bollongino, R., Tresset, A., & Vigne, J. D. (2008). Environment and excavation: Prelab impacts on ancient DNA analyses. Comptes Rendus Palevol, 7, 91–98.

Bunning, S. L., Jones, G., & Brown, T. A. (2012). Next generation sequencing of DNA in 3300-year-old charred cereal grains. Journal of Archaeological Science, 39, 2780–2784.

Castillo, C. C., Tanaka, K., Sato, Y. I., Ishikawa, R., Bellina, B., Higham, C., … Fuller, D. Q. (2016). Archaeogenetic study of prehistoric rice remains from Thailand and India: Evidence of early japonica in south and Southeast Asia. Archaeological and Anthropological Sciences, 8, 523–543.

Choi, J. Y., & Purugganan, M. D. (2018). Multiple origin but single domestication led to Oryza sativa. G3: Genes, Genomes, Genetics, 8, 797–803.

Civán, P., & Brown, T. A. (2018). Role of genetic introgression during the evolution of cultivated rice (Oryza sativa L.). BMC Evolutionary Biology, 18, 57.

Deng, Z., Qin, L., Gao, Y., Weisskopf, A. R., Zhang, C., & Fuller, D. Q. (2015). From early domesticated rice of the Middle Yangtze Basin to millet, rice and wheat agriculture: Archaeobotanical macro-remains from Baligang, Nanyang Basin, Central China (6700-500 BC). PLoS One, 10, e0139885.

Du, H., Yu, Y., Ma, Y., Gao, Q., Cao, Y., Chen, Z., … Liang, C. (2017). Sequencing and de novo assembly of a near complete indica rice genome. Nature Communications, 8, 15324.

Fuller, D. Q. (2007). Contrasting patterns in crop domestication and domestication rates: Recent archaeobotanical insights from the old world. Annals of Botany, 100, 903–924.

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

Fuller, D. Q., & Harvey, E. L. (2006). The archaeobotany of Indian pulses: Identification, processing and evidence for cultivation. Environmental Archaeology, 11, 219–246.

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

Fuller, D. Q., Sato, Y. I., Castillo, C., Qin, L., Weisskopf, A. R., Kingwell-Banham, E. J., … Etten, J. (2010). Consilience of genetics and archaeobotany in the entangled history of rice. Archaeological and Anthropological Sciences, 2, 115–131.

Gugerli, F., Parducci, L., & Petit, R. J. (2005). Ancient plant DNA: Review and prospects. New Phytology, 166, 409–418.

Hanamori, K., Ishikawa, S., Saito, H., Tanaka, K., Sato, Y. I., & Okada, Y. (2011). Making divergent marker of tropical and temperate types of Oryza sativa L. var. japonica based on insertion/ deletion DNA region and its utilization of carbonated rice from Toro I site. Journal of Marine Science and Technology, 9, 19–25 (in Japanese with English abstract).

Hofreiter, M., Serre, D., Poinar, H. N., Kuch, M., & Pääbo, S. (2001). Ancient DNA. Nature Reviews Genetics, 2, 353–359.

Hopf, M. (1955). Formveränderungen von Getreidekörnern beim Verkohlen. Berichten der Deutschen Botanischen Gesellschaft, 68, 191–193.

Kim, B., Kim, D. G., Lee, G., Seo, J., Choi, I. Y., Choi, B. S., … Koh, H. J. (2014). Defining the genome structure of ‘Tongil’ rice, an important cultivar in the Korean “Green revolution”. Rice, 7, 22.

Kistler, L., Montenegro, A., Smith, B. D., Gifford, J. A., Green, R. E., Newsom, L. A., & Shapiro, B. (2014). Transoceanic drift and the domestication of African bottle gourds in the Americas. Proceedings of the National Academy of Sciences of the United States of America, 111, 2937–2941.

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

Kumagai, M., Kanehara, M., Shoda, S., Fujita, S., Onuki, S., Ueda, S., & Wang, L. (2016). Rice varieties in archaic East Asia: Reduction of its diversity from past to present times. Molecular Biology and Evolution, 33, 2496–2505.

Li, C., Zhou, A., & Sang, T. (2006). Rice domestication by reducing shattering. Science, 311, 1936–1939.

Liu, L., Lee, G. A., Jiang, L., & Zhang, J. (2007). Evidence for the early beginning (c. 9000 cal. BP) of rice domestication in China: A response. The Holocene, 17, 1059–1068.

Manigbas, N. L., Madrid, L. B., & Badajos, A. T. (2019). Adaptability of Korean cultivars and its potential as genetic donor for rice breeding in the Philippines. Philippine Journal of Crop Science, 44, 25–35.

Murray, M. G., & Thompson, W. F. (1980). Rapid isolation of high molecular weight plant DNA. Nucleic Acids Research, 8, 4321–4326.

Mutou, C., Tanaka, K., & Ishikawa, R. (2014). DNA extraction from rice endosperm (Including a protocol for extraction of DNA from ancient Seed samples). In R. J. Henry, & A. Furtado (Eds.), Cereal genomics: Methods and protocols, methods in molecular biology, (vol. 1099, pp. 7–15). New York: Humana Press.

Nakamura, I., Kameya, N., Kato, Y., Yamanaka, S. I., Jomori, H., & Sato, Y. (1997). A proposal for identifying the short ID sequence which addresses the plastid subtype of higher plants. Breeding Science, 47, 385–388.

Nakamura, S. (2010). The origin of rice cultivation in the Lower Yangtze Region, China. Archaeological and Anthropological Sciences, 2, 107–113.

Nakamura, S. I. (2015). New observation by the study of the Liangzhu site complex. In S. I. Nakamura (Ed.), Archaeological study of the Liangzhu site complex, (pp. 1–15). Kanazawa: Center for Cultural Resource Study Kanazawa University (In Japanese).

Nistelberger, H. M., Smith, O., Wales, N., Star, B., & Boessenkool, S. (2016). The efficacy of high-throughput sequencing and target enrichment on charred archaeobotanical remains. Scientific Reports, 6, 37347.

Oka, H. I. (1953). Phylogenetic differentiation of the cultivated rice plant. I. variation of various characters and character combinations among rice varieties. The Japanese Journal of Breeding, 3, 33–43 (in Japanese with English Abstract).

Oka, H. I. (1958). Intervarietal variation and classification of cultivated rice. Indian Journal of Genetics and Plant Breeding, 18, 79–89.

Okoshi, M., Matsuno, K., Okuno, K., Ogawa, M., Itani, T., & Fujimura, T. (2016). Genetic diversity in Japanese aromatic rice (Oryza sativa L.) as revealed by nuclear and organelle DNA markers. Genetic Resources and Crop Evolution, 63, 199–208.

Pääbo, S., Poinar, H., Serre, D., Jaenicke-Després, V., Hebler, J., Rohland, N., … Hofreiter, M. (2004). Genetic analyses from ancient DNA. Annual Review of Genetics, 38, 645–679.

Palmer, S. A., Moore, J. D., Clapham, A. J., Rose, P., & Allaby, R. G. (2009). Archaeogenetic evidence of ancient Nubian barley evolution from six to two-row indicates local adaptation. PLoS One, 4, e6301.

Palmer, S. A., Smith, O., & Allaby, R. G. (2012). The blossoming of plant archaeogenetics. Annals of Anatomy, 194, 146–156.

Qin, L., Liu, B., Wang, N., & Wu, X. (2015). Development of the Liangzhu site complex -Enery-level research by carbon dating. In S. I. Nakamura (Ed.), Archaeological study of the Liangzhu site complex, (pp. 33–43). Kanazawa: Center for Cultural Resource Study Kanazawa University (In Chinese).

Ramos-Madrigal, J., Smith, B. D., Moreno-Mayar, J. V., Gopalakrishnan, S., Ross-Ibarra, J., Gilbert, M. T. P., & Wales, N. (2016). Genome sequence of a 5,310-year-old maize cob provides insights into the early stages of maize domestication. Current Biology, 26, 3195–3201.

Renfrew, J. M. (1973). The survival of the evidence. In J. M. Renfrew (Ed.), Paleoethnobotany, (pp. 7–19). New York: Columbia University Press.

Sabato, D., Esteras, C., Grillo, O., Peña-Chocarro, L., Leida, C., Ucchesu, M., … Picó, B. (2019). Molecular and morphological characterization of the oldest Cucumis melo L. seeds found in the Western Mediterranean Basin. Archaeological and Anthropological Sciences, 11, 789–810.

Schlumbaum, A., Tensen, M., & Jaenicke-Després, V. (2008). Ancient plant DNA in archaeobotany. Vegetation History and Archaeobotany, 17, 233–244.

Smith, B. D. (2014). The domestication of Helianthus annuus L. (sunflower). Vegetation History & Archaeobotany, 23, 57–74.

Takahashi, H., Sato, Y. I., & Nakamura, I. (2008). Evolutionary analysis for two plastid DNA sequences in cultivated and wild species of Oryza. Breeding Science, 58, 225–233.

Tanaka, K., Kamijo, N., Tabuchi, H., Hanamori, K., Matsuda, R., Suginomori, J., … Ishikawa, R. (2016). Morphological and molecular genetics of ancient remains and modern rice confirm diversity in ancient Japan. Genetic Resources and Crop Evolution, 63, 447–464.

Tang, J., Xia, H., Cao, M., Zhang, X., Zeng, W., Hu, S., … Zhu, L. (2004). A comparison of rice chloroplast genomes. Plant Physiology, 135, 412–420.

Threadgold, J., & Brown, T. A. (2003). Degradation of DNA in artificially charred wheat seeds. Journal of Archaeological Science, 30, 1067–1076.

Untergasser, A., Cutcutache, I., Koressaar, T., Ye, J., Faircloth, B. C., Remm, M., & Rozen, S. G. (2012). Primer3 - new capabilities and interfaces. Nucleic Acids Research, 40, e115.

Wang, S., Ma, B., Gao, Q., Jiang, G., Zhou, L., Tu, B., … Li, S. (2018). Dissecting the genetic basis of heavy panicle hybrid rice uncovered Gn1a and GS3 as key genes. Theoretical and Applied Genetics, 131, 1391–1403.

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

Zheng, Y., Crawford, G. W., Jiang, L., & Chen, X. (2016). Rice domestication revealed by reduced shattering of archaeological rice from the lower Yangtze valley. Scientific Reports, 6, 28136.

Zuo, X., Lu, H., Jiang, L., Zhang, J., Yang, X., Huan, X., … Wu, N. (2017). Dating rice remains through phytolith carbon-14 study reveals domestication at the beginning of the Holocene. Proceedings of the National Academy of Sciences of the United States of America, 114, 6486–6491.

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Food Production, Processing and Nutrition

Tập 2 Số 1

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