Abstract
Main conclusion
Whole-genome re-sequencing of weedy rice from southern China reveals that weedy rice can originate from hybridization of domesticated indica and japonica rice.
Abstract
Weedy rice (Oryza sativa f. spontanea Rosh.), which harbors phenotypes of both wild and domesticated rice, has become one of the most notorious weeds in rice fields worldwide. While its formation is poorly understood, massive amounts of rice genomic data may provide new insights into this issue. In this study, we determined genomes of three weedy rice samples from the lower Yangtze region, China, and investigated their phylogenetics, population structure and chromosomal admixture patterns. The phylogenetic tree and principle component analysis based on 46,005 SNPs with 126 other Oryza accessions suggested that the three weedy rice accessions were intermediate between japonica and indica rice. An ancestry inference study further demonstrated that weedy rice had two dominant genomic components (temperate japonica and indica). This strongly suggests that weedy rice originated from indica-japonica hybridization. Furthermore, 22,443 novel fixed single nucleotide polymorphisms were detected in the weedy genomes and could have been generated after indica-japonica hybridization for environmental adaptation.
Similar content being viewed by others
References
Allston RFW (1846) The rice plant. DeBow’s Rev I:320–356 (Available online from U. Michigan)
Baki BB, Chin DV, Mortimer M (eds) (2000) Wild and weedy rice in rice ecosystems in Asia—a review, Los Baños. International Rice Research Institute, Philippines 118
Bres-Patry C, Bangratz M, Ghesquiere A (2001) Genetic diversity and population dynamics of weedy rice in Camargue area. Genet Sel Evol 33:S425–S440
Cao Q, Lu BR, Xia H, Rong J, Sala F, Spada A, Grassi F (2006) Genetic diversity and origin of weedy rice (Oryza sativa f. spontanea) populations found in North-eastern China revealed by simple sequence repeat (SSR) markers. Ann Bot 98:1241–1252
Chen W, Xu Z, Zhang L, Zhang W, Ma D (2007) Theories and practices of breeding japonica rice for super high yield. Sci Agric Sin 40:869–874 (in Chinese)
Cingolani P, Platts A, le Wang L, Coon M, Nguyen T, Wang L, Land SJ, Lu X, Ruden DM (2012) A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso–2; iso–3. Fly 6:80–92
De Wet JMJ, Harlan JR (1975) Weeds and domesticates: evolution in the man-made habitat. Econ Bot 29:99–107
Ding Y (1983) Classification of Chinese culture rice. Anthology of Ding Ying’s paper in rice. Agricultural Publishing Company, Beijing (in Chinese)
Du Z, Zhou X, Ling Y, Zhang ZH, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38:W64–W70
Ferrero A, Vidotto F, Balsari P, Airoldi G (1999) Mechanical and chemical control of red rice (Oryza sativa L-var. sylvatica) in rice (Oryza sativa L.) pre-planting. Crop Prot 18:245–251
Gealy DR, Tai TH, Sneller CH (2002) Identification of red rice, rice, and hybrid populations using microsatellite markers. Weed Sci 50:333–339
Gross BL, Reagon M, Hsu SC, Caicedo AL, Jia Y, Olsen KM (2010) Seeing red: the origin of grain pigmentation in US weedy rice. Mol Ecol 19:3380–3393
Gu XY, Foley ME, Horvath DP, Anderson JV, Feng JH, Zhang LH, Mowry CR, Ye H, Suttle JC, Kadowaki K, Chen ZX (2011) Association between seed dormancy and pericarp color is controlled by a pleiotropic gene that regulates abscisic acid and flavonoid synthesis in weedy red rice. Genetics 189:1515–1524
Harlan J (1992) Crops and Man. American Society of Agronomy, Crop Science Society of America, Madison, pp 117–130
Huang X, Kurata N, Wei X, Wang ZX, Wang A, Zhao Q, Zhao Y, Liu K, Lu H, Li W, Guo Y, Lu Y, Zhou C, Fan D, Weng Q, Zhu C, Huang T, Zhang L, Wang Y, Feng L, Furuumi H, Kubo T, Miyabayashi T, Yuan X, Xu Q, Dong G, Zhan Q, Li C, Fujiyama A, Toyoda A, Lu T, Feng Q, Qian Q, Li J, Han B (2012) A map of rice genome variation reveals the origin of cultivated rice. Nature 490:497–501
Huang X, Lu T, Han B (2013) Resequencing rice genomes: an emerging new era of rice genomics. Trends Genet 29:225–232
Hufford MB, Lubinksy P, Pyhajarvi T, Devengenzo MT, Ellstrand NC, Ross-Ibarra J (2013) The genomic signature of crop-wild introgression in maize. PLoS Genet 9:e1003477
Ishikawa R, Toki N, Imai K, Sato YI, Yamagishi H, Shimamoto Y, Ueno K, Morishima H, Sato T (2005) Origin of weedy rice grown in Bhutan and the force of genetic diversity. Genet Resour Crop Evol 52:395–403
Jiang ZX, Xia HB, Basso B, Lu BR (2012) Introgression from cultivated rice influences genetic differentiation of weedy rice populations at a local spatial scale. Theor Appl Genet 124:309–322
Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:U354–U357
Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760
Liang DY, Qiang S (2011) Current situation and control strategy of weedy rice in China. China PlantProt 31:21–24 (in Chinese)
Londo JP, Schaal BA (2007) Origins and population genetics of weedy red rice in the USA. Mol Ecol 16:4523–4535
Lu BR, Snow AA (2005) Gene flow from genetically modified rice and its environmental consequences. Bioscience 55:669–678
McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo MA (2010) The genome analysis toolkit: a mapreduce framework for analyzing next-generation DNA sequencing data. Genome Res 20:1297–1303
Mortimer M, Pandey S, Piggin C (2000) Weedy rice: approaches to ecological appraisal and implications for research priorities. In: Baki BB, Chin DV, Mortimer M (eds.) Proceedings of wild and weedy rice in rice ecosystems in Asia—a review. Limited proceedings no. 2, International Rice Research Institute, Los Baños, pp 97–105
Noldin JA, Chandler JM, McCauley GN (1999) Red rice (Oryza sativa) biology. I. Characterization of red rice ecotypes. Weed Technol 13:12–18
Patel RK, Jain M (2012) NGS QC Toolkit: a toolkit for quality control of next generation sequencing data. PLoS One 7:e30619
Pugach I, Matveyev R, Wollstein A, Kayser M, Stoneking M (2011) Dating the age of admixture via wavelet transform analysis of genome-wide data. Genome Biol 12:R19
Reagon M, Thurber CS, Gross BL, Olsen KM, Jia Y, Caicedo AL (2010) Genomic patterns of nucleotide diversity in divergent populations of US weedy rice. BMC Evol Biol 10:180
Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138
Shao Q, Dai WM, Zhang LJ, Song XL, Qiang S (2011) Genetic diversity and origin of weedy rice in central region of Jiangsu Province, China. Acta Agronomica Sinica 37:1324–1332 (in Chinese with English abstract)
Sherry ST, Ward MH, Kholodov M, Baker J, Phan L, Smigielski EM, Sirotkin K (2001) dbSNP: the NCBI database of genetic variation. Nucleic Acids Res 29:308–311
Subudhi PK, Singh PK, DeLeon T, Parco A, Karan R, Biradar H, Cohn MA, Sasaki T (2014) Mapping of seed shattering Loci provides insights into origin of weedy rice and rice domestication. J Hered 105:276–287
Sun J, Liu D, Wang JY, Ma DR, Tang L, Gao H, Xu ZJ, Chen WF (2012) The contribution of intersubspecific hybridization to the breeding of super-high-yielding japonica rice in northeast China. Theor Appl Genet 125:1149–1157
Sun J, Qian Q, Ma DR, Xu ZJ, Liu D, Du HB, Chen WF (2013) Introgression and selection shaping the genome and adaptive loci of weedy rice in northern China. New Phytol 197:290–299
Sweeney MT, Thomson MJ, Pfeil BE, McCouch S (2006) Caught red-handed: Rc encodes a basic helix-loop-helix protein conditioning red pericarp in rice. Plant Cell 18:283–294
Sweeney MT, Thomson MJ, Cho YG, Park YJ, Williamson SH, Bustamante CD, McCouch SR (2007) Global dissemination of a single mutation conferring white pericarp in rice. PLoS Genet 3:1418–1424
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Tang LH, Morishima H (1996) Genetic characteristics and origin of weedy rice. In: Origin and differentiation of Chinese cultivated rice. China Agricultural University Press, Beijing, pp 211–2180
Tang H, Peng J, Wang P, Risch NJ (2005) Estimation of individual admixture: analytical and study design considerations. Genet Epidemiol 28:289–301
Thurber CS, Reagon M, Gross BL, Olsen KM, Jia Y, Caicedo AL (2010) Molecular evolution of shattering loci in US weedy rice. Mol Ecol 19:3271–3284
Vaughan LK, Ottis BV, Prazak-Havey AM, Bormans CA, Sneller C, Chandler JM, Park WD (2001) Is all red rice found in commercial rice really Oryza sativa? Weed Sci 49:468–476
Vaughan DA, Lu BR, Tomooka N (2008) The evolving story of rice evolution. Plant Sci 174:394–408
Wang J, Yang J, Yang JH, Chen ZD, Fan FJ, Zhu JY, Zhong WG (2012) Genetic similarity and origin of weedy rice in Yangzhong region of Jiangsu province. Jiangsu J Agric Sci 28:748–753 (in Chinese with English abstract)
Xiong HB, Xu HY, Xu Q, Zhu Q, Gan SX, Feng DD, Zhang XL, Xie XD, Zhang H, Li J, Han YL, Wen JC, Li DX, Shi YM, Wei XH, Chen LJ (2012) Origin and evolution of weedy rice revealed by inter-subspecific and inter-varietal hybridizations in rice. Mol Plant Breed 10:131–139 (in Chinese with English abstract)
Xu X, Liu X, Ge S, Jensen JD, Hu F, Li X, Dong Y, Gutenkunst RN, Fang L, Huang L, Li J, He W, Zhang G, Zheng X, Zhang F, Li Y, Yu C, Kristiansen K, Zhang X, Wang J, Wright M, McCouch S, Nielsen R, Wang J, Wang W (2012) Resequencing 50 accessions of cultivated and wild rice yields markers for identifying agronomically important genes. Nat Biotechnol 30:105–111
Yi X, Du Z, Su Z (2013) PlantGSEA: a gene set enrichment analysis toolkit for plant community. Nucleic Acids Res 41:W98–W103
Yu Y, Tang T, Qian Q, Wang Y, Yan M, Zeng D, Han B, Wu CI, Shi S, Li J (2008) Independent losses of function in a polyphenol oxidase in rice: differentiation in grain discoloration between subspecies and the role of positive selection under domestication. Plant Cell 20:2946–2959
Zhang J, Nilda RB, Ma K, Zhou YJ, Geng RM, Yu LQ (2008) Genetic diversity and relationship of weedy rice in Taizhou City, Jiangsu Province, China. Rice Sci 15:295–302
Zhang LB, Zhu QH, Wu ZQ, Ross-Ibarra J, Gaut BS, Ge S, Sang T (2009) Selection on grain shattering genes and rates of rice domestication. New Phytol 184:708–720
Zhang Z, Dai W, Song X, Qiang S (2014) A model of the relationship between weedy rice seed-bank dynamics and rice-crop infestation and damage in Jiangsu Province, China. Pest Manag Sci 70:716–724
Zheng XW, Levine D, Shen J, Gogarten SM, Laurie C, Weir BS (2012) A high-performance computing toolset for relatedness and principal component analysis of SNP data. Bioinformatics 28:3326–3328
Zhou Y, Lu D, Li C, Luo J, Zhu BF, Zhu J, Shangguan Y, Wang Z, Sang T, Zhou B, Han B (2012) Genetic control of seed shattering in rice by the APETALA2 transcription factor shattering abortion1. Plant Cell 24:1034–1048
Zhu Y, Ellstrand NC, Lu BR (2012) Sequence polymorphisms in wild, weedy, and cultivated rice suggest seed-shattering locus sh4 played a minor role in Asian rice domestication. Ecol Evol 2:2106–2113
Acknowledgments
We thank Xunbin Guo and Junsen Jiao for collecting the weedy rice samples. This work was financially supported in part by grants from the China Agriculture Research System (CARS-01-02A) and the Natural Science Foundation of China (31171863).
Conflict of interest
We declare that we have no financial or personal relationships with other people or organizations that may have inappropriately influenced our work, and there is no professional or other personal interest of any nature or kind in any product, service and/or company that could be construed as influencing the position presented in or the review of the manuscript.
Ethical standard
This manuscript has not been published previously and there is no prior interaction with Planta. We confirm that there are no known conflicts of interest associated with the publication. The manuscript has been read and approved by all of the authors.
Author information
Authors and Affiliations
Corresponding authors
Electronic supplementary material
Below is the link to the electronic supplementary material.
Fig. S1
StepPCO plots for all chromosomes of the three weedy rice samples. Indica (blue) and japonica (orange) were treated as ancestral groups. Chromosomal regions of the admixed genome are attributed to either the “orange” or “blue” ancestry with admixed regions in the middle (YG02: yellow; YJ06: green; YJ07: red). The mean PC1 coordinates for each parental population are centered at 1 and -1, and the progressively lighter shading surrounding the mean of each parental group indicates ±1, ±2 or ±3 SDs from the mean. Supplementary material 1 (PDF 955 kb)
Table S1 Rice accessions used in this study.
Table S2 Summary of the genomic distribution of SNPs of weedy rice relative to two reference rice genomes.
Table S3 GO and plant metabolic pathway enrichment analysis of genes with fixed novel SNPs that cause moderate effects in weedy rice.
Rights and permissions
About this article
Cite this article
Qiu, J., Zhu, J., Fu, F. et al. Genome re-sequencing suggested a weedy rice origin from domesticated indica-japonica hybridization: a case study from southern China. Planta 240, 1353–1363 (2014). https://doi.org/10.1007/s00425-014-2159-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-014-2159-2