A derived weedy rice × ancestral cultivar cross identifies evolutionarily relevant weediness QTLs.
QTL mapping
evolutionarily relevant QTL
flowering time
plant height
seed shattering
weedy rice
Journal
Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478
Informations de publication
Date de publication:
Nov 2023
Nov 2023
Historique:
revised:
02
09
2023
received:
02
05
2023
accepted:
06
10
2023
medline:
7
11
2023
pubmed:
20
10
2023
entrez:
20
10
2023
Statut:
ppublish
Résumé
Weedy rice (Oryza spp.) is a weedy relative of the cultivated rice that competes with the crop and causes significant production loss. The BHA (blackhull awned) US weedy rice group has evolved from aus cultivated rice and differs from its ancestors in several important weediness traits, including flowering time, plant height and seed shattering. Prior attempts to determine the genetic basis of weediness traits in plants using linkage mapping approaches have not often considered weed origins. However, the timing of divergence between crossed parents can affect the detection of quantitative trait loci (QTL) relevant to the evolution of weediness. Here, we used a QTL-seq approach that combines bulked segregant analysis and high-throughput whole genome resequencing to map the three important weediness traits in an F
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
5971-5985Subventions
Organisme : National Science Foundation
ID : IOS-1947609
Informations de copyright
© 2023 John Wiley & Sons Ltd.
Références
Bagavathiannan, M. V., Graham, S., Ma, Z., Barney, J. N., Coutts, S. R., Caicedo, A. L., de Clerck-Floate, R., West, N. M., Blank, L., Metcalf, A. L., Lacoste, M., Moreno, C. R., Evans, J. A., Burke, I., & Beckie, H. (2019). Considering weed management as a social dilemma bridges individual and collective interests. Nature Plants, 5(4), 343-351.
Bin Rahman, A. N. M. R., & Zhang, J. (2022). Trends in rice research: 2030 and beyond. Food and Energy Security, 12, e390. https://doi.org/10.1002/fes3.390
Bolger, A. M., Lohse, M., & Usadel, B. (2014). Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics, 30(15), 2114-2120.
Bres-Patry, C., Lorieux, M., Clément, G., Bangratz, M., & Ghesquière, A. (2001). Heredity and genetic mapping of domestication-related traits in a temperate japonica weedy rice. Theoretical and Applied Genetics, 102(1), 118-126.
Burgos, N. R., Norman, R. J., Gealy, D. R., & Black, H. (2006). Competitive N uptake between rice and weedy rice. Field Crops Research, 99(2), 96-105.
Burgos, N. R., Singh, V., Tseng, T. M., Black, H., Young, N. D., Huang, Z., Hyma, K. E., Gealy, D. R., & Caicedo, A. L. (2014). The impact of herbicide-resistant rice technology on phenotypic diversity and population structure of United States weedy rice. Plant Physiology, 166(3), 1208-1220.
Casartelli, A., Riewe, D., Hubberten, H. M., Altmann, T., Hoefgen, R., & Heuer, S. (2018). Exploring traditional aus-type rice for metabolites conferring drought tolerance. Rice, 11(1), 9.
Chauhan, B. S., & Johnson, D. E. (2011). Competitive interactions between weedy rice and cultivated rice as a function of added nitrogen and the level of competition. Weed Biology and Management, 11(4), 202-209.
Choi, J. Y., Platts, A. E., Fuller, D. Q., Hsing, Y.-I., Wing, R. A., & Purugganan, M. D. (2017). The rice paradox: Multiple origins but single domestication in Asian rice. Molecular Biology and Evolution, 34(4), 969-979.
Cingolani, P., Platts, A., Wang, L. L., Coon, M., Nguyen, T., Wang, L., Land, S. J., Lu, X., & Ruden, D. M. (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(2), 80-92.
Civáň, P., Craig, H., Cox, C. J., & Brown, T. A. (2015). Three geographically separate domestications of Asian rice. Nature Plants, 1, 15164.
Danecek, P., Auton, A., Abecasis, G., Albers, C. A., Banks, E., DePristo, M. A., Handsaker, R. E., Lunter, G., Marth, G. T., Sherry, S. T., McVean, G., Durbin, R., & 1000 Genomes Project Analysis Group. (2011). The variant call format and VCFtools. Bioinformatics, 27(15), 2156-2158.
Das, S., Parida, S. K., Agarwal, P., & Tyagi, A. K. (2019). Transcription factor OsNF-YB9 regulates reproductive growth and development in rice. Planta, 250(6), 1849-1865.
Ding, X., Cao, Y., Huang, L., Zhao, J., Xu, C., Li, X., & Wang, S. (2008). Activation of the indole-3-acetic acid-amido synthetase GH3-8 suppresses expansin expression and promotes salicylate- and jasmonate-independent basal immunity in Rice. The Plant Cell, 20(1), 228-240.
Du, D., Gao, X., Geng, J., Li, Q., Li, L., Lv, Q., & Li, X. (2016). Identification of key proteins and networks related to grain development in wheat (Triticum aestivum L.) by comparative transcription and proteomic analysis of allelic variants in TaGW2-6A. Frontiers in Plant Science, 7, 922.
Du, H., Yu, Y., Ma, Y., Gao, Q., Cao, Y., Chen, Z., Ma, B., Qi, M., Li, Y., Zhao, X., Wang, J., Liu, K., Qin, P., Yang, X., Zhu, L., Li, S., & Liang, C. (2017). Sequencing and de novo assembly of a near complete indica rice genome. Nature Communications, 8, 15324.
Durand-Morat, A., Nalley, L. L., & Thoma, G. (2018). The implications of red rice on food security. Global Food Security, 18, 62-75.
Ellstrand, N. C., Heredia, S. M., Leak-Garcia, J. A., Heraty, J. M., Burger, J. C., Yao, L., Nohzadeh-Malakshah, S., & Ridley, C. E. (2010). Crops gone wild: Evolution of weeds and invasives from domesticated ancestors. Evolutionary Applications, 3(5-6), 494-504.
Falster, D. S., & Westoby, M. (2003). Plant height and evolutionary games. Trends in Ecology & Evolution, 18(7), 337-343.
Fujino, K., Yamanouchi, U., & Yano, M. (2013). Roles of the Hd5 gene controlling heading date for adaptation to the northern limits of rice cultivation. Theoretical and Applied Genetics, 126(3), 611-618.
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(5921), 1607-1610.
Fuller, D. Q., Sato, Y.-I., Castillo, C., Qin, L., Weisskopf, A. R., Kingwell-Banham, E. J., Song, J., Ahn, S.-M., & van Etten, J. (2010). Consilience of genetics and archaeobotany in the entangled history of rice. Archaeological and Anthropological Sciences, 2(2), 115-131.
Gao, H., Jin, M., Zheng, X.-M., Chen, J., Yuan, D., Xin, Y., Wang, M., Huang, D., Zhang, Z., Zhou, K., Sheng, P., Ma, J., Ma, W., Deng, H., Jiang, L., Liu, S., Wang, H., Wu, C., Yuan, L., & Wan, J. (2014). Days to heading 7, a major quantitative locus determining photoperiod sensitivity and regional adaptation in rice. Proceedings of the National Academy of Sciences of the United States of America, 111(46), 16337-16342.
Gross, B. L., & Zhao, Z. (2014). Archaeological and genetic insights into the origins of domesticated rice. Proceedings of the National Academy of Sciences of the United States of America, 111(17), 6190-6197.
Gu, X.-Y., Kianian, S. F., Hareland, G. A., Hoffer, B. L., & Foley, M. E. (2005). Genetic analysis of adaptive syndromes interrelated with seed dormancy in weedy rice (Oryza sativa). Theoretical and Applied Genetics, 110(6), 1108-1118.
Hartl, D. L., & Clark, A. G. (1997). Principles of population genetics. Sinauer Associates.
He, W., Chen, C., Xiang, K., Wang, J., Zheng, P., Tembrock, L. R., Jin, D., & Wu, Z. (2021). The history and diversity of Rice domestication as resolved from 1464 complete plastid genomes. Frontiers in Plant Science, 12, 781793.
Hoyos, V., Plaza, G., Li, X., & Caicedo, A. L. (2020). Something old, something new: Evolution of Colombian weedy rice (Oryza spp.) through de novo de-domestication, exotic gene flow, and hybridization. Evolutionary Applications, 13(8), 1968-1983.
Huang, Z., Kelly, S., Matsuo, R., Li, L.-F., Li, Y., Olsen, K. M., Jia, Y., & Caicedo, A. L. (2018). The role of standing variation in the evolution of weedines traits in South Asian weedy rice (Oryza spp.). G3 Genes|Genomes|Genetics, 8(11), 3679-3690.
Huang, Z., Rodriguez, J. A., Matsuo, R., & Caicedo, A. L. (2021). Assessing physiological and genetic evidence for evolution of shared weedy rice traits at the vegetative growth stage. Frontiers in Agronomy, 3, 601414. https://doi.org/10.3389/fagro.2021.601414
Huang, Z., Young, N. D., Reagon, M., Hyma, K. E., Olsen, K. M., Jia, Y., & Caicedo, A. L. (2017). All roads lead to weediness: Patterns of genomic divergence reveal extensive recurrent weedy rice origins from South Asian Oryza. Molecular Ecology, 26(12), 3151-3167.
Hui, L., Liu, D., Wang, Y., Li, S., Yin, L., & Wang, S. (2022). Overexpression of rice monogalactosyldiacylglycerol synthase OsMGD leads to enhanced salt tolerance in rice. Agronomy, 12(3), 568.
Imaizumi, T., Ebana, K., Kawahara, Y., Muto, C., Kobayashi, H., Koarai, A., & Olsen, K. M. (2021). Genomic divergence during feralization reveals both conserved and distinct mechanisms of parallel weediness evolution. Communications Biology, 4(1), 952.
Izawa, T., Mihara, M., Suzuki, Y., Gupta, M., Itoh, H., Nagano, A. J., Motoyama, R., Sawada, Y., Yano, M., Hirai, M. Y., Makino, A., & Nagamura, Y. (2011). Os-GIGANTEA confers robust diurnal rhythms on the global transcriptome of rice in the field. The Plant Cell, 23(5), 1741-1755.
Kassambara, A. (2022). ggpubr: “ggplot2” Based publication ready plots. R package version 0.6.0. https://rpkgs.datanovia.com/ggpubr/
Kawahara, Y., de la Bastide, M., Hamilton, J. P., Kanamori, H., McCombie, W. R., Ouyang, S., Schwartz, D. C., Tanaka, T., Wu, J., Zhou, S., Childs, K. L., Davidson, R. M., Lin, H., Quesada-Ocampo, L., Vaillancourt, B., Sakai, H., Lee, S. S., Kim, J., Numa, H., … Matsumoto, T. (2013). Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data. Rice, 6(1), 4.
Li, C., Zhou, A., & Sang, T. (2006). Rice domestication by reducing shattering. Science, 311(5769), 1936-1939.
Li, H. (2011). A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics, 27(21), 2987-2993.
Li, H., & Durbin, R. (2009). Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25(14), 1754-1760.
Li, L., Li, Y., Jia, Y., Caicedo, A. L., & Olsen, K. M. (2017). Signatures of adaptation in the weedy rice genome. Nature Genetics, 49(5), 811-814.
Li, X., Zhang, S., Amaro-Blanco, I., Perera, S., Khandekar, N. S., Lowey, D., Osuna, M. D., & Caicedo, A. L. (2022). Multiple compensatory mutations contribute to the de-domestication of Iberian weedy rice. Plants, People, Planet, 4, 499-510. https://doi.org/10.1002/ppp3.10286
Liu, F., Wang, P., Zhang, X., Li, X., Yan, X., Fu, D., & Wu, G. (2018). The genetic and molecular basis of crop height based on a rice model. Planta, 247(1), 1-26.
Moner, A. M., Furtado, A., & Henry, R. J. (2020). Two divergent chloroplast genome sequence clades captured in the domesticated rice gene pool may have significance for rice production. BMC Plant Biology, 20(1), 472.
Nemoto, Y., Nonoue, Y., Yano, M., & Izawa, T. (2016). Hd1,a CONSTANS ortholog in rice, functions as an Ehd1 repressor through interaction with monocot-specific CCT-domain protein Ghd7. The Plant Journal: For Cell and Molecular Biology, 86(3), 221-233.
Oerke, E.-C. (2006). Crop losses to pests. The Journal of Agricultural Science, 144(1), 31-43.
Qi, X., Liu, Y., Vigueira, C. C., Young, N. D., Caicedo, A. L., Jia, Y., Gealy, D. R., & Olsen, K. M. (2015). More than one way to evolve a weed: Parallel evolution of US weedy rice through independent genetic mechanisms. Molecular Ecology, 24(13), 3329-3344.
Qiu, J., Jia, L., Wu, D., Weng, X., Chen, L., Sun, J., Chen, M., Mao, L., Jiang, B., Ye, C., Turra, G. M., Guo, L., Ye, G., Zhu, Q.-H., Imaizumi, T., Song, B.-K., Scarabel, L., Merotto, A., Jr., Olsen, K. M., & Fan, L. (2020). Diverse genetic mechanisms underlie worldwide convergent rice feralization. Genome Biology, 21(1), 70.
Qiu, J., Zhou, Y., Mao, L., Ye, C., Wang, W., Zhang, J., Yu, Y., Fu, F., Wang, Y., Qian, F., Qi, T., Wu, S., Sultana, M. H., Cao, Y.-N., Wang, Y., Timko, M. P., Ge, S., Fan, L., & Lu, Y. (2017). Genomic variation associated with local adaptation of weedy rice during de-domestication. Nature Communications, 8(1), 1-12.
R Core Team. (2022). R: A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R-project.org/
Reagon, M., Thurber, C. S., Gross, B. L., Olsen, K. M., Jia, Y., & Caicedo, A. L. (2010). Genomic patterns of nucleotide diversity in divergent populations of U.S. weedy rice. BMC Evolutionary Biology, 10, 180.
Reagon, M., Thurber, C. S., Olsen, K. M., Jia, Y., & Caicedo, A. L. (2011). The long and the short of it: SD1 polymorphism and the evolution of growth trait divergence in U.S. weedy rice. Molecular Ecology, 20(18), 3743-3756.
Sales, M. A., Shivrain, V. K., Burgos, N. R., & Kuk, Y. I. (2008). Amino acid substitutions in the acetolactate synthase gene of red rice (Oryza sativa) confer resistance to imazethapyr. Weed Science, 56(4), 485-489.
Sheng, C., Song, S., Zhou, R., Li, D., Gao, Y., Cui, X., Tang, X., Zhang, Y., Tu, J., Zhang, X., & Wang, L. (2021). QTL-seq and transcriptome analysis disclose major QTL and candidate genes controlling leaf size in sesame (Sesamum indicum L.). Frontiers in Plant Science, 12, 580846.
Shivrain, V. K., Burgos, N. R., Scott, R. C., Gbur, E. E., Estorninos, L. E., & McClelland, M. R. (2010). Diversity of weedy red rice (Oryza sativa L.) in Arkansas, U.S.A. in relation to weed management. Crop Protection, 29(7), 721-730.
Spielmeyer, W., Ellis, M. H., & Chandler, P. M. (2002). Semidwarf (sd-1), “green revolution” rice, contains a defective gibberellin 20-oxidase gene. Proceedings of the National Academy of Sciences of the United States of America, 99(13), 9043-9048.
Subudhi, P. K., Singh, P. K., DeLeon, T., Parco, A., Karan, R., Biradar, H., Cohn, M. A., & Sasaki, T. (2014). Mapping of seed shattering loci provides insights into origin of weedy rice and rice domestication. The Journal of Heredity, 105(2), 276-287.
Sun, J., Ma, D., Tang, L., Zhao, M., Zhang, G., Wang, W., Song, J., Li, X., Liu, Z., Zhang, W., Xu, Q., Zhou, Y., Wu, J., Yamamoto, T., Dai, F., Lei, Y., Li, S., Zhou, G., Zheng, H., … Chen, W. (2019). Population genomic analysis and de novo assembly reveal the origin of weedy Rice as an evolutionary game. Molecular Plant, 12(5), 632-647.
Takagi, H., Abe, A., Yoshida, K., Kosugi, S., Natsume, S., Mitsuoka, C., Uemura, A., Utsushi, H., Tamiru, M., Takuno, S., Innan, H., Cano, L. M., Kamoun, S., & Terauchi, R. (2013). QTL-seq: Rapid mapping of quantitative trait loci in rice by whole genome resequencing of DNA from two bulked populations. The Plant Journal: For Cell and Molecular Biology, 74(1), 174-183.
Takahashi, Y., Teshima, K. M., Yokoi, S., Innan, H., & Shimamoto, K. (2009). Variations in Hd1 proteins, Hd3a promoters, and Ehd1 expression levels contribute to diversity of flowering time in cultivated rice. Proceedings of the National Academy of Sciences of the United States of America, 106(11), 4555-4560.
Thurber, C. S., Jia, M. H., Jia, Y., & Caicedo, A. L. (2013). Similar traits, different genes? Examining convergent evolution in related weedy rice populations. Molecular Ecology, 22(3), 685-698.
Thurber, C. S., Reagon, M., Gross, B. L., Olsen, K. M., Jia, Y., & Caicedo, A. L. (2010). Molecular evolution of shattering loci in U.S. weedy rice. Molecular Ecology, 19(16), 3271-3284.
Thurber, C. S., Reagon, M., Olsen, K. M., Jia, Y., & Caicedo, A. L. (2014). The evolution of flowering strategies in US weedy rice. American Journal of Botany, 101(10), 1737-1747.
Vanneste, S., & Friml, J. (2009). Auxin: A trigger for change in plant development. Cell, 136(6), 1005-1016.
Vigueira, C. C., Olsen, K. M., & Caicedo, A. L. (2013). The red queen in the corn: Agricultural weeds as models of rapid adaptive evolution. Heredity, 110(4), 303-311.
Wedger, M. J., Roma-Burgos, N., & Olsen, K. M. (2022). Genomic revolution of US weedy rice in response to 21st century agricultural technologies. Communications Biology, 5(1), 885.
Wei, X., Xu, J., Guo, H., Jiang, L., Chen, S., Yu, C., Zhou, Z., Hu, P., Zhai, H., & Wan, J. (2010). DTH8 suppresses flowering in rice, influencing plant height and yield potential simultaneously. Plant Physiology, 153(4), 1747-1758.
Wen, J., Jiang, F., Weng, Y., Sun, M., Shi, X., Zhou, Y., Yu, L., & Wu, Z. (2019). Identification of heat-tolerance QTLs and high-temperature stress-responsive genes through conventional QTL mapping, QTL-seq and RNA-seq in tomato. BMC Plant Biology, 19(1), 398.
Wu, D., Qiu, J., Sun, J., Song, B.-K., Olsen, K. M., & Fan, L. (2022). Weedy rice, a hidden gold mine in the paddy field. Molecular Plant, 15(4), 566-568.
Wu, W., Zheng, X.-M., Lu, G., Zhong, Z., Gao, H., Chen, L., Wu, C., Wang, H. J., Wang, Q., Zhou, K., Wang, J.-L., Wu, F., Zhang, X., Guo, X., Cheng, Z., Lei, C., Lin, Q., Jiang, L., Wang, H., … Wan, J. (2013). Association of functional nucleotide polymorphisms at DTH2 with the northward expansion of rice cultivation in Asia. Proceedings of the National Academy of Sciences of the United States of America, 110(8), 2775-2780.
Xia, L., Zou, D., Sang, J., Xu, X., Yin, H., Li, M., Wu, S., Hu, S., Hao, L., & Zhang, Z. (2017). Rice expression database (RED): An integrated RNA-Seq-derived gene expression database for rice. Journal of Genetics and Genomics, 44(5), 235-241.
Yan, W. H., Wang, P., Chen, H. X., Zhou, H.-J., Li, Q. P., Wang, C. R., Ding, Z. H., Zhang, Y. S., Yu, S. B., Xing, Y. Z., & Zhang, Q. F. (2011). A major QTL, Ghd8, plays pleiotropic roles in regulating grain productivity, plant height, and heading date in rice. Molecular Plant, 4(2), 319-330.
Yano, M., Katayose, Y., Ashikari, M., Yamanouchi, U., Monna, L., Fuse, T., Baba, T., Yamamoto, K., Umehara, Y., Nagamura, Y., & Sasaki, T. (2000). Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. The Plant Cell, 12(12), 2473-2484.
Zhao, Q., Feng, Q., Lu, H., Li, Y., Wang, A., Tian, Q., Zhan, Q., Lu, Y., Zhang, L., Huang, T., Wang, Y., Fan, D., Zhao, Y., Wang, Z., Zhou, C., Chen, J., Zhu, C., Li, W., Weng, Q., … Huang, X. (2018). Pan-genome analysis highlights the extent of genomic variation in cultivated and wild rice. Nature Genetics, 50(2), 278-284.
Zhou, J., Yang, Y., Lv, Y., Pu, Q., Li, J., Zhang, Y., Deng, X., Wang, M., Wang, J., & Tao, D. (2022). Interspecific hybridization is an important driving force for origin and diversification of Asian cultivated Rice Oryza sativa L. Frontiers in Plant Science, 13, 932737.
Zhou, Y., Lu, D., Li, C., Luo, J., Zhu, B.-F., 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. The Plant Cell, 24(3), 1034-1048.
Ziska, L. H., Gealy, D. R., Burgos, N., Caicedo, A. L., Gressel, J., Lawton-Rauh, A. L., Avila, L. A., Theisen, G., Norsworthy, J., Ferrero, A., Vidotto, F., Johnson, D. E., Ferreira, F. G., Marchesan, E., Menezes, V., Cohn, M. A., Linscombe, S., Carmona, L., Tang, R., & Merotto, A. (2015). Chapter three-weedy (red) rice: An emerging constraint to global rice production. In D. L. Sparks (Ed.), Advances in Agronomy (Vol. 129, pp. 181-228). Academic Press.