Hostname: page-component-76fb5796d-r6qrq Total loading time: 0 Render date: 2024-04-26T21:18:30.069Z Has data issue: false hasContentIssue false
  • English
  • Français

Distribution of Weedy Red Rice (Oryza sativa) Resistant to Imidazolinone Herbicides and its Relationship to Rice Cultivars and Wild Oryza Species

Published online by Cambridge University Press:  20 January 2017

Ives C. G. R. Goulart ,
Tereza C. O. Borba ,
Valmir G. Menezes  and
Aldo Merotto Jr.
Ives C. G. R. Goulart
Affiliation:
Crop Science Department of the Federal University of Rio Grande do Sul, Porto Alegre, RS, Brazil, 91501-970
Tereza C. O. Borba
Affiliation:
Brazilian Agricultural Research Corporation–Embrapa, Santo Antônio de Goiás, GO, Brazil, 75375-000
Valmir G. Menezes
Affiliation:
Rice Institute of the Rio Grande do Sul, Cachoeirinha, RS, Brazil, 94930-030
Aldo Merotto Jr.*
Affiliation:
Crop Science Department of the Federal University of Rio Grande do Sul, Porto Alegre, RS, Brazil, 91501-970
*
Corresponding author's E-mail: merotto@ufrgs.br
Get access Rights & Permissions [Opens in a new window]

Abstract

Several weedy red rice populations have evolved resistance to imidazolinone herbicides worldwide. The understanding of the factors related to the herbicide resistance in weedy red rice is important to prevent its occurrence in new areas where imidazolinone-resistant rice cultivars are being used, and to manage the new rice cultivars resistant to herbicides with modes of action other than the acetolactate synthase (ALS)-inhibitors that are being developed. The objectives of this study were to analyze the relationship of weedy red rice populations from southern Brazil with rice cultivars and wild Oryza species and to evaluate the occurrence of introgression from rice cultivars and seed migration as the origin of resistance to imidazolinone herbicides in weedy rice. The study was based on 27 weedy red rice populations, seven rice cultivars, and four wild Oryza species that were genotyped with 24 simple sequence repeats and three ALS-specific single-nucleotide polymorphism markers. A large proportion of the genetic variation of the weedy red rice populations was found within (74%) rather than among populations (26%). The weedy red rice populations were more closely related to the newer rice cultivars that are imidazolinone-resistant than to the older cultivars. The South American native Oryza glumaepatula and the other wild Oryza species—Oryza rufipogon, Oryza longistaminata, and Oryza glaberrima—clustered separately from weedy red rice populations, indicating a low likelihood of introgression among weedy red rice and these wild species. Seed migration was an important factor in the genetic structure of the evaluated weedy red rice populations, although gene flow by pollen from resistant cultivars was the principal reason for the spread of herbicide resistance.

Keywords

Weedy red rice, Oryza sativa L. ORYSArice, Oryza sativa L. ORYSAbrownbeard rice, Oryza rufipogon Griffithslongstamen rice, Oryza longistaminata A. Chev. & Roehr.and African rice, Oryza glaberrima Steud.Acetohydroxyacid synthaseClearfield™genetic diversityherbicide resistance
Type
Weed Biology and Ecology
Information
Weed Science , Volume 62 , Issue 2 , June 2014 , pp. 280 - 293
Copyright
Copyright © Weed Science Society of America 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

Current address: Technology Transfer, Brazilian Agricultural Research Corporation–Embrapa, Colombo, PR, Brazil, 83411-000.

References

Literature Cited

Al-Ahmad, H, Gressel, J (2006) Mitigation using a tandem construct containing a selectively unfit gene precludes establishment ofBrassica napus transgenes in hybrids and backcrosses with weedy Brassica rapa . Plant Biotechnol J. 4:23–33 Google Scholar
Borba, TDO, Brondani, R, Rangel, P, Brondani, C (2009) Microsatellite marker-mediated analysis of the EMBRAPA rice core collection genetic diversity. Genetica. 137:293–304 Google Scholar
Botstein, D, White, RL, Skolnick, M, Davis, RW (1980) Construction of a genetic-linkage map in man using restriction fragment length polymorphisms. Am J Hum Genet. 32:314–331 Google Scholar
Burgos, NR, Norsworthy, JK, Scott, RC, Smith, KL (2008) Red rice (Oryza sativa) status after 5 years of imidazolinone-resistant rice technology in Arkansas. Weed Technol. 22:200–208 Google Scholar
Busconi, M, Rossi, D, Lorenzoni, C, Baldi, G, Fogher, C (2012) Spread of herbicide-resistant weedy rice (red rice, Oryza sativa L.) after 5 years of Clearfield rice cultivation in Italy. Plant Biol. 14:751–759 Google Scholar
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 Google Scholar
Cao, Q-J, Xia, H, Yang, X, Lu, BR (2009) Performance of hybrids between weedy rice and insect-resistant transgenic rice under field experiments: implication for environmental biosafety assessment. J Integr Plant Biol. 51:1138–1148 Google Scholar
Chung, JW, Park, YJ (2010) Population structure analysis reveals the maintenance of isolated sub-populations of weedy rice. Weed Res. 50:606–620 Google Scholar
Courtois, B, Froulin, J, Greco, R, Brusch, G, Droc, G, Hamelin, C, Ruiz, M, Clément, G, Evrard, JC, Coppenol, S, Katsantonis, D, Oliveira, M, Negrão, S, Matos, C, Cavigiolo, S, Lupotto, E, Piffanelli, Ahmadia, N (2012) Genetic diversity and population structure in a European collection of rice. Crop Sci. 52:1663–1675 Google Scholar
Delouche, JC, Burgos, NR, Gealy, DR, Martin, GZS, Labrada, R, Larinde, M, Rosell, C (2007) Weedy Rices—Origin, Biology, Ecology, and Control. Rome Food and Agriculture Organization. 155 pGoogle Scholar
Doyle, JJ, Doyle, JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull. 19:11–15 Google Scholar
Ellstrand, NC (2009) Evolution of invasiveness in plants following hybridization. Biol Invasions. 11:1089–1091 Google Scholar
Evanno, G, Regnaut, S, Goudet, J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol. 14:2611–2620 Google Scholar
Garris, AJ, Tai, TH, Coburn, J, Kresovich, S, McCouch, S (2005) Genetic structure and diversity in Oryza sativa L. Genetics. 169:1631–1638 Google Scholar
Gealy, DR, Agrama, HA, Eizenga, GC (2009) Exploring genetic and spatial structure of US weedy red rice (Oryza sativa) in relation to rice relatives worldwide. Weed Sci. 57:627–643 Google Scholar
Gealy, DH, Agrama, H, Jia, MH (2012) Genetic analysis of a typical U.S. red rice phenotypes: indications of prior gene flow in rice fields? Weed Sci. 60:451–461 Google Scholar
Gealy, DR, Mitten, DH, Rutger, JN (2003) Gene flow between red rice (Oryza sativa) and herbicide-resistant rice (O. sativa): implications for weed management. Weed Technol. 17:627–645 Google Scholar
Goulart, ICGR, Matzenbacher, FO, Merotto, A Jr. (2012a) Differential germination pattern of rice cultivars resistant to imidazolinone herbicides carrying different acetolactate synthase gene mutations. Weed Res. 52:224–232 Google Scholar
Goulart, ICGR, Pacheco, M, Nunes, A, Merotto, A Jr. (2012b) Identification of origin and analysis of population structure of field-selected imidazolinone-herbicide resistant red rice. Euphytica. 187:437–447 Google Scholar
Gressel, J, Valverde, BE (2009) A strategy to provide long-term control of weedy rice while mitigating herbicide resistance transgene flow, and its potential use for other crops with related weeds. Pest Manag Sci. 65:723–731 Google Scholar
Hu, T, Qv, X, Xiao, G, Huang, X (2009) Enhanced tolerance to herbicide of rice plants by over-expression of a glutathione S-transferase. Mol Breed. 24:409–418 Google Scholar
Ishikawa, R, Toki, N, Imai, K, Sato, HI, 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 Google Scholar
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 ApplGenet. 124:309–322 Google Scholar
Jung, HI, Kuk, YI, Back, K, Lee, DJ, Lee, S, Burgos, NR (2010) Resistance levels and fitness of protoporphyrinogen oxidase (PROTOX) inhibitor-resistant transgenic rice in paddy fields. Field Crops Res. 115:125–131 Google Scholar
Karasawa, MMG, Vencovsky, R, Silva, CM, Zucchi, MI, Oliveira, GCX, Veasey, EA (2007) Genetic structure of Brazilian wild rice (Oryza glumaepatula Steud., Poaceae) populations analyzed using microsatellite markers. Genet Mol Biol. 30:400–410 Google Scholar
Kawasaki, A, Imai, K, Ushiki, J, Ishii, T, Ishikawa, R (2009) Molecular constitution of weedy rice (Oryza sativa L.) found in Okayama prefecture, Japan. Breed Sci. 59:229–236 Google Scholar
Kuk, YI, Burgos, NR, Shivrain, VK (2008) Natural tolerance to imazethapyr in red rice (Oryza sativa). Weed Sci. 56:1–11 Google Scholar
Lentini, Z, Espinoza, AM (2005) Coexistence of weedy rice and rice in tropical america—gene flow and genetic diversity. Pages 305–322 in Gressel, J, ed. Crop Ferality and Volunteerism. Boca Raton, FL CRC Google Scholar
Lin, C, Fang, J, Xu, W, Zhao, T, Cheng, J, Tu, J, Ye, G, Shen, Z (2008) A built-in strategy for containment of transgenic plants: creation of selectively terminable transgenic rice. PLoS ONE. 3:e1818 Google Scholar
Liu, K, Muse, SV (2005) PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinformatics. 21:2128–2129 Google Scholar
Livore, AB, Prina, AR, Birk, I, Singh, B, inventors; Instituto Nacional de Technologia Agropecuaria assignee (2005) March 10. Rice plants having increased tolerance to imidazolinone herbicides. U.S. patent 20070028318Google Scholar
Londo, JP, Schaal, BA (2007) Origins and population genetics of weedy red rice in the USA. Mol Ecol. 16:4523–4535 Google Scholar
Mantel, N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res. 27:209–220 Google Scholar
Marchezan, E, Menezes, NLD, Siqueira, CDA (2001) Controle da qualidade das sementes de arroz irrigado utilizadas em Santa Maria/RS. Ciência Rural. 31:375–379 Google Scholar
Menezes, VG, Mariot, CHP, Kalsing, A, Goulart, ICGR (2009) Arroz-vermelho (Oryza sativa) resistente aos herbicidas imidazolinonas. Planta Daninha. 27:1047–1052 Google Scholar
Merotto, A Jr., Kalsing, A, Lopes, SIG (2013) Development of rice cultivars related to the technologies applied to the red rice control—public institutions—Brazil. CD. Proceedings of the II Latin-American Symposium of Red Rice. Porto Alegre, RS, Brazil Institute Riograndense of Rice and Federal University of Rio Grande do Sul Google Scholar
Michiels, F, Johnson, K, inventors; Plant Genetic Systems, N.V. (Gent, BE) assignee (2001) January 25. Glufosinate tolerant rice. U.S. patent 6333449Google Scholar
Nei, M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics. 89:583–590 Google Scholar
Nei, M, Tajima, F, Tateno, Y (1983) Accuracy of estimated phylogenetic trees from molecular data. J Mol Evol. 19:153–170 Google Scholar
Peakall, ROD, Smouse, PE (2006) Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes. 6:288–295 Google Scholar
Prathepha, P (2011) Microsatellite analysis of weedy rice (Oryza sativa f. spontanea) from Thailand and Lao PDR. Aust J Crop Sci. 5:49–54 Google Scholar
Pritchard, JK, Stephens, M, Donnelly, P (2000) Inference of population structure using multilocus genotype data. Genetics. 155:945–959 Google Scholar
Rajguru, SN, Burgos, NR, Shivrain, VK, McD Stewart, J (2005) Mutations in the red rice ALS gene associated with resistance to imazethapyr. Weed Sci. 53:946–946 Google Scholar
Reagon, M, Thurber, CS, Gros, BL, Olsen, KM, Jia, Y, Caicedo, AL (2010) Genomic patterns of nucleotide diversity in divergent populations of U.S. weedy rice. BMC Evol Biol. 10:180 Google Scholar
Roso, AC, Merotto, A Jr., Delatorre, CA, Menezes, VG (2010) Regional scale distribution of imidazolinone herbicide-resistant alleles in red rice (Oryza sativa L.) determined through SNP markers. Field Crops Res. 119:175–182 Google Scholar
Scarabel, L, Cenghialta, C, Manuello, D, Sattin, M (2012) monitoring and management of imidazolinone-resistant red rice (Oryza sativa L., var. sylvatica) in Clearfield® Italian paddy rice. Agronomy. 2:371–383 Google Scholar
Shivrain, VK, Burgos, NR, Agrama, HA, Lawton-Rauh, A, Lu, BR, Sales, MA, Boyett, V, Gealy, DR, Moldenhauer, KAK (2010a) Genetic diversity of weedy red rice (Oryza sativa) in Arkansas, USA. Weed Res. 50:289–302 Google Scholar
Shivrain, VK, Burgos, NR, Sales, MA, Kuk, YI (2010b) Polymorphisms in the ALS gene of weedy rice (Oryza sativa L.) accessions with differential tolerance to imazethapyr. Crop Prot. 29:336–341 Google Scholar
Song, X, Liu, L, Wang, Z, Qiang, S (2009) Potential gene flow from transgenic rice (Oryza sativa L.) to different weedy rice (Oryza sativa f. spontanea) accessions based on reproductive compatibility. Pest Manag Sci. 65:862–869 Google Scholar
Song, Z, Lu, BR, Chen, J (2004) Pollen flow of cultivated rice measured under experimental conditions. Biodivers Conserv. 13:579–590 Google Scholar
Tamura, K, Dudley, J, Nei, M, Kumar, S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol. 24:1596–1599 Google Scholar
Templeton, AR (2006) Gene flow and population subdivision. Pages 168–203 in Templeton, AR. Population Genetics and Microevolutionary Theory. Hoboken, NJ J Wiley Google Scholar
Thurber, CS, Jia, MH, Jia, YL, Caicedo, AL (2013) Similar traits, different genes? Examining convergent evolution in related weedy rice populations. Mol Ecol. 22:685–698 Google Scholar
Wright, S (1949) The genetical structure of populations. Ann Eugenics. 15:323–354 Google Scholar
Xia, HB, Wang, W, Xia, H, Zhao, W, Lu, BR (2011) Conspecific crop–weed introgression influences evolution of weedy rice (Oryza sativa f. spontanea) across a geographical range. PLoS ONE. 6:e16189 Google Scholar
Yoshida, H, Itoh, J, Ohmori, S, Miyoshi, K, Horigome, A, Uchida, E, Kimizu, M, Matsumura, Y, Kusaba, M, Satoh, H, Nagato, Y (2007) Superwoman1-cleistogamy, a hopeful allele for gene containment in GM rice. Plant Biotechnol J. 5:835–846 Google Scholar
Zhang, DL, Zhang, HL, Qi, YW, Wang, MX, Sun, JL, Ding, L, Li, ZC (2013) Genetic structure and eco-geographical differentiation of cultivated Hsien rice (Oryza sativa L. subsp. indica) in China revealed by microsatellites. Chin Sci Bull. 58:344–352 Google Scholar
Zhang, DL, Zhang, H, Wang, M, Sun, J, Qi, Y, Wang, F, Wei, X, Han, L, Wang, X, Li, Z (2009) Genetic structure and differentiation of Oryza sativa L. in China revealed by microsatellites. Theor Appl Genet. 119:1105–1117 Google Scholar
Zhou, M, Xu, H, Wei, X, Ye, Z, Wei, L, Gong, W, Wang, Y, Zhu, Z (2006) Identification of a glyphosate-resistant mutant of rice 5-enolpyruvylshikimate 3-phosphate synthase using a directed evolution strategy. Plant Physiol. 140:184–195 Google Scholar
Ziska, LH, Gealy, DR, Tomecek, MB, Jackson, AK, Black, HL (2012) Recent and projected increases in atmospheric CO2 concentration can enhance gene flow between wild and genetically altered rice (Oryza sativa). PLoS ONE. 7(5):e37522 Google Scholar