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Development of elite rice restorer lines in the genetic background of R022 possessing tolerance to brown planthopper, stem borer, leaf folder and herbicide through marker-assisted breeding

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Abstract

Rice leaf folder, stem borer and brown planthopper (BPH) are the most devastating rice insect pests. Developing and planting insect-resistant rice varieties is the most economical and effective measure for controlling these pests. BPH can be controlled with native BPH-resistance genes in rice, while at present rice leaf folder and stem borer can only be controlled through planting transgenic Bt rice. In this study, the breeding of a new restorer line KR022 possessing stacked BPH-resistance genes Bph14 and Bph15, Bt gene cry1C and glufosinate-resistance gene bar, is reported for the first time. A rice restorer line R022 with BPH-resistance genes Bph14 and Bph15 was used as a recurrent parent to cross with the transgenic rice T1C-19 of cry1C and bar genes during the breeding process. The restorer line KR022 was developed from the backcross populations of R022 and T1C-19 through molecular marker-assisted selection and glufosinate-resistance selection. The cry1C and bar genes were found to integrate on chromosome 11 of KR022, and the genome recovery of KR022 was up to 95.8 % of the R022 genome. The quantification of Cry1C protein expression showed that it was expressed at different levels in the leaf, stem, panicle, endosperm, and root of KR022 and its hybrid rice. The insect-resistance evaluation indicated that KR022 and its hybrid rice had good resistance to rice leaf folder and stem borer, both in laboratory settings and in the field. Furthermore, they exhibited increased resistance to BPH at both the seedling and mature stage. The field trial showed there was no significant difference in key agronomic traits between KR022 and its recurrent parent R022, and four hybrids from KR022 yield much higher than the control II-You 838. Moreover, KR022 and its hybrid rice were found to have resistance to the herbicide glufosinate. These results demonstrate that KR022 is effective as a rice restorer line for the breeding of “green super rice”, possessing multiple tolerances to rice BPH, stem borer, leaf folder and glufosinate.

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Abbreviations

BPH:

Brown planthopper

Bt:

Bacillus thuringiensis

dNTP:

Deoxy-ribonucleoside triphosphate

ELISA:

Enzyme-linked immunosorbent assay

GM:

Genetically-modified

MAS:

Molecular marker-assisted selection

PCR:

Polymerase chain reaction

PPT:

Phosphinothricin

SSB:

Striped stem borer

YSB:

Yellow stem borer

References

  • Bharathkumara S, Paulraja RSD, Brindhaa PV, Kavithaa S, Gnanamanickam SS (2008) Improvement of bacterial blight resistance in rice cultivars Jyothi and IR50 via marker-assisted backcross breeding. J Crop Improve 21:101–116

    Article  Google Scholar 

  • Block MD, Botterman J, Vandewiele M, Dockx J, Thoen C, Gosselé V, Movva NR, Thompson C, Montagu MV, Leemans J (1987) Engineering herbicide resistance in plants by expression of a detoxifying enzyme. EMBO J 6:2513–2518

    PubMed  CAS  Google Scholar 

  • Block MD, Brouwer DD, Tenning P (1989) Transformation of Brassica napus and Brassica oleracea using Agrobacterium tumefaciens and the expression of the bar and neo genes in the transgenic plants. Plant Physol 91:694–701

    Article  Google Scholar 

  • Chen XW, Li SG, Ma YQ, Li HY, Zhou KD, Zhu LH (2004) Marker-assisted selection and pyramiding for three blast resistance genes, Pi-d(t)1, Pi-b, Pi-ta2, in rice. Chin J Biotech 20:708–714

    Google Scholar 

  • Chen H, Tang W, Xu C, Li X, Lin Y, Zhang Q (2005) Transgenic indica rice plants harboring a synthetic cry2A* gene of Bacillus thuringiensis exhibit enhanced resistance against lepidopteran rice pests. Theor Appl Genet 111:1330–1337

    Article  PubMed  CAS  Google Scholar 

  • Cornejo MJ, Luth D, Blankenship KM, Anderson OD, Blechl AE (1993) Activity of a maize ubiquitin promoter in transgenic rice. Plant Mol Biol 23:567–581

    Article  PubMed  CAS  Google Scholar 

  • Datta K, Baisakh N, Maung Thet K, Tu J, Datta SK (2002) Pyramiding transgenes for multiple resistance in rice against bacterial blight, yellow stem borer and sheath blight. Theor Appl Genet 106:1–8

    PubMed  CAS  Google Scholar 

  • Du B, Zhang W, Liu B, Hu J, Wei Z, Shi Z, He R, Zhu L, Chen R, Han B, He G (2009) Identification and characterization of Bph14, a gene conferring resistance to brown planthopper in rice. Proc Natl Acad Sci USA 106:22163–22168

    Article  PubMed  CAS  Google Scholar 

  • Farooq M, Siddique KHM, Rehman H, Aziz T, Leed DJ, Wahide A (2011) Rice direct seeding: experiences, challenges and opportunities. Soil Tillage Res 111:87–98

    Article  Google Scholar 

  • Fu YP, Zhu ZG, Xiao H, Hu GC, Si HM, Yu YH, Sun ZX (2001) Primary study of mechanization of seed production of hybrid rice by introducing bar gene to Pei’ai 64S. Chinese J Rice Sci 15:97–100

    Google Scholar 

  • Fujimoto H, Itoh K, Yamamoto M, Kyozuka J, Shimamoto K (1993) Insect resistant rice generated by introduction of a modified δ-endotoxin gene of Bacillus thuringiensis. Nat Biotech 11:1151–1155

    Article  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Harini AS, Lakshmi SS, Kumar SS, Sivaramakrishnan S, Kadirvel P (2010) Validation and fine-mapping of genetic locus associated with resistance to brown plant hopper [Nilaparvata lugens (Stal.)] in rice (Oryza sativa L.). Asian J Bio Sci 5:32–37

    Google Scholar 

  • Hu J, Li X, Wu C, Yang C, Hua H, Gao G, Xiao J, He Y (2012) Pyramiding and evaluation of the brown planthopper resistance genes Bph14 and Bph15 in hybrid rice. Mol Breed 29:61–69

    Article  Google Scholar 

  • Huang D, Li J, Zhang S, Xue R, Yang W, Hua Z, Xie X, Wang X (1998) New technology to examine and improve the purity of hybrid rice with herbicide resistant gene. Chin Sci Bull 43:784–787

    Article  Google Scholar 

  • Huang J, Hu R, Pray C, Qiao F, Rozelle S (2003) Biotechnology as an alternative to chemical pesticides: a case study of Bt cotton in China. Agri Econ 29:55–67

    Article  Google Scholar 

  • Hyde J, Martin MA, Preckel PV, Edwards CR (1999) The economics of Bt corn: valuing protection from the European corn borer. Appl Econ Perspect Pol 21:442–454

    Article  Google Scholar 

  • Jena KK, Kim SM (2010) Current status of brown planthopper (BPH) resistance and genetics. Rice 3:161–171

    Article  Google Scholar 

  • Jiang GH, Xu CG, Tu JM, Li XH, He YQ (2004) Pyramiding of insect-and disease-resistance genes into an elite indica, cytoplasm male sterile restorer line of rice, ‘Minghui 63′. Plant Breed 123:112–116

    Article  CAS  Google Scholar 

  • Li J, Xia M, Qi H, He G, Wan B, Zha Z (2006) Marker-assisted selection for brown planthopper (Nilaparvata lugens Stl) resistance genes Bph14 and Bph15 in rice. Sci Agric Sin 39:2132–2137

    Google Scholar 

  • Li J, Wan B, Xia M, Qi H, Shi H, Xin F (2011) Breeding of the brown planthopper resistant rice varieties. Chin J Appl Entomol 48:1348–1353

    CAS  Google Scholar 

  • Lu L, Wu X, Yin X, Morrand J, Chen X, Folk WR, Zhang Z (2009) Development of marker-free transgenic sorghum [Sorghum bicolor (L.) Moench] using standard binary vectors with bar as a selectable marker. Plant Cell Tiss Organ Cult 99:97–108

    Article  CAS  Google Scholar 

  • Myint KKM, Fujita D, Matsumura M, Sonoda T, Yoshimura A, Yasui H (2012) Mapping and pyramiding of two major genes for resistance to the brown planthopper (Nilaparvata lugens [Stål]) in the rice cultivar ADR52. Theor Appl Genet 124:495–504

    Article  PubMed  CAS  Google Scholar 

  • Peñalver Cruz A, Arida A, Heong KL, Horgan FG (2011) Aspects of brown planthopper adaptation to resistant rice varieties with the Bph3 gene. Entomol Exp Appl 141:245–257

    Article  Google Scholar 

  • Phipps RH, Park JR (2002) Environmental benefits of genetically modified crops: global and European perspectives on their ability to reduce pesticide use. J Anim Feed Sci 11:1–18

    Google Scholar 

  • Pray CE, Jhuang J, Hu R, Rozelle S (2002) Five years of Bt cotton in China the benefits continue. Plant J 31:423–430

    Article  PubMed  CAS  Google Scholar 

  • Rooke L, Byrne D, Salgueiro S (2005) Marker gene expression driven by the maize ubiquitin promoter in transgenic wheat. Ann Appl Biol 136:167–172

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • Stewart SD, Adamczyk JJ, Knighten KS, Davis FM (2001) Impact of Bt cottons expressing one or two insecticidal proteins of Bacillus thuringiensis Berliner on growth and survival of noctuid (Lepidoptera) larvae. J Econ Entomol 94:752–760

    Article  PubMed  CAS  Google Scholar 

  • Tang W, Chen H, Xu C, Li X, Lin Y, Zhang Q (2006) Development of insect-resistant transgenic indica rice with a synthetic cry1C* gene. Mol Breed 18:1–10

    Article  CAS  Google Scholar 

  • Toki S, Takamatsu S, Nojiri C, Ooba S, Anzai H, Iwata M, Christensen AH, Quail PH, Uchimiya H (1992) Expression of a maize ubiquitin gene promoter-bar chimeric gene in transgenic rice plants. Plant Physol 100:1503–1507

    Article  CAS  Google Scholar 

  • Tu J, Zhang G, Datta K, Xu C, He Y, Zhang Q, Khush GS, Datta SK (2000) Field performance of transgenic elite commercial hybrid rice expressing Bacillus thuringiensis δ-endotoxin. Nat Biotech 18:1101–1104

    Article  CAS  Google Scholar 

  • Wang Y (2006) Analysis on the occurrence and development of rice diseases and insects in China. Chin Agric Sci Bull 22:343–347

    CAS  Google Scholar 

  • Wang ZX, Wang XJ, Jia SR (2011) Data survey and analysis of the gene flow frequencies and distances in major crops II. Rice J Agri Sci Technol 13:30–34

    Google Scholar 

  • Wei Y, Yao F, Zhu C, Jiang M, Li G, Song Y, Wen F (2008) Breeding of transgenic rice restorer line for multiple resistance against bacterial blight, striped stem borer and herbicide. Euphytica 163:177–184

    Article  CAS  Google Scholar 

  • Wu M, Lin J, Hua Z, Yan M, Huang D (2000) Application of bar gene in directed seeded rice. Acta Agriculturae Zhejiangensis 12:290–293

    Google Scholar 

  • Yang H, You A, Yang Z, Zhang F, He R, Zhu L, He G (2004) High-resolution genetic mapping at the Bph15 locus for brown planthopper resistance in rice (Oryza sativa L.). Theor Appl Genet 10:182–191

    Article  Google Scholar 

  • Yang Z, Chen H, Tang W, Hua H, Lin Y (2011) Development and characterization of transgenic rice expressing two Bacillus thuringiensis genes. Pest Manag Sci 67:414–422

    Article  PubMed  CAS  Google Scholar 

  • Yao KM, Hu N, Chen WL, Li RZ, Yuan QH, Wang F, Qian Q, Jia SR (2008) Establishment of a rice transgene flow model for predicting maximum distances of gene flow in southern China. New Phyt 180:217–228

    Article  Google Scholar 

  • Ye G, Tu J, Hu C, Datta K, Datta SK (2001) Transgenic IR72 with fused Bt gene cry1Ab/cry1Ac from Bacillus thuringiensis is resistant against four lepidopteran species under field conditions. Plant Biotechnol 18:125–133

    Article  CAS  Google Scholar 

  • Yorobe JM, Quicoy CB (2006) Economic impact of Bt corn in the Philippines. Philipp Agric Sci 89:258–267

    Google Scholar 

  • Zhang Q (2007) Strategies for developing green super rice. Proc Natl Acad Sci USA 104:16402–16409

    Article  PubMed  CAS  Google Scholar 

  • Zheng X, Yang Y, Xu H, Chen H, Wang B, Lin Y, Lu Z (2011) Resistance performances of transgenic Bt rice lines T2A-1 and T1c-19 against Cnaphalocrocis medinalis (Lepidoptera: pyralidae). J Econom Entomol 104:1730–1735

    Article  CAS  Google Scholar 

  • Zhou Y, Xu J, Zhou S, Yu J, Xie X, Xu M, Sun Y, Zhu L, Fu B, Gao Y (2009) Pyramiding Xa23 and Rxo1 for resistance to two bacterial diseases into an elite indica rice variety using molecular approaches. Mol Breed 23:279–287

    Article  CAS  Google Scholar 

  • Zuo J, Zhang LJ, Song XL, Dai WM, Qiang S (2011) Innate factors causing differences in gene flow frequency fromtransgenic rice to different weedy rice biotypes. Pest Manag Sci 67:677–690

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Dr. Weihua Ma in the National Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research (Wuhan, China) for the help in SSB bioassay. This work was supported by the National Program of Transgenic Variety Development of China (2011ZX08001-001) and the Hubei Centre of Innovation for Agricultural Science and Technology (China).

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Correspondence to Bingliang Wan.

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Wan, B., Zha, Z., Li, J. et al. Development of elite rice restorer lines in the genetic background of R022 possessing tolerance to brown planthopper, stem borer, leaf folder and herbicide through marker-assisted breeding. Euphytica 195, 129–142 (2014). https://doi.org/10.1007/s10681-013-0988-x

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