Advertisement

Molecular Breeding

, 39:15 | Cite as

An LTR retrotransposon insertion was the cause of world’s first low erucic acid Brassica rapa oilseed cultivar

  • Eigo FukaiEmail author
  • Md. Masud Karim
  • Daniel J. Shea
  • Nazmoon Naher Tonu
  • Kevin C. Falk
  • Taketo Funaki
  • Keiichi OkazakiEmail author
Article

Abstract

Brassica rapa is an important oilseed crop species next to B. napus in Brassicaceae. However, genetic improvement of B. rapa oilseeds has not been intensively conducted compared to B. napus, which resulted in the limited number of low erucic acid (LEA) cultivars, which is an essential trait for edible oil materials. Candle and Tobin are LEA B. rapa cultivars bred in Canada that are closely related to each other; however, the causal mutation has not been identified. This study was initially aimed to investigate whether the alleles of BrFAE1, the gene encoding a key enzyme for erucic acid synthesis, in Candle and Tobin have mutations impairing their functions. An insertion of the long terminal repeat (LTR) retrotransposon, designated as BRACOPIA, was identified in the 5′ end of the coding region of the gene in both Candle and Tobin. BRACOPIA disrupted the transcription in developing seeds, resulting in a loss of function allele designated as brfae1re. Next, we found that Span, the world’s first LEA B. rapa cultivar developed in Canada, has brfae1re, suggesting that the BRACOPIA insertion is the founder mutation of Canadian LEA B. rapa cultivars. Finally, we investigated the distribution of BRACOPIA family retrotransposons in the Brassica genus, and found that they are present in both the A and C genomes, but the activity has been kept rather modest. Since brfae1re is easily distinguishable from the wild-type allele by PCR, the identification of this mutation could enhance LEA breeding in B. rapa.

Keywords

Brassica rapa Oilseeds Low erucic acid Retrotransposon 

Abbreviations

LEA

Low erucic acid

HEA

High erucic acid

LTR

Long terminal repeat

BRACOPIA

Brassica rapa Copia retrotransposon

BOLCOPIA

Brassica oleracea Copia retrotransposon

BNACOPIA

Brassica napus Copia retrotransposon

FAE1

FATTY ACID ELONGATION 1

VLCFA

Very long-chain fatty acids

Notes

Acknowledgments

Authors would like to thank Dr. Christina Eynck for proving Canadian B. rapa cultivars; Dr. Fengqun Yu for her generous support to conduct DNA experiments with these cultivars at Saskatoon Research and Development Centre, Agriculture and Agri-Food Canada (AAFC); and Dr. Mohammad Shakhawat Hossain, Oilseed Research Centre, Bangladesh Agricultural Research Institute (BARI), for his support to the fatty acid composition analysis.

Supplementary material

11032_2018_916_MOESM1_ESM.docx (19 kb)
Table S1 (DOCX 18 kb)
11032_2018_916_MOESM2_ESM.docx (125 kb)
ESM 1 (DOCX 125 kb)
11032_2018_916_MOESM3_ESM.pptx (42 kb)
Fig S1 (PPTX 41 kb)
11032_2018_916_MOESM4_ESM.pptx (46 kb)
Fig S2 (PPTX 46 kb)

References

  1. Barret P, Delourme R, Renard M, Domergue F, Lessire R, Delseny M, Roscoe TJ (1998) A rapeseed FAE1 gene is linked to the E1 locus associated with variation in the content of erucic acid. Theor Appl Genet 96:177–186Google Scholar
  2. Beare JL, Campbell JA, Youngs CG, Craig BM (1963) Effects of saturated fat in rats fed rapeseed oil. Can J Biochem Physiol 41:605–612CrossRefGoogle Scholar
  3. Bhattacharjee S, Halane MK, Kim SH, Gassmann W (2011) Pathogen effectors target Arabidopsis EDS1 and alter its interactions with immune regulators. Science 334:1405–1408.  https://doi.org/10.1126/science.1211592 CrossRefPubMedGoogle Scholar
  4. Chalhoub B, Denoeud F, Liu S, Parkin IAP, Tang H, Wang X, Chiquet J, Belcram H, Tong C, Samans B, Correa M, Da Silva C, Just J, Falentin C, Koh CS, Le Clainche I, Bernard M, Bento P, Noel B, Labadie K, Alberti A, Charles M, Arnaud D, Guo H, Daviaud C, Alamery S, Jabbari K, Zhao M, Edger PP, Chelaifa H, Tack D, Lassalle G, Mestiri I, Schnel N, Le Paslier M-C, Fan G, Renault V, Bayer PE, Golicz AA, Manoli S, Lee T-H, Thi VHD, Chalabi S, Hu Q, Fan C, Tollenaere R, Lu Y, Battail C, Shen J, Sidebottom CHD, Wang X, Canaguier A, Chauveau A, Berard A, Deniot G, Guan M, Liu Z, Sun F, Lim YP, Lyons E, Town CD, Bancroft I, Wang X, Meng J, Ma J, Pires JC, King GJ, Brunel D, Delourme R, Renard M, Aury J-M, Adams KL, Batley J, Snowdon RJ, Tost J, Edwards D, Zhou Y, Hua W, Sharpe AG, Paterson AH, Guan C, Wincker P (2014) Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 345:950–953.  https://doi.org/10.1126/science.1253435
  5. Cheng F, Sun R, Hou X, Zheng H, Zhang F, Zhang Y, Liu B, Liang J, Zhuang M, Liu Y, Liu D, Wang X, Li P, Liu Y, Lin K, Bucher J, Zhang N, Wang Y, Wang H, Deng J, Liao Y, Wei K, Zhang X, Fu L, Hu Y, Liu J, Cai C, Zhang S, Zhang S, Li F, Zhang H, Zhang J, Guo N, Liu Z, Liu J, Sun C, Ma Y, Zhang H, Cui Y, Freeling MR, Borm T, Bonnema G, Wu J, Wang X (2016) Subgenome parallel selection is associated with morphotype diversification and convergent crop domestication in Brassica rapa and Brassica oleracea. Nat Genet 48:1218–1224.  https://doi.org/10.1038/ng.3634
  6. Daun JK, DeClercq DR (1988) Quality of yellow and dark seeds in Brassica campestris canola varieties Candle and Tobin. J Am Oil Chemists' Soc 65:122–126CrossRefGoogle Scholar
  7. Fourmann M, Barret P, Renard M, Pelletier G, Delourme R, Brunel D (1998) The two genes homologous to Arabidopsis FAE1 co-segregate with the two loci governing erucic acid content in Brassica napus. Theor Appl Genet 96:852–858Google Scholar
  8. Fu Y-B, Gugel RK (2009) Genetic variability of Canadian elite cultivars of summer turnip rape (Brassica rapa L.) revealed by simple sequence repeat markers. Can J Plant Sci 89:865–874.  https://doi.org/10.4141/CJPS09021 CrossRefGoogle Scholar
  9. Fukai E, Umehara Y, Sato S, Endo M, Kouchi H, Hayashi M, Stougaard J, Hirochika H (2010) Derepression of the plant chromovirus LORE1 induces germline transposition in regenerated plants. PLoS Genet 6:e1000868.  https://doi.org/10.1371/journal.pgen.1000868
  10. Han J, Lühs W, Sonntag K, Zähringer U, Borchardt DS, Wolter FP, Heinz E, Frentzen M (2001) Functional characterization of β-ketoacyl-CoA synthase genes from Brassica napus L. Plant Mol Biol 46:229–239Google Scholar
  11. Harper AL, Trick M, Higgins J, Fraser F, Clissold L, Wells R, Hattori C, Werner P, Bancroft I (2012) Associative transcriptomics of traits in the polyploid crop species Brassica napus. Nat Biotechnol 30:798–802.  https://doi.org/10.1038/nbt.2302
  12. Hirochika H, Sugimoto K, Otsuki Y, Tsugawa H, Kanda M (1996) Retrotransposons of rice involved in mutations induced by tissue culture. Proc Natl Acad Sci 93:7783–7788.  https://doi.org/10.1073/pnas.93.15.7783 CrossRefPubMedGoogle Scholar
  13. Ito H, Gaubert H, Bucher E, Mirouze M, Vaillant I, Paszkowski J (2011) An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature 472:115–119.  https://doi.org/10.1038/nature09861 CrossRefPubMedGoogle Scholar
  14. James DW (1995) Directed tagging of the Arabidopsis FATTY ACID ELONGATION1 (FAE1) gene with the maize transposon activator. Plant Cell 7:309–319Google Scholar
  15. Karim MM, Tonu NN, Hossain MS, Funaki T, Meah MB, Hossain DM, Asad ud-doullah M, Fukai E, Okazaki K (2016) Marker-assisted selection of low erucic acid quantity in short duration Brassica rapa. Euphytica 208:535–544.  https://doi.org/10.1007/s10681-015-1596-8
  16. Katavic V, Mietkiewska E, Barton DL, Giblin EM, Reed DW, Taylor DC (2002) Restoring enzyme activity in nonfunctional low erucic acid Brassica napus fatty acid elongase 1 by a single amino acid substitution: restoring enzyme activity in Brassica napus FAE1. Eur J Biochem 269:5625–5631.  https://doi.org/10.1046/j.1432-1033.2002.03270.x
  17. Kim SH, Kwon SI, Saha D, Anyanwu NC, Gassmann W (2009) Resistance to the Pseudomonas syringae effector HopA1 is governed by the TIR-NBS-LRR protein RPS6 and is enhanced by mutations in SRFR1. Plant Physiol 150:1723–1732.  https://doi.org/10.1104/pp.109.139238
  18. Kumar A, Bennetzen JL (1999) Plant retrotransposons. Ann Rev Genet 33:479–532CrossRefGoogle Scholar
  19. Matsunaga W, Ohama N, Tanabe N, Masuta Y, Masuda S, Mitani N, Yamaguchi-Shinozaki K, Ma JF, Kato A, Ito H (2015) A small RNA mediated regulation of a stress-activated retrotransposon and the tissue specific transposition during the reproductive period in Arabidopsis. Front Plant Sci 6:48CrossRefGoogle Scholar
  20. Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325CrossRefGoogle Scholar
  21. Oliver KR, McComb JA, Greene WK (2013) Transposable elements: powerful contributors to angiosperm evolution and diversity. Genome Biol Evol 5:1886–1901CrossRefGoogle Scholar
  22. Parkin IA, Koh C, Tang H, Robinson SJ, Kagale S, Clarke WE, Town CD, Nixon J, Krishnakumar V, Bidwell SL, Denoeud F, Belcram H, Links MG, Just J, Clarke C, Bender T, Huebert T, Mason AS, Pires J, Barker G, Moore J, Walley PG, Manoli S, Batley J, Edwards D, Nelson MN, Wang X, Paterson AH, King G, Bancroft I, Chalhoub B, Sharpe AG (2014) Transcriptome and methylome profiling reveals relics of genome dominance in the mesopolyploid Brassica oleracea. Genome Biol 15:R77.  https://doi.org/10.1186/gb-2014-15-6-r77 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Perrière G, Gouy M (1996) WWW-query: an on-line retrieval system for biological sequence banks. Biochimie 78:364–369.  https://doi.org/10.1016/0300-9084(96)84768-7 CrossRefPubMedGoogle Scholar
  24. Qiu D, Morgan C, Shi J, Long Y, Liu J, Li R, Zhuang X, Wang Y, Tan X, Dietrich E, Weihmann T, Everett C, Vanstraelen S, Beckett P, Fraser F, Trick M, Barnes S, Wilmer J, Schmidt R, Li J, Li D, Meng J, Bancroft I (2006) A comparative linkage map of oilseed rape and its use for QTL analysis of seed oil and erucic acid content. Theor Appl Genet 114:67–80.  https://doi.org/10.1007/s00122-006-0411-2 CrossRefPubMedGoogle Scholar
  25. Rahman MH, Stolen O, Rahman L, Rarman MM (1999) Composition and correlation studies of fatty acids in seed oil of Yellow Sarson (Brassica campestris L.) cultivars and backcross derived zero erucic acid Yellow Sarson populations. J Natl Sci Found Sri Lanka 27:99–106CrossRefGoogle Scholar
  26. SanMiguel P, Gaut BS, Tikhonov A, Nakajima Y, Bennetzen JL (1998) The paleontology of intergene retrotransposons of maize. Nat Genet 20:43–45.  https://doi.org/10.1038/1695 CrossRefPubMedGoogle Scholar
  27. Sebedio JL, Ackman RG (1981) Fatty acids of canola Brassica campestris var Candle seed and oils at various stages of refining. J Am Oil Chemists' Soc 58:972–973CrossRefGoogle Scholar
  28. Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJM, Birol I (2009) ABySS: a parallel assembler for short read sequence data. Genome Res 19:1117–1123.  https://doi.org/10.1101/gr.089532.108 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Takeda S, Sugimoto K, Otsuki H, Hirochika H (1999) A 13-bp cis-regulatory element in the LTR promoter of the tobacco retrotransposon Tto1 is involved in responsiveness to tissue culture, wounding, methyl jasmonate and fungal elicitors. Plant J 18:383–393CrossRefGoogle Scholar
  30. The Brassica rapa Genome Sequencing Project Consortium, Wang X, Wang H, Wang J, Sun R, Wu J, Liu S, Bai Y, Mun J-H, Bancroft I, Cheng F, Huang S, Li X, Hua W, Wang J, Wang X, Freeling M, Pires JC, Paterson AH, Chalhoub B, Wang B, Hayward A, Sharpe AG, Park B-S, Weisshaar B, Liu B, Li B, Liu B, Tong C, Song C, Duran C, Peng C, Geng C, Koh C, Lin C, Edwards D, Mu D, Shen D, Soumpourou E, Li F, Fraser F, Conant G, Lassalle G, King GJ, Bonnema G, Tang H, Wang H, Belcram H, Zhou H, Hirakawa H, Abe H, Guo H, Wang H, Jin H, Parkin IAP, Batley J, Kim J-S, Just J, Li J, Xu J, Deng J, Kim JA, Li J, Yu J, Meng J, Wang J, Min J, Poulain J, Wang J, Hatakeyama K, Wu K, Wang L, Fang L, Trick M, Links MG, Zhao M, Jin M, Ramchiary N, Drou N, Berkman PJ, Cai Q, Huang Q, Li R, Tabata S, Cheng S, Zhang S, Zhang S, Huang S, Sato S, Sun S, Kwon S-J, Choi S-R, Lee T-H, Fan W, Zhao X, Tan X, Xu X, Wang Y, Qiu Y, Yin Y, Li Y, Du Y, Liao Y, Lim Y, Narusaka Y, Wang Y, Wang Z, Li Z, Wang Z, Xiong Z, Zhang Z (2011) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43:1035–1039.  https://doi.org/10.1038/ng.919 CrossRefGoogle Scholar
  31. Töpfer R, Nartini N, Schell J (1995) Modification of plant lipid synthesis. Science 268:681–686CrossRefGoogle Scholar
  32. Wang N, Shi L, Tian F, Ning H, Wu X, Long Y, Meng J (2010) Assessment of FAE1 polymorphisms in three Brassica species using EcoTILLING and their association with differences in seed erucic acid contents. BMC Plant Biol 10:137CrossRefGoogle Scholar
  33. Wereab BA, Onkware AO, Gudu S, Welander M, Carlsson AS (2006) Seed oil content and fatty acid composition in East African sesame (Sesamum indicum L.) accessions evaluated over 3 years. Field Crop Res 97:254–260Google Scholar
  34. Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, Flavell A, Leroy P, Morgante M, Panaud O, Paux E, SanMiguel P, Schulman AH (2007) A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8:973–982CrossRefGoogle Scholar
  35. Wu G, Wu Y, Xiao L, Li X, Lu C (2008) Zero erucic acid trait of rapeseed (Brassica napus L.) results from a deletion of four base pairs in the fatty acid elongase 1 gene. Theor Appl Genet 116:491–499.  https://doi.org/10.1007/s00122-007-0685-z
  36. Yan G, Li D, Cai M, Gao G, Chen B, Xu K, Li J, Li F, Wang N, Qiao J, Li H, Zhang T, Wu X (2015) Characterization of FAE1 in the zero erucic acid germplasm of Brassica rapa L. Breed Sci 65:257–264.  https://doi.org/10.1270/jsbbs.65.257 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Yang J, Liu D, Wang X, Ji C, Cheng F, Liu B, Hu Z, Chen S, Pental D, Ju Y, Yao P, Li X, Xie K, Zhang J, Wang J, Liu F, Ma W, Shopan J, Zheng H, Mackenzie SA, Zhang M (2016) The genome sequence of allopolyploid Brassica juncea and analysis of differential homoeolog gene expression influencing selection. Nat Genet 48:1225–1232.  https://doi.org/10.1038/ng.3657 CrossRefPubMedGoogle Scholar
  38. Zeng F, Cheng B (2014) Transposable element insertion and epigenetic modification cause the multiallelic variation in the expression of FAE1 in Sinapis alba. Plant Cell 26:2648–2659CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Graduate School of Science and TechnologyNiigata UniversityNiigataJapan
  2. 2.Saskatoon Research and Development Centre, Agriculture and Agri-Food Canada (AAFC)SaskatoonCanada
  3. 3.Department of Plant PathologySher-e-Bangla Agricultural UniversityDhakaBangladesh

Personalised recommendations