Abstract
Canola growers in the North Central Region of the United States and Canada are highly concerned about possible early frost. Plants can be killed due to their cells rupture when exposed to a freezing temperature. There are different methods to evaluate frost tolerance including field evaluation. Due to environmental variations, it is difficult to get an ideal condition for frost tolerance evaluation under field conditions. In this study, canola seedlings were grown in a greenhouse for 14 days at 20 °C and cold acclimated for 7–14 days at 4 °C. The acclimated seedlings were placed outside under field conditions based on predicted outside temperature between − 4 and − 8 °C to be exposed to a natural freezing condition. After an overnight freezing exposure, the seedlings were brought back to greenhouse to score the freezing induced seedling damage. The experiment was conducted in a randomized complete black design with two replications, and repeated the trial eight times. A genome-wide association study was conducted on 147 spring, winter, and semi-winter germplasm accessions obtained from 15 countries. A total of 37,111 single nucleotide polymorphism markers were used for the analysis. Three mixed populations with no growth type or geographic patterns were identified. One QTL that explained about 5% of the phenotypic variation and located on chromosome C04 was identified associated with frost tolerance of canola. Five potential genes related to frost tolerance and abiotic stress tolerance were identified.
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Abbreviations
- DREB :
-
Dehydration responsive element binding
- AP2 :
-
Adipocyte protein 2
- GWAS :
-
Genome wide association study
- GBS :
-
Genotyping-by-sequencing
- SNP :
-
Single nucleotide polymorphism
- QTL :
-
Quantitative trait locus
- LD :
-
Linkage disequilibrium
- GRIN :
-
Germplasm Resources Information Network
References
Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23(19):2633–2635. https://doi.org/10.1093/bioinformatics/btm308
Bus A, Köber N, Snowdon RJ, Stich B (2011) Patterns of molecular variation in a species wide germplasm set of Brassica napus. Theor Appl Genet 123:1413–1423
Chalhoub B, Denoeud F, Liu S et al (2014) Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 345(6199):950–953
Delourme R, Falentin C, Fomeju BF et al (2013) High-density SNP-based genetic map development and linkage disequilibrium assessment in Brassica napus L. BMC Genom 14:120. https://doi.org/10.1186/1471-2164-14-120
Diers BW, Osborn TC (1994) Genetic diversity of oilseed Brassica napus germplasm based on restriction fragment length polymorphisms. Theor Appl Genet 88:662–668
Ehret GB (2010) Genome-wide association studies: contribution of genomics to understanding blood pressure and essential hypertension. Curr Hypertens Rep 12(1):17–25. https://doi.org/10.1007/s11906-009-0086-6
Elshire RJ, Glaubitz JC, Poland JA, Kawamoto K, Buckler ES, Mitchell ES (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6(5):e19379
Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587
Fiebelkorn D, Rahman M (2016) Development of a protocol for frost-tolerance evaluation in rapeseed/canola (Brassica napus L.). Crop J 4:147–152
Gajardo HA, Wittkop B, Soto-Cerda B, Higgins EE, Parkin IAP, Snowdon RJ, Federico ML, Iniguez-Luy FL (2015) Association mapping of seed quality traits in Brassica napus L. using GWAS and candidate QTL approaches. Mol Breed 35:143
Gao MJ, Allard G, Byass L, Flanagan AM, Singh J (2002) Regulation and characterization of four CBF transcription factors from Brassica napus. Plant Mol Biol 49:459–471
Gilmour SJ, Sebolt AM, Salazar MP, Everard JD, Thomashow MF (2000) Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol 124:1854–1865
Gómez-Campo C, Prakash S (1999) Origin and domestication. Dev Plant Genet Breed 4:33–58
Gurung S, Mamidi S, Bonman JM, Xiong M, Brown-Guedira G, Adhikari TB (2014) Genome-wide association study reveals novel quantitative trait loci associated with resistance to multiple leaf spot diseases of spring wheat. PLoS ONE 9(9):e108179
Gutha LR, Reddy AR (2008) Rice DREB1B promoter shows distinct stress-specific responses, and the overexpression of cDNA in tobacco confers improved abiotic and biotic stress tolerance. Plant Mol Biol 68:533–555
Haake V, Cook D, Riechmann JL, Pineda O, Thomashow MF, Zhang JZ (2002) Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis. Plant Physiol 130:639–648
Hansen M, Kraft T, Ganestam S, Säll T, Nilsson NO (2001) Linkage disequilibrium mapping of the bolting gene in sea beet using AFLP markers. Genet Res 77(1):61–66
Hasan M, Friedt W, Pons-Kuhnemann J, Freitag NM, Link K, Snowdon RJ (2008) Association of gene-linked SSR markers to seed glucosinolate content in oilseed rape (Brassica napus ssp.napus). Theor Appl Genet 116:1035–1049
Hatzig SV, Frisch M, Breuer F, Nesi N, Ducournau S, Wagner MH, Leckband G, Abbadi A, Snowdon RJ (2015) Genome-wide association mapping unravels the genetic control of seed germination and vigor in Brassica napus. Front Plant Sci 6:221. https://doi.org/10.3389/fpls.2015.00221
Hong EP, Park JW (2012) Sample size and statistical power calculation in genetic association studies. Genom Inform 10:117–122
Hong SW, Vierling E (2000) Mutants of Arabidopsis thaliana defective in the acquisition of tolerance to high temperature stress. PNAS 97(8):4392–4397
Hume DJ, Jackson AKH (1981) Frost tolerance in soybeans. Crop Sci 21:689–692
Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280:104–106
Jia L, Yan W, Zhu C, Agrama HA, Jackson A, Yeater K, Li X, Huang B, Hu B, McClung A, Wu D (2012) Allelic analysis of sheath blight resistance with association mapping in rice. PLoS ONE 7(3):e32703
Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17:287–291
Koboldt DC, Zhang Q, Larson DE, Shen D, McLellan MD, Lin L, Miller CA, Mardis ER, Ding L, Wilson RK (2012) VarScan 2: somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genome Res 22:568–576
Körber N, Bus A, Li J, Parkin ISP, Wittkop B, Snowdon RJ, Stich B (2016) Agronomic and seed quality traits dissected by genome-wide association mapping in Brassica napus. Front Plant Sci 7:386. https://doi.org/10.3389/fpls.2016.00386
Kraakman ATW, Niks RE, Van den Berg PM, Stam P, Van Eeuwijk FA (2004) Linkage disequilibrium mapping of yield and yield stability in modern spring barley cultivars. Genetics 168:435–446
Kraakman ATW, Martínez F, Mussiraliev B, van Eeuwijk FA, Niks RE (2006) Linkage disequilibrium mapping of morphological, resistance, and other agronomically relevant traits in modern spring barley cultivars. Mol Breed 17(1):41–58
Lagercrantz U (1998) Comparative mapping between Arabidopsis thaliana and Brassica nigra indicates that Brassica genomes have evolved through extensive genome replication accompanied by chromosome fusions and frequent rearrangements. Genetics 150:1217–1228
Lagercrantz U, Lydiate DJ (1996) Comparative genome mapping in Brassica. Genetics 144:1903–1910
Li H (2013) Aligning sequence reads, clone sequences, and assembly contigs with BWA-MEM. arXiv:1303.3997 http://arxiv.org/abs/1303.3997
Li XP, Tian AG, Luo GZ, Gong ZZ, Zhang JS, Chen SY (2005) Soybean DRE-binding transcription factors that are responsive to abiotic stresses. Theor Appl Genet 110:1355–1362
Li X, Yan W, Agrama H et al (2011) Mapping QTLs for improving grain yield using the USDA rice minicore collection. Planta 234:347–361
Li F, Chen B, Xu K et al (2014) Genome-wide association study dissects the genetic architecture of seed weight and seed quality in rapeseed (Brassica napus L.). DNA Res 21:355–367
Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively in Arabidopsis. Plant Cell 10:1391–1406
Liu J, Wang W, Mei D, Wang H, Fu L, Liu D, Li Y, Hu Q (2016) Characterizing variation of branch angle and genome-wide association mapping in rapeseed (Brassica napus L.). Front. Plant Sci 7:21
Mamidi S, Chikara S, Goos RJ et al (2011) Genome-wide association analysis identifies candidate genes associated with iron deficiency chlorosis in soybean. Plant Genome 4:154–164
Mamidi S, Lee RK, Goos RJ, McClean PE (2014) Genome-wide association studies identifies seven major regions responsible for iron deficiency chlorosis in soybean (Glycine max). PLoS ONE 9(9):e107469
Michalak JM, Mamidi S, McClean PE, Rahman M (unpublished) Low level of linkage disequilibrium and population structure in a core collection of Brassica napus discovered using SNPs derived from GBS. USA
Mohammadi M, Blake TK, Budde AD, Chao S, Hayes PM, Horsley RD, Obert DE, Ullrich SE, Smith KP (2015) A genome-wide association study of malting quality across eight U.S. barley breeding programs. Theor Appl Genet 128:705–721
Morran S, Eini O, Pyvovarenko T, Parent B et al (2011) Improvement of stress tolerance of wheat and barley by modulation of expression of DREB/CBF factors. Plant Biotechnol J 9:230–249
Nakashima K, Shinwari ZK, Sakuma Y, Seki M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K (2000) Organization and expression of two Arabidopsis DREB2 genes encoding DRE-binding proteins involved in dehydration- and high-salinity-responsive gene expression. Plant Mol Biol 42:657–665
NDAWN (2017) North Dakota Agricultural Weather Network. https://ndawn.ndsu.nodak.edu/. Accessed 3 Mar 2017
Nishimura N, Sarkeshik A, Nito K et al (2010) PYR/PYL/RCAR family members are major in vivo ABI1 protein phosphatase 2C-interacting proteins in Arabidopsis. Plant J 61:290–299. https://doi.org/10.1111/j.1365-313X.2009.04054.x
Oh SJ, Kwon CW, Choi DW, Song SI, Kim JK (2007) Expression of barley HvCBF4 enhances tolerance to abiotic stress in transgenic rice. Plant Biotechnol J 5:646–656
Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet 38(8):904–909
Pritchard JK, Przeworski M (2001) Linkage disequilibrium in humans: models and data. Am J Hum Genet 69:1–14
Pritchard JK, Stephens M, Donnelly P (2000a) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Pritchard JK, Stephens M, Rosenberg NA, Donnelly P (2000b) Association mapping in structured populations. Am J Hum Genet 676:170–181
Qian L, Qian W, Snowdon RJ (2014) Sub-genomic selection patterns as a signature of breeding in the allopolyploid Brassica napus genome. BMC Genom 15:1170. https://doi.org/10.1186/1471-2164-15-1170
Qin F, Sakuma Y, Li J, Liu Q, Li YQ, Shinozaki K, Yamaguchi-Shinozaki KY (2004) Cloning and functional analysis of a novel DREB1/CBF transcription factor involved in cold-responsive gene expression in Zea mays L. Plant Cell Physiol 45:1042–1052
Qu C, Jia L, Fu F, Zhao H, Lu K, Wei L, Xu X, Liang Y, Li S, Wang R, Li J (2017) Genome-wide association mapping and Identification of candidate genes for fatty acid composition in Brassica napus L. using SNP markers. BMC Genom 18:232
Rafalski A (2002) Applications of single nucleotide polymorphisms in crop genetics. Curr Opin Plant Biol 5:94–100
Rahaman M, Mamidi S, Rahman M (2017) Genome-wide association study of heat stress-tolerance traits in spring-type Brassica napus L. under controlled conditions. Crop J 6:115–125
Rahman M, Mamidi S, del Rio L, Ross A, Kadir MM, Rahaman MM, Arifuzzaman M (2016) Association mapping in Brassica napus (L.) accessions identifies a major QTL for blackleg disease resistance on chromosome A01. Mol Breed 36:90. https://doi.org/10.1007/s11032-016-0513-8
Raman H, Dalton-Morgan J, Diffey S, Raman R, Alamery S, Edwards D, Batley J (2014) SNP markers-based map construction and genome-wide linkage analysis in Brassica napus. Plant Biotechnol J 12:851–860
Rapacz M, Markowski F (1999) Winter hardiness, frost resistance and vernalization requirement of European winter oilseed rape (Brassica napus var. oleifera) cultivars within the last 20 years. Crop Sci 183:243–253
Reňák D, Dupláková N, Honys D (2012) Wide-scale screening of T-DNA lines for transcription factor genes affecting male gametophyte development in Arabidopsis. Sex Plant Reprod 25:39–60. https://doi.org/10.1007/s00497-011-0178-8
Rezaeizad A, Wittkop B, Snowdon RJ, Hasan M, Mohammadi V, Zali A, Friedt W (2011) Identification of QTLs for phenolic compounds in oilseed rape (Brassica napus L.) by association mapping using SSR markers. Euphytica 177:335–342
Scheet P, Stephens M (2006) A fast and flexible statistical model for large-scale population genotype data: applications to inferring missing genotypes and haplotypic phase. Am J Hum Genet 78:629–644
Steponkus PL (1978) Cold hardiness and freezing injury of agronomic crop. In: Brady NC (ed) Advances in agronomy. Academic Press, New York, pp 51–98
Stockinger EJ, Gilmour SJ, Thomashow MF (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc Natl Acad Sci USA 94:1035–1040
Sun J, Guo N, Lei J, Li L, Hu G, Xing H (2014) Association mapping for partial resistance to Phytophthora sojae in soybean (Glycine max L.). J Genet 2:355–363
U N (1935) Genome analysis in Brassica with special reference to the experimental formation of Brassica napus and peculiar mode of fertilization. Jpn J Bot 7:389–452
Visioni A, Tondelli A, Francia E et al (2013) Denome-wide association mapping of frost tolerance in barley (Hordeum vulgare L). BMC Genom 14:424–437. http://www.biomedcentral.com/1471-2164/14/424
Vogel JT, Zarka DG, van Buskirk HA, Fowler SG, Thomashow MF (2005) Roles of CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Plant J 41:195–211
Wang N, Li F, Chen B et al (2014) Genome-wide investigation of genetic changes during modern breeding of Brassica napus. Theor Appl Genet 127:1817–1829
Waugh R, Jannink JL, Muller K, Ramsay L (2009) The emergence of whole genome association scans in barley. Curr Opin Plant Biol 12:1–5
Wilson JM (1997) Mechanisms of chilling resistance in plants. In: Basra AS, Basra RK (eds) Mechanisms of environmental stress resistance in plants. Harwood Academic Publishers, Amsterdam, pp 111–122
Xiao Y, Chen L, Zou J, Tian E, Xia W, Meng J (2010) Development of a population for substantial new type Brassica napus diversified at both A/C genomes. Theor Appl Genet 121:1141–1150
Yu JM, Buckler ES (2006) Genetic association mapping and genome organization of maize. Curr Opin Biotechnol 17:155–160
Yu J, Pressoir G, Briggs WH et al (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208
Zhang JY, Broeckling CD, Blancaflor EB, Sledge MK, Sumner LW, Wang ZY (2005) Overexpression of WXP1, a putative Medicago truncatula AP2 domain-containing transcription factor gene, increases cuticular wax accumulation and enhances drought tolerance in transgenic alfalfa (Medicago sativa). Plant J 42:689–707
Zhao K, Aranzana MJ, Kim S, Lister C, Shindo C, Tang C, Toomajian C, Zheng H, Dean C, Marjoram P, Nordborg M (2007) An Arabidopsis example of association mapping in structured samples. PLoS Genet 3:e4. https://doi.org/10.1371/journal.pgen.0030004
Zhou GA, Chang RZ, Qiu LJ (2010) Overexpression of soybean ubiquitin-conjugating enzyme gene GmUBC2 confers enhanced drought and salt tolerance through modulating abiotic stress-responsive gene expression in Arabidopsis. Plant Mol Biol 72:357–367. https://doi.org/10.1007/s11103-009-9575-x
Zhu J, Jeong JC, Zhu Y, Sokolchik I, Miyazaki S, Zhu JK, Hasegawa PM, Bohnert HJ, Shi H, Yun DJ, Bressan RA (2008) Involvement of Arabidopsis HOS15 in histone deacetylation and cold tolerance. PNAS 105(12):4945–4950
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The study was funded by the Northern Canola Growers Association (NCGA-2013), and U.S. Department of Agriculture—National Institute of Food and Agriculture (Hatch Project No. ND01581).
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Wrucke, D.F., Mamidi, S. & Rahman, M. Genome-wide association study for frost tolerance in canola (Brassica napus L.) under field conditions. J. Plant Biochem. Biotechnol. 28, 211–222 (2019). https://doi.org/10.1007/s13562-018-0472-8
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DOI: https://doi.org/10.1007/s13562-018-0472-8