High yield is the most important goal in crop breeding, and boron (B) is an essential micronutrient for plants. However, B deficiency, leading to yield decreases, is an agricultural problem worldwide. Brassica napus is one of the most sensitive crops to B deficiency, and considerable genotypic variation exists among different cultivars in response to B deficiency. To dissect the genetic basis of tolerance to B deficiency in B. napus, we carried out QTL analysis for seed yield and yield-related traits under low and normal B conditions using the double haploid population (TNDH) by two-year and the BQDH population by three-year field trials. In total, 80 putative QTLs and 42 epistatic interactions for seed yield, plant height, branch number, pod number, seed number, seed weight and B efficiency coefficient (BEC) were identified under low and normal B conditions, singly explaining 4.15–23.16% and 0.53–14.38% of the phenotypic variation. An additive effect of putative QTLs was a more important controlling factor than the additive-additive effect of epistatic interactions. Four QTL-by-environment interactions and 7 interactions between epistatic interactions and the environment contributed to 1.27–4.95% and 1.17–3.68% of the phenotypic variation, respectively. The chromosome region on A2 of SYLB-A2 for seed yield under low B condition and BEC-A2 for BEC in the two populations was equivalent to the region of a reported major QTL, BE1. The B. napus homologous genes of Bra020592 and Bra020595 mapped to the A2 region and were speculated to be candidate genes for B efficiency. These findings reveal the complex genetic basis of B efficiency in B. napus. They provide a basis for the fine mapping and cloning of the B efficiency genes and for breeding B-efficient cultivars by marker-assisted selection (MAS).
References
[1]
Warington K (1923) The effect of boric acid and borax on the broad bean and certain other plants. Ann Bot 37: 629–672.
[2]
O'Neill MA, Warrenfeltz D, Kates K, Pellerin P, Doco T, et al. (1996) Rhamnogalacturonan-II, a pectic polysaccharide in the walls of growing plant cell, forms a dimer that Is covalently cross-linked by a borate ester. Journal of Biological Chemistry 271: 22923–22930.
[3]
Ishii T, Matsunaga T, Hayashi N (2001) Formation of rhamnogalacturonan II-borate dimer in pectin determines cell wall thickness of pumpkin tissue. Plant Physiol 126: 1698–1705.
[4]
Marschner P (1995) Marschner's mineral nutrition of higher plants, Second Edition. 2nd ed. Academic Press. 889 p.
[5]
González-Fontes A, Rexach J, Navarro-Gochicoa MT, Herrera-Rodríguez MB, Beato VM, et al. (2008) Is boron involved solely in structural roles in vascular plants? Plant Signal Behav 3: 24–26.
[6]
Raven JA (1980) Short- and long-distance transport of boric acid in plants. New Phytologist 84: 231–249.
[7]
Dannel F, Pfeffer H, R？mheld V (2000) Characterization of root boron pools, boron uptake and boron translocation in sunflower using the stable isotopes 10 B and 11 B. Functional Plant Biol 27: 397–405.
[8]
Takano J, Noguchi K, Yasumori M, Kobayashi M, Gajdos Z, et al. (2002) Arabidopsis boron transporter for xylem loading. Nature 420: 337–340.
[9]
Takano J, Miwa K, Yuan L, von Wirén N, Fujiwara T (2005) Endocytosis and degradation of BOR1, a boron transporter of Arabidopsis thaliana, regulated by boron availability. Proc Natl Acad Sci USA 102: 12276–12281.
[10]
Nakagawa Y, Hanaoka H, Kobayashi M, Miyoshi K, Miwa K, et al. (2007) Cell-type specificity of the expression of OsBOR1, a rice efflux boron transporter gene, is regulated in response to boron availability for efficient boron uptake and xylem loading. Plant Cell 19: 2624–2635.
[11]
Sun J, Shi L, Zhang C, Xu F (2011) Cloning and characterization of boron transporters in Brassica napus. Mol Biol Rep 39: 1963–1973.
[12]
Kaya A, Karakaya HC, Fomenko DE, Gladyshev VN, Koc A (2009) Identification of a novel system for boron transport: Atr1 is a main boron exporter in yeast. Mol Cell Biol 29: 3665–3674.
[13]
Takano J, Wada M, Ludewig U, Schaaf G, von Wirén N, et al. (2006) The Arabidopsis major intrinsic protein NIP5;1 is essential for efficient boron uptake and plant development under boron limitation. Plant Cell 18: 1498–1509.
[14]
Tanaka M, Wallace IS, Takano J, Roberts DM, Fujiwara T (2008) NIP6;1 is a boric acid channel for preferential transport of boron to growing shoot tissues in Arabidopsis. Plant Cell 20: 2860–2875.
[15]
Kasajima I, Ide Y, Yokota Hirai M, Fujiwara T (2010) WRKY6 is involved in the response to boron deficiency in Arabidopsis thaliana. Physiol Plant 139: 80–92.
[16]
Miwa K, Takano J, Fujiwara T (2006) Improvement of seed yields under boron-limiting conditions through overexpression of BOR1, a boron transporter for xylem loading, in Arabidopsis thaliana. Plant J 46: 1084–1091.
[17]
Kato Y, Miwa K, Takano J, Wada M, Fujiwara T (2009) Highly boron deficiency-tolerant plants generated by enhanced expression of NIP5;1, a boric acid channel. Plant Cell Physiol 50: 58–66.
[18]
Meyer M (2009) Rapeseed oil fuel - the crisis-proof home-made eco-fuel. Agrarforschung 16: 262–267.
[19]
Shorrocks V (1997) The occurrence and correction of boron deficiency. Plant and soil 193: 121–148.
[20]
Yan X, Liao H, Beebe SE, Blair MW, Lynch JP (2004) QTL mapping of root hair and acid exudation traits and their relationship to phosphorus uptake in common bean. Plant and Soil 265: 17–29.
[21]
Xu F, Wang Y, Meng J (2001) Mapping boron efficiency gene(s) in Brassica napus using RFLP and AFLP markers. Plant Breeding 120: 319–324.
[22]
Paran I, Zamir D (2003) Quantitative traits in plants: beyond the QTL. Trends Genet 19: 303–306.
[23]
Cooper M, van Eeuwijk FA, Hammer GL, Podlich DW, Messina C (2009) Modeling QTL for complex traits: detection and context for plant breeding. Curr Opin Plant Biol 12: 231–240.
[24]
Xue W, Xing Y, Weng X, Zhao Y, Tang W, et al. (2008) Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat Genet 40: 761–767.
[25]
El-Din El-Assal S, Alonso-Blanco C, Peeters AJM, Raz V, Koornneef M (2001) A QTL for flowering time in Arabidopsis reveals a novel allele of CRY2. Nat Genet 29: 435–440.
[26]
Quijada PA, Udall JA, Lambert B, Osborn TC (2006) Quantitative trait analysis of seed yield and other complex traits in hybrid spring rapeseed (Brassica napus L.): 1. Identification of genomic regions from winter germplasm. Theor Appl Genet 113: 549–561.
[27]
Chen W, Zhang Y, Liu X, Chen B, Tu J, et al. (2007) Detection of QTL for six yield-related traits in oilseed rape (Brassica napus) using DH and immortalized F(2) populations. Theor Appl Genet 115: 849–858.
[28]
Radoev M, Becker HC, Ecke W (2008) Genetic analysis of heterosis for yield and yield components in rapeseed (Brassica napus L.) by quantitative trait locus mapping. Genetics 179: 1547–1558.
[29]
Fan C, Cai G, Qin J, Li Q, Yang M, et al. (2010) Mapping of quantitative trait loci and development of allele-specific markers for seed weight in Brassica napus. Theor Appl Genet 121: 1289–1301.
[30]
Zhao J, Becker HC, Zhang D, Zhang Y, Ecke W (2006) Conditional QTL mapping of oil content in rapeseed with respect to protein content and traits related to plant development and grain yield. Theor Appl Genet 113: 33–38.
[31]
Shi L, Wang Y, Nian F, Lu J, Meng J, et al. (2009) Inheritance of boron efficiency in oilseed rape. Pedosphere 19 (3) 403–408.
[32]
Zhao H, Shi L, Duan X, Xu F, Wang Y, et al. (2008) Mapping and validation of chromosome regions conferring a new boron-efficient locus in Brassica napus. Mol Breeding 22: 495–506.
[33]
Long Y, Shi J, Qiu D, Li R, Zhang C, et al. (2007) Flowering time quantitative trait loci analysis of oilseed Brassica in multiple environments and genomewide alignment with Arabidopsis. Genetics 177: 2433–2444.
[34]
Qiu D, Morgan C, Shi J, Long Y, Liu J, et al. (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.
[35]
Shi L, Nian F, Zhao H, Xu F, Meng J, et al. (2004) Responses to boron deficiency in 7 varieties of rape (Brassica napus L.). Chin J Oil Crop Sci 26: 50–53 (in Chinese with English abstract).
[36]
Masclaux-Daubresse C, Daniel-Vedele F, Dechorgnat J, Chardon F, Gaufichon L, et al. (2010) Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture. Ann Bot 105: 1141–1157.
[37]
Xu G, Fan X, Miller AJ (2011) Plant nitrogen assimilation and use efficiency. Annu Rev Plant Biol 2012.63: 5.1–5.30.
[38]
Zeng C, Han Y, Shi L, Peng L, Wang Y, et al. (2008) Genetic analysis of the physiological responses to low boron stress in Arabidopsis thaliana. Plant Cell Environ 31: 112–122.
[39]
Xu Y (1997) Quantitative Trait Loci: Separating, Pyramiding, and Cloning 85–139.
[40]
Shi J, Li R, Qiu D, Jiang C, Long Y, et al. (2009) Unraveling the complex trait of crop yield with quantitative trait loci mapping in Brassica napus. Genetics 182: 851–861.
[41]
Wang L, Zhao J, Xu F, Liu R, Meng J (2002) Integration of DNA clones related to important economic traits of Brassica napus onto Arabidopsis genetic map. Acta Genetica Sinica 29 (8) 741–746.
[42]
Arcade A, Labourdette A, Falque M, Mangin B, Chardon F, et al. (2004) BioMercator: integrating genetic maps and QTL towards discovery of candidate genes. Bioinformatics 20: 2324–2326.
[43]
Ding G, Zhao Z, Liao Y, Hu Y, Shi L, et al. (2012) Quantitative trait loci for seed yield and yield-related traits, and their responses to reduced phosphorus supply in Brassica napus. Ann Bot doi:10.1093/aob/mcr323.
[44]
Yu S, Li J, Xu C, Tan Y, Gao Y, et al. (1997) Importance of epistasis as the genetic basis of heterosis in an elite rice？hybrid. Proc Natl Acad Sci U S A 94: 9226–9231.
[45]
Liu J, Yang J, Li R, Shi L, Zhang C, et al. (2009) Analysis of genetic factors that control shoot mineral concentrations in rapeseed (Brassica napus) in different boron environments. Plant and Soil 320: 255–266.
[46]
Wang Z, Wang Z, Shi L, Wang L, Xu F (2010) Proteomic alterations of Brassica napus root in response to boron deficiency. Plant Mol Biol 74: 265–278.
[47]
Quirino BF, Reiter WD, Amasino RD (2001) One of two tandem Arabidopsis genes homologous to monosaccharide transporters is senescence-associated. Plant Mol Biol 46: 447–457.
[48]
Qin Y, Leydon AR, Manziello A, Pandey R, Mount D, et al. (2009) Penetration of the stigma and style elicits a novel transcriptome in pollen tubes, pointing to genes critical for growth in a pistil. PLoS Genet 5: e1000621.
[49]
Parkin IAP, Gulden SM, Sharpe AG, Lukens L, Trick M, et al. (2005) Segmental structure of the Brassica napus genome based on comparative analysis with Arabidopsis thaliana. Genetics 171: 765–781.
[50]
Schranz ME, Lysak MA, Mitchell-Olds T (2006) The ABC's of comparative genomics in the Brassicaceae: building blocks of crucifer genomes. Trends Plant Sci 11: 535–542.
[51]
Yang M, Ding G, Shi L, Feng J, Xu F, et al. (2010) Quantitative trait loci for root morphology in response to low phosphorus stress in Brassica napus. Theor Appl Genet 121: 181–193.
[52]
Kobayashi M, Mutoh T, Matoh T (2004) Boron nutrition of cultured tobacco BY-2 cells. IV. Genes induced under low boron supply. J Exp Bot 55: 1441–1443.
[53]
Wang Z, Wang Z, Chen S, Shi L, Xu F (2011) Proteomics reveals the adaptability mechanism of Brassica napus to short-term boron deprivation. Plant Soil 347: 195–210.
[54]
Doyle JI (1990) Isolation of plant DNA from fresh tissue. Focus 12: 13–15.
[55]
Suwabe K, Iketani H, Nunome T, Kage T, Hirai M (2002) Isolation and characterization of microsatellites in Brassica rapa L. Theor Appl Genet 104: 1092–1098.
[56]
Piquemal J, Cinquin E, Couton F, Rondeau C, Seignoret E, et al. (2005) Construction of an oilseed rape (Brassica napus L.) genetic map with SSR markers. Theor Appl Genet 111: 1514–1523.
[57]
Ding G, Liao Y, Yang M, Zhao Z, Shi L, et al. (2011) Development of gene-based markers from functional Arabidopsis thaliana genes involved in phosphorus homeostasis and mapping in Brassica napus. Euphytica 181: 305–322.
[58]
Cheng X, Xu J, Xia S, Gu J, Yang Y, et al. (2009) Development and genetic mapping of microsatellite markers from genome survey sequences in Brassica napus. Theor Appl Genet 118: 1121–1131.
[59]
Li H, Chen X, Yang Y, Xu J, Gu J, et al. (2010) Development and genetic mapping of microsatellite markers from whole genome shotgun sequences in Brassica oleracea. Mol Breeding 28: 585–596.
[60]
Wang X, Wang H, Wang J, Sun R, Wu J, et al. (2011) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43: 1035–1039.
[61]
Li, Quiros CF (2001) Sequence-related amplified polymorphism (SRAP), a new marker system based on a simple PCR reaction: its application to mapping and gene tagging in Brassica. Theor Appl Genet 103: 455–461.
[62]
Van Ooijen JW (2006) JoinMap？4.0: software for the calculation of genetic linkage maps in experimental populations. Kyazma BV, Wageningen, Netherlands
[63]
Kosambi DD (1943) The estimation of map distances from recombination values. Annals of Human Genetics 12: 172–175.
[64]
Zeng Z (1994) Precision mapping of quantitative trait loci. Genetics 136: 1457–1468.
[65]
Wang S, Bastern J, Zeng Z (2006) Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh, NC, USA.
Yang J, Hu C, Hu H, Yu R, Xia Z, et al. (2008) QTLNetwork: mapping and visualizing genetic architecture of complex traits in experimental populations. Bioinformatics 24: 721–723.
[68]
Yang J, Zhu J, Williams RW (2007) Mapping the genetic architecture of complex traits in experimental populations. Bioinformatics 23: 1527–1536.
