Haplotype hitchhiking promotes trait coselection in Brassica napus

Plant Biotechnology Journal

Volumn 14, Issue 7, 2016, Pages 1578-1588

  Qian, Lunwen ^a   Qian, Wei ^b   Snowdon, Rod J ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b SOUTHWEST UNIVERSITY   (China)

Author keywords

breeding; haplogroups; LD; linkage disequilibrium; oilseed rape; selection

Indexed keywords

CHLOROPHYLL; CHLOROPLAST PROTEIN; GENETIC MARKER;

GENETIC MARKER; GENETIC VARIATION; GENETICS; HAPLOTYPE; METABOLISM; PLANT CHROMOSOME; PLANT LEAF; PLANT SEED; RAPESEED;

BRASSICA NAPUS; CHLOROPHYLL; CHLOROPLAST PROTEINS; CHROMOSOMES, PLANT; GENETIC MARKERS; GENETIC VARIATION; HAPLOTYPES; PLANT LEAVES; SEEDS;

EID: 84975459927     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12521     Document Type: Article

References (46)

1. Abraham, V. and Deman, J.M. (1986) Hydrogenation of Canola Oil as effected by chlorophyll. J. Am. Oil Chem. Soc. 63, 1185–1188.
2. Bauer, J., Chen, K., Hiltbunner, A., Wehrli, E., Eugster, M., Schnell, D. and Kessler, F. (2000) The major protein import receptor of plastids is essential for chloroplast biogenesis. Nature, 403, 203–207.
3. Benjamini, Y. and Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B, 57, 289–300.
4. Bradbury, P.J., Zhang, Z., Kroon, D.E., Casstevens, T.M., Ramdoss, Y. and Buckler, E.S. (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics, 23, 2633–2635.
5. Buntjer, J.B., Sørensen, A.P. and Peleman, J.D. (2005) Haplotype diversity: the link between statistical and biological association. Trends Plant Sci. 10, 466– 471.
6. Chalhoub, B., Denoeud, F., Liu, S., Parkin, I.A.P., Tang, H., Wang, X., Chiquet, J. et al. (2014) Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science, 345, 950–953.
7. Chen, Y.Z., Pang, Q.Y., He, Y., Zhu, N., Branstrom, I., Yan, X.F. and Chen, S. (2012) Proteomics and metabolomics of Arabidopsis responses to perturbation of glucosinolate biosynthesis. Mol. Plant, 5, 1138–1150.
8. Clement, M., Posada, D. and Crandall, K.A. (2000) TCS: a computer program to estimate gene genealogies. Mol. Ecol. 9, 1657–1660.
9. Corradin, O., Saiakhova, A., Akhtar-Zaidi, B., Myeroff, L., Willis, J., Cowper-Sallari, R., Lupien, M. et al. (2014) Combinatorial effects of multiple enhancer variants in linkage disequilibrium dictate levels of gene expression to confer susceptibility to common traits. Genome Res. 24, 1–13.
10. Czyczyło-Mysza, I., Tyrka, M., Marci�nska, I., Skrzypek, E., Karbarz, M., Dziurka, M., Hura, T. et al. (2013) Quantitative trait loci for leaf chlorophyll fluorescence parameters, chlorophyll and carotenoid contents in relation to biomass and yield in bread wheat and their chromosome deletion bin assignments. Mol. Breed. 32, 189–210.
11. Delmas, F., Sankaranarayanan, S., Deb, S., Widdup, E., Bournonville, C., Bollier, N., Northey, J.G. et al. (2013) ABI3 controls embryo degreening through Mendel’s I locus. Proc. Natl Acad. Sci. USA, 110, 3888–3894.
12. Edwards, D., Batley, J. and Snowdon, R.J. (2013) Accessing complex crop genomes with next-generation sequencing. Theor. Appl. Genet. 126, 1–11.
13. Fernandez, L., Le Cunff, L., Tello, J., Lacombe, T., Boursiquot, J.M., Fournier-Level, A., Bravo, G. et al. (2014) Haplotype diversity of VvTFL1A gene and association with cluster traits in grapevine (V. vinifera). BMC Plant Biol. 14, 209.
14. Ferro, M., Brugi�ere, S., Salvi, D., Seigneurin-Berny, D., Court, M., Moyet, L., Ramus, C. et al. (2010) AT_CHLORO, a comprehensive chloroplast proteome database with subplastidial localization and curated information on envelope proteins. Mol. Cell Proteomics, 9, 1063–1084.
15. Field, B., Cardon, G., Traka, M., Botterman, J., Vancanneyt, G. and Mithen, R. (2004) Glucosinolate and Amino Acid Biosynthesis in Arabidopsis. Plant Physiol. 135, 828–839.
16. Friedt, W. and Snowdon, R.J. (2010) Oilseed rape. In Handbook of Plant Breeding, Vol. 4 (Vollmann, J. and Istvan, R., eds), pp. 91–126., Oil Crops Breeding. Berlin/Heidelberg: Springer Verlag.
17. Friso, G., Giacomelli, L., Ytterberg, A.J., Peltier, J.B., Rudella, A., Sun, Q. and Wijk, K.J. (2004) In-depth analysis of the thylakoid membrane proteome of Arabidopsis thaliana chloroplasts: new proteins, new functions, and a plastid proteome database. Plant Cell, 16, 478–499.
18. Gotoh, E., Kobayashi, Y. and Tsuyama, M. (2010) The post-illumination chlorophyll fluorescence transient indicates the RuBP regeneration limitation of photosynthesis in low light in Arabidopsis. FEBS Lett. 14, 3061–3064.
19. Harrell, F.E. and Dupont, M.C. (2012) Package ‘Hmisc’. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.
20. Heilmann, I., Mekhedov, S., King, B., Browse, J. and Shanklin, J. (2004) Identification of the Arabidopsis palmitoyl-monogalactosyldiacylglycerol delta7-desaturase gene FAD5, and effects of plastidial retargeting of Arabidopsis desaturases on the FAD5 mutant phenotype. Plant Physiol. 136, 4237–4245.
21. Heyndrickx, K.S. and Vandepoele, K. (2012) Systematic identification of functional plant modules through the integration of complementary data sources. Plant Physiol. 159, 884–901.
22. Kroymann, J., Textor, S., Tokuhisa, J.G., Falk, K.L., Bartram, S., Gershenzon, J. and Mitchell-Olds, T. (2001) A gene controlling variation in Arabidopsis glucosinolate composition is part of the methionine chain elongation pathway. Plant Physiol. 127, 1077–88.
23. Li, P., Filiault, D., Box, M.S., Kerdaffrec, E., van Oosterhout, C., Wilczek, A.M., Schmitt, J. et al. (2014) Multiple FLC haplotypes defined by independent cis-regulatory variation underpin life history diversity in Arabidopsis thaliana. Genes Dev. 15, 1635–1640.
24. Liu, K.J. and Muse, S.V. (2005) PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinformatics, 21, 2128–2129.
25. Mace, E.S., Tai, S., Gilding, E.K., Li, Y., Prentils, P.J., Bian, L., Campbell, B.C. et al. (2013) Whole-genome sequencing reveals untapped genetic potential in Africa’s indigenous cereal crop sorghum. Nat. Commun. 4, 2320.
26. Murillo, G. and Mehta, R.G. (2001) Cruciferous vegetables and cancer prevention. Nutr. Cancer, 41, 17–28.
27. Oster, U. and R€udiger, W. (1998) The G4 gene of Arabidopsis thaliana encodes a chlorophyll synthase of etiolated plants. Bot. Acta, 110, 420–423.
28. Qian, L., Qian, W. and Snowdon, R.J. (2014) Sub-genomic variation patterns as a signature of breeding in rapeseed. BMC Genom. 15, 1170.
29. Rambaut, A. (2009) Fig Tree version 1.3.1. [computer program]. [Hattp:// tree.bio.ed.ac.uk].
30. Revelle, W. (2014) Psych: Procedures for Personality and Psychological Research. Evanston, lllinois, USA: Northwestern University. http://CRAN.R-project.org/package=p-sych Version=1.4.8.
31. Shin, J.-H., Blay, S., McNeney, B. and Graham, J. (2006) LDheatmap: an R function for graphical display of pairwise linkage disequilibria between single nucleotide polymorphisms. J. Stat. Soft. 16, 1–9.
32. Smith, M.D., Rounds, C.M., Wang, F., Chen, K., Afitlhile, M. and Schnell, D.J. (2004) atToc159 is a selective transit peptide receptor for the import of nucleus-encoded chloroplast proteins. J. Cell Biol. 165, 323–334.
33. Snowdon, R.J., Abbadi, A., Kox, T., Schmutzer, T. and Leckband, G. (2015) Heterotic haplotype capture: precision breeding for hybrid performance. Trends Plant Sci. 20, 410–413.
34. Soderlund, C., Bomhoff, M. and Nelson, W. (2011) SyMAP: a turnkey synteny system with application to multiple large duplicated plant sequenced genomes. Nucleic Acids Res. 39, e68.
35. Stephens, J.C., Schneider, J.A., Tanguay, D.A., Choi, J., Acharya, T., Stanley, S.E., Jiang, R. et al. (2001) Haplotype variation and linkage disequilibrium in 313 human genes. Science, 293, 489–493.
36. Takahashi, H., Kopriva, S., Giordano, M., Saito, K. and Hell, R. (2011) Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes. Annu. Rev. Plant Biol. 62, 157–184.
37. Textor, S., de Kraker, J.W., Hause, B., Gershenzon, J. and Tokuhisa, J.G. (2007) MAM3 catalyzes the formation of all aliphatic glucosinolate chain lengths in Arabidopsis. Plant Physiol. 144, 60–71.
38. Tautorus, C.L. and Low, N.H. (1993) Chemical aspects of chlorophyll breakdown products and their relevance to canola oil stability. J. Am. Oil Chem. Soc. 70, 843–847.
39. Thomas, H. and Ougham, H. (2014) The stay-green trait. J. Exp. Bot. 65, 3889– 3900.
40. Tzvetkova-Chevolleau, T., Franck, F., Alawady, A.E., Dall’Osto, L., Carri�ere, F., Bassi, R., Grimm, B. et al. (2007) The light stress-induced protein ELIP2 is a regulator of chlorophyll synthesis in Arabidopsis thaliana. Plant J., 50, 795–809.
41. Voss-Fels, K. and Snowdon, R.J. (2015) Understanding and utilizing crop genome diversity via high-resolution genotyping. Plant Biotechnol. J. doi: 10.1111/pbi.12456.
42. Voss-Fels, K., Frisch, M., Qian, L., Kontowski, S., Friedt, W., Gottwald, S. and Snowdon, R.J. (2015) Subgenomic diversity patterns caused by directional selection in bread wheat gene pools. Plant Genome, 8. doi: 10.3835/plantgenome2015.03.0013.
43. Wang, F., Wang, G., Li, X., Huang, J. and Zheng, J. (2008) Heredity, physiology and mapping of a chlorophyll content gene of rice (Oryza sativa L.). J. Plant Physiol. 165, 324–330.
44. Yang, J. and Zhu, Z.J. (2009) Glucosinolates in Pakchoi (Brassica Campestris L. ssp. Chinensis) as Affected by Nutrient Status and Postharvest. PhD thesis, Zhejiang University, China. http://www.dissertationtopic.net/down/1524719.
45. Yang, Q., Li, Z., Li, W., Ku, L., Wang, C., Ye, J., Li, K et al. (2013) CACTA-like transposable element in ZmCCT attenuated photoperiod sensitivity and accelerated the postdomestication spread of maize. Proc. Natl Acad. Sci. USA, 42, 16969–16974.
46. Yu, J., Pressoir, G., Briggs, W.H., Vroh Bi, I., Yamasaki, M., Doebley, J.F., McMullen, M.D. et al. (2006) Aunified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat. Genet. 38, 203–208.