Deletion of a Stay-Green Gene Associates with Adaptive Selection in Brassica napus

Molecular Plant

Volumn 9, Issue 12, 2016, Pages 1559-1569

  Qian, Lunwen ^a   Voss Fels, Kai ^a   Cui, Yixin ^b   Jan, Habib U ^a   Samans, Birgit ^a   Obermeier, Christian ^a   Qian, Wei ^b   Snowdon, Rod J ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b SOUTHWEST UNIVERSITY   (China)

Author keywords

breeding; chlorophyll; PAV; photosynthesis; presence absence variation; rapeseed

Indexed keywords

CHLOROPHYLL;

BRASSICA RAPA; BREEDING; GENETICS; HAPLOTYPE; METABOLISM; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT GENOME; RAPESEED;

BRASSICA NAPUS; BRASSICA RAPA; BREEDING; CHLOROPHYLL; GENOME, PLANT; HAPLOTYPES; PHOTOSYNTHESIS;

EID: 85000995988     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1016/j.molp.2016.10.017     Document Type: Article

References (53)

1. Alam, A.M., Somta, P., Jompuk, C., Chatwachirawong, P., Srinives, P., Evaluation of mungbean genotypes based on yield stability and reaction to mungbean yellow mosaic virus disease. Plant Pathol. J. 30 (2014), 261–268.
2. Armstead, I., Donnison, I., Aubry, S., Harper, J., Hörtensteiner, S., James, C., Mani, J., Moffet, M., Ougham, H., Roberts, L., et al. Cross-species identification of Mendel's I locus. Science, 315, 2007, 373.
3. Barry, C.S., McQuinn, R.P., Chung, M.Y., Besuden, A., Giovannoni, J.J., Amino acid substitutions in homologs of the STAY-GREEN protein are responsible for the green-flesh and chlorophyll retainer mutations of tomato and pepper. Plant Physiol. 147 (2008), 179–187.
4. Benjamini, Y., Hochberg, Y., Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Statist. Soc. B 57 (1995), 289–300.
5. Berry, J., Bjorkman, O., Photosynthetic response and adaptation to temperature in higher plants. Annu. Rev. Plant Physiol. 31 (1980), 491–543.
6. Boguszewska, D., Zagdańska, B., ROS as signaling molecules and enzymes of plant response to unfavorable environmental conditions. Lushchak, W., Semchyshyn, H.M., (eds.) Oxidative Stress-Molecular Mechanisms and Biological Effects, 2012, InTech, Rijeka, 341–362.
7. Bouchet, A.S., Laperche, A., Bissuel-Belaygue, C., Snowdon, R.J., Nesi, N., Stahl, A., Nitrogen use efficiency in rapeseed: a review. Agron. Sustain. Dev., 2016, 10.1007/s13593-016-0371-0.
8. Bradbury, P.J., Zhang, Z., Kroon, D.E., Casstevens, T.M., Ramdoss, Y., Buckler, E.S., TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23 (2007), 2633–2635.
9. Brown, D.E., Rashotte, A.M., Murphy, A.S., Normanly, J., Tague, B.W., Peer, W.A., Taiz, L., Muday, G.K., Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis. Plant Physiol. 126 (2001), 524–535.
10. Bus, A., Körber, N., Snowdon, R.J., Stich, B., Patterns of molecular variation in a species-wide germplasm set of Brassica napus. Theor. Appl. Genet. 123 (2011), 1413–1423.
11. Chalhoub, B., Denoeud, F., Liu, S., Parkin, I.A., Tang, H., Wang, X., Chiquet, J., Belcram, H., Tong, C., Samans, B., et al. Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 345 (2014), 950–953.
12. Chen, S., Nelson, M.N., Ghamkhar, K., Fu, T., Cowling, W.A., Divergent patterns of allelic diversity from similar origins: thecase of oilseed rape (Brassica napus L.) in China and Australia. Genome 51 (2008), 1–10.
13. Cornille, A., Gladieux, P., Smulders, M.J.M., Roldan-Ruiz, I., Laurens, F., Le Cam, B., Nersesyan, A., Clavel, J., Olonova, M., Feugey, L., et al. New insight into the history of domesticated apple: secondary contribution of the European wild apple to the genome of cultivated varieties. PLoS Genet., 8, 2012, e1002703.
14. Danilevskaya, O.N., Meng, X., Hou, Z., Ananiev, E.V., Simmons, C.R., A genomic and expression compendium of the expanded PEBP gene family from maize. Plant Physiol. 146 (2008), 250–264.
15. Edwards, D., Batley, J., Snowdon, R.J., Accessing complex crop genomes with next-generation sequencing. Theor. Appl. Genet. 126 (2013), 1–11.
16. Gapper, C., Dolan, L., Control of plant development by reactive oxygen species. Plant Physiol. 141 (2006), 341–345.
17. Hallauer, A.R., Miranda, J.B., Quantitative Genetics in Maize Breeding. 2nd Edition, 1988, Iowa State University Press, Ames, IA, USA.
18. Harrell, F.E. Jr., Dupont, M.C., Package ‘Hmisc’. R: A Language and Environment for Statistical Computing. 2012, R Foundation for Statistical Computing, Vienna, Austria.
19. Hatzig, S.V., Frisch, M., Breuer, F., Nesi, N., Ducournau, S., Wagner, M.H., Leckband, G., Abbadi, A., Snowdon, R.J., Genome-wide association mapping unravels the genetic control of seed germination and vigor in Brassica napus. Front. Plant Sci., 6, 2015, 221.
20. Hua, S.J., Chen, Z.H., Zhang, Y.F., Yu, H.S., Lin, B.G., Zhang, D.Q., Chlorophyll and carbohydrate metabolism in developing silique and seed are prerequisite to seed oil content of Brassica napus L. Bot. Stud., 55, 2014, 34.
21. Jan, H.U., Abbadi, A., Lücke, S., Nichols, R.A., Snowdon, R.J., Genomic prediction of testcross performance in canola (Brassica napus). PLoS One, 11, 2016, e0147769.
22. Kakizaki, T., Inaba, T., New insights into the retrograde signaling pathway between the plastids and the nucleus. Plant Signal. Behav. 5 (2010), 196–199.
23. Krishnamurthy, A., Rathinasabapathi, B., Oxidative stress tolerance in plants: novel interplay between auxin and reactive oxygen species signaling. Plant Signal. Behav., 8, 2013, e25761.
24. Kusakina, J., Dodd, A.N., Phosphorylation in the plant circadian system. Trends Plant Sci. 17 (2012), 575–583.
25. Liu, H., Rapeseed Genetics and Breeding. 1985, Shanghai Science and Technology Press, Shanghai, 559–566.
26. Liu, K.J., Muse, S.V., PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinformatics 21 (2005), 2128–2129.
27. Liu, Y., Ji, X., Nie, X., Qu, M., Zheng, L., Tan, Z., Zhao, H., Huo, L., Liu, S., Zhang, B., et al. Arabidopsis AtbHLH112 regulates the expression of genes involved in abiotic stress tolerance by binding to their E-box and GCG-box motifs. New Phytol. 207 (2015), 692–709.
28. Luo, M.C., Yang, Z.L., You, F.M., Kawahara, T., Waines, J.G., Dvorak, J., The structure of wild and domesticated emmer wheat populations, gene flow between them, and the site of emmer domestication. Theor. Appl. Genet. 114 (2007), 947–959.
29. Mace, E.S., Tai, S., Gilding, E.K., Li, Y., Prentils, P.J., Bian, L., Campbell, B.C., Hu, W., Innes, D.J., Han, X., et al. Whole-genome sequencing reveals untapped genetic potential in Africa's indigenous cereal crop sorghum. Nat. Commun., 4, 2013, 2320.
30. Macduff, J., Raistrick, N., Humphreys, M., Differences in growth and nitrogen productivity between a stay-green genotype and a wild-type of Lolium perenne under limiting relative addition rates of nitrate supply. Physiol. Plant 116 (2002), 52–61.
31. Mason, A.S., Zhang, J., Tollenaere, R., Vasquez Teuber, P., Dalton-Morgan, J., Hu, L., Yan, G., Edwards, D., Redden, R., Batley, J., High-throughput genotyping for species identification and diversity assessment in germplasm collections. Mol. Ecol. Resour. 15 (2015), 1091–1101.
32. Mattioli, R., Costantino, P., Trovato, M., Proline accumulation in plants. Plant Signal. Behav. 4 (2009), 1016–1018.
33. Myles, S., Boyko, A.R., Owens, C.L., Brown, P.J., Grassi, F., Aradhya, M.K., Prins, B., Reynolds, A., Chia, J.M., Ware, D., et al. Genetic structure and domestication history of the grape. Proc. Natl. Acad. Sci. USA 108 (2011), 3530–3535.
34. Nei, M., Genetic distance between populations. Am. Nat. 106 (1972), 283–292.
35. Park, S.Y., Yu, J.W., Park, J.S., Li, J., Yoo, S.C., Lee, N.Y., Lee, S.K., Jeong, S.W., Seo, H.S., Koh, H.J., et al. The senescence-induced stay green protein regulates chlorophyll degradation. Plant Cell 19 (2007), 1649–1664.
36. Qian, W., Meng, J., Li, M., Frauen, M., Sass, O., Noack, J., Jung, C., Introgression of genomic components from Chinese Brassica rapa contributes to widening the genetic diversity in rapeseed (Brassica napus L.), with emphasis on the evolution of Chinese rapeseed. Theor. Appl. Genet. 113 (2006), 49–54.
37. Qian, L., Qian, W., Snowdon, R.J., Sub-genomic variation patterns as a signature of breeding in rapeseed. BMC Genomics, 15, 2014, 1170.
38. Qian, L., Qian, W., Snowdon, R.J., Haplotype hitchhiking promotes trait co-selection in Brassica napus. Plant Biotechnol. J. 14 (2016), 1578–1588.
39. Rambaut, A. (2009). Fig Tree Version 1.3.1. [Computer Program]. [http://tree.bio.ed.ac.uk/software/figtree/].
40. Ren, G., An, K., Liao, Y., Zhou, X., Cao, Y., Zhao, H., Ge, X., Kuai, B., Identification of a novel chloroplast protein AtNYE1 regulating chlorophyll degradation during leaf senescence in Arabidopsis. Plant Physiol. 144 (2007), 1429–1441.
41. Sakuraba, Y., Schelbert, S., Park, S.Y., Han, S.H., Lee, B.D., Andres, C.B., Kessler, F., Hörtensteiner, S., Paek, N.C., STAY-GREEN and chlorophyll catabolic enzymes interact at light-harvesting complex II for chlorophyll detoxification during leaf senescence in Arabidopsis. Plant Cell 24 (2012), 507–518.
42. Sato, Y., Morita, R., Nishimura, M., Yamaguchi, H., Kusaba, M., Mendel's green cotyledon gene encodes a positive regulator of the chlorophyll-degrading pathway. Proc. Natl. Acad. Sci. USA 104 (2007), 14169–14174.
43. Schmutzer, T., Samans, B., Dyrszka, E., Ulpinnis, C., Weise, S., Stengel, D., Colmsee, C., Lespinasse, D., Micic, Z., Abel, S., et al. Species-wide genome sequence and nucleotide polymorphisms from the model allopolyploid plant Brassica napus. Sci. Data, 2, 2015, 150072.
44. Shimoda, Y., Ito, H., Tanaka, A., Arabidopsis STAY-GREEN, Mendel's green cotyledon gene, encodes magnesium-dechelatase. Plant Cell, 2016, 10.1105/tpc.16.00428.
45. Shin, J.H., Blay, S., McNeney, B., Graham, J., LDheatmap: an R function for graphical display of pairwise linkage disequilibria between single nucleotide polymorphisms. J. Stat. Soft. 16 (2006), 1–9.
46. Thomas, H., Howarth, C.J., Five ways to stay green. J. Exp. Bot. 51 (2000), 329–337.
47. Thomas, H., Ougham, H., The stay-green trait. J. Exp. Bot. 65 (2014), 3889–3900.
48. Thomas, H., Stoddart, L., Separation of chlorophyll degradation from other senescence processes in leaves of a mutant genotype of medow fescue (Festuca pratensis L.). Plant Physiol. 56 (1975), 438–441.
49. Tripathy, B.C., Oelmüller, R., Reactive oxygen species generation and signaling in plants. Plant Signal. Behav. 7 (2012), 1621–1633.
50. Voss-Fels, K., Snowdon, R.J., Understanding and utilizing crop genome diversity via high-resolution genotyping. Plant Biotechnol. J. 14 (2015), 1086–1094.
51. Voss-Fels, K., Frisch, M., Qian, L., Kontowski, S., Friedt, W., Gottwald, S., Snowdon, R.J., Subgenomic diversity patterns caused by directional selection in bread wheat gene pools. Plant Genome, 8, 2015, 2.
52. Wu, X.L., Liu, Z.H., Hu, Z.H., Huang, R.Z., BnWRI1 coordinates fatty acid biosynthesis and photosynthesis pathways during oil accumulation in rapeseed. J. Integr. Plant Biol. 56 (2014), 582–593.
53. Yu, J., Pressoir, G., Briggs, W.H., Vroh Bi, I., Yamasaki, M., Doebley, J.F., McMullen, M.D., Gaut, B.S., Nielsen, D.M., Holland, J.B., et al. Aunified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat. Genet. 38 (2006), 203–208.