Hybridity has a greater effect than paternal genome dosage on heterosis in sugar beet (Beta vulgaris)

BMC Plant Biology

Volumn 18, Issue 1, 2018, Pages

  Hallahan, Brendan F ^a   Fernandez Tendero, Eva ^a   Fort, Antoine ^a   Ryder, Peter ^a   Dupouy, Gilles ^a   Deletre, Marc ^a   Curley, Edna ^a   Brychkova, Galina ^a   Schulz, Britta ^b   Spillane, Charles ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^b KWS SAAT SE   (Germany)

Author keywords

F1 hybrid; Genome dosage; Heterosis; Hybrid vigor; Hybridity; Polyploidy; Triploid

Indexed keywords

CARBOHYDRATE; MONOXERUTIN;

BEET; DIPLOIDY; DNA SEQUENCE; GENE DOSAGE; GENETICS; GROWTH, DEVELOPMENT AND AGING; HETEROSIS; HYBRIDIZATION; METABOLISM; PLANT GENE; PLANT ROOT; QUANTITATIVE TRAIT; SEEDLING; SINGLE NUCLEOTIDE POLYMORPHISM; TRIPLOIDY;

BETA VULGARIS; DIPLOIDY; GENE DOSAGE; GENES, PLANT; HYBRID VIGOR; HYBRIDIZATION, GENETIC; HYDROXYETHYLRUTOSIDE; PLANT ROOTS; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT, HERITABLE; SEEDLINGS; SEQUENCE ANALYSIS, DNA; SUGARS; TRIPLOIDY;

EID: 85048629147     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/s12870-018-1338-x     Document Type: Article

References (60)

1. Schnable PS, Springer NM. Progress toward understanding heterosis in crop plants. Annu Rev Plant Biol. 2013;64:71-88.
2. Comai L. The advantages and disadvantages of being polyploid. Nat Rev Genet. 2005;6(11):836.
3. Paterson AH, Wendel JF. Unraveling the fabric of polyploidy. Nat Biotechnol. 2015;33(5):491-3.
4. Roulin A, Auer PL, Libault M, Schlueter J, Farmer A, May G, Stacey G, Doerge RW, Jackson SA. The fate of duplicated genes in a polyploid plant genome. Plant J:Cell Mol Bio. 2013;73(1):143-53.
5. Tan C, Pan Q, Cui C, Xiang Y, Ge X, Li Z. Genome-wide gene/genome dosage imbalance regulates gene expressions in synthetic Brassica napus and derivatives (AC, AAC, CCA, CCAA). Front Plant Sci. 2016;7:1432.
6. Washburn JD, Birchler JA. Polyploids as a "model system" for the study of heterosis. Plant Reprod. 2014;27(1):1-5.
7. Chen ZJ. Molecular mechanisms of polyploidy and hybrid vigor. Trends Plant Sci. 2010;15(2):57-71.
8. Ryder P, McKeown PC, Fort A, Spillane C. Epigenetics and heterosis in crop plants. In: Epigenetics in plants of agronomic importance: fundamentals and applications. Cham: Springer; 2014. p. 13-31.
9. Jiang K, Liberatore KL, Park SJ, Alvarez JP, Lippman ZB. Tomato yield heterosis is triggered by a dosage sensitivity of the florigen pathway that fine-tunes shoot architecture. PLoS Genet. 2013;9(12):e1004043.
10. Wang J, Tian L, Lee H-S, Wei NE, Jiang H, Watson B, Madlung A, Osborn TC, Doerge R, Comai L. Genomewide nonadditive gene regulation in Arabidopsis allotetraploids. Genetics. 2006;172(1):507-17.
11. Fort A, Ryder P, McKeown PC, Wijnen C, Aarts MG, Sulpice R, Spillane C. Disaggregating polyploidy, parental genome dosage and hybridity contributions to heterosis in Arabidopsis thaliana. New Phytol. 2016;209(2):590-9.
12. Fort A, Tuteja R, Braud M, McKeown PC, Spillane C. Parental-genome dosage effects on the transcriptome of F1 hybrid triploid embryos of Arabidopsis thaliana. Plant J: Cell Mol Bio. 2017;92(6):1044-58.
13. Donoghue MT, Fort A, Clifton R, Zhang X, McKeown PC, Voigt-Zielinksi ML, Borevitz JO, Spillane C. C(m)CGG methylation-independent parent-of-origin effects on genome-wide transcript levels in isogenic reciprocal F1 triploid plants. DNA Res. 2014;21(2):141-51.
14. Auger, D.L., Gray, A.D., Ream, T.S., Kato, A., Coe, E.H. and Birchler, J.A., 2005. Nonadditive gene expression in diploid and triploid hybrids of maize. Genetics, 169(1), pp.389-397.
15. Donoghue MT, Fort A, Clifton R, Zhang X, McKeown PC, Voigt-Zielinksi M, Borevitz JO, Spillane C. CmCGG methylation-independent parent-of-origin effects on genome-wide transcript levels in isogenic reciprocal F1 triploid plants. DNA Res. 2013;21(2):141-51.
16. Duszynska D, McKeown PC, Juenger TE, Pietraszewska-Bogiel A, Geelen D, Spillane C. Gamete fertility and ovule number variation in selfed reciprocal F1 hybrid triploid plants are heritable and display epigenetic parent-of-origin effects. New Phytol. 2013;198(1):71-81.
17. Miller M, Zhang C, Chen ZJ. Ploidy and hybridity effects on growth vigor and gene expression in Arabidopsis thaliana hybrids and their parents. G3: Genes, Genomes, Genetics. 2012;2(4):505-13.
18. Guo M, Davis D, Birchler JA. Dosage effects on gene expression in a maize ploidy series. Genetics. 1996;142(4):1349-55.
19. Yao H, Dogra Gray A, Auger DL, Birchler JA. Genomic dosage effects on heterosis in triploid maize. Proc Natl Acad Sci. 2013;110(7):2665-9.
20. Moll R, Lonnquist J, Fortuno JV, Johnson E. The relationship of heterosis and genetic divergence in maize. Genetics. 1965;52(1):139.
21. Reif JC, Fischer S, Schrag TA, Lamkey KR, Klein D, Dhillon BS, Utz HF, Melchinger AE. Broadening the genetic base of European maize heterotic pools with US Cornbelt germplasm using field and molecular marker data. Theor Appl Genet. 2010;120(2):301-10.
22. Frisch M, Thiemann A, Fu J, Schrag TA, Scholten S, Melchinger AE. Transcriptome-based distance measures for grouping of germplasm and prediction of hybrid performance in maize. Theor Appl Genet. 2010;120(2):441-50.
23. Benchimol LL, de Souza CL, Garcia AAF, Kono PMS, Mangolin CA, Barbosa AMM, Coelho ASG, de Souza AP. Genetic diversity in tropical maize inbred lines: heterotic group assignment and hybrid performance determined by RFLP markers. Plant Breed. 2000;119(6):491-6.
24. Meyer RC, Törjék O, Becher M, Altmann T. Heterosis of biomass production in Arabidopsis. Establishment during early development. Plant Physiol. 2004;134(4):1813-23.
25. Stokes D, Morgan C, O'Neill C, Bancroft I. Evaluating the utility of Arabidopsis thaliana as a model for understanding heterosis in hybrid crops. Euphytica. 2007;156(1-2):157-71.
26. Ali M, Copeland LO, Elias SG, Kelly JD. Relationship between genetic distance and heterosis for yield and morphological traits in winter canola (Brassica napus L.). Theor Appl Genet. 1995;91(1):118-21.
27. Riaz A, Li G, Quresh Z, Swati MS, Quiros CF. Genetic diversity of oilseed Brassica napus inbred lines based on sequence-related amplified polymorphism and its relation to hybrid performance. Plant Breed. 2001;120(5):411-5.
28. Diers B, McVetty P, Osborn T. Relationship between heterosis and genetic distance based on restriction fragment length polymorphism markers in oilseed rape (Brassica napus L.). Crop Sci. 1996;36(1):79-83.
29. Geleta L, Labuschagne M, Viljoen C. Relationship between heterosis and genetic distance based on morphological traits and AFLP markers in pepper. Plant Breed. 2004;123(5):467-73.
30. Zhang Q, Gao Y, Maroof MS, Yang S, Li J. Molecular divergence and hybrid performance in rice. Mol Breed. 1995;1(2):133-42.
31. Martin J, Talbert L, Lanning S, Blake N. Hybrid performance in wheat as related to parental diversity. Crop Sci. 1995;35(1):104-8.
32. Draycott AP. Sugar beet. New York: Wiley; 2008.
33. Peto F, Boyes J. Comparison of diploid and triploid sugar beets. Can J Res. 1940;18((7):273-82.
34. Savitsky V. Monogerm sugar beets in the United States. Proc Amer Soc Sugar Beet Tech. 1950;6:156-9.
35. Biancardi E, McGrath JM, Panella LW, Lewellen RT, Stevanato P. Sugar beet. In: Root and tuber crops: Springer; New York, NY. 2010. p. 173-219.
36. Hedtke SM, Hillis DM. The potential role of Androgenesis in cytoplasmic-nuclear phylogenetic discordance. Syst Biol. 2011;60(1):87-96.
37. Van Dyke F. Conservation biology: foundations, concepts, Applications: Springer Science & Business Media; 2008.
38. Li H, Durbin R. Fast and accurate short read alignment with burrows-wheeler transform. Bioinformatics. 2009;25(14):1754-60.
39. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. The sequence alignment/map format and SAMtools. Bioinformatics. 2009;25(16):2078-9.
40. Wang K, Li M, Hakonarson H. ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res. 2010;38(16):e164.
41. Kenter C, Hoffmann C, Märländer B. Sugarbeet as raw material-advanced storage management to gain good processing quality/Optimierung der Rohstoffqualität von Zuckerrüben durch verbessertes Lagerungsmanagement. Zuckerindustrie. 2006;131:706-20.
42. De Whalley HCS. ICUMSA methods of sugar analysis: official and tentative methods recommended by the International Commission for Uniform Methods of sugar analysis (ICUMSA): Elsevier; Amsterdam 2013.
43. Buchholz K, Märländer B, Puke H, Glattkowski H, Thielecke K. Neubewertung des technischen Wertes von Zuckerrueben. Zuckerindustrie. 1995;120(2), pp.113-121.
44. Hecker R, Stafford R, Helmerick R, Maag G. Comparison of the same sugarbeet F1 hybrids as diploids, triploids and tetraploids. J Am Soc Sugar Beet Technol. 1970;16(2):106-16.
45. Smith G, Hecker R, Martin S. Effects of ploidy level on the components of sucrose yield and quality in sugarbeet. Crop Sci. 1979;19(3):319-23.
46. Lasa J, Romagosa I, Hecker R, Sanz J. Combining ability in diploid and triploid sugarbeet hybrids from diverse parents. J Sugar Beet Res. 1989;26:10-8.
47. Islam MS, Thyssen GN, Jenkins JN, Fang DD. Detection, validation, and application of genotyping-by-sequencing based single nucleotide polymorphisms in upland cotton. Plant Gen. 2015;8(1):1-10
48. Sonah H, Bastien M, Iquira E, Tardivel A, Légaré G, Boyle B, Normandeau É, Laroche J, Larose S, Jean M. An improved genotyping by sequencing (GBS) approach offering increased versatility and efficiency of SNP discovery and genotyping. PLoS One. 2013;8(1):e54603.
49. Ma X-F, Jensen E, Alexandrov N, Troukhan M, Zhang L, Thomas-Jones S, Farrar K, Clifton-Brown J, Donnison I, Swaller T. High resolution genetic mapping by genome sequencing reveals genome duplication and tetraploid genetic structure of the diploid Miscanthus sinensis. PLoS One. 2012;7(3):e33821.
50. Azmach G, Gedil M, Menkir A, Spillane C. Marker-trait association analysis of functional gene markers for provitamin a levels across diverse tropical yellow maize inbred lines. BMC Plant Biol. 2013;13(1):227.
51. Girma G, Hyma KE, Asiedu R, Mitchell SE, Gedil M, Spillane C. Next-generation sequencing based genotyping, cytometry and phenotyping for understanding diversity and evolution of Guinea yams. Theor Appl Genet. 2014;127(8):1783-94.
52. Hermann K, Meinhard J, Dobrev P, Linkies A, Pesek B, Heß B, Macháčková I, Fischer U, Leubner-Metzger G. 1-Aminocyclopropane-1-carboxylic acid and abscisic acid during the germination of sugar beet (Beta vulgaris L.): a comparative study of fruits and seeds. J Exp Bot. 2007;58(11):3047-60.
53. Lawrence DM, Halmer P, Bowles DJ. Mobilisation of storage reserves during germination and early seedling growth of sugar beet. Physiol Plant. 1990;78(3):421-9.
54. Elamrani A, Raymond P, Saglio P. Nature and utilization of seed reserves during germination and heterotrophic growth of young sugar beet seedlings. Seed Sci Res. 1992;2(1):1-8.
55. Catusse J, Strub JM, Job C, Van Dorsselaer A, Job D. Proteome-wide characterization of sugarbeet seed vigor and its tissue specific expression. Proc Natl Acad Sci U S A. 2008;105(29):10262-7.
56. Costa LM, Gutièrrez-Marcos JF, Dickinson HG. More than a yolk: the short life and complex times of the plant endosperm. Trends Plant Sci. 2004;9(10):507-14.
57. Baroux C, Spillane C, Grossniklaus U. Evolutionary origins of the endosperm in flowering plants. Genome Biol. 2002;3(9):reviews1026.
58. Bergen P. Seasonal patterns of sucrose accumulation and weight increase in sugar beets. J Am Soc Sugar Beet Technol. 1967;14:538-45.
59. Oldemeyer R. Introgressive hybridization as a breeding method in Beta vulgaris. J Am Soc Sugar Beet Technol. 1975;18:269-73.
60. Carter J. Sucrose production as affected by root yield and sucrose concentration of sugarbeets. J Am Soc Sugar Beet Technol. 1987;24(1):14-31.