Heterosis

Plant Cell

Volumn 22, Issue 7, 2010, Pages 2105-2112

  Birchler, James A ^a   Yao, Hong ^a   Chudalayandi, Sivanandan ^a   Vaiman, Daniel ^b,c   Veitia, Reiner A ^d  

^a UNIVERSITY OF MISSOURI   (United States)

^b INSTITUT COCHIN   (France)

^c Inst Natl S et de la Rech U129   (France)

^d INSTITUT JACQUES MONOD   (France)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 77956795823     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.110.076133     Document Type: Article

References (91)

1. Alexander, D.E., and Sonnemaker, E.H. (1961). Inbreeding depression in autotetraploid maize. Maize Genet. Coop. News Lett. 35: 45.
2. Andorf, S., Selbig, J., Altmann, T., Poos, K., Witucka-Wall, H., and Repsilber, D. (2010). Enriched partial correlations in genome-wide gene expression profiles of hybrids (A. thaliana): A systems biological approach towards the molecular basis of heterosis. Theor. Appl. Genet. 120: 249-259.
3. Bingham, E.T., Groose, R.W., Woodfield, D.R., and Kidwell, K.K. (1994). Complementary gene interactions in alfalfa are greater in autotetraploids than diploids. Crop Sci. 34: 823-829.
4. Birchler, J.A. (1979). A study of enzyme activities in a dosage series of the long arm of chromosome one in maize. Genetics 92: 1211-1229.
5. Birchler, J.A., Bhadra, U., Pal Bhadra, M., and Auger, D.L. (2001). Dosage dependent gene regulation in multicellular eukaryotes: Implications for dosage compensation, aneuploid syndromes and quantitative traits. Dev. Biol. 234: 275-288.
6. Birchler, J.A., and Newton, K.J. (1981). Modulation of protein levels in chromosomal dosage series of maize: The biochemical basis of aneuploid syndromes. Genetics 99: 247-266.
7. Birchler, J.A., Riddle, N.C., Auger, D.L., and Veitia, R.A. (2005). Dosage balance in gene regulation: Biological implications. Trends Genet. 21: 219-226.
8. Birchler, J.A., and Veitia, R.A. (2007). The gene balance hypothesis: From classical genetics to modern genomics. Plant Cell 19: 395-402.
9. Birchler, J.A., and Veitia, R.A. (2010). The gene balance hypothesis: Implications for gene regulation, quantitative traits and evolution. New Phytol. 186: 54-62.
10. Briggle, L.W. (1963). Heterosis in wheat-A review. Crop Sci. 3: 407-412.
11. Bruce, A.B. (1910). The Mendelian theory of heredity and the augmentation of vigor. Science 32: 627-628.
12. Buckler, E.S., Holland, J.B., Bradbury, P.J., Acharya, C.B., Brown, P.J., Browne, C., Ersoz, E., Flint-Garcia, S., Garcia, A., Glaubitz, J.C., Goodman, M.M., Harjes, C., et al. (2009). The genetic architecture of maize flowering time. Science 325: 714-718.
13. Busbice, T.H., and Wilsie, C.P. (1966). Inbreeding depression and heterosis in autotetraploids with application to Medicago sativa L. Euphytica 15: 52-67.
14. Charlesworth, D., and Willis, J.H. (2009). The genetics of inbreeding depression. Nat. Rev. Genet. 10: 783-796.
15. Chase, S.S. (1980). Studies of monoploid, diploid and tetraploids of maize in relation to heterosis and inbreeding depression. Proceedings of the Argentine Society of Genetics.
16. Chen, X., Li, M., Shi, J., Fu, D., Qian, W., Zou, J., Zhang, C., and Meng, J. (2008). Gene expression profiles associated with intersubgenomic heterosis in Brassica napus. Theor. Appl. Genet. 117: 1031-1040.
17. Chen, Z.J. (2010). Molecular mechanisms of polyploidy and hybrid vigor. Trends Plant Sci. 15: 57-71.
18. Comai, L. (2005). The advantages and disadvantages of being polyploidy. Nat. Rev. Genet. 6: 836-846.
19. Darwin, C.R. (1876). The Effects of Cross and Self Fertilization in the Vegetable Kingdom. (London: John Murray).
20. Delneri, D., Hoyle, D.C., Gkargkas, K., Cross, E.J.M., Rash, B., Zeef, L., Leong, H.-S., Davey, H.M., Hayes, A., Kell, D.B., Griffith, G.W., and Oliver, S.G. (2008). Identification and characterization of highflux-control genes in yeast through competition analyses in continuous cultures. Nat. Genet. 40: 113-117.
21. Dollinger, E.J. (1985). Effects of visible recessive alleles on vigor characteristics in a maize hybrid. Genetics 25: 819-821.
22. Duvick, D.N. (1999). Heterosis: Feeding people and protecting natural resources. In Genetics and Exploitation of Heterosis in Crops, J.G. Coors and S. Pandey, eds (Madison, WI: American Society of Agronomy and Crop Science Society of America), pp. 19-29.
23. East, E.M. (1936). Heterosis. Genetics 21: 375-397.
24. Eshed, Y., and Zamir, D. (1995). An introgression line population of Lycopersicon pennelli in the cultivated tomato enables the identification and fine mapping of yield-associated QTL. Genetics 141: 1147-1162.
25. Fievet, J.B., Dilman, C., and de Vienne, D. (2010). Systemic properties of metabolic networks lead to an epistasis-based model for heterosis. Theor. Appl. Genet. 120: 463-473.
26. Flint-Garcia, S.A., Buckler, E.S., Tiffin, P., Ersoz, E., and Springer, N.M. (2009). Heterosis is prevalent for multiple traits in diverse maize germplasm. PLoS ONE 4: e7433.
27. Frary, A., Nesbitt, T.C., Grandillo, S., Knaap, E., Cong, B., Liu, J., Meller, J., Elber, R., Alpert, K.B., and Tanksley, S.D. (2000). Fw2.2: A quantitative trait locus key to the evolution of tomato fruit size. Science 99: 85-88.
28. Frascaroli, E., Cane, M.A., Landi, P., Pea, G., Gianfranceschi, L., Villa, M., Morgante, M., and Pe, M.E. (2007). Classical genetic and quantitative trait loci analysis of heterosis in a maize hybrid betweentwo elite inbred lines. Genetics 176: 625-644.
29. Freeling, M., Lyons, E., Pedersen, B., Alam, M., Ming, R., and Lisch, D. (2008). Many or most genes in Arabidopsis transposed after the origin of the order Brassicales. Genome Res. 18: 1924-1937.
30. Freeling, M., and Thomas, B.C. (2006). Gene-balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexity. Genome Res. 16: 805-814.
31. Frisch, M., Thiemann, A., Fu, J., Schrag, T.A., Scholten, S., and Melchinger, A.E. (2010). Transcriptome-based distance measures for grouping of germplasm and prediction of hybrid performance in maize. Theor. Appl. Genet. 120: 441-450.
32. Fu, H., and Dooner, H.K. (2002). Intraspecific violation of genetic colinearity and its implications in maize. Proc. Natl. Acad. Sci. USA 99: 9573-9578.
33. Gartner, T., Steinfath, M., Andorf, S., Lisec, J., Meyer, R.C., Altman, R., Willmitzer, L., and Delbig, J. (2009). Improved heterosis prediction by combining information on DNA- and metabolic markers. PLoS ONE 4: e5220.
34. Goral, H., Tyrka, M., and Spiss, L. (2005). Assessing genetic variation to predict the breeding value of winter triticale cultivars and lines.J. Appl. Genet. 46: 125-131.
35. Groose, R.W., Talbert, L.E., Kojis, W.P., and Bingham, E.T. (1989). Progressive heterosis in autotetraploid alfalfa: Studies using two types of inbreds. Crop Sci. 29: 1173-1177.
36. Guo, M., and Birchler, J.A. (1994). Trans-acting dosage effects on the expression of model gene systems in maize aneuploids. Science 266: 1999-2002.
37. Guo, M., Rupe, M.A., Dieter, J.A., Zou, J., Spielbauer, D., Duncan, K.E., Howard, R.J., Hou, Z., and Simmons, C.R. (2010). Cell Number Regulator1 affects plant and organ size in maize: Implications for crop yield enhancement and heterosis. Plant Cell 22: 1057-1073.
38. Guo, M., Yang, S., Rupe, M., Hu, B., Bickel, D.R., Arthur, L., and Smith, O. (2008). Genome-wide allele-specific expression analysis using Massively Parallel Signature Sequencing (MPSS) reveals cisand trans-effects on gene expression in maize hybrid meristem tissue. Plant Mol. Biol. 66: 551-563.
39. Gustafson, A. (1946). The effect of heterozygosity on viability and vigor. Hereditas 32: 263-286.
40. Hammerle, B., and Ferrus, A. (2003). Expression of enhancers is altered in Drosophila melanogaster hybrids. Evol. Dev. 5: 221-230.
41. He, G., Zhu, X., Elling, A.A., Chen, L., Wang, X., Guo, L., Liang, M., He, H., Zhang, H., Chen, F., Qi, Y., Chen, R., et al. (2010). Global epigenetic and transcriptional trends in two rice subspecies and their reciprocal hybrids. Plant Cell 22: 17-33.
42. Hoecker, N., Keller, B., Muthreich, N., Chollet, D., Descombe, P., Piepho, H.P., and Hockholdinger, F. (2008). Comparison of maize (Zea mays L.) F1-hybrid and parental line primary root transcriptomes suggests organ-specific patterns of nonadditive gene expression and conserved expression trends. Genetics 179: 1275-1283.
43. Jahnke, S., Sarholz, B., Thiemann, A., Kuhr, V., Gutierrez-Marcos, J.F., Geiger, H.H., Piepho, H.P., and Scholten, S. (2010). Heterosis in early seed development: A comparative study of F1 embryo and endosperm tissues 6 days after fertilization. Theor. Appl. Genet. 120: 389-400.
44. Jones, D.F. (1917). Dominance of linked factors as a means of accounting for heterosis. Genetics 2: 466-479.
45. Karpechenko, G.D. (1927). Polyploid hybrids of Raphanus sativus L. 3 Brassica oleracea L. Bull. Appl. Bot. 17: 305-410.
46. Krieger, U., Lippman, Z.B., and Zamir, D. (2010). The flowering gene SINGLE FLOWER TRUSS drives heterosis for yield in tomato. Nat. Genet. 10.1038/ng.550.
47. Lee, E.A., Darrah, L.L., and Coe, E.H. (1996). Dosage effects on morphological and quantitative traits in maize aneuploids. Genome 39: 898-908.
48. Leitch, I.J., Hanson, L., Lim, K.Y., Kovarik, A., Chase, M.W., Clarkson, J.J., and Leitch, A.R. (2008). The ups and downs of genome size evolution in polyploidy species of Nicotiana (Solanaceae). Ann. Bot. (Lond.) 101: 805-814.
49. Levings, C.S., Dudley, J.W., and Alexander, D.E. (1967). Inbreeding and crossing in autotetraploid maize. Crop Sci. 7: 72-73.
50. Li, X., Wei, Y., Nettleton, D., and Brummer, E.C. (2009). Comparative gene expression profiles between heterotic and non-heterotic hybrids of tetraploid Medicago sativa. BMC Plant Biol. 9: 107.
51. Liang, H., Rogale-Plazonic, K., Chen, J., Li, W.H., and Fernandez, A. (2008). Protein under-wrapping causes dosage sensitivity and decreases gene duplicability. PLoS Genet. 4: 11.
52. Libault, M., Zhang, X.C., Govindarajulu, M., Qiu, J., Ong, Y.T., Brechenmacher, L., Howard Berg, R., Hurley-Sommer, A., Taylor, C.G., and Stacey, G. (2010). A member of the highly conserved FWL (tomato FW2.2-like) gene family is essential for soybean nodule organogenesis. Plant J.
53. Liu, J., Cong, B., and Tanksley, S.D. (2003). Generation and analysis of an artificial gene dosage series in tomato to study the mechanisms by which the cloned quantitative trait locus fw2.2 controls fruit size. Plant Physiol. 132: 292-299.
54. McMullen, M.D., Kresovich, S., Villeda, H.S., Bradbury, P., Li, H., Sun, Q., Flint-Garcia, S., Thornsberry, J., Acharya, C., Bottoms, C., Brown, P., Browne, C., et al. (2009). Genetic properties of the maize nested association mapping population. Science 325: 737-740.
55. Meyer, R.C., Kusterer, B., Lisec, J., Steinfath, M., Becher, M., Scharr, H., Melchinger, A.E., Selbig, J., Schurr, U., Willmitzer, L., and Altmann, T. (2010). QTL analysis of early stage heterosis for biomass in Arabidopsis. Theor. Appl. Genet. 120: 227-237.
56. Meyer, S., Pospisil, H., and Scholten, S. (2007). Heterosis associated gene expression in maize embryos 6 days after fertilization exhibits additive, dominant and overdominant pattern. Plant Mol. Biol. 63: 381-391.
57. Mok, D.W.S., and Peloquin, S.J. (1975). Breeding value of 2n pollen (diploandroids) in tetraploid 3 diploid crosses in potato. Theor. Appl. Genet. 46: 307-314.
58. Ni, Z., Kim, E.-D., Ha, M., Lackey, E., Liu, J., Zhang, Y., Sun, Q., and Chen, Z.J. (2009). Altered circadian rhythms regulate growth vigor in hybrids and allopolyploids. Nature 457: 327-331.
59. Papp, B., Pal, C., and Hurst, L.D. (2003). Dosage sensitivity and the evolution of gene families in yeast. Nature 424: 194-197.
60. Paschold, A., Marcon, C., Hoecker, N., and Hochholdinger, F. (2010). Molecular dissection of heterosis manifestation during early maize root development. Theor. Appl. Genet. 120: 441-450.
61. Pea, G., Ferron, S., Gianfranceschi, L., Krajewski, P., and Enrico Pe, M. (2008). Gene expression non-additivity in immature ears of a heterotic F1 maize hybrid. Plant Sci. 174: 17-24.
62. Randolph, L.F. (1942). The influence of heterozygosis on fertility and vigor in autotetraploid maize. Genetics 27: 163.
63. Redei, G.P. (1962). Single loci heterosis. Z. Vererbungsl. 93: 164-170.
64. Rice, J.S., and Dudley, J.W. (1974). Gene effects responsible for inbreeding depression in autotetraploid maize. Crop Sci. 14: 390-393.
65. Riddle, N.C., and Birchler, J.A. (2008). Comparative analysis of inbred and hybrid maize at the diploid and tetraploid levels. Theor. Appl. Genet. 116: 563-576.
66. Riddle, N.C., Jiang, H., An, L., Doerge, R.W., and Birchler, J.A. (2010). Gene expression analysis at the intersection of ploidy and hybridity in maize. Theor. Appl. Genet. 120: 341-353.
67. Rosado, A., and Raikhel, N.V. (2010). Application of the gene dosage balance hypothesis to auxin-related ribosomal mutants in Arabidopsis. Plant Signal. Behav. 5: 450-452.
68. Schon, C.C., Dhillon, B.S., Utz, H.F., and Melchinger, A.E. (2010). High congruency of QTL positions for heterosis of grain yield in three crosses of maize. Theor. Appl. Genet. 120: 321-332.
69. Schuster-Bockler, B., Conrad, D., and Bateman, A. (2010). Dosage sensitivity shapes the evolution of copy-number varied regions. PLoS ONE 5: e9474.
70. Semel, Y., Nissenbaum, J., Menda, N., Zinder, M., Krieger, U., Issman, N., Pleban, T., Lippman, Z., Gur, A., and Zamir, D. (2006). Overdominant quantitative trait loci for yield and fitness in tomato. Proc. Natl. Acad. Sci. USA 103: 12981-12986.
71. Shull, G.H. (1908). The composition of a field of maize. Am. Breeders Assoc. Rep. 4: 296-301.
72. Sockness, B.A., and Dudley, J.W. (1989a). Performance of single and double cross autotetraploid maize hybrids with different levels of inbreeding. Crop Sci. 29: 875-879.
73. Sockness, B.A., and Dudley, J.W. (1989b). Morphology and yield of isogenic diploid and tetraploid maize inbreds and hybrids. Crop Sci. 29: 1029-1032.
74. Stupar, R.M., Gardiner, J.M., Oldre, A.G., Haun, W.J., Chandler, V.L., and Springer, N.M. (2008). Gene expression analysis in maize hybrids and hybrids with varying levels of heterosis. BMC Plant Biol. 8: 33.
75. Sun, Q.X., Wu, L.M., Ni, Z.F., Meng, F.R., Wang, Z.K., and Lin, Z. (2004). Differential gene expression patterns in leaves between hybrids and their parental inbreds are correlated with heterosis in a wheat diallel cross. Plant Sci. 166: 651-657.
76. Swanson-Wagner, R.A., DeCook, R., Jia, Y., Bancroft, T., Ji, T., Zhao, X., Nettleton, D., and Schnable, P.S. (2009). Paternal dominance of trans-eQTL influences gene expression patterns in maize hybrids. Science 326: 1118-1120.
77. Swanson-Wagner, R.A., Jia, Y., DeCook, R., Borsuk, L.A., Nettleton, D., and Schnable, P.S. (2006). All possible modes of gene action observed in a global comparison of gene expression in a maize F1 hybrid and its inbred parents. Proc. Natl. Acad. Sci. USA 103: 6805-6810.
78. Tanksley S.D. (1993). Mapping polygenes. Annu. Rev. Genet. 27: 205-233.
79. Thiemann, A., Fu, J., Schrag, T.A., Melchinger, A.E., Frisch, M., and Scholten, S. (2010). Correlation between parental transcriptome and field data for the characterization of heterosis in Zea mays L. Theor. Appl. Genet. 120: 401-413.
80. Tirosh, I., Reikhav, S., Levy, A.A., and Barkai, N. (2009). A yeast hybrid provides insight into the evolution of gene expression regulation. Science 324: 659-662.
81. Uzarowska, A., Keller, B., Piepho, H.P., Schwarz, G., Ingvardsen, C., Wenzel, G., and Lubberstedt, T. (2007). Comparative expression profiling in meristems of inbred-hybrid triplets of maize based on morphological investigations of heterosis for plant height. Plant Mol. Biol. 63: 21-34.
82. Van de Peer, Y., Maere, S., and Meyer, A. (2009). The evolutionary significance of ancient genome duplications. Nat. Rev. Genet. 10: 725-732.
83. Veitia, R.A. (2002). Exploring the etiology of haploinsufficiency. Bioessays 24: 175-184.
84. Veitia, R.A. (2010). A generalized model of gene dosage and dominant negative effects inmacromolecular complexes. FASEB J. 24: 994-1002.
85. Veitia, R.A., Bottani, S., and Birchler, J.A. (2008). Cellular reactions to gene dosage imbalance: Genomic, transcriptomic and proteomic effects. Trends Genet. 24: 390-397.
86. Wang, Z., Ni, Z., Wu, H., Nie, X., and Sun, Q. (2006). Heterosis in root development and differential gene expression between hybrids and their parental inbreds in wheat (Triticum aestivum L.). Theor. Appl. Genet. 113: 1283-1294.
87. Wei, G., Tao, Y., Liu, G., Chen, C., Luo, R., Xia, H., Gan, Q., Zeng, H., Lu, Z., Han, Y., Li, X., Song, G., et al. (2009). A transcriptomic analysis of superhybrid rice LYP9 and its parents. Proc. Natl. Acad. Sci. USA 106: 7695-7701.
88. Willis, J.H. (1999). Inbreeding load, average dominance and the mutation rate for mildly deleterious alleles in Mimulus guttatus. Genetics 153: 1885-1898.
89. Wood, T.E., Takebayashi, N., Barker, M.S., Mayrose, I., Greenspoon, P.B., and Rieseberg, L.H. (2009). The frequency of polyploidy speciation in vascular plants. Proc. Natl. Acad. Sci. USA 106: 13875-13879.
90. Zhang, H.-Y., He, H., Chen, L.-B., Li, L., Liang, M.-Z., Wang, X.-F., Liu, X.-G., He, G.-H., Chen, R.-S., Ma, L.-G., and Deng, X.W. (2008). A genome-wide transcription analysis reveals a close correlation of promoter INDEL polymorphism and heterotic gene expression in rice hybrids. Mol. Plant 1: 720-731.
91. Zhuang, Y., and Adams, K.L. (2007). Extensive allelic variation in gene expression in Populus F1 hybrids. Genetics 177: 1987-1996.