5.9
CiteScore
5.9
Impact Factor
Volume 46 Issue 8
Aug.  2019
Turn off MathJax
Article Contents

Progressive heterosis in genetically defined tetraploid maize

doi: 10.1016/j.jgg.2019.02.010
More Information
  • Corresponding author: E-mail address: birchlerj@missouri.edu (James A. Birchler)
  • Received Date: 2018-08-14
  • Accepted Date: 2019-02-20
  • Rev Recd Date: 2019-01-24
  • Available Online: 2019-08-09
  • Publish Date: 2019-08-20
  • Progressive heterosis, i.e., the additional hybrid vigor in double-cross tetraploid hybrids not found in their single-cross tetraploid parents, has been documented in a number of species including alfalfa, potato, and maize. In this study, four artificially induced maize tetraploids, directly derived from standard inbred lines, were crossed in pairs to create two single-cross hybrids. These hybrids were then crossed to create double-cross hybrids containing genetic material from all four original lines. Replicated field-based phenotyping of the materials over four years indicated a strong progressive heterosis phenotype in tetraploids but not in their diploid counterparts. In particular, the above ground dry weight phenotype of double-cross tetraploid hybrids was on average 34% and 56% heavier than that of the single-cross tetraploid hybrids and the double-cross diploid counterparts, respectively. Additionally, whole-genome resequencing of the original inbred lines and further analysis of these data did not show the expected spectrum of alleles to explain tetraploid progressive heterosis under the complementation of complete recessive model. These results underscore the reality of the progressive heterosis phenotype, its potential utility for increasing crop biomass production, and the need for exploring alternative hypothesis to explain it at a molecular level.
  • loading
  • [1]
    Alexander, D.E., Sonnemaker, E.H., 1961. Inbreeding depression in autotetraploid maize. Maize Genetics Cooperation Newsletter 35, 45.
    [2]
    Anderson, L.K., Doyle, G.G., Brigham, B., Carter, J., Hooker, K.D., Lai, A., Rice, M., Stack, S.M., 2003. High-resolution crossover maps for each bivalent of Zea mays using recombination nodules. Genetics 165, 849-865.
    [3]
    Ashby, E., 1932. Studies in the inheritance of physiological characters. II. Further experiments upon the basis of hybrid vigour and upon the inheritance of efficiency index and respiration rate in maize. Ann. Bot. 46, 1007-1032.
    [4]
    Ashby, E., 1930. Studies in the inheritance of physiological characters: I. A physiological Investigation of the nature of hybrid vigour in maize. Ann. Bot. 44, 457-467.
    [5]
    Bauer, E., Falque, M., Walter, H., Bauland, C., Camisan, C., Campo, L., Meyer, N., Ranc, N., Rincent, R., Schipprack, W., Altmann, T., Flament, P., Melchinger, A.E., Menz, M., Moreno-Gonzalez, J., Ouzunova, M., Revilla, P., Charcosset, A., Martin, O.C., Schon, C.-C., 2013. Intraspecific variation of recombination rate in maize. Genome Biol. 14, R103.
    [6]
    Beissinger, T.M., Wang, L., Crosby, K., Durvasula, A., Hufford, M.B., Ross-Ibarra, J., 2016. Recent demography drives changes in linked selection across the maize genome. Nat Plants 2, 16084.
    [7]
    Birchler, J.A., 2013. Genetic rules of heterosis in plants, in: Polyploid and Hybrid Genomics. John Wiley & Sons, Inc., pp. 313-321.
    [8]
    Birchler, J.A., Washburn, J.D., 2016. Polyploidy in maize: The impact of homozygosity and hybridity on phenotype, in: Mason, A.S. (Ed.), Polyploidy and Hybridization for Crop Improvement. CRC Press, Boca Raton.
    [9]
    Birchler, J.A., Yao, H., Chudalayandi, S., Vaiman, D., Veitia, R.A., 2010. Heterosis. Plant Cell 22, 2105-2112.
    [10]
    Bruce, A.B., 1910. The mendelian theory of heredity and the augmentation of vigor. Science 32, 627-628.
    [11]
    Busbice, T., Wilsie, C.P., 1966. Inbreeding depression and heterosis in autotetraploids with application to Medicago sativa L. Euphytica 15, 52-67.
    [12]
    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.
    [13]
    Chun, S., Fay, J.C., 2009. Identification of deleterious mutations within three human genomes. Genome Res. 19, 1553-1561.
    [14]
    Cingolani, P., Patel, V.M., Coon, M., Nguyen, T., Land, S.J., Ruden, D.M., Lu, X., 2012a. Using Drosophila melanogaster as a model for genotoxic chemical mutational studies with a new program, SnpSift. Front. Genet. 3. https://doi.org/10.3389/fgene.2012.00035
    [15]
    Cingolani, P., Platts, A., Wang, L.L., Coon, M., Nguyen, T., Wang, L., Land, S.J., Lu, X., Ruden, D.M., 2012b. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 6, 80-92.
    [16]
    Crow, J.F., 1998. 90 Years Ago: The Beginning of Hybrid Maize. Genetics 148, 923-928.
    [17]
    Darwin, C., 1876. The effects of cross and self fertilisation in the vegetable kingdom. John Murray.
    [18]
    Demarly, Y., 1963. Genetique des tetraploids et amelioration des plants. Annales de l’amelioration des plantes 13, 307-400.
    [19]
    Dunbier, M.W., Bingham, E.T., 1975. Maximum heterozygosity in Alfalfa: Results using haploid-derived autoteraploids. Crop Sci.
    [20]
    Duvick, D.N., 2001. Biotechnology in the 1930s: the development of hybrid maize. Nat. Rev. Genet. 2, 69-74.
    [21]
    Duvick, D.N., 1999. Heterosis: Feeding people and protecting natural resources, in: Coors, J.G., Pandey, S. (Eds.), The Genetics and Exploitation of Heterosis in Crops. American Society of Agronomy, Crop Science Society of America, Madison, WI, pp. 19-29.
    [22]
    East, E.M., 1936. Heterosis. Genetics 21, 375-397.
    [23]
    Gallais, A., 1984. An analysis of heterosis vs. inbreeding effects with an autotetraploid cross-fertilized plant: Medicago sativa L. Genetics 106, 123-137.
    [24]
    Gan, X., Stegle, O., Behr, J., Steffen, J.G., Drewe, P., Hildebrand, K.L., Lyngsoe, R., Schultheiss, S.J., Osborne, E.J., Sreedharan, V.T., Kahles, A., Bohnert, R., Jean, G., Derwent, P., Kersey, P., Belfield, E.J., Harberd, N.P., Kemen, E., Toomajian, C., Kover, P.X., Clark, R.M., Ratsch, G., Mott, R., 2011. Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature 477, 419-423.
    [25]
    Gerke, J.P., Edwards, J.W., Guill, K.E., Ross-Ibarra, J., McMullen, M.D., 2015. The Genomic Impacts of Drift and Selection for Hybrid Performance in Maize. Genetics 201, 1201-1211.
    [26]
    Greaves, I.K., Eichten, S.R., Groszmann, M., Wang, A., Ying, H., Peacock, W.J., Dennis, E.S., 2016. Twenty-four-nucleotide siRNAs produce heritable trans-chromosomal methylation in F1 Arabidopsis hybrids. Proc. Natl. Acad. Sci. U. S. A. 113, E6895-E6902.
    [27]
    Greaves, I.K., Groszmann, M., Ying, H., Taylor, J.M., Peacock, W.J., Dennis, E.S., 2012. Trans chromosomal methylation in Arabidopsis hybrids. Proceedings of the National Academy of Sciences 109, 3570-3575.
    [28]
    Groose, R.W., Talbert, L.E., Kojis, W.P., Bingham, E.T., 1989. Progressive heterosis in autotetraploid Alfalfa: Studies using two types of inbreds. Crop Sci. 29, 1173-1177.
    [29]
    Groszmann, M., Gonzalez-Bayon, R., Lyons, R.L., Greaves, I.K., Kazan, K., Peacock, W.J., Dennis, E.S., 2015. Hormone-regulated defense and stress response networks contribute to heterosis in Arabidopsis F1 hybrids. Proc. Natl. Acad. Sci. U. S. A. 112, E6397-E6406.
    [30]
    Herbst, R.H., Bar-Zvi, D., Reikhav, S., Soifer, I., Breker, M., Jona, G., Shimoni, E., Schuldiner, M., Levy, A.A., Barkai, N., 2017. Heterosis as a consequence of regulatory incompatibility. BMC Biol. 15. https://doi.org/10.1186/s12915-017-0373-7
    [31]
    Hirsch, C.N., Hirsch, C.D., Brohammer, A.B., Bowman, M.J., Soifer, I., Barad, O., Shem-Tov, D., Baruch, K., Lu, F., Hernandez, A.G., Fields, C.J., Wright, C.L., Koehler, K., Springer, N.M., Buckler, E., Buell, C.R., de Leon, N., Kaeppler, S.M., Childs, K.L., Mikel, M.A., 2016. Draft Assembly of Elite Inbred Line PH207 Provides Insights into Genomic and Transcriptome Diversity in Maize. Plant Cell 28, 2700-2714.
    [32]
    Jiao, Y., Peluso, P., Shi, J., Liang, T., Stitzer, M.C., Wang, B., Campbell, M.S., Stein, J.C., Wei, X., Chin, C.-S., Guill, K., Regulski, M., Kumari, S., Olson, A., Gent, J., Schneider, K.L., Wolfgruber, T.K., May, M.R., Springer, N.M., Antoniou, E., McCombie, W.R., Presting, G.G., McMullen, M., Ross-Ibarra, J., Dawe, R.K., Hastie, A., Rank, D.R., Ware, D., 2017. Improved maize reference genome with single-molecule technologies. Nature 546, 524-527.
    [33]
    Jones, D.F., 1917. Dominance of linked factors as a means of accounting for heterosis. Genetics 2, 466-479.
    [34]
    Kato, A., Birchler, J.A., 2006. Induction of tetraploid derivatives of maize inbred lines by nitrous oxide gas treatment. J. Hered. 97, 39-44.
    [35]
    Kawanabe, T., Ishikura, S., Miyaji, N., Sasaki, T., Wu, L.M., Itabashi, E., Takada, S., Shimizu, M., Takasaki-Yasuda, T., Osabe, K., Peacock, W.J., Dennis, E.S., Fujimoto, R., 2016. Role of DNA methylation in hybrid vigor in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U. S. A. 113, E6704-E6711.
    [36]
    Keeble, F., Pellew, C., 1910. The mode of inheritance of stature and of time of flowering in peas (Pisum sativum). J. Genet. 1, 47-56.
    [37]
    Kono, T.J.Y., Fu, F., Mohammadi, M., Hoffman, P.J., Liu, C., Stupar, R.M., Smith, K.P., Tiffin, P., Fay, J.C., Morrell, P.L., 2016. The role of deleterious substitutions in crop genomes. Mol. Biol. Evol. 33, 2307-2317.
    [38]
    Kono, T.J.Y., Lei, L., Shih, C.-H., Hoffman, P.J., Morrell, P.L., Fay, J.C., 2017. Comparative genomics approaches accurately predict deleterious variants in plants. https://doi.org/10.1101/112318
    [39]
    Kremling, K.A.G., Chen, S.-Y., Su, M.-H., Lepak, N.K., Romay, M.C., Swarts, K.L., Lu, F., Lorant, A., Bradbury, P.J., Buckler, E.S., 2018. Dysregulation of expression correlates with rare-allele burden and fitness loss in maize. Nature 555, 520-523.
    [40]
    Levings, C.S., Dudley, J.W., Alexander, D.E., 1967. Inbreeding and crossing in autotetraploid maize. Crop Sci. 7, 72-73.
    [41]
    Li, H., Durbin, R., 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760.
    [42]
    McCormick, R.F., Truong, S.K., Sreedasyam, A., Jenkins, J., Shu, S., Sims, D., Kennedy, M., Amirebrahimi, M., Weers, B.D., McKinley, B., Mattison, A., Morishige, D.T., Grimwood, J., Schmutz, J., Mullet, J.E., 2018. The Sorghum bicolor reference genome: improved assembly, gene annotations, a transcriptome atlas, and signatures of genome organization. Plant J. 93, 338-354.
    [43]
    Mezmouk, S., Ross-Ibarra, J., 2014. The Pattern and Distribution of Deleterious Mutations in Maize. G3: Genes|Genomes|Genetics 4, 163-171.
    [44]
    Mok, D.W.S., Peloquin, S.J., 1975. Breeding value of 2n pollen (diplandroids) in tetraploid x diploid crosses in potatoes. Theor. Appl. Genet. 46, 307-314.
    [45]
    Ramu, P., Esuma, W., Kawuki, R., Rabbi, I.Y., Egesi, C., Bredeson, J.V., Bart, R.S., Verma, J., Buckler, E.S., Lu, F., 2017. Cassava haplotype map highlights fixation of deleterious mutations during clonal propagation. Nat. Genet. 49, 959-963.
    [46]
    Rice, J.S., Dudley, J.W., 1974. Gene effects responsible for inbreeding depression in autotetraploid maize. Crop Sci. 14, 390-393.
    [47]
    Riddle, N., Birchler, J., 2008. Comparative analysis of inbred and hybrid maize at the diploid and tetraploid levels. Theor. Appl. Genet. 116, 563.
    [48]
    Riddle, N.C., Jiang, H., An, L., Doerge, R.W., Birchler, J.A., 2010. Gene expression analysis at the intersection of ploidy and hybridity in maize. Theor. Appl. Genet. 120, 341-353.
    [49]
    Rodgers-Melnick, E., Bradbury, P.J., Elshire, R.J., Glaubitz, J.C., Acharya, C.B., Mitchell, S.E., Li, C., Li, Y., Buckler, E.S., 2015. Recombination in diverse maize is stable, predictable, and associated with genetic load. Proc. Natl. Acad. Sci. U. S. A. 112, 3823-3828.
    [50]
    Rodgers-Melnick, E., Vera, D.L., Bass, H.W., Buckler, E.S., 2016. Open chromatin reveals the functional maize genome. Proc. Natl. Acad. Sci. U. S. A. 113, E3177-E3184.
    [51]
    Shull, G.H., 1948. What is “heterosis”? Genetics 33, 439-446.
    [52]
    Shull, G.H., 1911. The genotypes of maize. Am. Nat. 45, 234-252.
    [53]
    Shull, G.H., 1909. A pure line method of corn breeding. J. Hered. os-5, 51-59.
    [54]
    Shull, G.H., 1908. The composition of a field of maize. J. Hered. os-4, 296-301.
    [55]
    Sockness, B.A., Dudley, J.W., 1989a. Morphology and yield of isogenic diploid and tetraploid maize inbreds and hybrids. Crop Sci. 29, 1029-1032.
    [56]
    Sockness, B.A., Dudley, J.W., 1989b. Performance of single and double cross autotetraploid maize hybrids with different levels of Inbreeding. Crop Sci. 29, 875-879.
    [57]
    Troyer, A.F., 2006. Adaptedness and heterosis in Corn and Mule hybrids. Crop Sci. 46, 528-543.
    [58]
    Troyer, A.F., Wellin, E.J., 2009. Heterosis decreasing in hybrids: Yield test inbreds. Crop Sci. 49, 1969-1976.
    [59]
    Tysdal, H.M., Kiesselbach, T.A., Westover, H.L., 1942. Alfalfa breeding. Nebraska Agric Exp Stn Res Bull 124.
    [60]
    Wang, L., Greaves, I.K., Groszmann, M., Wu, L.M., Dennis, E.S., Peacock, W.J., 2015. Hybrid mimics and hybrid vigor in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 112, E4959-E4967.
    [61]
    Wang, L., Wu, L.M., Greaves, I.K., Zhu, A., Dennis, E.S., James Peacock, W., 2017. PIF4-controlled auxin pathway contributes to hybrid vigor in Arabidopsis thaliana. Proceedings of the National Academy of Sciences 114, E3555-E3562.
    [62]
    Washburn, J.D., Birchler, J.A., 2014. Polyploids as a “model system” for the study of heterosis. Plant Reprod. 27, 1-5.
    [63]
    Washburn, J.D., Schnable, J.C., Davidse, G., Pires, J.C., 2015. Phylogeny and photosynthesis of the grass tribe Paniceae. Am. J. Bot. 102, 1493-1505.
    [64]
    Williams, R.D., 1931. Self- and cross-fertility and flowering habits of certain herbage grasses and legumes. Welsh Plant Breeding Station Bulletin Series H 12, 217-220.
    [65]
    Wu, T.D., Nacu, S., 2010. Fast and SNP-tolerant detection of complex variants and splicing in short reads. Bioinformatics 26, 873-881.
    [66]
    Wu, T.D., Reeder, J., Lawrence, M., Becker, G., Brauer, M.J., 2016. GMAP and GSNAP for genomic sequence alignment: Enhancements to speed, accuracy, and functionality. Methods Mol. Biol. 1418, 283-334.
    [67]
    Xu, C., Ren, Y., Jian, Y., Guo, Z., Zhang, Y., Xie, C., Fu, J., Wang, H., Wang, G., Xu, Y., Li, P., Zou, C., 2017. Development of a maize 55 K SNP array with improved genome coverage for molecular breeding. Mol. Breed. 37, 20.
    [68]
    Yang, J., Mezmouk, S., Baumgarten, A., Buckler, E.S., Guill, K.E., McMullen, M.D., Mumm, R.H., Ross-Ibarra, J., 2017. Incomplete dominance of deleterious alleles contributes substantially to trait variation and heterosis in maize. PLoS Genet. 13, e1007019.
    [69]
    Yao, H., Dogra Gray, A., Auger, D.L., Birchler, J.A., 2013. Genomic dosage effects on heterosis in triploid maize. Proc. Natl. Acad. Sci. U. S. A. 110, 2665-2669.
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Article Metrics

    Article views (174) PDF downloads (5) Cited by ()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return