Magnitude of modulation of gene expression in aneuploid maize depends on the extent of genomic imbalance

Adam F. Johnson; Jie Hou; Hua Yang; Xiaowen Shi; Chen Chen; Md Soliman Islam; Tieming Ji; Jianlin Cheng; James A. Birchler

doi:10.1016/j.jgg.2020.02.002

Volume 47 Issue 2

Feb. 2020

Turn off MathJax

Article Contents

Article Navigation > Journal of Genetics and Genomics > 2020 > 47(2): 93-103

PDF( 4037 KB)

Magnitude of modulation of gene expression in aneuploid maize depends on the extent of genomic imbalance

doi: 10.1016/j.jgg.2020.02.002

a
Institute of Research and Development, Duy Tan University, Da Nang, 550000, Viet Nam
b
Department of Electrical Engineering and Computer Science, University of Missouri, Columbia, MO, 65211, USA
c
Division of Biological Sciences, University of Missouri, Columbia, MO, 65211, USA
d
Department of Statistics, University of Missouri, Columbia, MO, 65211, USA

More Information

Corresponding author: E-mail address: birchlerJ@missouri.edu (James A. Birchler)
Publish Date: 2020-02-25

Abstract

Abstract

Aneuploidy has profound effects on an organism, typically more so than polyploidy, and the basis of this contrast is not fully understood. A dosage series of the maize long arm of chromosome 1 (1L) was used to compare relative global gene expression in different types and degrees of aneuploidy to gain insights into how the magnitude of genomic imbalance as well as hypoploidy affects global gene expression. While previously available methods require a selective examination of specific genes, RNA sequencing provides a whole-genome view of gene expression in aneuploids. Most studies of global aneuploidy effects have concentrated on individual types of aneuploids because multiple dose aneuploidies of the same genomic region are difficult to produce in most model genetic organisms. The genetic toolkit of maize allows the examination of multiple ploidies and 1–4 doses of chromosome arms. Thus, a detailed examination of expression changes both on the varied chromosome arms and elsewhere in the genome is possible, in both hypoploids and hyperploids, compared with euploid controls. Previous studies observed the inverse trans effect, in which genes not varied in DNA dosage were expressed in a negative relationship to the varied chromosomal region. This response was also the major type of changes found globally in this study. Many genes varied in dosage showed proportional expression changes, though some were seen to be partly or fully dosage compensated. It was also found that the effects of aneuploidy were progressive, with more severe aneuploids producing effects of greater magnitude.
- Aneuploidy,
- Polyploidy,
- Inverse effect,
- Gene regulation,
- Dosage compensation,
- Gene balance hypothesis

FullText(HTML)

References(42)

References

[1]	Albert, P.S., Gao, Z., Danilova, T.V., Birchler, J.A., 2010. Diversity of chromosomal karyotypes in maize and its relatives. Cytogenet. Genome Res. 129, 6-16.
[2]	Andorf, C.M., Cannon, E.K., Portwood, J.L., Gardiner, J.M., Harper, L.C., Schaeffer, M.L., Braun, B.L., Campbell, D.A., Vinnakota, A.G., Sribalusu, V.V., Huerta, M., Cho, K.T., Wimalanathan, K., Richter, J.D., Mauch, E.D., Rao, B.S., Birkett, S.M., Sen, T.Z., Lawrence-Dill, C.J., 2016. MaizeGDB update: new tools, data and interface for the maize model organism database. Nucleic Acids Res. 44, D1195-D1201.
[3]	Bastiaanse, H., Zinkgraf, M., Canning, C., Tsai, H., Lieberman, M., Comai, L., Henry, I., Groover, A., 2019. A comprehensive genomic scan reveals gene dosage balance impacts on quantitative traits in Populus trees. Proc. Natl. Acad. Sci. U. S. A. 116, 13690-13699.
[4]	Bentley, D.R., Balasubramanian, S., Swerdlow, H.P., Smith, G.P., Milton, J., Brown, C.G., Hall, K.P., Evers, D.J., Barnes, C.L., Bignell, H.R., Boutell, J.M., Bryant, J., Carter, R.J., Keira Cheetham, R., Cox, A.J., Ellis, D.J., Flatbush, M.R., Gormley, N.A., Humphray, S.J., Irving, L.J., Karbelashvili, M.S., Kirk, S.M., Li, H., Liu, X., Maisinger, K.S., Murray, L.J., Obradovic, B., Ost, T., Parkinson, M.L., Pratt, M.R., Rasolonjatovo, I.M.J., Reed, M.T., Rigatti, R., Rodighiero, C., Ross, M.T., Sabot, A., Sankar, S.V., Scally, A., Schroth, G.P., Smith, M.E., Smith, V.P., Spiridou, A., Torrance, P.E., Tzonev, S.S., Vermaas, E.H., Walter, K., Wu, X., Zhang, L., Alam, M.D., Anastasi, C., Aniebo, I.C., Bailey, D.M.D., Bancarz, I.R., Banerjee, S., Barbour, S.G., Baybayan, P.A., Benoit, V.A., Benson, K.F., Bevis, C., Black, P.J., Boodhun, A., Brennan, J.S., Bridgham, J.A., Brown, R.C., Brown, A.A., Buermann, D.H., Bundu, A.A., Burrows, J.C., Carter, N.P., Castillo, N., Chiara E Catenazzi, M., Chang, S., Neil Cooley, R., Crake, N.R., Dada, O.O., Diakoumakos, K.D., Dominguez-Fernandez, B., Earnshaw, D.J., Egbujor, U.C., Elmore, D.W., Etchin, S.S., Ewan, M.R., Fedurco, M., Fraser, L.J., Fuentes Fajardo, K.V., Scott Furey, W., George, D., Gietzen, K.J., Goddard, C.P., Golda, G.S., Granieri, P.A., Green, D.E., Gustafson, D.L., Hansen, N.F., Harnish, K., Haudenschild, C.D., Heyer, N.I., Hims, M.M., Ho, J.T., Horgan, A.M., Hoschler, K., Hurwitz, S., Ivanov, D.V., Johnson, M.Q., James, T., Huw Jones, T.A., Kang, G.-D., Kerelska, T.H., Kersey, A.D., Khrebtukova, I., Kindwall, A.P., Kingsbury, Z., Kokko-Gonzales, P.I., Kumar, A., Laurent, M.A., Lawley, C.T., Lee, S.E., Lee, X., Liao, A.K., Loch, J.A., Lok, M., Luo, S., Mammen, R.M., Martin, J.W., McCauley, P.G., McNitt, P., Mehta, P., Moon, K.W., Mullens, J.W., Newington, T., Ning, Z., Ling Ng, B., Novo, S.M., O’Neill, M.J., Osborne, M.A., Osnowski, A., Ostadan, O., Paraschos, L.L., Pickering, L., Pike, Andrew C., Pike, Alger C., Chris Pinkard, D., Pliskin, D.P., Podhasky, J., Quijano, V.J., Raczy, C., Rae, V.H., Rawlings, S.R., Chiva Rodriguez, A., Roe, P.M., Rogers, John, Rogert Bacigalupo, M.C., Romanov, N., Romieu, A., Roth, R.K., Rourke, N.J., Ruediger, S.T., Rusman, E., Sanches-Kuiper, R.M., Schenker, M.R., Seoane, J.M., Shaw, R.J., Shiver, M.K., Short, S.W., Sizto, N.L., Sluis, J.P., Smith, M.A., Ernest Sohna Sohna, J., Spence, E.J., Stevens, K., Sutton, N., Szajkowski, L., Tregidgo, C.L., Turcatti, G., Vandevondele, S., Verhovsky, Y., Virk, S.M., Wakelin, S., Walcott, G.C., Wang, J., Worsley, G.J., Yan, J., Yau, L., Zuerlein, M., Rogers, Jane, Mullikin, J.C., Hurles, M.E., McCooke, N.J., West, J.S., Oaks, F.L., Lundberg, P.L., Klenerman, D., Durbin, R., Smith, A.J., 2008. Accurate whole human genome sequencing using reversible terminator chemistry. Nature 456, 53-59.
[5]	Birchler, J.A., 2014. Facts and artifacts in studies of gene expression in aneuploids and sex chromosomes. Chromosoma 123, 459-469.
[6]	Birchler, J.A., 1981. The genetic basis of dosage compensation of alcohol dehydrogenase-1 in maize. Genetics 97, 625-637.
[7]	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.
[8]	Birchler, J.A., Alfenito, M.R., 1993. Marker systems for B-A translocations in maize. J. Heredity 84, 135-138.
[9]	Birchler, J.A., Bhadra, U., Bhadra, M.P., 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.
[10]	Birchler, J.A., Johnson, A.F., Veitia, R.A., 2016. Kinetics genetics: Incorporating the concept of genomic balance into an understanding of quantitative traits. Plant Sci. 245, 128-134.
[11]	Birchler, J.A., Newton, K.J., 1981. Modulation of protein levels in chromosomal dosage series of maize: the biochemical basis of aneuploid syndromes. Genetics 99, 247-266.
[12]	Birchler, J.A., Riddle, N.C., Auger, D.L., Veitia, R.A., 2005. Dosage balance in gene regulation: biological implications. Trends Genet. 21, 219-226.
[13]	Birchler, J.A., Veitia, R.A., 2012. Gene balance hypothesis: connecting issues of dosage sensitivity across biological disciplines. Proc. Natl. Acad. Sci. U. S. A. 109, 14746-14753.
[14]	Birchler, J.A., Veitia, R.A., 2007. The gene balance hypothesis: from classical genetics to modern genomics. Plant Cell 19, 395-402.
[15]	Blakeslee, A.F., 1921. Types of mutations and their possible significance in evolution. Am. Nat. 55, 254-267.
[16]	Brunelle, D.C., Sheridan, W.F., 2014. The effects of varying chromosome arm dosage on maize plant morphogenesis. Genetics 198, 171-180.
[17]	Guo, M., Birchler, J.A., 1994. Trans-acting dosage effects on the expression of model gene systems in maize aneuploids. Science 266, 1999-2002.
[18]	Hooper, C.M., Castleden, I.R., Aryamanesh, N., Jacoby, R.P., Millar, A.H., 2016. Finding the subcellular location of barley, wheat, rice and maize proteins: the compendium of crop Proteins with Annotated Locations (cropPAL). Plant Cell Physiol. 57, e9.
[19]	Hou, J., Shi, X., Chen, C., Islam, M.S., Johnson, A.F., Kanno, T., Huettel, B., Yen, M.-R., Hsu, F.-M., Ji, T., Chen, P.-Y., Matzke, M., Matzke, A.J.M., Cheng, J., Birchler, J.A., 2018. Global impacts of chromosomal imbalance on gene expression in Arabidopsis and other taxa. Proc. Natl. Acad. Sci. U. S. A. 115, E11321-E11330.
[20]	Jin, J., Tian, F., Yang, D.-C., Meng, Y.-Q., Kong, L., Luo, J., Gao, G., 2017. PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res. 45, D1040-D1045.
[21]	Kato, A., Lamb, J.C., Birchler, J.A., 2004. Chromosome painting using repetitive DNA sequences as probes for somatic chromosome identification in maize. Proc. Natl. Acad. Sci. U. S. A. 101, 13554-13559.
[22]	Langmead, B., Trapnell, C., Pop, M., Salzberg, S.L., 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25.
[23]	Lee, E.A., Coe, E.H., Darrah, L.L., 1996a. Genetic variation in dosage effects in maize aneuploids. Genome 39, 711-721.
[24]	Lee, E.A., Darrah, L.L., Coe, E.H., 1996b. Dosage effects on morphological and quantitative traits in maize aneuploids. Genome 39, 898-908.
[25]	Li, J., Hou, J., Sun, L., Wilkins, J.M., Lu, Y., Niederhuth, C.E., Merideth, B.R., Mawhinney, T.P., Mossine, V.V., Greenlief, C.M., Walker, J.C., Folk, W.R., Hannink, M., Lubahn, D.B., Birchler, J.A., Cheng, J., 2015. From gigabyte to kilobyte: A bioinformatics protocol for mining large RNA-Seq transcriptomics data. PLoS ONE 10, e0125000.
[26]	Lindsley, D.L., Sandler, L., Baker, B.S., Carpenter, A.T., Denell, R.E., Hall, J.C., Jacobs, P.A., Miklos, G.L., Davis, B.K., Gethmann, R.C., Hardy, R.W., Steven, A.H., Miller, M., Nozawa, H., Parry, D.M., Gould-Somero, M., Gould-Somero, M., 1972. Segmental aneuploidy and the genetic gross structure of the Drosophila genome. Genetics 71, 157-184.
[27]	Livak, K.J., Schmittgen, T.D., 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402-408.
[28]	Rabinow, L., Nguyen-Huynh, A.T., Birchler, J.A., 1991. A trans-acting regulatory gene that inversely affects the expression of the white, brown and scarlet loci in Drosophila. Genetics 129, 463-480.
[29]	Randolph, L.F., 1941. Genetic characteristics of the B chromosomes in maize. Genetics 26, 608-631.
[30]	Rio, D.C., Ares, M., Hannon, G.J., Nilsen, T.W., 2010. Purification of RNA using TRIzol (TRI reagent). Cold Spring Harb. Protoc. 2010, pdb.prot5439.
[31]	Rober, F.K., Gordillo, G.A., Geiger, H.H., 2005. In vivo haploid induction in maize - Performance of new inducers and significance of doubled haploid lines in hybrid breeding. Maydica 50, 275-283.
[32]	Robinson, M.D., McCarthy, D.J., Smyth, G.K., 2010. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139-140.
[33]	Roman, H., 1948. Directed fertilization in maize. Proc. Natl. Acad. Sci. U. S. A. 34, 36-42.
[34]	Roman, H., 1947. Mitotic nondisjunction in the case of interchanges involving the B-type chromosome in maize. Genetics 32, 391-409.
[35]	Schinzel, A., 2001. Catalogue of unbalanced chromosome aberrations in man. 2nd rev. and expanded ed.. Walter de Gruyter, Berlin ; New York.
[36]	Sheridan, W.F., Auger, D.L., 2008. Chromosome segmental dosage analysis of maize morphogenesis using B-A-A translocations. Genetics 180, 755-769.
[37]	Springer, N.M., Anderson, S.N., Andorf, C.M., Ahern, K.R., Bai, F., Barad, O., Barbazuk, W.B., Bass, H.W., Baruch, K., Ben-Zvi, G., Buckler, E.S., Bukowski, R., Campbell, M.S., Cannon, E.K.S., Chomet, P., Dawe, R.K., Davenport, R., Dooner, H.K., Du, L.H., Du, C., Easterling, K.A., Gault, C., Guan, J.-C., Hunter, C.T., Jander, G., Jiao, Y., Koch, K.E., Kol, G., Kollner, T.G., Kudo, T., Li, Q., Lu, F., Mayfield-Jones, D., Mei, W., McCarty, D.R., Noshay, J.M., Portwood, J.L., Ronen, G., Settles, A.M., Shem-Tov, D., Shi, J., Soifer, I., Stein, J.C., Stitzer, M.C., Suzuki, M., Vera, D.L., Vollbrecht, E., Vrebalov, J.T., Ware, D., Wei, S., Wimalanathan, K., Woodhouse, M.R., Xiong, W., Brutnell, T.P., 2018. The maize W22 genome provides a foundation for functional genomics and transposon biology. Nat. Genet. 50, 1282-1288.
[38]	Sun, L., Johnson, A.F., Donohue, R.C., Li, J., Cheng, J., Birchler, J.A., 2013a. Dosage compensation and inverse effects in triple X metafemales of Drosophila. Proc. Natl. Acad. Sci. U. S. A. 110, 7383-7388..
[39]	Sun, L., Johnson, A.F., Li, J., Lambdin, A.S., Cheng, J., Birchler, J.A., 2013b. Differential effect of aneuploidy on the X chromosome and genes with sex-biased expression in Drosophila. Proc. Natl. Acad. Sci. U. S. A. 110, 16514-16519.
[40]	Trapnell, C., Pachter, L., Salzberg, S.L., 2009. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105-1111.
[41]	Wang, Z., Cao, R., Cheng, J., 2013. Three-level prediction of protein function by combining profile-sequence search, profile-profile search, and domain co-occurrence networks. BMC Bioinformatics 14 Suppl 3, S3.
[42]	Zuo, T., Zhang, J., Lithio, A., Dash, S., Weber, D.F., Wise, R., Nettleton, D., Peterson, T., 2016. Genes and small RNA transcripts exhibit dosage-dependent expression pattern in maize copy-number alterations. Genetics 203, 1133-1147.