Specific changes in total and mitochondrial proteomes are associated with higher levels of heterosis in maize hybrids

Plant Journal

Volumn 72, Issue 1, 2012, Pages 70-83

  Dahal, Diwakar ^a   Mooney, Brian P ^a,b   Newton, Kathleen J ^a  

^a UNIVERSITY OF MISSOURI   (United States)

^b University of Missouri   (United States)

Author keywords

2D DIGE; heterosis; label free MS; mitochondria; proteomics; Zeamays

Indexed keywords

2D DIGE; HETEROSIS; LABEL FREE; PROTEOMICS; ZEAMAYS;

ELECTROPHORESIS; MASS SPECTROMETRY; MITOCHONDRIA; MOLECULAR BIOLOGY; PROTEINS;

PLANTS (BOTANY);

ISOPROTEIN; MITOCHONDRIAL PROTEIN; PROTEOME; VEGETABLE PROTEIN;

ALLELE; ARTICLE; GENE EXPRESSION REGULATION; GENETICS; HETEROSIS; HYBRIDIZATION; MAIZE; MASS SPECTROMETRY; METABOLISM; MITOCHONDRION; PLANT; PROTEOMICS; TWO DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS;

ALLELES; GENE EXPRESSION REGULATION, PLANT; HYBRID VIGOR; HYBRIDIZATION, GENETIC; MASS SPECTROMETRY; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; PLANT PROTEINS; PLANT SHOOTS; PROTEIN ISOFORMS; PROTEOME; PROTEOMICS; TWO-DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS; ZEA MAYS;

ZEA MAYS;

EID: 84866731643     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2012.05056.x     Document Type: Article

References (72)

1. 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.
2. Bao, J., Lee, S., Chen, C., et al. (2005) Serial analysis of gene expression study of a hybrid rice strain (LYP9) and its parental cultivars. Plant Physiol. 138, 1216-1231.
3. Birchler, J.A., Auger, D.L., and, Riddle, N.C., (2003) In search of the molecular basis of heterosis. Plant Cell, 15, 2236-2239.
4. Birchler, J.A., Yao, H., Chudalayandi, S., Vaiman, D., and, Veitia, R.A., (2010) Heterosis. Plant Cell, 22, 2105-2112.
5. Brunner, S., Fengler, K., Morgante, M., Tingey, S., and, Rafalski, A., (2005) Evolution of DNA sequence nonhomologies among maize inbreds. Plant Cell, 17, 343-360.
6. Bykova, N.V., Stensballe, A., Egsgaard, H., Jensen, O.N., and, Moller, I.M., (2003) Phosphorylation of formate dehydrogenase in potato tuber mitochondria. J. Biol. Chem. 278, 26021-26030.
7. Candela, H., and, Hake, S., (2008) The art and design of genetic screens: maize. Nat. Rev. Genet. 9, 192-203.
8. Chen, Z.J., (2010) Molecular mechanisms of polyploidy and hybrid vigor. Trends Plant Sci. 15, 57-71.
9. Cooper, P., Butler, E., and, Newton, K.J., (1990) Identification of a maize nuclear gene which influences the size and number of cox2 transcripts in mitochondria of perennial teosintes. Genetics, 126, 461-467.
10. Dooki, A.D., Mayer-Posner, F.J., Askari, H., Zaiee, A.A., and, Salekdeh, G.H., (2006) Proteomic responses of rice young panicles to salinity. Proteomics, 6, 6498-6507.
11. Duvick, D.N., (1999) Heterosis: feeding people and protecting natural resources. In The Genetics and Exploitation of Heterosis in Crops (, Coors, J.G., and, Pandey, S., eds). Wisconsin: American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America, pp. 19-29.
12. Duvick, D.N., (2001) Biotechnology in the 1930s: the development of hybrid maize. Nat. Rev. Genet. 2, 69-74.
13. El-Hafid, L., Pham, A.T., Zuily-fodil, Y., and, da Silva, J.V., (1989) Enzymatic breakdown of polar lipids in cotton leaves under water stress. I. Degradation of monogalactosyl-diacylglycerol. Plant Physiol. Biochem. 27, 495-502.
14. Eprintsev, A.T., Fedorin, D.N., Selivanova, N.V., Akhmad, G.A., and, Popov, V.N., (2010) Role of differential expression of sdh1-1 and sdh1-2 genes in alteration of isoenzyme composition of succinate dehydrogenase in germinating maize seeds. Biology Bulletin 37, 268-276.
15. Flint-Garcia, S.A., Thuillet, A.C., Yu, J., Pressoir, G., Romero, S.M., Mitchell, S.E., Doebley, J., Kresovich, S., Goodman, M.M., and, Buckler, E.S., (2005) Maize association population: a high-resolution platform for quantitative trait locus dissection. Plant J. 44, 1054-1064.
16. 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.
17. 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 analyses of heterosis in a maize hybrid between two elite inbred lines. Genetics, 176, 625-644.
18. 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.
19. Fu, Z., Jin, X., Ding, D., Li, Y., and, Tang, J., (2011) Proteomic analysis of heterosis during maize seed germination. Proteomics, 11, 1462-1472.
20. Gaut, B.S., and, Doebley, J.F., (1997) DNA sequence evidence for the segmental allotetraploid origin of maize. Proc. Natl Acad. Sci. USA, 94, 6809-6814.
21. Gibson, G., and, Weir, B., (2005) The quantitative genetics of transcription. Trends Genet. 21, 616-623.
22. Gill, S.S., and, Tuteja, N., (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48, 909-930.
23. Goff, S.A., (2011) A unifying theory for general multigenic heterosis: energy efficiency, protein metabolism, and implications for molecular breeding. New Phytol. 189, 923-937.
24. Guo, M., Rupe, M.A., Zinselmeier, C., Habben, J., Bowen, B.A., and, Smith, O.S., (2004) Allelic variation of gene expression in maize hybrids. Plant Cell, 16, 1707-1716.
25. 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 cis- and trans-effects on gene expression in maize hybrid meristem tissue. Plant Mol. Biol. 66, 551-563.
26. Gygi, S.P., Rochon, Y., Franza, B.R., and, Aebersold, R., (1999) Correlation between protein and mRNA abundance in yeast. Mol. Cell. Biol. 19, 1720-1730.
27. He, G., Zhu, X., Elling, A.A., et al. (2010) Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids. Plant Cell, 22, 17-33.
28. Hoecker, N., Keller, B., Piepho, H.P., and, Hochholdinger, F., (2006) Manifestation of heterosis during early maize (Zea mays L.) root development. Theor. Appl. Genet. 112, 421-429.
29. Hourton-Cabassa, C., Ambard-Bretteville, F., Moreau, F., Davy de Virville, J., Remy, R., and, Francs-Small, C.C., (1998) Stress induction of mitochondrial formate dehydrogenase in potato leaves. Plant Physiol. 116, 627-635.
30. Huang, S., Taylor, N.L., Narsai, R., Eubel, H., Whelan, J., and, Millar, A.H., (2010) Functional and composition differences between mitochondrial complex II in Arabidopsis and rice are correlated with the complex genetic history of the enzyme. Plant Mol. Biol. 72, 331-342.
31. Hurkman, W.J., and, Tanaka, C.K., (1986) Solubilization of plant membrane proteins for analysis by two-dimensional electrophoresis. Plant Physiol. 81, 802-806.
32. 1 embryo and endosperm tissues 6 days after fertilization. Theor. Appl. Genet. 120, 389-400.
33. Ke, Y., Han, G., He, H., and, Li, J., (2009) Differential regulation of proteins and phosphoproteins in rice under drought stress. Biochem. Biophys. Res. Commun. 379, 133-138.
34. Kim, J.S., Jung, H.J., Lee, H.J., Kim, K.A., Goh, C.H., Woo, Y., Oh, S.H., Han, Y.S., and, Kang, H., (2008) Glycine-rich RNA-binding protein 7 affects abiotic stress responses by regulating stomata opening and closing in Arabidopsis thaliana. Plant J. 55, 455-466.
35. Krieger, U., Lippman, Z.B., and, Zamir, D., (2010) The flowering gene SINGLE FLOWER TRUSS drives heterosis for yield in tomato. Nat. Genet. 42, 459-463.
36. Laxalt, A.M., Cassia, R.O., Sanllorenti, P.M., Madrid, E.A., Andreu, A.B., Daleo, G.R., Conde, R.D., and, Lamattina, L., (1996) Accumulation of cytosolic glyceraldehyde-3-phosphate dehydrogenase RNA under biological stress conditions and elicitor treatments in potato. Plant Mol. Biol. 30, 961-972.
37. Lee, S.M., Hoang, M.H., Han, H.J., Kim, H.S., Lee, K., Kim, K.E., Kim, D.H., Lee, S.Y., and, Chung, W.S., (2009) Pathogen inducible voltage-dependent anion channel (AtVDAC) isoforms are localized to mitochondria membrane in Arabidopsis. Mol. Cells, 27, 321-327.
38. Leon, G., Holuigue, L., and, Jordana, X., (2007) Mitochondrial complex II is essential for gametophyte development in Arabidopsis. Plant Physiol. 143, 1534-1546.
39. 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.
40. Lippman, Z.B., and, Zamir, D., (2007) Heterosis: revisiting the magic. Trends Genet. 23, 60-66.
41. Marcon, C., Schutzenmeister, A., Schutz, W., Madlung, J., Piepho, H.P., and, Hochholdinger, F., (2010) Nonadditive protein accumulation patterns in maize (Zea mays L.) hybrids during embryo development. J. Proteome Res. 9, 6511-6522.
42. 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.
43. Meyer, R.C., Kusterer, B., Lisec, J., et al. (2010) QTL analysis of early stage heterosis for biomass in Arabidopsis. Theor. Appl. Genet. 120, 227-237.
44. Mooney, B.P., Miernyk, J.A., Greenlief, M.C., and, Thelen, J.J., (2006) Using quantitative proteomics of Arabidopsis roots and leaves to predict metabolic activity. Physiol. Plant. 128, 237-250.
45. Newton, K.J., and, Walbot, V., (1985) Maize mitochondria synthesize organ-specific polypeptides. Proc. Natl Acad. Sci. USA, 82, 6879-6883.
46. Ni, X.L., Zhang, T., Jiang, K.F., Yang, L., Yang, Q.H., Cao, Y.J., Wen, C.Y., and, Zheng, J.K., (2009) Correlations between specific combining ability, heterosis and genetic distance in hybrid rice. Yi Chuan, 31, 849-854 (in Chinese).
47. Ouellet, F., Carpentier, E., Cope, M.J., Monroy, A.F., and, Sarhan, F., (2001) Regulation of a wheat actin-depolymerizing factor during cold acclimation. Plant Physiol. 125, 360-368.
48. Pechanova, O., Pechan, T., Ozkan, S., McCarthy, F.M., Williams, W.P., and, Luthe, D.S., (2010) Proteome profile of the developing maize (Zea mays L.) rachis. Proteomics, 10, 3051-3055.
49. 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.
50. 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.
51. Sachs, M.M., and, Ho, T.H.D., (1986) Alteration of gene expression during environmental stress in plants. Annu. Rev. Plant Physiol. 37, 363-376.
52. Schnable, P.S., Ware, D., Fulton, R.S., et al. (2009) The B73 maize genome: complexity, diversity, and dynamics. Science, 326, 1112-1115.
53. 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.
54. Seo, J., and, Lee, K.J., (2004) Post-translational modifications and their biological functions: proteomic analysis and systematic approaches. J. Biochem. Mol. Biol. 37, 35-44.
55. Shull, G.H., (1908) The Composition of a Field of Maize. American Breeders Association Reports, 4, pp. 296-301.
56. Song, S., Qu, H., Chen, C., Hu, S., and, Yu, J., (2007) Differential gene expression in an elite hybrid rice cultivar (Oryza sativa, L) and its parental lines based on SAGE data. BMC Plant Biol. 7, 49.
57. Song, X., Ni, Z., Yao, Y., Zhang, Y., and, Sun, Q., (2009) Identification of differentially expressed proteins between hybrid and parents in wheat (Triticum aestivum L.) seedling leaves. Theor. Appl. Genet. 118, 213-225.
58. Springer, N.M., and, Stupar, R.M., (2007) Allelic variation and heterosis in maize: how do two halves make more than a whole? Genome Res. 17, 264-275.
59. Springer, N.M., Ying, K., Fu, Y., et al. (2009) Maize inbreds exhibit high levels of copy number variation (CNV) and presence/absence variation (PAV) in genome content. PLoS Genet. 5, e1000734.
60. Stern, D.B., and, Newton, K.J., (1985) Mitochondrial gene expression in Cucurbitaceae: conserved and variable features. Curr. Genet. 9, 395-404.
61. Stupar, R.M., Hermanson, P.J., and, Springer, N.M., (2007) Nonadditive expression and parent-of-origin effects identified by microarray and allele-specific expression profiling of maize endosperm. Plant Physiol. 145, 411-425.
62. Stupar, R.M., Gardiner, J.M., Oldre, A.G., Haun, W.J., Chandler, V.L., and, Springer, N.M., (2008) Gene expression analyses in maize inbreds and hybrids with varying levels of heterosis. BMC Plant Biol. 8, 33.
63. 1 hybrid and its inbred parents. Proc. Natl Acad. Sci. USA, 103, 6805-6810.
64. 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.
65. Veitia, R.A., and, Vaiman, D., (2011) Exploring the mechanistic bases of heterosis from the perspective of macromolecular complexes. FASEB J. 25, 476-482.
66. Wang, Z., and, Pesacreta, T.C., (2004) A subclass of myosin XI is associated with mitochondria, plastids, and the molecular chaperone subunit TCP-1α in maize. Cell Motil. Cytoskel. 57, 218-232.
67. 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.
68. Wang, W., Meng, B., Ge, X., Song, S., Yang, Y., Yu, X., Wang, L., Hu, S., Liu, S., and, Yu, J., (2008) Proteomic profiling of rice embryos from a hybrid rice cultivar and its parental lines. Proteomics, 8, 4808-4821.
69. Wei, G., Tao, Y., Liu, G., et al. (2009) A transcriptomic analysis of superhybrid rice LYP9 and its parents. Proc. Natl Acad. Sci. USA, 106, 7695-7701.
70. Wei, L., Fei, Z., Wu, X., Dong, H., Zhou, P., and, Zhang, Z., (2010) Mitochondrial comparative proteomic analysis of sterile line and its maintain line of purple cytoplasmic rice (Oryza sativa). Adv. Biosci. Biotechnol. 1, 145-151.
71. Yao, H., Kato, A., Mooney, B., and, Birchler, J.A., (2011) Phenotypic and gene expression analyses of a ploidy series of maize inbred Oh43. Plant Mol. Biol. 75, 237-251.
72. Zhang, C., Yin, Y., Zhang, A., Lu, Q., Wen, X., Zhu, Z., Zhang, L., and, Lu, C., (2012) Comparative proteomic study reveals dynamic proteome changes between superhybrid rice LYP9 and its parents at different developmental stages. J. Plant Physiol. 169, 387-398.