Natural variation in timing of stress-responsive gene expression predicts heterosis in intraspecific hybrids of Arabidopsis

Nature Communications

Volumn 6, Issue , 2015, Pages

  Miller, Marisa ^a   Song, Qingxin ^a   Shi, Xiaoli ^a   Juenger, Thomas E ^a   Chen, Z Jeffrey ^a,b  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b NANJING AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOSPERM; CIRCADIAN RHYTHM; GENE EXPRESSION; HETEROSIS; HYBRID;

ABIOTIC STRESS; ARABIDOPSIS THALIANA; BIOMASS; CIRCADIAN RHYTHM; ECOTYPE; EPIGENETICS; GENE EXPRESSION; GENE INACTIVATION; GENETIC DISTANCE; GENOME; HETEROSIS; PLANT MODEL; QUANTITATIVE TRAIT LOCUS; STRESS; ARABIDOPSIS; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; HYBRIDIZATION; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOMASS; CIRCADIAN RHYTHM; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, PLANT; HYBRID VIGOR; HYBRIDIZATION, GENETIC; STRESS, PHYSIOLOGICAL;

EID: 84947607252     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms8453     Document Type: Article

References (64)

1. Darwin, C. R. The Effects of Cross-and Self-fertilization in the Vegetable Kingdom (John Murry, 1876).
2. Duvick, D. N. Biotechnology in the 1930 s: the development of hybrid maize. Nat. Rev. Genet. 2, 69-74 (2001).
3. Schnable, P. S. , Springer, N. M. Progress toward understanding heterosis in crop plants. Annu. Rev. Plant Biol. 64, 71-88 (2013).
4. Goff, S. A. A unifying theory for general multigenic heterosis: energy efficiency, protein metabolism, and implications for molecular breeding. New Phytol. 189, 923-937 (2011).
5. Birchler, J. A., Yao, H., Chudalayandi, S., Vaiman, D. , Veitia, R. A. Heterosis. Plant Cell 22, 2105-2112 (2010).
6. Krieger, U., Lippman, Z. B. , Zamir, D. The flowering gene SINGLE FLOWER TRUSS drives heterosis for yield in tomato. Nat. Genet. 42, 459-463 (2010).
7. Steinmetz, L. M. et al. Dissecting the architecture of a quantitative trait locus in yeast. Nature 416, 326-330 (2002).
8. Lippman, Z. B. , Zamir, D. Heterosis: revisiting the magic. Trends Genet. 23, 60-66 (2007).
9. East, E. M. Heterosis. Genetics 21, 375-397 (1936).
10. Chen, Z. J. Genomic and epigenetic insights into the molecular bases of heterosis. Nat. Rev. Genet. 14, 471-482 (2013).
11. Troyer, A. F. Adaptedness and heterosis in corn and mule hybrids. Crop Sci. 46, 528-543 (2006).
12. Atwell, S. et al. Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465, 627-631 (2010).
13. Fournier-Level, A. et al. A map of local adaptation in Arabidopsis thaliana. Science 334, 86-89 (2011).
14. Wijnen, H. , Young, M. W. Interplay of circadian clocks and metabolic rhythms. Annu. Rev. Genet. 40, 409-448 (2006).
15. Dodd, A. N. et al. Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309, 630-633 (2005).
16. Michael, T. P. et al. Enhanced fitness conferred by naturally occurring variation in the circadian clock. Science 302, 1049-1053 (2003).
17. Ni, Z. et al. Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature 457, 327-331 (2009).
18. Ng, D. W. et al. A role for CHH methylation in the parent-of-origin effect on altered circadian rhythms and biomass heterosis in Arabidopsis intraspecific hybrids. Plant Cell 26, 2430-2440 (2014).
19. Dong, M. A., Farre, E. M. , Thomashow, M. F. Circadian clock-associated 1 and late elongated hypocotyl regulate expression of the C-repeat binding factor (CBF) pathway in Arabidopsis. Proc. Natl Acad. Sci. USA 108, 7241-7246 (2011).
20. Legnaioli, T., Cuevas, J. , Mas, P. TOC1 functions as a molecular switch connecting the circadian clock with plant responses to drought. EMBO J. 28, 3745-3757 (2009).
21. Wang, W. et al. Timing of plant immune responses by a central circadian regulator. Nature 470, 110-114 (2011).
22. Goodspeed, D., Chehab, E. W., Min-Venditti, A., Braam, J. , Covington, M. F. Arabidopsis synchronizes jasmonate-mediated defense with insect circadian behavior. Proc. Natl Acad. Sci. USA 109, 4674-4677 (2012).
23. Zhang, C. et al. Crosstalk between the circadian clock and innate immunity in Arabidopsis. PLoS Pathog. 9, e1003370 (2013).
24. Tian, D., Traw, M. B., Chen, J. Q., Kreitman, M. , Bergelson, J. Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423, 74-77 (2003).
25. Kasuga, M., Liu, Q., Miura, S., Yamaguchi-Shinozaki, K. , Shinozaki, K. Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat. Biotechnol. 17, 287-291 (1999).
26. Todesco, M. et al. Natural allelic variation underlying a major fitness trade-off in Arabidopsis thaliana. Nature 465, 632-636 (2010).
27. Wang, J. et al. Genomewide nonadditive gene regulation in Arabidopsis allotetraploids. Genetics 172, 507-517 (2006).
28. Kempel, A., Schadler, M., Chrobock, T., Fischer, M. , van Kleunen, M. Tradeoffs associated with constitutive and induced plant resistance against herbivory. Proc. Natl Acad. Sci. USA 108, 5685-5689 (2011).
29. Miller, M., Zhang, C. , Chen, Z. J. Ploidy and hybridity effects on growth vigor and gene expression in Arabidopsis thaliana hybrids and their parents. G3 (Bethesda) 2, 505-513 (2012).
30. Meyer, R. C., Torjek, O., Becher, M. , Altmann, T. Heterosis of biomass production in Arabidopsis. Establishment during early development. Plant Physiol. 134, 1813-1823 (2004).
31. Fujimoto, R., Taylor, J. M., Shirasawa, S., Peacock, W. J. , Dennis, E. S. Heterosis of Arabidopsis hybrids between C24 and Col is associated with increased photosynthesis capacity. Proc. Natl Acad. Sci. USA 109, 7109-7114 (2012).
32. Shi, X. et al. Cis-and trans-regulatory divergence between progenitor species determines gene-expression novelty in Arabidopsis allopolyploids. Nat. Commun. 3, 950 (2012).
33. Tirosh, I., Reikhav, S., Levy, A. A. , Barkai, N. A yeast hybrid provides insight into the evolution of gene expression regulation. Science 324, 659-662 (2009).
34. Michael, T. P. et al. A morning-specific phytohormone gene expression program underlying rhythmic plant growth. PLoS Biol. 6, e225 (2008).
35. Goodspeed, D. et al. Postharvest circadian entrainment enhances crop pest resistance and phytochemical cycling. Curr. Biol. 23, 1235-1241 (2013).
36. Jones, J. D. , Dangl, J. L. The plant immune system. Nature 444, 323-329 (2006).
37. Dodd, A. N. et al. Time of day modulates low-temperature Ca signals in Arabidopsis. Plant J. 48, 962-973 (2006).
38. Lai, A. G. et al. CIRCADIAN CLOCK-ASSOCIATED 1 regulates ROS homeostasis and oxidative stress responses. Proc. Natl Acad. Sci. USA 109, 17129-17134 (2012).
39. Covington, M. F., Maloof, J. N., Straume, M., Kay, S. A. , Harmer, S. L. Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development. Genome Biol. 9, R130 (2008).
40. Bechtold, U. et al. Constitutive salicylic acid defences do not compromise seed yield, drought tolerance and water productivity in the Arabidopsis accession C24. Plant Cell Environ. 33, 1959-1973 (2010).
41. Korn, M. et al. Predicting Arabidopsis freezing tolerance and heterosis in freezing tolerance from metabolite composition. Mol. Plant 3, 224-235 (2010).
42. Rohde, P., Hincha, D. K. , Heyer, A. G. Heterosis in the freezing tolerance of crosses between two Arabidopsis thaliana accessions (Columbia-0 and C24) that show differences in non-acclimated and acclimated freezing tolerance. Plant J. 38, 790-799 (2004).
43. Meyer, R. C. et al. QTL analysis of early stage heterosis for biomass in Arabidopsis. Theor. Appl. Genet. 120, 227-237 (2010).
44. van Hulten, M., Pelser, M., van Loon, L. C., Pieterse, C. M. , Ton, J. Costs and benefits of priming for defense in Arabidopsis. Proc. Natl Acad. Sci. USA 103, 5602-5607 (2006).
45. Heil, M. , Baldwin, I. T. Fitness costs of induced resistance: emerging experimental support for a slippery concept. Trends Plant Sci. 7, 61-67 (2002).
46. Lapin, D., Meyer, R. C., Takahashi, H., Bechtold, U. , Van den Ackerveken, G. Broad-spectrum resistance of Arabidopsis C24 to downy mildew is mediated by different combinations of isolate-specific loci. New Phytol. 196, 1171-1181 (2012).
47. Hannah, M. A. et al. Natural genetic variation of freezing tolerance in Arabidopsis. Plant Physiol. 142, 98-112 (2006).
48. Shen, H. et al. Genome-wide analysis of DNA methylation and gene expression changes in two Arabidopsis ecotypes and their reciprocal hybrids. Plant Cell 24, 875-892 (2012).
49. Feher, K. et al. Deducing hybrid performance from parental metabolic profiles of young primary roots of maize by using a multivariate diallel approach. PLoS ONE 9, e85435 (2014).
50. Dowen, R. H. et al. Widespread dynamic DNA methylation in response to biotic stress. Proc. Natl Acad. Sci. USA 109, E2183-E2191 (2012).
51. Kurihara, Y. et al. Identification of the candidate genes regulated by RNA-directed DNA methylation in Arabidopsis. Biochem. Biophys. Res. Commun. 376, 553-557 (2008).
52. Bomblies, K. et al. Autoimmune response as a mechanism for a Dobzhansky-Muller-type incompatibility syndrome in plants. PLoS Biol. 5, e236 (2007).
53. Clough, S. J. , Bent, A. F. Floral dip: a simplified method for Agrobacteriummediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743 (1998).
54. van Wees, S. Phenotypic analysis of Arabidopsis mutants: trypan blue stain for fungi, oomycetes, and dead plant cells. CSH Protoc. 1, doi: 10.1101/pdb.prot4982 (2008).
55. Homer, N., Merriman, B. , Nelson, S. F. BFAST: an alignment tool for large scale genome resequencing. PLoS ONE 4, e7767 (2009).
56. James, A. B. et al. Alternative splicing mediates responses of the Arabidopsis circadian clock to temperature changes. Plant Cell 24, 961-981 (2012).
57. Wang, L., Feng, Z., Wang, X. , Zhang, X. DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26, 136-138 (2010).
58. Mockler, T. C. et al. The DIURNAL project: DIURNAL and circadian expression profiling, model-based pattern matching, and promoter analysis. Cold Spring Harb. Symp. Quant. Biol. 72, 353-363 (2007).
59. Du, Z., Zhou, X., Ling, Y., Zhang, Z. , Su, Z. agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res. 38, W64-W70 (2010).
60. Katari, M. S. et al. VirtualPlant: a software platform to support systems biology research. Plant Physiol. 152, 500-515 (2010).
61. McClung, C. R. A modern circadian clock in the common angiosperm ancestor of monocots and eudicots. BMC Biol. 8, 55 (2010).
62. Michael, T. P. , McClung, C. R. Phase-specific circadian clock regulatory elements in Arabidopsis. Plant Physiol. 130, 627-638 (2002).
63. Haydon, M. J., Mielczarek, O., Robertson, F. C., Hubbard, K. E. , Webb, A. A. Photosynthetic entrainment of the Arabidopsis thaliana circadian clock. Nature 502, 689-692 (2013).
64. Schneider, C. A., Rasband, W. S. , Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671-675 (2012).