Natural Variation Identifies , a Universal Gene Required for Cell Proliferation and Growth at High Temperatures in
The increase in average temperatures across the globe has been predicted to have negative impacts on agricultural productivity. Therefore, there is a need to understand the molecular mechanisms that underlie plant growth responses to varying temperature regimes. At present, very little is known about the genes and pathways that modulate thermo-sensory growth responses in plants. In this article, the authors exploit natural variation in the commonly occurring weed thale cress (Arabidopsis thaliana) and identify a gene referred to as ICARUS1 to be required for plant growth at higher ambient temperatures. Plants carrying lesions in this gene stop growing at high temperatures and revert to growth when temperatures reduce. Using a combination of computational, molecular and cell biological approaches, the authors demonstrate that allelic variation at ICARUS1, which encodes an enzyme required for the fundamental biochemical process of tRNAHis maturation, underlies variation in thermo-sensory growth responses of A. thaliana. Furthermore, the authors discover that the deleterious impact of a natural mutation in ICARUS1 is suppressed through alternative splicing, thus suggesting the potential for alternative splicing to buffer the impacts of some natural mutations. These results support that modulation of fundamental processes, in addition to transcriptional regulation, mediate thermo-sensory growth responses in plants.
Vyšlo v časopise:
Natural Variation Identifies , a Universal Gene Required for Cell Proliferation and Growth at High Temperatures in. PLoS Genet 11(5): e32767. doi:10.1371/journal.pgen.1005085
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1005085
Souhrn
The increase in average temperatures across the globe has been predicted to have negative impacts on agricultural productivity. Therefore, there is a need to understand the molecular mechanisms that underlie plant growth responses to varying temperature regimes. At present, very little is known about the genes and pathways that modulate thermo-sensory growth responses in plants. In this article, the authors exploit natural variation in the commonly occurring weed thale cress (Arabidopsis thaliana) and identify a gene referred to as ICARUS1 to be required for plant growth at higher ambient temperatures. Plants carrying lesions in this gene stop growing at high temperatures and revert to growth when temperatures reduce. Using a combination of computational, molecular and cell biological approaches, the authors demonstrate that allelic variation at ICARUS1, which encodes an enzyme required for the fundamental biochemical process of tRNAHis maturation, underlies variation in thermo-sensory growth responses of A. thaliana. Furthermore, the authors discover that the deleterious impact of a natural mutation in ICARUS1 is suppressed through alternative splicing, thus suggesting the potential for alternative splicing to buffer the impacts of some natural mutations. These results support that modulation of fundamental processes, in addition to transcriptional regulation, mediate thermo-sensory growth responses in plants.
Zdroje
1. Queitsch C, Sangster TA, Lindquist S. Hsp90 as a capacitor of phenotypic variation. Nature. 2002;417(6889):618–24. Epub 2002/06/07. 12050657
2. Gibson G, Dworkin I. Uncovering cryptic genetic variation. Nature Reviews Genetics. 2004;5(9):681–90. Epub 2004/09/17. 15372091
3. Sureshkumar S, Todesco M, Schneeberger K, Harilal R, Balasubramanian S, Weigel D. A genetic defect caused by a triplet repeat expansion in Arabidopsis thaliana. Science. 2009;323(5917):1060–3. Epub 2009/01/20. doi: 10.1126/science.1164014 19150812
4. Ledon-Rettig CC, Pfennig DW, Chunco AJ, Dworkin I. Cryptic Genetic Variation in Natural Populations: A Predictive Framework. Integrative and comparative biology. 2014;54(5):783–93. Epub 2014/06/20. doi: 10.1093/icb/icu077 24944116
5. Paaby AB, Rockman MV. Cryptic genetic variation: evolution's hidden substrate. Nature Reviews Genetics. 2014;15(4):247–58. Epub 2014/03/13. doi: 10.1038/nrg3688 24614309
6. Casal JJ. Photoreceptor signaling networks in plant responses to shade. Annual review of plant biology. 2013;64:403–27. Epub 2013/02/05. doi: 10.1146/annurev-arplant-050312-120221 23373700
7. Chen M, Chory J. Phytochrome signaling mechanisms and the control of plant development. Trends Cell Biol. 2011;21(11):664–71. Epub 2011/08/20. doi: 10.1016/j.tcb.2011.07.002 21852137
8. Kami C, Lorrain S, Hornitschek P, Fankhauser C. Light-regulated plant growth and development. Curr Top Dev Biol. 2010;91:29–66. Epub 2010/08/14. doi: 10.1016/S0070-2153(10)91002-8 20705178
9. Fankhauser C, Chory J. Light control of plant development. Annual review of cell and developmental biology. 1997;13:203–29. Epub 1997/01/01. 9442873
10. Knight MR, Knight H. Low-temperature perception leading to gene expression and cold tolerance in higher plants. The New phytologist. 2012;195(4):737–51. Epub 2012/07/24. doi: 10.1111/j.1469-8137.2012.04239.x 22816520
11. Kotak S, Larkindale J, Lee U, von Koskull-Doring P, Vierling E, Scharf KD. Complexity of the heat stress response in plants. Current opinion in plant biology. 2007;10(3):310–6. Epub 2007/05/08. 17482504
12. Penfield S. Temperature perception and signal transduction in plants. The New phytologist. 2008;179(3):615–28. Epub 2008/05/10. doi: 10.1111/j.1469-8137.2008.02478.x 18466219
13. Fitter AH, Fitter RS. Rapid changes in flowering time in British plants. Science. 2002;296(5573):1689–91. 12040195
14. Wigge PA. Ambient temperature signalling in plants. Current opinion in plant biology. 2013;16(5):661–6. Epub 2013/09/12. doi: 10.1016/j.pbi.2013.08.004 24021869
15. Samach A, Wigge PA. Ambient temperature perception in plants. Current opinion in plant biology. 2005;8(5):483–6. 16054430
16. Wang ZW, Wu Z, Raitskin O, Sun Q, Dean C. Antisense-mediated FLC transcriptional repression requires the P-TEFb transcription elongation factor. Proc Natl Acad Sci U S A. 2014;111(20):7468–73. Epub 2014/05/07. doi: 10.1073/pnas.1406635111 24799695
17. Baulcombe DC, Dean C. Epigenetic regulation in plant responses to the environment. Cold Spring Harbor perspectives in biology. 2014;6(9):a019471. Epub 2014/09/04. doi: 10.1101/cshperspect.a019471 25183832
18. Gray WM, Ostin A, Sandberg G, Romano CP, Estelle M. High temperature promotes auxin-mediated hypocotyl elongation in Arabidopsis. Proc Natl Acad Sci U S A. 1998;95(12):7197–202. Epub 1998/06/17. 9618562
19. Todesco M, Balasubramanian S, Cao J, Ott F, Sureshkumar S, Schneeberger K, et al. Natural variation in biogenesis efficiency of individual Arabidopsis thaliana microRNAs. Curr Biol. 2012;22(2):166–70. Epub 2011/12/31. doi: 10.1016/j.cub.2011.11.060 22206705
20. Koini MA, Alvey L, Allen T, Tilley CA, Harberd NP, Whitelam GC, et al. High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4. Curr Biol. 2009;19(5):408–13. Epub 2009/03/03. doi: 10.1016/j.cub.2009.01.046 19249207
21. Balasubramanian S, Sureshkumar S, Lempe J, Weigel D. Potent induction of Arabidopsis thaliana flowering by elevated growth temperature. PLoS genetics. 2006;2(7):e106. Epub 2006/07/15. 16839183
22. Boden SA, Kavanova M, Finnegan EJ, Wigge PA. Thermal stress effects on grain yield in Brachypodium distachyon occur via H2A.Z-nucleosomes. Genome biology. 2013;14(6):R65. Epub 2013/06/27.
23. Kumar SV, Wigge PA. H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell. 2010;140(1):136–47. Epub 2010/01/19. doi: 10.1016/j.cell.2009.11.006 20079334
24. Franklin KA. Plant chromatin feels the heat. Cell. 2010;140(1):26–8. Epub 2010/01/21. doi: 10.1016/j.cell.2009.12.035 20085701
25. Sidaway-Lee K, Costa MJ, Rand DA, Finkenstadt B, Penfield S. Direct measurement of transcription rates reveals multiple mechanisms for configuration of the Arabidopsis ambient temperature response. Genome biology. 2014;15(3):R45. Epub 2014/03/04. doi: 10.1186/gb-2014-15-3-r45 24580780
26. Franklin KA, Lee SH, Patel D, Kumar SV, Spartz AK, Gu C, et al. Phytochrome-interacting factor 4 (PIF4) regulates auxin biosynthesis at high temperature. Proc Natl Acad Sci U S A. 2011;108(50):20231–5. Epub 2011/11/30. doi: 10.1073/pnas.1110682108 22123947
27. Kumar SV, Lucyshyn D, Jaeger KE, Alos E, Alvey E, Harberd NP, et al. Transcription factor PIF4 controls the thermosensory activation of flowering. Nature. 2012;484(7393):242–5. Epub 2012/03/23. doi: 10.1038/nature10928 22437497
28. Lee JH, Yoo SJ, Park SH, Hwang I, Lee JS, Ahn JH. Role of SVP in the control of flowering time by ambient temperature in Arabidopsis. Genes & development. 2007;21(4):397–402.
29. Mizuno T, Nomoto Y, Oka H, Kitayama M, Takeuchi A, Tsubouchi M, et al. Ambient temperature signal feeds into the circadian clock transcriptional circuitry through the EC night-time repressor in Arabidopsis thaliana. Plant & cell physiology. 2014;55(5):958–76. Epub 2014/02/07.
30. Alonso-Blanco C, Mendez-Vigo B. Genetic architecture of naturally occurring quantitative traits in plants: an updated synthesis. Current opinion in plant biology. 2014;18:37–43. Epub 2014/02/26. doi: 10.1016/j.pbi.2014.01.002 24565952
31. Patel D, Basu M, Hayes S, Majlath I, Hetherington FM, Tschaplinski TJ, et al. Temperature-dependent shade avoidance involves the receptor-like kinase ERECTA. Plant J. 2013;73(6):980–92. Epub 2012/12/04. doi: 10.1111/tpj.12088 23199031
32. Balasubramanian S, Weigel D. Temperature Induced Flowering in Arabidopsis thaliana. Plant Signal Behav. 2006;1(5):227–8. Epub 2006/09/01. 19704664
33. Pose D, Verhage L, Ott F, Yant L, Mathieu J, Angenent G, et al. Temperature-dependent regulation of flowering by antagonistic FLM variants. Nature. 2013. 503(7476): 414–417. doi: 10.1038/nature12633 24067612
34. Jackman JE, Gott JM, Gray MW. Doing it in reverse: 3'-to-5' polymerization by the Thg1 superfamily. RNA (New York, NY. 2012;18(5):886–99. Epub 2012/03/30. doi: 10.1261/rna.032300.112 22456265
35. Heinemann IU, Nakamura A, O'Donoghue P, Eiler D, Soll D. tRNAHis-guanylyltransferase establishes tRNAHis identity. Nucleic acids research. 2012;40(1):333–44. Epub 2011/09/06. doi: 10.1093/nar/gkr696 21890903
36. Gu W, Jackman JE, Lohan AJ, Gray MW, Phizicky EM. tRNAHis maturation: an essential yeast protein catalyzes addition of a guanine nucleotide to the 5' end of tRNAHis. Genes & development. 2003;17(23):2889–901. Epub 2003/11/25.
37. Placido A, Sieber F, Gobert A, Gallerani R, Giege P, Marechal-Drouard L. Plant mitochondria use two pathways for the biogenesis of tRNAHis. Nucleic acids research. 2010;38(21):7711–7. Epub 2010/07/28. doi: 10.1093/nar/gkq646 20660484
38. Hyde SJ, Eckenroth BE, Smith BA, Eberley WA, Heintz NH, Jackman JE, et al. tRNA(His) guanylyltransferase (THG1), a unique 3'-5' nucleotidyl transferase, shares unexpected structural homology with canonical 5'-3' DNA polymerases. Proc Natl Acad Sci U S A. 2010;107(47):20305–10. Epub 2010/11/10. doi: 10.1073/pnas.1010436107 21059936
39. Eden E, Navon R, Steinfeld I, Lipson D, Yakhini Z. GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC bioinformatics. 2009;10:48. Epub 2009/02/05. doi: 10.1186/1471-2105-10-48 19192299
40. Supek F, Bosnjak M, Skunca N, Smuc T. REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS ONE. 2011;6(7):e21800. Epub 2011/07/27. doi: 10.1371/journal.pone.0021800 21789182
41. Menges M, Hennig L, Gruissem W, Murray JA. Genome-wide gene expression in an Arabidopsis cell suspension. Plant molecular biology. 2003;53(4):423–42. Epub 2004/03/11. 15010610
42. Ferreira PC, Hemerly AS, Engler JD, van Montagu M, Engler G, Inze D. Developmental expression of the arabidopsis cyclin gene cyc1At. Plant Cell. 1994;6(12):1763–74. Epub 1994/12/01. 7866022
43. Colon-Carmona A, You R, Haimovitch-Gal T, Doerner P. Technical advance: spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. Plant J. 1999;20(4):503–8. Epub 1999/12/22. 10607302
44. Jacqmard A, De Veylder L, Segers G, de Almeida Engler J, Bernier G, Van Montagu M, et al. Expression of CKS1At in Arabidopsis thaliana indicates a role for the protein in both the mitotic and the endoreduplication cycle. Planta. 1999;207(4):496–504. Epub 1999/03/27. 10093894
45. Menges M, de Jager SM, Gruissem W, Murray JA. Global analysis of the core cell cycle regulators of Arabidopsis identifies novel genes, reveals multiple and highly specific profiles of expression and provides a coherent model for plant cell cycle control. Plant J. 2005;41(4):546–66. Epub 2005/02/03. 15686519
46. Roeder AH, Chickarmane V, Cunha A, Obara B, Manjunath BS, Meyerowitz EM. Variability in the control of cell division underlies sepal epidermal patterning in Arabidopsis thaliana. PLoS biology. 2010;8(5):e1000367. Epub 2010/05/21. doi: 10.1371/journal.pbio.1000367 20485493
47. Lobrich M, Jeggo PA. The impact of a negligent G2/M checkpoint on genomic instability and cancer induction. Nature reviews Cancer. 2007;7(11):861–9. Epub 2007/10/19. 17943134
48. Adachi S, Minamisawa K, Okushima Y, Inagaki S, Yoshiyama K, Kondou Y, et al. Programmed induction of endoreduplication by DNA double-strand breaks in Arabidopsis. Proc Natl Acad Sci U S A. 2011;108(24):10004–9. Epub 2011/05/27. doi: 10.1073/pnas.1103584108 21613568
49. Kandasamy MK, McKinney EC, Deal RB, Smith AP, Meagher RB. Arabidopsis actin-related protein ARP5 in multicellular development and DNA repair. Developmental biology. 2009;335(1):22–32. Epub 2009/08/15. doi: 10.1016/j.ydbio.2009.08.006 19679120
50. Rosa M, Von Harder M, Cigliano RA, Schlogelhofer P, Mittelsten Scheid O. The Arabidopsis SWR1 chromatin-remodeling complex is important for DNA repair, somatic recombination, and meiosis. Plant Cell. 2013;25(6):1990–2001. Epub 2013/06/20. doi: 10.1105/tpc.112.104067 23780875
51. Mendez-Vigo B, Pico FX, Ramiro M, Martinez-Zapater JM, Alonso-Blanco C. Altitudinal and climatic adaptation is mediated by flowering traits and FRI, FLC, and PHYC genes in Arabidopsis. Plant Physiol. 2011;157(4):1942–55. Epub 2011/10/13. doi: 10.1104/pp.111.183426 21988878
52. Pico FX, Mendez-Vigo B, Martinez-Zapater JM, Alonso-Blanco C. Natural genetic variation of Arabidopsis thaliana is geographically structured in the Iberian peninsula. Genetics. 2008;180(2):1009–21. Epub 2008/08/22. doi: 10.1534/genetics.108.089581 18716334
53. Rice TS, Ding M, Pederson DS, Heintz NH. The highly conserved tRNAHis guanylyltransferase Thg1p interacts with the origin recognition complex and is required for the G2/M phase transition in the yeast Saccharomyces cerevisiae. Eukaryotic cell. 2005;4(4):832–5. Epub 2005/04/12. 15821142
54. Guo D, Hu K, Lei Y, Wang Y, Ma T, He D. Identification and characterization of a novel cytoplasm protein ICF45 that is involved in cell cycle regulation. The Journal of biological chemistry. 2004;279(51):53498–505. Epub 2004/10/02. 15459185
55. Hyde SJ, Rao BS, Eckenroth BE, Jackman JE, Doublie S. Structural studies of a bacterial tRNA(HIS) guanylyltransferase (Thg1)-like protein, with nucleotide in the activation and nucleotidyl transfer sites. PLoS ONE. 2013;8(7):e67465. Epub 2013/07/12. doi: 10.1371/journal.pone.0067465 23844012
56. Nakamura A, Nemoto T, Heinemann IU, Yamashita K, Sonoda T, Komoda K, et al. Structural basis of reverse nucleotide polymerization. Proc Natl Acad Sci U S A. 2013;110(52):20970–5. Epub 2013/12/11. doi: 10.1073/pnas.1321312111 24324136
57. Jackman JE, Phizicky EM. tRNAHis guanylyltransferase catalyzes a 3'-5' polymerization reaction that is distinct from G-1 addition. Proc Natl Acad Sci U S A. 2006;103(23):8640–5. Epub 2006/05/30. 16731615
58. Rao BS, Maris EL, Jackman JE. tRNA 5'-end repair activities of tRNAHis guanylyltransferase (Thg1)-like proteins from Bacteria and Archaea. Nucleic acids research. 2011;39(5):1833–42. Epub 2010/11/06. doi: 10.1093/nar/gkq976 21051361
59. Brennan AC, Mendez-Vigo B, Haddioui A, Martinez-Zapater JM, Pico FX, Alonso-Blanco C. The genetic structure of Arabidopsis thaliana in the south-western Mediterranean range reveals a shared history between North Africa and southern Europe. BMC plant biology. 2014;14:17. Epub 2014/01/15. doi: 10.1186/1471-2229-14-17 24411008
60. Clough SJ, Bent AF. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1998;16(6):735–43. Epub 1999/03/09. 10069079
61. Schwab R, Ossowski S, Riester M, Warthmann N, Weigel D. Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell. 2006;18(5):1121–33. 16531494
62. Feiler HS, Desprez T, Santoni V, Kronenberger J, Caboche M, Traas J. The higher plant Arabidopsis thaliana encodes a functional CDC48 homologue which is highly expressed in dividing and expanding cells. The EMBO journal. 1995;14(22):5626–37. Epub 1995/11/15. 8521820
63. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics (Oxford, England). 2010;26(1):139–40. Epub 2009/11/17. doi: 10.1093/bioinformatics/btp616 19910308
64. Liao Y, Smyth GK, Shi W. The Subread aligner: fast, accurate and scalable read mapping by seed-and-vote. Nucleic acids research. 2013;41(10):e108. Epub 2013/04/06. doi: 10.1093/nar/gkt214 23558742
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2015 Číslo 5
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Drosophila Spaghetti and Doubletime Link the Circadian Clock and Light to Caspases, Apoptosis and Tauopathy
- Autoselection of Cytoplasmic Yeast Virus Like Elements Encoding Toxin/Antitoxin Systems Involves a Nuclear Barrier for Immunity Gene Expression
- Parp3 Negatively Regulates Immunoglobulin Class Switch Recombination
- PERK Limits Lifespan by Promoting Intestinal Stem Cell Proliferation in Response to ER Stress