#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Temperature preference can bias parental genome retention during hybrid evolution


Autoři: Caiti S. Smukowski Heil aff001;  Christopher R. L. Large aff001;  Kira Patterson aff001;  Angela Shang-Mei Hickey aff001;  Chiann-Ling C. Yeh aff001;  Maitreya J. Dunham aff001
Působiště autorů: Genome Sciences Department, University of Washington, Seattle, Washington, United States of America aff001
Vyšlo v časopise: Temperature preference can bias parental genome retention during hybrid evolution. PLoS Genet 15(9): e1008383. doi:10.1371/journal.pgen.1008383
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008383

Souhrn

Interspecific hybridization can introduce genetic variation that aids in adaptation to new or changing environments. Here, we investigate how hybrid adaptation to temperature and nutrient limitation may alter parental genome representation over time. We evolved Saccharomyces cerevisiae x Saccharomyces uvarum hybrids in nutrient-limited continuous culture at 15°C for 200 generations. In comparison to previous evolution experiments at 30°C, we identified a number of responses only observed in the colder temperature regime, including the loss of the S. cerevisiae allele in favor of the cryotolerant S. uvarum allele for several portions of the hybrid genome. In particular, we discovered a genotype by environment interaction in the form of a loss of heterozygosity event on chromosome XIII; which species’ haplotype is lost or maintained is dependent on the parental species’ temperature preference and the temperature at which the hybrid was evolved. We show that a large contribution to this directionality is due to a temperature dependent fitness benefit at a single locus, the high affinity phosphate transporter gene PHO84. This work helps shape our understanding of what forces impact genome evolution after hybridization, and how environmental conditions may promote or disfavor the persistence of hybrids over time.

Klíčová slova:

Research and analysis methods – Animal studies – Experimental organism systems – Model organisms – Yeast and fungal models – Biology and life sciences – Organisms – Eukaryota – Fungi – Yeast – Saccharomyces – Saccharomyces cerevisiae – Genetics – Genetic loci – Alleles – Genomics – Genome evolution – Heredity – Heterozygosity – Mutation – Point mutation – Computational biology – Evolutionary biology – Molecular evolution – Molecular biology – Molecular biology techniques – Cloning – Physical sciences – Chemistry – Chemical compounds – Phosphates – Salts – Sulfates


Zdroje

1. Emery M, Willis MMS, Hao Y, Barry K, Oakgrove K, et al. (2018) Preferential retention of genes from one parental genome after polyploidy illustrates the nature and scope of the genomic conflicts induced by hybridization. PLoS Genetics 14: e1007267. doi: 10.1371/journal.pgen.1007267 29590103

2. Louis VL, Despons L, Friedrich A, Martin T, Durrens P, et al. (2012) Pichia sorbitophila, an Interspecies Yeast Hybrid, Reveals Early Steps of Genome Resolution After Polyploidization. G3-Genes Genomes Genetics 2: 299–311.

3. Pryszcz LP, Nemeth T, Gacser A, Gabaldon T (2014) Genome Comparison of Candida orthopsilosis Clinical Strains Reveals the Existence of Hybrids between Two Distinct Subspecies. Genome Biology and Evolution 6: 1069–1078. doi: 10.1093/gbe/evu082 24747362

4. Buggs RJ, Chamala S, Wu W, Gao L, May GD, et al. (2010) Characterization of duplicate gene evolution in the recent natural allopolyploid Tragopogon miscellus by next-generation sequencing and Sequenom iPLEX MassARRAY genotyping. Molecular Ecology 19 Suppl 1: 132–146.

5. Wang J, Tian L, Lee HS, Wei NE, Jiang H, et al. (2006) Genomewide nonadditive gene regulation in Arabidopsis allotetraploids. Genetics 172: 507–517. doi: 10.1534/genetics.105.047894 16172500

6. Cheng F, Wu J, Fang L, Sun SL, Liu B, et al. (2012) Biased Gene Fractionation and Dominant Gene Expression among the Subgenomes of Brassica rapa. PLoS One 7 (5): e36442. doi: 10.1371/journal.pone.0036442 22567157

7. Schnable JC, Springer NM, Freeling M (2011) Differentiation of the maize subgenomes by genome dominance and both ancient and ongoing gene loss. Proc Natl Acad Sci U S A 108: 4069–4074. doi: 10.1073/pnas.1101368108 21368132

8. Albertin W, Marullo P (2012) Polyploidy in fungi: evolution after whole-genome duplication. Proceedings of the Royal Society B-Biological Sciences 279: 2497–2509.

9. Soltis DE, Visger CJ, Soltis PS (2014) The Polyploidy Revolution Then …And Now: Stebbins Revisited. American Journal of Botany 101: 1057–1078. doi: 10.3732/ajb.1400178 25049267

10. Coyne JA, Orr HA (2004) Speciation. Sunderland, Mass.: Sinauer Associates.

11. Schumer M, Xu CL, Powell DL, Durvasula A, Skov L, et al. (2018) Natural selection interacts with recombination to shape the evolution of hybrid genomes. Science 360: 656–659. doi: 10.1126/science.aar3684 29674434

12. Sankararaman S, Mallick S, Dannemann M, Prufer K, Kelso J, et al. (2014) The genomic landscape of Neanderthal ancestry in present-day humans. Nature 507: 354–357. doi: 10.1038/nature12961 24476815

13. Juric I, Aeschbacher S, Coop G (2016) The Strength of Selection against Neanderthal Introgression. PLoS Genetics 12 (11): e1006340. doi: 10.1371/journal.pgen.1006340 27824859

14. Huerta-Sanchez E, Jin X, Asan, Bianba Z, Peter BM, et al. (2014) Altitude adaptation in Tibetans caused by introgression of Denisovan-like DNA. Nature 512: 194–197. doi: 10.1038/nature13408 25043035

15. Dasmahapatra KK, Walters JR, Briscoe AD, Davey JW, Whibley A, et al. (2012) Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature 487: 94–98. doi: 10.1038/nature11041 22722851

16. Suarez-Gonzalez A, Lexer C, Cronk QCB (2018) Adaptive introgression: a plant perspective. Biology Letters 14.

17. Norris LC, Main BJ, Lee Y, Collier TC, Fofana A, et al. (2015) Adaptive introgression in an African malaria mosquito coincident with the increased usage of insecticide-treated bed nets. Proc Natl Acad Sci U S A 112: 815–820. doi: 10.1073/pnas.1418892112 25561525

18. Song Y, Endepols S, Klemann N, Richter D, Matuschka FR, et al. (2011) Adaptive Introgression of Anticoagulant Rodent Poison Resistance by Hybridization between Old World Mice. Current Biology 21: 1296–1301. doi: 10.1016/j.cub.2011.06.043 21782438

19. Jones MR, Mills LS, Alves PC, Callahan CM, Alves JM, et al. (2018) Adaptive introgression underlies polymorphic seasonal camouflage in snowshoe hares. Science 360: 1355–1358. doi: 10.1126/science.aar5273 29930138

20. Racimo F, Sankararaman S, Nielsen R, Huerta-Sanchez E (2015) Evidence for archaic adaptive introgression in humans. Nature Reviews Genetics 16: 359–371. doi: 10.1038/nrg3936 25963373

21. Richards EJ, Martin CH (2017) Adaptive introgression from distant Caribbean islands contributed to the diversification of a microendemic adaptive radiation of trophic specialist pupfishes. PLoS Genetics 13 (8):e1006919. doi: 10.1371/journal.pgen.1006919 28796803

22. Oziolor EM, Reid NM, Yair S, Lee KM, Guberman VerPloeg S, et al. (2019) Adaptive introgression enables evolutionary rescue from extreme environmental pollution. Science 364: 455–457. doi: 10.1126/science.aav4155 31048485

23. Lee HY, Chou JY, Cheong L, Chang NH, Yang SY, et al. (2008) Incompatibility of Nuclear and Mitochondrial Genomes Causes Hybrid Sterility between Two Yeast Species. Cell 135: 1065–1073. doi: 10.1016/j.cell.2008.10.047 19070577

24. Hou J, Friedrich A, Gounot JS, Schacherer J (2015) Comprehensive survey of condition-specific reproductive isolation reveals genetic incompatibility in yeast. Nature Communications 6: 7214. doi: 10.1038/ncomms8214 26008139

25. Chen C, Chen H, Lin YS, Shen JB, Shan JX, et al. (2014) A two-locus interaction causes interspecific hybrid weakness in rice. Nature Communications 5: 3357. doi: 10.1038/ncomms4357 24556665

26. Fu CY, Wang F, Sun BR, Liu WG, Li JH, et al. (2013) Genetic and cytological analysis of a novel type of low temperature-dependent intrasubspecific hybrid weakness in rice. PLoS One 8: e73886. doi: 10.1371/journal.pone.0073886 24023693

27. Shii CT, Mok MC, Temple SR, Mok DWS (1980) Expression of Developmental Abnormalities in Hybrids of Phaseolus-Vulgaris L—Interaction between Temperature and Allelic Dosage. Journal of Heredity 71: 218–222.

28. Bomblies K, Lempe J, Epple P, Warthmann N, Lanz C, et al. (2007) Autoimmune response as a mechanism for a Dobzhansky-Muller-type incompatibility syndrome in plants. PLoS Biology 5: 1962–1972.

29. Jeuken MJW, Zhang NW, McHale LK, Pelgrom K, den Boer E, et al. (2009) Rin4 Causes Hybrid Necrosis and Race-Specific Resistance in an Interspecific Lettuce Hybrid. Plant Cell 21: 3368–3378. doi: 10.1105/tpc.109.070334 19855048

30. Saito T, Ichitani K, Suzuki T, Marubashi W, Kuboyama T (2007) Developmental observation and high temperature rescue from hybrid weakness in a cross between Japanese rice cultivars and Peruvian rice cultivar 'Jamaica'. Breeding Science 57: 281–288.

31. Arnold ML, Ballerini ES, Brothers AN (2012) Hybrid fitness, adaptation and evolutionary diversification: lessons learned from Louisiana Irises. Heredity 108: 159–166. doi: 10.1038/hdy.2011.65 21792222

32. Grant PR, Grant BR (2002) Unpredictable evolution in a 30-year study of Darwin's finches. Science 296: 707–711. doi: 10.1126/science.1070315 11976447

33. Grant PR, Grant BR (2010) Natural selection, speciation and Darwin's finches. Proceedings of the California Academy of Sciences 61: 245–260.

34. Salzburger W, Baric S, Sturmbauer C (2002) Speciation via introgressive hybridization in East African cichlids? Molecular Ecology 11: 619–625. 11918795

35. Rieseberg LH, Raymond O, Rosenthal DM, Lai Z, Livingstone K, et al. (2003) Major ecological transitions in wild sunflowers facilitated by hybridization. Science 301: 1211–1216. doi: 10.1126/science.1086949 12907807

36. Seehausen O (2004) Hybridization and adaptive radiation. Trends in Ecology & Evolution 19: 198–207.

37. Schwarz D, Matta BM, Shakir-Botteri NL, McPheron BA (2005) Host shift to an invasive plant triggers rapid animal hybrid speciation. Nature 436: 546–549. doi: 10.1038/nature03800 16049486

38. Martin NH, Bouck AC, Arnold ML (2006) Detecting adaptive trait introgression between Iris fulva and I. brevicaulis in highly selective field conditions. Genetics 172: 2481–2489. doi: 10.1534/genetics.105.053538 16415358

39. Anderson TM, vonHoldt BM, Candille SI, Musiani M, Greco C, et al. (2009) Molecular and Evolutionary History of Melanism in North American Gray Wolves. Science 323: 1339–1343. doi: 10.1126/science.1165448 19197024

40. Johnson WE, Onorato DP, Roelke ME, Land ED, Cunningham M, et al. (2010) Genetic Restoration of the Florida Panther. Science 329: 1641–1645. doi: 10.1126/science.1192891 20929847

41. Zhang Z, Bendixsen DP, Janzen T, Nolte AW, Greig D, et al. (2019) Recombining your way out of trouble: the genetic architecture of hybrid fitness under enviornmental stress. BioRxiv.

42. Marcet-Houben M, Gabaldon T (2015) Beyond the Whole-Genome Duplication: Phylogenetic Evidence for an Ancient Interspecies Hybridization in the Baker's Yeast Lineage. PLoS Biology 13: e1002220. doi: 10.1371/journal.pbio.1002220 26252497

43. Wolfe KH (2015) Origin of the Yeast Whole-Genome Duplication. PLoS Biology 13 (8): e1002221. doi: 10.1371/journal.pbio.1002221 26252643

44. Barbosa R, Almeida P, Safar SVB, Santos RO, Morais PB, et al. (2016) Evidence of Natural Hybridization in Brazilian Wild Lineages of Saccharomyces cerevisiae. Genome Biology and Evolution 8: 317–329. doi: 10.1093/gbe/evv263 26782936

45. Belloch C, Perez-Torrado R, Gonzalez SS, Perez-Ortin JE, Garcia-Martinez J, et al. (2009) Chimeric genomes of natural hybrids of Saccharomyces cerevisiae and Saccharomyces kudriavzevii. Applied Environmental Microbiology 75: 2534–2544. doi: 10.1128/AEM.02282-08 19251887

46. Gonzalez SS, Barrio E, Gafner J, Querol A (2006) Natural hybrids from Saccharomyces cerevisiae, Saccharomyces bayanus and Saccharomyces kudriavzevii in wine fermentations. FEMS Yeast Research 6: 1221–1234. doi: 10.1111/j.1567-1364.2006.00126.x 17156019

47. Leducq JB, Nielly-Thibault L, Charron G, Eberlein C, Verta JP, et al. (2016) Speciation driven by hybridization and chromosomal plasticity in a wild yeast. Nature Microbiology 1: 15003. doi: 10.1038/nmicrobiol.2015.3 27571751

48. Hittinger CT (2013) Saccharomyces diversity and evolution: a budding model genus. Trends in Genetics 29: 309–317. doi: 10.1016/j.tig.2013.01.002 23395329

49. Marsit S, Leducq JB, Durand E, Marchant A, Filteau M, et al. (2017) Evolutionary biology through the lens of budding yeast comparative genomics. Nature Reviews Genetics 18: 581–598. doi: 10.1038/nrg.2017.49 28714481

50. Selmecki AM, Maruvka YE, Richmond PA, Guillet M, Shoresh N, et al. (2015) Polyploidy can drive rapid adaptation in yeast. Nature 519: 349–352. doi: 10.1038/nature14187 25731168

51. Dunn B, Sherlock G (2008) Reconstruction of the genome origins and evolution of the hybrid lager yeast Saccharomyces pastorianus. Genome Research 18: 1610–1623. doi: 10.1101/gr.076075.108 18787083

52. Gibson B, Liti G (2015) Saccharomyces pastorianus: genomic insights inspiring innovation for industry. Yeast 32: 17–27. doi: 10.1002/yea.3033 25088523

53. Baker E, Wang B, Bellora N, Peris D, Hulfachor AB, et al. (2015) The Genome Sequence of Saccharomyces eubayanus and the Domestication of Lager-Brewing Yeasts. Molecular Biology and Evolution 32: 2818–2831. doi: 10.1093/molbev/msv168 26269586

54. Nakao Y, Kanamori T, Itoh T, Kodama Y, Rainieri S, et al. (2009) Genome sequence of the lager brewing yeast, an interspecies hybrid. DNA Research 16: 115–129. doi: 10.1093/dnares/dsp003 19261625

55. Peris D, Langdon QK, Moriarty RV, Sylvester K, Bontrager M, et al. (2016) Complex Ancestries of Lager-Brewing Hybrids Were Shaped by Standing Variation in the Wild Yeast Saccharomyces eubayanus. PLoS Genetics 12: e1006155. doi: 10.1371/journal.pgen.1006155 27385107

56. Walther A, Hesselbart A, Wendland J (2014) Genome sequence of Saccharomyces carlsbergensis, the world's first pure culture lager yeast. G3 (Bethesda) 4: 783–793.

57. Dunn B, Paulish T, Stanbery A, Piotrowski J, Koniges G, et al. (2013) Recurrent Rearrangement during Adaptive Evolution in an Interspecific Yeast Hybrid Suggests a Model for Rapid Introgression. PLoS Genetics 9 (3): e1003366. doi: 10.1371/journal.pgen.1003366 23555283

58. Piotrowski JS, Nagarajan S, Kroll E, Stanbery A, Chiotti KE, et al. (2012) Different selective pressures lead to different genomic outcomes as newly-formed hybrid yeasts evolve. BMC Evolutionary Biology 12:46. doi: 10.1186/1471-2148-12-46 22471618

59. Peris D, Moriarty RV, Alexander WG, Wrobel RL, Hittinger CT (2019) Allododecaploid yeasts: synthetic hybrids of six species. BioRxiv.

60. Almeida P, Goncalves C, Teixeira S, Libkind D, Bontrager M, et al. (2014) A Gondwanan imprint on global diversity and domestication of wine and cider yeast Saccharomyces uvarum. Nature Communications 5: 4044. doi: 10.1038/ncomms5044 24887054

61. Fernandez-Espinar MT, Barrio E, Querol A (2003) Analysis of the genetic variability in the species of the Saccharomyces sensu stricto complex. Yeast 20: 1213–1226. doi: 10.1002/yea.1034 14587104

62. Rainieri S, Zambonelli C, Hallsworth JE, Pulvirenti A, Giudici P (1999) Saccharomyces uvarum, a distinct group within Saccharomyces sensu stricto. FEMS Microbiology Letters 177: 177–185. doi: 10.1111/j.1574-6968.1999.tb13729.x 10436934

63. Rodriguez ME, Perez-Traves L, Sangorrin MP, Barrio E, Querol A, et al. (2017) Saccharomyces uvarum is responsible for the traditional fermentation of apple chicha in Patagonia. FEMS Yeast Research 17(1).

64. Perez-Torrado R, Barrio E, Querol A (2018) Alternative yeasts for winemaking: Saccharomyces non-cerevisiae and its hybrids. Crit Rev Food Sci Nutr 58: 1780–1790. doi: 10.1080/10408398.2017.1285751 28362111

65. Krogerus K, Preiss R, Gibson B (2018) A Unique Saccharomyces cerevisiae × Saccharomyces uvarum Hybrid Isolated From Norwegian Farmhouse Beer: Characterization and Reconstruction. Frontiers in Microbiology 9: 2253. doi: 10.3389/fmicb.2018.02253 30319573

66. Smukowski Heil CS, DeSevo CG, Pai DA, Tucker CM, Hoang ML, et al. (2017) Loss of Heterozygosity Drives Adaptation in Hybrid Yeast. Molecular Biology and Evolution 34: 1596–1612. doi: 10.1093/molbev/msx098 28369610

67. Schroder MS, Martinez de San Vicente K, Prandini TH, Hammel S, Higgins DG, et al. (2016) Multiple Origins of the Pathogenic Yeast Candida orthopsilosis by Separate Hybridizations between Two Parental Species. PLoS Genetics 12: e1006404. doi: 10.1371/journal.pgen.1006404 27806045

68. Li ZK, Zhang F (2013) Rice breeding in the post-genomics era: from concept to practice. Current Opinion in Plant Biology 16: 261–269. doi: 10.1016/j.pbi.2013.03.008 23571011

69. Stuart-Smith RD, Edgar GJ, Bates AE (2017) Thermal limits to the geographic distributions of shallow-water marine species. Nature Ecology & Evolution 1: 1846–1852.

70. Chen IC, Hill JK, Ohlemuller R, Roy DB, Thomas CD (2011) Rapid Range Shifts of Species Associated with High Levels of Climate Warming. Science 333: 1024–1026. doi: 10.1126/science.1206432 21852500

71. Guisan A, Thuiller W (2005) Predicting species distribution: offering more than simple habitat models. Ecology Letters 8: 993–1009.

72. Gresham D, Desai MM, Tucker CM, Jenq HT, Pai DA, et al. (2008) The repertoire and dynamics of evolutionary adaptations to controlled nutrient-limited environments in yeast. PLoS Genetics 4: e1000303. doi: 10.1371/journal.pgen.1000303 19079573

73. Dunn B, Paulish T, Stanbery A, Piotrowski J, Koniges G, et al. (2013) Recurrent rearrangement during adaptive evolution in an interspecific yeast hybrid suggests a model for rapid introgression. PLoS Genetics 9: e1003366. doi: 10.1371/journal.pgen.1003366 23555283

74. Piotrowski JS, Nagarajan S, Kroll E, Stanbery A, Chiotti KE, et al. (2012) Different selective pressures lead to different genomic outcomes as newly-formed hybrid yeasts evolve. BMC Evolutionary Biology 12: 46. doi: 10.1186/1471-2148-12-46 22471618

75. Hong J, Brandt N, Abdul-Rahman F, Yang A, Hughes T, et al. (2018) An incoherent feedforward loop facilitates adaptive tuning of gene expression. eLife 7:e32323. doi: 10.7554/eLife.32323 29620523

76. Gresham D, Usaite R, Germann SM, Lisby M, Botstein D, et al. (2010) Adaptation to diverse nitrogen-limited environments by deletion or extrachromosomal element formation of the GAP1 locus. Proc Natl Acad Sci U S A 107: 18551–18556. doi: 10.1073/pnas.1014023107 20937885

77. Lauer S, Avecilla G, Spealman P, Sethia G, Brandt N, et al. (2018) Single-cell copy number variant detection reveals the dynamics and diversity of adaptation. PLoS Biology 16(12): e3000069. doi: 10.1371/journal.pbio.3000069 30562346

78. Sunshine AB, Payen C, Ong GT, Liachko I, Tan KM, et al. (2015) The fitness consequences of aneuploidy are driven by condition-dependent gene effects. PLoS Biology 13(5):e1002155. doi: 10.1371/journal.pbio.1002155 26011532

79. Dunham MJ, Badrane H, Ferea T, Adams J, Brown PO, et al. (2002) Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 99: 16144–16149. doi: 10.1073/pnas.242624799 12446845

80. Payen C, Di Rienzi SC, Ong GT, Pogachar JL, Sanchez JC, et al. (2014) The dynamics of diverse segmental amplifications in populations of Saccharomyces cerevisiae adapting to strong selection. G3 (Bethesda) 4: 399–409.

81. Sanchez MR, Miller AW, Liachko I, Sunshine AB, Lynch B, et al. (2017) Differential paralog divergence modulates genome evolution across yeast species. PLoS Genetics 13: e1006585. doi: 10.1371/journal.pgen.1006585 28196070

82. Bergstrom A, Simpson JT, Salinas F, Barre B, Parts L, et al. (2014) A high-definition view of functional genetic variation from natural yeast genomes. Molecular Biology and Evolution 31: 872–888. doi: 10.1093/molbev/msu037 24425782

83. Samyn DR, Van der Veken J, Van Zeebroeck G, Persson BL, Karlsson BC (2016) Key Residues and Phosphate Release Routes in the Saccharomyces cerevisiae Pho84 Transceptor: THE ROLE OF TYR179 IN FUNCTIONAL REGULATION. J Biol Chem 291: 26388–26398. doi: 10.1074/jbc.M116.738112 27875295

84. Samyn DR, Ruiz-Pavon L, Andersson MR, Popova Y, Thevelein JM, et al. (2012) Mutational analysis of putative phosphate- and proton-binding sites in the Saccharomyces cerevisiae Pho84 phosphate:H(+) transceptor and its effect on signalling to the PKA and PHO pathways. Biochem J 445: 413–422. doi: 10.1042/BJ20112086 22587366

85. Lagerstedt JO, Voss JC, Wieslander A, Persson BL (2004) Structural modeling of dual-affinity purified Pho84 phosphate transporter. FEBS Lett 578: 262–268. doi: 10.1016/j.febslet.2004.11.012 15589830

86. Popova Y, Thayumanavan P, Lonati E, Agrochao M, Thevelein JM (2010) Transport and signaling through the phosphate-binding site of the yeast Pho84 phosphate transceptor. Proc Natl Acad Sci U S A 107: 2890–2895. doi: 10.1073/pnas.0906546107 20133652

87. Tai SL, Daran-Lapujade P, Walsh MC, Pronk JT, Daran JM (2007) Acclimation of Saccharomyces cerevisiae to low temperature: A chemostat-based transcriptome analysis. Molecular Biology of the Cell 18: 5100–5112. doi: 10.1091/mbc.E07-02-0131 17928405

88. Abe F, Minegishi H (2008) Global screening of genes essential for growth in high-pressure and cold environments: Searching for basic adaptive strategies using a yeast deletion library. Genetics 178: 851–872. doi: 10.1534/genetics.107.083063 18245339

89. Garcia-Rios E, Ramos-Alonso L, Guillamon JM (2016) Correlation between Low Temperature Adaptation and Oxidative Stress in Saccharomyces cerevisiae. Frontiers in Microbiology 7:1199. doi: 10.3389/fmicb.2016.01199 27536287

90. Lashkari DA, DeRisi JL, McCusker JH, Namath AF, Gentile C, et al. (1997) Yeast microarrays for genome wide parallel genetic and gene expression analysis. Proc Natl Acad Sci U S A 94: 13057–13062. doi: 10.1073/pnas.94.24.13057 9371799

91. Kandror O, Bretschneider N, Kreydin E, Cavalieri D, Goldberg AL (2004) Yeast adapt to near-freezing temperatures by STRE/Msn2,4-dependent induction of trehalose synthesis and certain molecular chaperones. Molecular Cell 13: 771–781. 15053871

92. Sahara T, Goda T, Ohgiya S (2002) Comprehensive expression analysis of time-dependent genetic responses in yeast cells to low temperature. Journal of Biological Chemistry 277: 50015–50021. doi: 10.1074/jbc.M209258200 12379644

93. Robertson LS, Fink GR (1998) The three yeast A kinases have specific signaling functions in pseudohyphal growth. Proc Natl Acad Sci U S A 95: 13783–13787. doi: 10.1073/pnas.95.23.13783 9811878

94. Conlan RS, Tzamarias D (2001) Sfl1 functions via the co-repressor Ssn6-Tup1 and the cAMP-dependent protein kinase Tpk2. Journal of Molecular Biology 309: 1007–1015. doi: 10.1006/jmbi.2001.4742 11399075

95. Hope EA, Amorosi CJ, Miller AW, Dang K, Heil CS, et al. (2017) Experimental Evolution Reveals Favored Adaptive Routes to Cell Aggregation in Yeast. Genetics 206: 1153–1167. doi: 10.1534/genetics.116.198895 28450459

96. Liu H, Styles CA, Fink GR (1996) Saccharomyces cerevisiae S288C has a mutation in FLO8, a gene required for filamentous growth. Genetics 144: 967–978. 8913742

97. Weiss C, Roop JI, Hackley R, Chuong J, Grigoriev IV, et al. (2018) Genetic dissection of interspecific differences in yeast thermotolerance. Nature Genetics 50: 1501–1504. doi: 10.1038/s41588-018-0243-4 30297967

98. Singer MA, Lindquist S (1998) Thermotolerance in Saccharomyces cerevisiae: the Yin and Yang of trehalose. Trends Biotechnol 16: 460–468. 9830154

99. Goncalves P, Valerio E, Correia C, de Almeida JM, Sampaio JP (2011) Evidence for divergent evolution of growth temperature preference in sympatric Saccharomyces species. PLoS One 6: e20739. doi: 10.1371/journal.pone.0020739 21674061

100. Aguilera J, Randez-Gil F, Prieto JA (2007) Cold response in Saccharomyces cerevisiae: new functions for old mechanisms. FEMS Microbiol Rev 31: 327–341. doi: 10.1111/j.1574-6976.2007.00066.x 17298585

101. Homma T, Iwahashi H, Komatsu Y (2003) Yeast gene expression during growth at low temperature. Cryobiology 46: 230–237. 12818212

102. Phadtare S, Alsina J, Inouye M (1999) Cold shock response and cold-shock proteins. Current Opinion in Microbiology 2: 175–180. doi: 10.1016/S1369-5274(99)80031-9 10322168

103. Rodriguez-Vargas S, Estruch F, Randez-Gil F (2002) Gene expression analysis of cold and freeze stress in baker's yeast. Applied and Environmental Microbiology 68: 3024–3030. doi: 10.1128/AEM.68.6.3024-3030.2002 12039763

104. Paget CM, Schwartz JM, Delneri D (2014) Environmental systems biology of cold-tolerant phenotype in Saccharomyces species adapted to grow at different temperatures. Molecular Ecology 23: 5241–5257. doi: 10.1111/mec.12930 25243355

105. Greig D, Louis EJ, Borts RH, Travisano M (2002) Hybrid speciation in experimental populations of yeast. Science 298: 1773–1775. doi: 10.1126/science.1076374 12459586

106. Li XC, Peris D, Hittinger CT, Sia EA, Fay JC (2019) Mitochondria-encoded genes contribute to the evolution of heat and cold tolerance among Saccharomyces species. Science Advances 5(1): eaav1848. doi: 10.1126/sciadv.aav1848 30729162

107. Hebly M, Brickwedde A, Bolat I, Driessen MRM, de Hulster EAF, et al. (2015) S. cerevisiae x S. eubayanus interspecific hybrid, the best of both worlds and beyond. FEMS Yeast Research 15(3).

108. Libkind D, Hittinger CT, Valerio E, Goncalves C, Dover J, et al. (2011) Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast. Proc Natl Acad Sci U S A 108: 14539–14544. doi: 10.1073/pnas.1105430108 21873232

109. Nikulin J, Krogerus K, Gibson B (2018) Alternative Saccharomyces interspecies hybrid combinations and their potential for low-temperature wort fermentation. Yeast 35: 113–127. doi: 10.1002/yea.3246 28755430

110. Baker EP, Peris D, Moriarty RV, Li XC, Fay JC, et al. (2019) Mitochondrial DNA and temperature tolerance in lager yeasts. Science Advances 5(1):eaav1869. doi: 10.1126/sciadv.aav1869 30729163

111. Parrou JL, Teste MA, Francois J (1997) Effects of various types of stress on the metabolism of reserve carbohydrates in Saccharomyces cerevisiae: Genetic evidence for a stress-induced recycling of glycogen and trehalose. Microbiology-Uk 143: 1891–1900.

112. Francois J, Parrou JL (2001) Reserve carbohydrates metabolism in the yeast Saccharomyces cerevisiae. FEMS Microbiology Reviews 25: 125–145. doi: 10.1111/j.1574-6976.2001.tb00574.x 11152943

113. Secco D, Wang C, Shou HX, Whelan J (2012) Phosphate homeostasis in the yeast Saccharomyces cerevisiae, the key role of the SPX domain-containing proteins. FEBS Letters 586: 289–295. doi: 10.1016/j.febslet.2012.01.036 22285489

114. Vicent I, Navarro A, Mulet JM, Sharma S, Serrano R (2015) Uptake of inorganic phosphate is a limiting factor for Saccharomyces cerevisiae during growth at low temperatures. FEMS Yeast Research 15(3).

115. Hoffmann AA, Sgro CM (2011) Climate change and evolutionary adaptation. Nature 470: 479–485. doi: 10.1038/nature09670 21350480

116. Abbott R, Albach D, Ansell S, Arntzen JW, Baird SJ, et al. (2013) Hybridization and speciation. J Evol Biol 26: 229–246. doi: 10.1111/j.1420-9101.2012.02599.x 23323997

117. Grabenstein KC, Taylor SA (2018) Breaking Barriers: Causes, Consequences, and Experimental Utility of Human-Mediated Hybridization. Trends in Ecology & Evolution 33: 198–212.

118. Kelly B, Whiteley A, Tallmon D (2010) The Arctic melting pot. Nature 468: 891–891. doi: 10.1038/468891a 21164461

119. Pashkova N, Gakhar L, Winistorfer SC, Sunshine AB, Rich M, et al. (2013) The Yeast Alix Homolog Bro1 Functions as a Ubiquitin Receptor for Protein Sorting into Multivesicular Endosomes. Developmental Cell 25: 520–533. doi: 10.1016/j.devcel.2013.04.007 23726974

120. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, et al. (2011) Integrative genomics viewer. Nature Biotechnology 29: 24–26. doi: 10.1038/nbt.1754 21221095

121. Miller AW, Dunham MJ (2013) Design and use of multiplexed chemostat arrays. Journal of Visualized Experiments 72.

122. Omasits U, Ahrens CH, Muller S, Wollscheid B (2014) Protter: interactive protein feature visualization and integration with experimental proteomic data. Bioinformatics 30: 884–886. doi: 10.1093/bioinformatics/btt607 24162465

Štítky
Genetika Reprodukční medicína

Článek vyšel v časopise

PLOS Genetics


2019 Číslo 9
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Důležitost adherence při depresivním onemocnění
nový kurz
Autoři: MUDr. Eliška Bartečková, Ph.D.

Koncepce osteologické péče pro gynekology a praktické lékaře
Autoři: MUDr. František Šenk

Sekvenční léčba schizofrenie
Autoři: MUDr. Jana Hořínková, Ph.D.

Hypertenze a hypercholesterolémie – synergický efekt léčby
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Multidisciplinární zkušenosti u pacientů s diabetem
Autoři: Prof. MUDr. Martin Haluzík, DrSc., prof. MUDr. Vojtěch Melenovský, CSc., prof. MUDr. Vladimír Tesař, DrSc.

Všechny kurzy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#