173:
produce biomass at a faster rate than the yeast. Producing a toxic compound, like ethanol, can slow the growth of bacteria, allowing the yeast to be more competitive. However, the yeast still had to use a portion of the sugar it consumes to produce ethanol. Crabtree-positive yeasts also have increased glycolytic flow, or increased uptake of glucose and conversion to pyruvate, which compensates for using a portion of the glucose to produce ethanol rather than biomass. Therefore, it is believed that the original driving force was to kill competitors. This is supported by research that determined the kinetic behavior of the ancestral ADH protein, which was found to be optimized to make ethanol, rather than consume it.
563:), the fermentation enzyme ADH is abundant, regardless of the oxygen level. In tobacco pollen, PDC is also highly expressed in this tissue and transcript levels are not influenced by oxygen concentration. Tobacco pollen, similar to Crabtree-positive yeast, perform high levels of fermentation dependent on the sugar supply, and not oxygen availability. In these tissues, respiration and alcoholic fermentation occur simultaneously with high sugar availability. Fermentation produces the toxic acetaldehyde and ethanol, that can build up in large quantities during pollen development. It has been hypothesized that acetaldehyde is a pollen factor that causes
386:
394:
water. During the domestication process, organisms shift from natural environments that are more variable and complex to simple and stable environments with a constant substrate. This often favors specialization adaptations in domesticated microbes, associated with relaxed selection for non-useful genes in alternative metabolic strategies or pathogenicity. Domestication might be partially responsible for the traits that promote aerobic fermentation in industrial species. Introgression and HGT is common in
604:
303:(Pdh). The kinetics of the enzymes are such that when pyruvate concentrations are high, due to a high rate of glycolysis, there is increased flux through Pdc and thus the fermentation pathway. The WGD is believed to have played a beneficial role in the evolution of the Crabtree effect in post-WGD species partially due to this increase in copy number of glycolysis genes.
123:(CNV) and differential expression in metabolic genes, and regulatory reprogramming. Research is still needed to fully understand the genomic basis of this complex phenomenon. Many Crabtree-positive yeast species are used for their fermentation ability in industrial processes in the production of wine, beer, sake, bread, and bioethanol. Through
567:. Cytoplasmic male sterility is a trait observed in maize, tobacco and other plants in which there is an inability to produce viable pollen. It is believed that this trait might be due to the expression of the fermentation genes, ADH and PDC, a lot earlier on in pollen development than normal and the accumulation of toxic aldehyde.
331:. Adh1 is the major enzyme responsible for catalyzing the fermentation step from acetaldehyde to ethanol. Adh2 catalyzes the reverse reaction, consuming ethanol and converting it to acetaldehyde. The ancestral, or original, Adh had a similar function as Adh1 and after a duplication in this gene, Adh2 evolved a lower K
579:
parasites degrade glucose via aerobic fermentation. In this group, this phenomenon is not a pre-adaptation to/or remnant of anaerobic life, shown through their inability to survive in anaerobic conditions. It is believed that this phenomenon developed due to the capacity for a high glycolytic flux
508:
One of the hallmarks of cancer is altered metabolism or deregulating cellular energetics. Cancers cells often have reprogrammed their glucose metabolism to perform lactic acid fermentation, in the presence of oxygen, rather than send the pyruvate made through glycolysis to the mitochondria. This is
356:
is grown on glucose in aerobic conditions, respiration-related gene expression is repressed. Mitochondrial ribosomal proteins expression is only induced under environmental stress conditions, specifically low glucose availability. Genes involving mitochondrial energy generation and phosphorylation
269:
gene results in decreased ethanol production or fully respiratory metabolism. Thus, having an efficient glucose uptake system appears to be essential to ability of aerobic fermentation. There is a significant positive correlation between the number of hexose transporter genes and the efficiency of
172:
It is believed that a major driving force in the origin of aerobic fermentation was its simultaneous origin with modern fruit (~125 mya). These fruits provided an abundance of simple sugar food source for microbial communities, including both yeast and bacteria. Bacteria, at that time, were able to
163:
Crabtree-positive yeasts likely occurred in the interval between the ability to grow under anaerobic conditions, horizontal transfer of anaerobic DHODase (encoded by URA1 with bacteria), and the loss of respiratory chain
Complex I. A more pronounced Crabtree effect, the second step, likely occurred
599:
cytochrome oxidase mutant) strain by removing three terminal cytochrome oxidases (cydAB, cyoABCD, and cbdAB) to reduce oxygen uptake. After 60 days of adaptive evolution on glucose media, the strain displayed a mixed phenotype. In aerobic conditions, some populations' fermentation solely produced
393:
Aerobic fermentation is essential for multiple industries, resulting in human domestication of several yeast strains. Beer and other alcoholic beverages, throughout human history, have played a significant role in society through drinking rituals, providing nutrition, medicine, and uncontaminated
517:
This phenomenon is often seen as counterintuitive, since cancer cells have higher energy demands due to the continued proliferation and respiration produces significantly more ATP than glycolysis alone (fermentation produces no additional ATP). Typically, there is an up-regulation in glucose
105:, and tumor cells. Crabtree-positive yeasts will respire when grown with very low concentrations of glucose or when grown on most other carbohydrate sources. The Crabtree effect is a regulatory system whereby respiration is repressed by fermentation, except in low sugar conditions. When
294:
reaction pathway were retained in post-WGD species, significantly higher than the overall retention rate. This has been associated with an increased ability to metabolize glucose into pyruvate, or higher rate of glycolysis. After glycolysis, pyruvate can either be further broken down by
279:
335:
for ethanol. Adh2 is believed to have increased yeast species' tolerance for ethanol and allowed
Crabtree-positive species to consume the ethanol they produced after depleting sugars. However, Adh2 and consumption of ethanol is not essential for aerobic fermentation.
518:
transporters and enzymes in the glycolysis pathway (also seen in yeast). There are many parallel aspects of aerobic fermentation in tumor cells that are also seen in
Crabtree-positive yeasts. Further research into the evolution of aerobic fermentation in yeast such as
159:(ADH) encoding genes and hexose transporters. However, recent evidence has shown that aerobic fermentation originated before the WGD and evolved as a multi-step process, potentially aided by the WGD. The origin of aerobic fermentation, or the first step, in
513:
and is associated with high consumption of glucose and a high rate of glycolysis. ATP production in these cancer cells is often only through the process of glycolysis and pyruvate is broken down by the fermentation process in the cell's cytoplasm.
176:
Further evolutionary events in the development of aerobic fermentation likely increased the efficiency of this lifestyle, including increased tolerance to ethanol and the repression of the respiratory pathway. In high sugar environments,
111:
is grown below the sugar threshold and undergoes a respiration metabolism, the fermentation pathway is still fully expressed, while the respiration pathway is only expressed relative to the sugar availability. This contrasts with the
191:
to dominate in high sugar environments evolved more recently than aerobic fermentation and is dependent on the type of high-sugar environment. Other yeasts' growth is dependent on the pH and nutrients of the high-sugar environment.
164:
near the time of the WGD event. Later evolutionary events that aided in the evolution of aerobic fermentation are better understood and outlined in the section discussing the genomic basis of the
Crabtree effect.
34:
is a metabolic process by which cells metabolize sugars via fermentation in the presence of oxygen and occurs through the repression of normal respiratory metabolism. Preference of aerobic fermentation over
1044:
Alfarouk, Khalid O.; Verduzco, Daniel; Rauch, Cyril; Muddathir, Abdel Khalig; Adil, H. H. Bashir; Elhassan, Gamal O.; Ibrahim, Muntaser E.; David Polo Orozco, Julian; Cardone, Rosa Angela (2014-01-01).
155:(WGD). A majority of Crabtree-positive yeasts are post-WGD yeasts. It was believed that the WGD was a mechanism for the development of the Crabtree effect in these species due to the duplication of
249:
lineage, and detects glucose via the cAMP-signaling pathway. The number of transporter genes vary significantly between yeast species and has continually increased during the evolution of the
357:
oxidation, which are involved in respiration, have the largest expression difference between aerobic fermentative yeast species and respiratory species. In a comparative analysis between
200:
The genomic basis of the
Crabtree effect is still being investigated, and its evolution likely involved multiple successive molecular steps that increased the efficiency of the lifestyle.
365:, both of which evolved aerobic fermentation independently, the expression pattern of these two fermentative yeasts were more similar to each other than a respiratory yeast,
1814:
Legras, Jean-Luc; Merdinoglu, Didier; Cornuet, Jean-Marie; Karst, Francis (2007-05-01). "Bread, beer and wine: Saccharomyces cerevisiae diversity reflects human history".
1172:
Baumann, Kristin; Carnicer, Marc; Dragosits, Martin; Graf, Alexandra B; Stadlmann, Johannes; Jouhten, Paula; Maaheimo, Hannu; Gasser, Brigitte; Albiol, Joan (2010-10-22).
235:
encode for glucose sensors. The number of glucose sensor genes have remained mostly consistent through the budding yeast lineage, however glucose sensors are absent from
257:
also has a high number of transporter genes compared to its close relatives. Glucose uptake is believed to be a major rate-limiting step in glycolysis and replacing
1781:
Lin, Zhenguo; Li, Wen-Hsiung (2014-01-01). "Comparative
Genomics and Evolutionary Genetics of Yeast Carbon Metabolism". In Piškur, Jure; Compagno, Concetta (eds.).
686:
Piškur, Jure; Rozpędowska, Elżbieta; Polakova, Silvia; Merico, Annamaria; Compagno, Concetta (2006-04-01). "How did
Saccharomyces evolve to become a good brewer?".
543:
to allow for glycolysis to continue. For most plant tissues, fermentation only occurs in anaerobic conditions, but there are a few exceptions. In the pollen of
1478:
Libkind, Diego; Hittinger, Chris Todd; Valério, Elisabete; Gonçalves, Carla; Dover, Jim; Johnston, Mark; Gonçalves, Paula; Sampaio, José Paulo (2011-08-30).
1047:"Glycolysis, tumor metabolism, cancer growth and dissemination. A new pH-based etiopathogenic perspective and therapeutic approach to an old cancer question"
402:
species. HGT and introgression are less common in nature than is seen during domestication pressures. For example, the important industrial yeast strain
522:
can be a useful model for understanding aerobic fermentation in tumor cells. This has a potential for better understanding cancer and cancer treatments.
580:
and the high glucose concentrations of their natural environment. The mechanism for repression of respiration in these conditions is not yet known.
119:
The evolution of aerobic fermentation likely involved multiple successive molecular steps, which included the expansion of hexose transporter genes,
2087:
Bringaud, Frédéric; Rivière, Loïc; Coustou, Virginie (2006-09-01). "Energy metabolism of trypanosomatids: Adaptation to available carbon sources".
1412:"The Evolution of Aerobic Fermentation in Schizosaccharomyces pombe Was Associated with Regulatory Reprogramming but not Nucleosome Reorganization"
311:
The fermentation reaction only involves two steps. Pyruvate is converted to acetaldehyde by Pdc and then acetaldehyde is converted to ethanol by
1798:
286:
After a WGD, one of the duplicated gene pair is often lost through fractionation; less than 10% of WGD gene pairs have remained in
2049:
Tadege, Million; Dupuis, Isabelle; Kuhlemeier, Cris (1999-08-01). "Ethanolic fermentation: new functions for an old pathway".
55:(ATP) in high yield, it allows proliferating cells to convert nutrients such as glucose and glutamine more efficiently into
1358:
Thomson, J Michael; Gaucher, Eric A; Burgan, Michelle F; Kee, Danny W De; Li, Tang; Aris, John P; Benner, Steven A (2005).
1115:"Yeast "Make-Accumulate-Consume" Life Strategy Evolved as a Multi-Step Process That Predates the Whole Genome Duplication"
352:
In
Crabtree-negative species, respiration related genes are highly expressed in the presence of oxygen. However, when
595:
mutant strains have been bioengineered to ferment glucose under aerobic conditions. One group developed the ECOM3 (
385:
564:
473:
398:
domesticated strains. Many commercial wine strains have significant portions of their DNA derived from HGT of non-
2010:"The Warburg and Crabtree effects: On the origin of cancer cell energy metabolism and of yeast glucose repression"
510:
404:
237:
44:
485:
389:
A close up picture of ripening wine grapes. The light white "dusting" is a film that also contains wild yeasts.
152:
136:
107:
253:
lineage. Most of the transporter genes have been generated by tandem duplication, rather than from the WGD.
414:
183:
1230:"Expansion of Hexose Transporter Genes Was Associated with the Evolution of Aerobic Fermentation in Yeasts"
536:
469:
300:
296:
52:
477:
312:
156:
120:
377:. Regulatory rewiring was likely important in the evolution of aerobic fermentation in both lineages.
986:"Aerobic Fermentation of D-Glucose by an Evolved Cytochrome Oxidase-Deficient Escherichia coli Strain"
319:
genes in
Crabtree-positive compared to Crabtree-negative species and no correlation between number of
1491:
1126:
997:
742:
493:
433:
128:
116:, which is the inhibition of fermentation in the presence of oxygen and observed in most organisms.
2138:
211:(HXT) are a group of proteins that are largely responsible for the uptake of glucose in yeast. In
208:
97:
36:
419:
This hybrid is commonly used in lager-brewing, which requires slow, low temperature fermentation.
131:, to better fit their environment. Strains evolved through mechanisms that include interspecific
2128:
1990:
1847:
957:
905:
68:
17:
1480:"Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast"
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771:
730:
113:
64:
2062:
245:
is a
Crabtree-positive yeast, which developed aerobic fermentation independently from
2122:
2100:
1827:
124:
85:
1851:
961:
731:"Understanding the Warburg Effect: The Metabolic Requirements of Cell Proliferation"
1994:
1174:"A multi-level study of recombinant Pichia pastoris in different oxygen conditions"
465:
909:
535:
Alcoholic fermentation is often used by plants in anaerobic conditions to produce
480:, which is then converted to acetic acid. Both of these processes either generate
2026:
2009:
1622:
1139:
1790:
944:
927:
453:
428:
151:
Approximately 100 million years ago (mya), within the yeast lineage there was a
1942:
1925:
1662:"Evolution of ecological dominance of yeast species in high-sugar environments"
729:
Heiden, Matthew G. Vander; Cantley, Lewis C.; Thompson, Craig B. (2009-05-22).
181:
outcompetes and dominants all other yeast species, except its closest relative
1883:
1569:
1296:"Increased glycolytic flux as an outcome of whole-genome duplication in yeast"
885:
699:
648:
631:
603:
457:
291:
83:
Aerobic fermentation evolved independently in at least three yeast lineages (
60:
1986:
1892:
1835:
1744:
1685:
1513:
1435:
1253:
1070:
1062:
893:
828:
762:
707:
1965:
Warburg, Prof Otto (1925-03-01). "über den Stoffwechsel der Carcinomzelle".
1504:
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489:
72:
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1951:
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1554:"The genomics of microbial domestication in the fermented food environment"
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1209:
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1088:
1027:
846:
803:
Dashko, Sofia; Zhou, Nerve; Compagno, Concetta; Piškur, Jure (2014-09-01).
780:
715:
607:
Myc and HIF-1 regulate glucose metabolism and stimulate the Warburg effect.
282:
A scheme of transformation of glucose to alcohol by alcoholic fermentation.
1752:
953:
901:
657:
1009:
461:
441:
48:
101:). It has also been observed in plant pollen, trypanosomatids, mutated
1978:
1311:
1113:
Hagman, Arne; Säll, Torbjörn; Compagno, Concetta; Piskur, Jure (2013).
984:
Portnoy, Vasiliy A.; Herrgård, Markus J.; Palsson, Bernhard Ø. (2008).
552:
497:
481:
449:
445:
91:
56:
1677:
1865:
Yating, H; Zhenzhen, X; Wolfgang, L; Hirohide, T; Fusheng, C (2022).
437:
1375:
540:
219:
genes have been identified and 17 encode for glucose transporters (
602:
544:
384:
277:
1867:"Oxidative Fermentation of Acetic Acid Bacteria and Its Products"
1660:
Williams, Kathryn M.; Liu, Ping; Fay, Justin C. (2015-08-01).
456:, in a process called AAB oxidative fermentation (AOF). After
805:"Why, when, and how did yeast evolve alcoholic fermentation?"
2008:
Diaz-Ruiz, Rodrigo; Rigoulet, Michel; Devin, Anne (2011).
1360:"Resurrecting ancestral alcohol dehydrogenases from yeast"
315:(Adh). There is no significant increase in the number of
867:"Aerobic fermentation during tobacco pollen development"
600:
lactate, while others performed mixed-acid fermentation.
1719:"The molecular genetics of hexose transport in yeasts"
323:
genes and efficiency of fermentation. There are five
290:
genome. A little over half of WGD gene pairs in the
928:"Aerobic fermentation of glucose by trypanosomatids"
340:
and other Crabtree positive species do not have the
2014:
Biochimica et Biophysica Acta (BBA) - Bioenergetics
632:"The Crabtree Effect: A Regulatory System in Yeast"
127:, these yeast species have evolved, often through
1294:Conant, Gavin C; Wolfe, Kenneth H (2007-01-01).
1785:. Springer Berlin Heidelberg. pp. 97–120.
1783:Molecular Mechanisms in Yeast Carbon Metabolism
1484:Proceedings of the National Academy of Sciences
526:Aerobic fermentation in other non-yeast species
476:. Ethanol is first oxidized to acetaldehyde by
1606:"Origin of the Yeast Whole-Genome Duplication"
472:, which in turn is oxidized to acetic acid by
51:. While aerobic fermentation does not produce
1558:Current Opinion in Genetics & Development
8:
423:Aerobic fermentation in acetic acid bacteria
1717:Boles, E.; Hollenberg, C. P. (1997-08-01).
1410:Lin, Zhenguo; Li, Wen-Hsiung (2011-04-01).
1228:Lin, Zhenguo; Li, Wen-Hsiung (2011-01-01).
1926:"Hallmarks of Cancer: The Next Generation"
492:. This process is exploited in the use of
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1552:Gibbons, John G; Rinker, David C (2015).
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865:Tadege, M.; Kuhlemeier, C. (1997-10-01).
836:
770:
647:
429:Acetic acid § Oxidative fermentation
227:encodes for a galactose transporter, and
617:
344:gene and consumes ethanol very poorly.
2089:Molecular and Biochemical Parasitology
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381:Domestication and aerobic fermentation
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204:Expansion of hexose transporter genes
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196:Genomic basis of the Crabtree effect
143:, pseudogenization, and gene loss.
1736:10.1111/j.1574-6976.1997.tb00346.x
575:When grown in glucose-rich media,
147:Origin of Crabtree effect in yeast
25:
1924:Hanahan, Douglas (4 March 2011).
63:oxidation of such nutrients into
18:Evolution of aerobic fermentation
2101:10.1016/j.molbiopara.2006.03.017
1828:10.1111/j.1365-294X.2007.03266.x
484:, or shuttle electrons into the
1416:Molecular Biology and Evolution
1234:Molecular Biology and Evolution
1:
2063:10.1016/S1360-1385(99)01450-8
408:is an interspecies hybrid of
79:Aerobic fermentation in yeast
43:in yeast, and is part of the
2027:10.1016/j.bbabio.2010.08.010
1623:10.1371/journal.pbio.1002221
1140:10.1371/journal.pone.0068734
373:is evolutionarily closer to
265:genes with a single chimera
1791:10.1007/978-3-642-55013-3_5
945:10.1096/fasebj.6.13.1397837
926:Cazzulo, Juan José (1992).
436:(AAB) incompletely oxidize
2155:
1943:10.1016/j.cell.2011.02.013
1604:Wolfe, Kenneth H. (2015).
565:cytoplasmic male sterility
474:acetaldehyde dehydrogenase
426:
1884:10.3389/fmicb.2022.879246
1871:Frontiers in Microbiology
1723:FEMS Microbiology Reviews
1570:10.1016/j.gde.2015.07.003
1300:Molecular Systems Biology
700:10.1016/j.tig.2006.02.002
649:10.1099/00221287-44-2-149
561:Nicotiana plumbaginifolia
405:Saccharomyces pastorianus
307:CNV in fermentation genes
238:Schizosaccharomyces pombe
1063:10.18632/oncoscience.109
990:Appl. Environ. Microbiol
630:De Deken, R. H. (1966).
486:electron transport chain
153:whole genome duplication
137:horizontal gene transfer
108:Saccharomyces cerevisiae
59:by avoiding unnecessary
2051:Trends in Plant Science
1967:Klinische Wochenschrift
1505:10.1073/pnas.1105430108
1191:10.1186/1752-0509-4-141
886:10.1023/A:1005837112653
874:Plant Molecular Biology
821:10.1111/1567-1364.12161
755:10.1126/science.1160809
348:Differential expression
274:CNV in glycolysis genes
184:Saccharomyces paradoxus
608:
470:pyruvate decarboxylase
412:and the cold tolerant
390:
301:pyruvate dehydrogenase
297:pyruvate decarboxylase
283:
53:adenosine triphosphate
39:is referred to as the
1428:10.1093/molbev/msq324
1246:10.1093/molbev/msq184
606:
478:alcohol dehydrogenase
388:
313:alcohol dehydrogenase
281:
157:alcohol dehydrogenase
121:copy number variation
1010:10.1128/AEM.00880-08
494:acetic acid bacteria
434:Acetic acid bacteria
270:ethanol production.
129:artificial selection
28:Aerobic fermentation
1496:2011PNAS..10814539L
1490:(35): 14539–14544.
1178:BMC Systems Biology
1131:2013PLoSO...868734H
1002:2008ApEnM..74.7561P
809:FEMS Yeast Research
747:2009Sci...324.1029V
741:(5930): 1029–1033.
509:referred to as the
209:Hexose transporters
98:Schizosaccharomyces
69:carbon-carbon bonds
37:aerobic respiration
1979:10.1007/BF01726151
1312:10.1038/msb4100170
688:Trends in Genetics
609:
464:is broken down to
391:
284:
32:aerobic glycolysis
1822:(10): 2091–2102.
1816:Molecular Ecology
1678:10.1111/evo.12707
996:(24): 7561–7569.
636:J. Gen. Microbiol
557:Nicotiana tabacum
187:. The ability of
16:(Redirected from
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1672:(8): 2079–2093.
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141:gene duplication
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2118:
2117:
2116:
2086:
2085:
2078:
2048:
2047:
2043:
2007:
2006:
2002:
1973:(12): 534–536.
1964:
1963:
1959:
1923:
1922:
1918:
1864:
1863:
1859:
1813:
1812:
1808:
1801:
1780:
1779:
1760:
1716:
1715:
1711:
1659:
1658:
1649:
1616:(8): e1002221.
1603:
1602:
1595:
1551:
1550:
1539:
1477:
1476:
1461:
1409:
1408:
1401:
1364:Nature Genetics
1357:
1356:
1337:
1293:
1292:
1279:
1227:
1226:
1217:
1171:
1170:
1166:
1112:
1111:
1096:
1057:(12): 777–802.
1043:
1042:
1035:
983:
982:
969:
938:(13): 3153–61.
925:
924:
917:
869:
864:
863:
854:
802:
801:
788:
728:
727:
723:
685:
684:
665:
629:
628:
619:
614:
589:
573:
571:Trypanosomatids
539:and regenerate
533:
528:
506:
460:, the produced
431:
425:
383:
350:
334:
309:
276:
206:
198:
170:
149:
81:
41:Crabtree effect
23:
22:
15:
12:
11:
5:
2152:
2150:
2142:
2141:
2136:
2131:
2121:
2120:
2115:
2114:
2076:
2057:(8): 320–325.
2041:
2020:(6): 568–576.
2000:
1957:
1936:(5): 646–674.
1916:
1857:
1806:
1799:
1758:
1709:
1647:
1593:
1537:
1459:
1399:
1376:10.1038/ng1553
1370:(6): 630–635.
1335:
1277:
1240:(1): 131–142.
1215:
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694:(4): 183–186.
663:
642:(2): 149–156.
616:
615:
613:
610:
588:
582:
577:trypanosomatid
572:
569:
532:
529:
527:
524:
511:Warburg effect
505:
502:
424:
421:
382:
379:
349:
346:
332:
308:
305:
275:
272:
205:
202:
197:
194:
169:
168:Driving forces
166:
148:
145:
114:Pasteur effect
80:
77:
71:and promoting
65:carbon dioxide
45:Warburg effect
24:
14:
13:
10:
9:
6:
4:
3:
2:
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2127:
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2110:
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2098:
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2068:
2064:
2060:
2056:
2052:
2045:
2042:
2037:
2033:
2028:
2023:
2019:
2015:
2011:
2004:
2001:
1996:
1992:
1988:
1984:
1980:
1976:
1972:
1969:(in German).
1968:
1961:
1958:
1953:
1949:
1944:
1939:
1935:
1931:
1927:
1920:
1917:
1912:
1908:
1903:
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1807:
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1800:9783642550126
1796:
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1769:
1767:
1765:
1763:
1759:
1754:
1750:
1746:
1742:
1737:
1732:
1729:(1): 85–111.
1728:
1724:
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932:FASEB Journal
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566:
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520:S. cerevisiae
515:
512:
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410:S. cerevisiae
407:
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401:
400:Saccharomyces
397:
396:Saccharomyces
387:
380:
378:
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372:
371:S. cerevisiae
368:
364:
363:S. cerevisiae
360:
355:
354:S. cerevisiae
347:
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343:
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329:S. cerevisiae
326:
322:
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306:
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302:
298:
293:
289:
288:S. cerevisiae
280:
273:
271:
268:
264:
260:
259:S. cerevisiae
256:
252:
251:S. cerevisiae
248:
247:Saccharomyces
244:
240:
239:
234:
230:
226:
222:
218:
214:
213:S. cerevisiae
210:
203:
201:
195:
193:
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189:S. cerevisiae
186:
185:
180:
179:S. cerevisiae
174:
167:
165:
162:
161:Saccharomyces
158:
154:
146:
144:
142:
138:
134:
133:hybridization
130:
126:
125:domestication
122:
117:
115:
110:
109:
104:
100:
99:
94:
93:
88:
87:
86:Saccharomyces
78:
76:
74:
70:
67:, preserving
66:
62:
58:
54:
50:
46:
42:
38:
33:
29:
19:
2092:
2088:
2054:
2050:
2044:
2017:
2013:
2003:
1970:
1966:
1960:
1933:
1929:
1919:
1874:
1870:
1860:
1819:
1815:
1809:
1782:
1726:
1722:
1712:
1669:
1665:
1613:
1610:PLOS Biology
1609:
1561:
1557:
1487:
1483:
1419:
1415:
1367:
1363:
1303:
1299:
1237:
1233:
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1177:
1167:
1122:
1118:
1054:
1050:
993:
989:
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931:
877:
873:
812:
808:
738:
734:
724:
691:
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639:
635:
596:
592:
591:A couple of
590:
584:
574:
560:
556:
548:
534:
519:
516:
507:
466:acetaldehyde
432:
415:S. eubayanus
413:
409:
403:
399:
395:
392:
374:
370:
369:. However,
366:
362:
358:
353:
351:
341:
337:
328:
324:
320:
316:
310:
287:
285:
266:
262:
258:
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236:
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220:
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212:
207:
199:
188:
182:
178:
175:
171:
160:
150:
118:
106:
102:
96:
90:
84:
82:
31:
27:
26:
1051:Oncoscience
504:Tumor cells
496:to produce
454:acetic acid
375:C. albicans
367:C. albicans
49:tumor cells
2139:Metabolism
2123:Categories
2095:(1): 1–9.
1184:(1): 141.
612:References
458:glycolysis
444:, usually
427:See also:
359:Sch. pombe
338:Sch. pombe
292:glycolysis
255:Sch. pombe
243:Sch. pombe
221:HXT1-HXT17
2129:Evolution
1987:0023-2173
1893:1664-302X
1836:0962-1083
1745:0168-6445
1686:1558-5646
1666:Evolution
1514:0027-8424
1436:0737-4038
1254:0737-4038
1071:2331-4737
894:0167-4412
829:1567-1364
763:0036-8075
708:0168-9525
490:ubiquinol
327:genes in
299:(Pdc) or
73:anabolism
61:catabolic
2109:16682088
2071:10431222
2036:20804724
1952:21376230
1911:35685922
1852:13157807
1844:17498234
1704:26087012
1642:26252643
1588:26338497
1532:21873232
1454:21127171
1394:15864308
1330:17667951
1272:20660490
1210:20969759
1159:23869229
1119:PLOS ONE
1089:25621294
1028:18952873
962:35191022
847:24824836
781:19460998
716:16499989
549:Zea mays
462:pyruvate
442:alcohols
1995:2034590
1902:9171043
1753:9299703
1695:4751874
1633:4529243
1579:4695309
1564:: 1–8.
1523:3167505
1492:Bibcode
1445:3058771
1385:3618678
1321:1943425
1306:: 129.
1263:3002240
1201:2987880
1150:3711898
1127:Bibcode
1080:4303887
1019:2607145
998:Bibcode
954:1397837
902:9349258
838:4262006
772:2849637
743:Bibcode
735:Science
658:5969497
597:E. coli
587:mutants
585:E. coli
553:tobacco
498:vinegar
482:NAD(P)H
450:ethanol
446:glucose
263:HXT1-17
139:(HGT),
103:E. coli
92:Dekkera
57:biomass
2134:Yeasts
2107:
2069:
2034:
1993:
1985:
1950:
1909:
1899:
1891:
1850:
1842:
1834:
1797:
1751:
1743:
1702:
1692:
1684:
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1630:
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1512:
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1318:
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1208:
1198:
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1016:
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900:
892:
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835:
827:
779:
769:
761:
714:
706:
656:
559:&
551:) and
531:Plants
438:sugars
1991:S2CID
1848:S2CID
958:S2CID
906:S2CID
870:(PDF)
545:maize
452:, to
215:, 20
2105:PMID
2067:PMID
2032:PMID
2018:1807
1983:ISSN
1948:PMID
1930:Cell
1907:PMID
1889:ISSN
1840:PMID
1832:ISSN
1795:ISBN
1749:PMID
1741:ISSN
1700:PMID
1682:ISSN
1638:PMID
1584:PMID
1528:PMID
1510:ISSN
1450:PMID
1432:ISSN
1390:PMID
1326:PMID
1268:PMID
1250:ISSN
1206:PMID
1155:PMID
1085:PMID
1067:ISSN
1024:PMID
950:PMID
898:PMID
890:ISSN
843:PMID
825:ISSN
777:PMID
759:ISSN
712:PMID
704:ISSN
654:PMID
488:via
448:and
440:and
361:and
342:ADH2
233:RGT2
231:and
229:SNF3
225:GAL2
2097:doi
2093:149
2059:doi
2022:doi
1975:doi
1938:doi
1934:144
1897:PMC
1879:doi
1824:doi
1787:doi
1731:doi
1690:PMC
1674:doi
1628:PMC
1618:doi
1574:PMC
1566:doi
1518:PMC
1500:doi
1488:108
1440:PMC
1424:doi
1380:PMC
1372:doi
1316:PMC
1308:doi
1258:PMC
1242:doi
1196:PMC
1186:doi
1145:PMC
1135:doi
1075:PMC
1059:doi
1014:PMC
1006:doi
940:doi
882:doi
833:PMC
817:doi
767:PMC
751:doi
739:324
696:doi
644:doi
541:NAD
537:ATP
468:by
325:Adh
321:Pdc
317:Pdc
267:HXT
261:'s
241:.
223:),
217:HXT
47:in
30:or
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2030:.
2016:.
2012:.
1989:.
1981:.
1946:.
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Text is available under the Creative Commons Attribution-ShareAlike License. Additional terms may apply.
