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• W2086867029 abstract "The domestication of animals, plants, and microbes fundamentally transformed the lifestyle and demography of the human species [1Diamond J. Evolution, consequences and future of plant and animal domestication.Nature. 2002; 418: 700-707Crossref PubMed Scopus (964) Google Scholar]. Although the genetic and functional underpinnings of animal and plant domestication are well understood, little is known about microbe domestication [2Hyma K.E. Saerens S.M. Verstrepen K.J. Fay J.C. Divergence in wine characteristics produced by wild and domesticated strains of Saccharomyces cerevisiae.FEMS Yeast Res. 2011; 11: 540-551Crossref PubMed Scopus (46) Google Scholar, 3Legras J.L. Merdinoglu D. Cornuet J.M. Karst F. Bread, beer and wine: Saccharomyces cerevisiae diversity reflects human history.Mol. Ecol. 2007; 16: 2091-2102Crossref PubMed Scopus (390) Google Scholar, 4Libkind D. Hittinger C.T. Valério E. Gonçalves C. Dover J. Johnston M. Gonçalves P. Sampaio J.P. Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast.Proc. Natl. Acad. Sci. USA. 2011; 108: 14539-14544Crossref PubMed Scopus (442) Google Scholar, 5Liti G. Carter D.M. Moses A.M. Warringer J. Parts L. James S.A. Davey R.P. Roberts I.N. Burt A. Koufopanou V. et al.Population genomics of domestic and wild yeasts.Nature. 2009; 458: 337-341Crossref PubMed Scopus (1052) Google Scholar, 6Rokas A. The effect of domestication on the fungal proteome.Trends Genet. 2009; 25: 60-63Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar]. Here, we systematically examined genome-wide sequence and functional variation between the domesticated fungus Aspergillus oryzae, whose saccharification abilities humans have harnessed for thousands of years to produce sake, soy sauce, and miso from starch-rich grains, and its wild relative A. flavus, a potentially toxigenic plant and animal pathogen [7Machida M. Asai K. Sano M. Tanaka T. Kumagai T. Terai G. Kusumoto K. Arima T. Akita O. Kashiwagi Y. et al.Genome sequencing and analysis of Aspergillus oryzae.Nature. 2005; 438: 1157-1161Crossref PubMed Scopus (992) Google Scholar]. We discovered dramatic changes in the sequence variation and abundance profiles of genes and wholesale primary and secondary metabolic pathways between domesticated and wild relative isolates during growth on rice. Our data suggest that, through selection by humans, an atoxigenic lineage of A. flavus gradually evolved into a “cell factory” for enzymes and metabolites involved in the saccharification process. These results suggest that whereas animal and plant domestication was largely driven by Neolithic “genetic tinkering” of developmental pathways, microbe domestication was driven by extensive remodeling of metabolism. The domestication of animals, plants, and microbes fundamentally transformed the lifestyle and demography of the human species [1Diamond J. Evolution, consequences and future of plant and animal domestication.Nature. 2002; 418: 700-707Crossref PubMed Scopus (964) Google Scholar]. Although the genetic and functional underpinnings of animal and plant domestication are well understood, little is known about microbe domestication [2Hyma K.E. Saerens S.M. Verstrepen K.J. Fay J.C. Divergence in wine characteristics produced by wild and domesticated strains of Saccharomyces cerevisiae.FEMS Yeast Res. 2011; 11: 540-551Crossref PubMed Scopus (46) Google Scholar, 3Legras J.L. Merdinoglu D. Cornuet J.M. Karst F. Bread, beer and wine: Saccharomyces cerevisiae diversity reflects human history.Mol. Ecol. 2007; 16: 2091-2102Crossref PubMed Scopus (390) Google Scholar, 4Libkind D. Hittinger C.T. Valério E. Gonçalves C. Dover J. Johnston M. Gonçalves P. Sampaio J.P. Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast.Proc. Natl. Acad. Sci. USA. 2011; 108: 14539-14544Crossref PubMed Scopus (442) Google Scholar, 5Liti G. Carter D.M. Moses A.M. Warringer J. Parts L. James S.A. Davey R.P. Roberts I.N. Burt A. Koufopanou V. et al.Population genomics of domestic and wild yeasts.Nature. 2009; 458: 337-341Crossref PubMed Scopus (1052) Google Scholar, 6Rokas A. The effect of domestication on the fungal proteome.Trends Genet. 2009; 25: 60-63Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar]. Here, we systematically examined genome-wide sequence and functional variation between the domesticated fungus Aspergillus oryzae, whose saccharification abilities humans have harnessed for thousands of years to produce sake, soy sauce, and miso from starch-rich grains, and its wild relative A. flavus, a potentially toxigenic plant and animal pathogen [7Machida M. Asai K. Sano M. Tanaka T. Kumagai T. Terai G. Kusumoto K. Arima T. Akita O. Kashiwagi Y. et al.Genome sequencing and analysis of Aspergillus oryzae.Nature. 2005; 438: 1157-1161Crossref PubMed Scopus (992) Google Scholar]. We discovered dramatic changes in the sequence variation and abundance profiles of genes and wholesale primary and secondary metabolic pathways between domesticated and wild relative isolates during growth on rice. Our data suggest that, through selection by humans, an atoxigenic lineage of A. flavus gradually evolved into a “cell factory” for enzymes and metabolites involved in the saccharification process. These results suggest that whereas animal and plant domestication was largely driven by Neolithic “genetic tinkering” of developmental pathways, microbe domestication was driven by extensive remodeling of metabolism. Aspergillus oryzae was likely domesticated from an atoxigenic A. flavus ancestor Domestication was driven by wholesale genetic and functional changes in metabolism Secondary metabolic pathways were targets of selection and downregulation α-amylase is the most abundant A. oryzae transcript and protein during rice growth Examination of several plants and animals suggests that domestication was driven by genetic changes in diverse developmental pathways that ultimately led to large fruits, naked grains, small brains, and big bodies [1Diamond J. Evolution, consequences and future of plant and animal domestication.Nature. 2002; 418: 700-707Crossref PubMed Scopus (964) Google Scholar, 8Doebley J.F. Gaut B.S. Smith B.D. The molecular genetics of crop domestication.Cell. 2006; 127: 1309-1321Abstract Full Text Full Text PDF PubMed Scopus (1296) Google Scholar, 9Purugganan M.D. Fuller D.Q. The nature of selection during plant domestication.Nature. 2009; 457: 843-848Crossref PubMed Scopus (603) Google Scholar]. Although the molecular genetics and phenotypic outcomes of crop and livestock domestication have been extensively studied [8Doebley J.F. Gaut B.S. Smith B.D. The molecular genetics of crop domestication.Cell. 2006; 127: 1309-1321Abstract Full Text Full Text PDF PubMed Scopus (1296) Google Scholar, 9Purugganan M.D. Fuller D.Q. The nature of selection during plant domestication.Nature. 2009; 457: 843-848Crossref PubMed Scopus (603) Google Scholar, 10Andersson L. Georges M. Domestic-animal genomics: deciphering the genetics of complex traits.Nat. Rev. Genet. 2004; 5: 202-212Crossref PubMed Scopus (422) Google Scholar], the evolutionary paths traversed by domesticated microbes remain poorly understood [2Hyma K.E. Saerens S.M. Verstrepen K.J. Fay J.C. Divergence in wine characteristics produced by wild and domesticated strains of Saccharomyces cerevisiae.FEMS Yeast Res. 2011; 11: 540-551Crossref PubMed Scopus (46) Google Scholar, 3Legras J.L. Merdinoglu D. Cornuet J.M. Karst F. Bread, beer and wine: Saccharomyces cerevisiae diversity reflects human history.Mol. Ecol. 2007; 16: 2091-2102Crossref PubMed Scopus (390) Google Scholar, 4Libkind D. Hittinger C.T. Valério E. Gonçalves C. Dover J. Johnston M. Gonçalves P. Sampaio J.P. Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast.Proc. Natl. Acad. Sci. USA. 2011; 108: 14539-14544Crossref PubMed Scopus (442) Google Scholar, 5Liti G. Carter D.M. Moses A.M. Warringer J. Parts L. James S.A. Davey R.P. Roberts I.N. Burt A. Koufopanou V. et al.Population genomics of domestic and wild yeasts.Nature. 2009; 458: 337-341Crossref PubMed Scopus (1052) Google Scholar, 6Rokas A. The effect of domestication on the fungal proteome.Trends Genet. 2009; 25: 60-63Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar]. In China, evidence for a fermented beverage based on rice mixed with honey and fruit dates back to 7,000 B.C.E. [11McGovern P.E. Zhang J.H. Tang J.G. Zhang Z.Q. Hall G.R. Moreau R.A. Nuñez A. Butrym E.D. Richards M.P. Wang C.S. et al.Fermented beverages of pre- and proto-historic China.Proc. Natl. Acad. Sci. USA. 2004; 101: 17593-17598Crossref PubMed Scopus (530) Google Scholar]. Over the millennia that followed, the gradual development of the saccharification process, in which filamentous fungi break down the starch-rich rice to sugars that yeast ferments, morphed the beverage into the high-alcohol rice wine known as sake [11McGovern P.E. Zhang J.H. Tang J.G. Zhang Z.Q. Hall G.R. Moreau R.A. Nuñez A. Butrym E.D. Richards M.P. Wang C.S. et al.Fermented beverages of pre- and proto-historic China.Proc. Natl. Acad. Sci. USA. 2004; 101: 17593-17598Crossref PubMed Scopus (530) Google Scholar, 12Abe K. Gomi K. Hasegawa F. Machida M. Impact of Aspergillus oryzae genomics on industrial production of metabolites.Mycopathologia. 2006; 162: 143-153Crossref PubMed Scopus (88) Google Scholar, 13Kobayashi T. Abe K. Asai K. Gomi K. Juvvadi P.R. Kato M. Kitamoto K. Takeuchi M. Machida M. Genomics of Aspergillus oryzae.Biosci. Biotechnol. Biochem. 2007; 71: 646-670Crossref PubMed Scopus (138) Google Scholar, 14Machida M. Yamada O. Gomi K. Genomics of Aspergillus oryzae: learning from the history of Koji mold and exploration of its future.DNA Res. 2008; 15: 173-183Crossref PubMed Scopus (266) Google Scholar, 15Teramoto Y. Hano T. Ueda S. Production and characteristics of an ancient form of sake made with shitogi.J. Inst. Brewing. 2000; 106: 95-99Crossref Scopus (5) Google Scholar]. The filamentous fungus used in saccharification for making sake, as well as other traditional Japanese food products such as soy sauce and miso, is Aspergillus oryzae (class Eurotiomycetes, phylum Ascomycota). For sake making, A. oryzae spores (koji-kin) are first spread onto steamed rice. After an ∼2-day growth period, the resulting A. oryzae-rice mixture (koji) is mixed with additional steamed rice and water and fermented by Saccharomyces cerevisiae, such that the breakdown of the rice starch by A. oryzae occurs in parallel with the conversion of sugars to alcohol by S. cerevisiae [16Yoshizawa K. Sake: Production and flavor.Food Rev. Int. 1999; 15: 83-107Crossref Scopus (38) Google Scholar]. However, the saccharific and more generally proteolytic and metabolic activities of A. oryzae not only fuel the yeast but also contribute metabolites that influence the flavor and aroma of sake [16Yoshizawa K. Sake: Production and flavor.Food Rev. Int. 1999; 15: 83-107Crossref Scopus (38) Google Scholar]. A. oryzae is closely related to the wild species A. flavus [17Geiser D.M. Pitt J.I. Taylor J.W. Cryptic speciation and recombination in the aflatoxin-producing fungus Aspergillus flavus.Proc. Natl. Acad. Sci. USA. 1998; 95: 388-393Crossref PubMed Scopus (444) Google Scholar, 18Kurtzman C.P. Smiley M.J. Robnett C.J. Wicklow D.T. DNA relatedness among wild and domesticated species in the Aspergillus flavus group.Mycologia. 1986; 78: 955-959Crossref Google Scholar], the two species sharing 99.5% genome-wide nucleotide similarity [19Rokas A. Payne G. Fedorova N.D. Baker S.E. Machida M. Yu J. Georgianna D.R. Dean R.A. Bhatnagar D. Cleveland T.E. et al.What can comparative genomics tell us about species concepts in the genus Aspergillus?.Stud. Mycol. 2007; 59: 11-17Crossref PubMed Scopus (63) Google Scholar]. However, A. oryzae is an atoxigenic domesticate recognized by the United States Department of Agriculture as a Generally Regarded As Safe (GRAS) organism [7Machida M. Asai K. Sano M. Tanaka T. Kumagai T. Terai G. Kusumoto K. Arima T. Akita O. Kashiwagi Y. et al.Genome sequencing and analysis of Aspergillus oryzae.Nature. 2005; 438: 1157-1161Crossref PubMed Scopus (992) Google Scholar], whereas A. flavus is a destructive agricultural pest of several seed crops and producer of the potent natural carcinogen aflatoxin [20Murakami H. Takase S. Ishii T. Non-productivity of aflatoxin by Japanese industrial strains of Aspergillus.J. Gen. Appl. Microbiol. 1967; 13: 323-334Crossref Scopus (18) Google Scholar]. This striking contrast between genomic and phenotypic variation makes the A. oryzae-A. flavus lineage an excellent microbe domestication model for the study of the functional changes associated with microbe domestication and the impact of the process on genome variation [6Rokas A. The effect of domestication on the fungal proteome.Trends Genet. 2009; 25: 60-63Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar, 7Machida M. Asai K. Sano M. Tanaka T. Kumagai T. Terai G. Kusumoto K. Arima T. Akita O. Kashiwagi Y. et al.Genome sequencing and analysis of Aspergillus oryzae.Nature. 2005; 438: 1157-1161Crossref PubMed Scopus (992) Google Scholar, 21Hunter A.J. Jin B. Kelly J.M. Independent duplications of α-amylase in different strains of Aspergillus oryzae.Fungal Genet. Biol. 2011; 48: 438-444Crossref PubMed Scopus (18) Google Scholar, 22Kato N. Tokuoka M. Shinohara Y. Kawatani M. Uramoto M. Seshime Y. Fujii I. Kitamoto K. Takahashi T. Takahashi S. et al.Genetic safeguard against mycotoxin cyclopiazonic acid production in Aspergillus oryzae.ChemBioChem. 2011; 12: 1376-1382Crossref PubMed Scopus (25) Google Scholar]. Domesticated organisms have typically been selected for beneficial traits conferred by certain genetic loci and have undergone several rounds of population bottlenecks. Although we previously did not find evidence that the A. oryzae genome exhibited a relaxation of selective constraints, a common characteristic accompanying plant and animal domestication [6Rokas A. The effect of domestication on the fungal proteome.Trends Genet. 2009; 25: 60-63Abstract Full Text Full Text PDF PubMed Scopus (33) Google Scholar], whether the A. oryzae genome has experienced positive selection during the domestication process remained an open question. To address this question, we Illumina sequenced 14 geographically and industrially diverse isolates from A. oryzae and A. flavus and jointly analyzed them with the two species' reference genomes [7Machida M. Asai K. Sano M. Tanaka T. Kumagai T. Terai G. Kusumoto K. Arima T. Akita O. Kashiwagi Y. et al.Genome sequencing and analysis of Aspergillus oryzae.Nature. 2005; 438: 1157-1161Crossref PubMed Scopus (992) Google Scholar, 23Payne G.A. Nierman W.C. Wortman J.R. Pritchard B.L. Brown D. Dean R.A. Bhatnagar D. Cleveland T.E. Machida M. Yu J. Whole genome comparison of Aspergillus flavus and A. oryzae.Med. Mycol. 2006; 44: S9-S11Crossref Scopus (209) Google Scholar] (A. oryzae RIB 40 and A. flavus NRRL 3357; see Tables S1 and S2 available online). Analysis of the genome-wide nucleotide diversity across the 16 isolates showed that the genetic diversity of the A. oryzae isolates was ∼25% of that found in the A. flavus isolates (chromosome average nucleotide variation ΘA. oryzae = 0.0006 versus ΘA. flavus = 0.0024; t test, p = 4.1 × 10−7), consistent with previous gene-level estimates [17Geiser D.M. Pitt J.I. Taylor J.W. Cryptic speciation and recombination in the aflatoxin-producing fungus Aspergillus flavus.Proc. Natl. Acad. Sci. USA. 1998; 95: 388-393Crossref PubMed Scopus (444) Google Scholar, 24Chang P.K. Ehrlich K.C. What does genetic diversity of Aspergillus flavus tell us about Aspergillus oryzae?.Int. J. Food Microbiol. 2010; 138: 189-199Crossref PubMed Scopus (65) Google Scholar, 25Geiser D.M. Dorner J.W. Horn B.W. Taylor J.W. The phylogenetics of mycotoxin and sclerotium production in Aspergillus flavus and Aspergillus oryzae.Fungal Genet. Biol. 2000; 31: 169-179Crossref PubMed Scopus (205) Google Scholar] (Figure 1A). Evolutionary analysis of 100,084 high-quality SNPs (see Supplemental Experimental Procedures) suggested that the A. oryzae isolates were monophyletic, in agreement with the previous hypotheses that A. oryzae originated via a single domestication event [17Geiser D.M. Pitt J.I. Taylor J.W. Cryptic speciation and recombination in the aflatoxin-producing fungus Aspergillus flavus.Proc. Natl. Acad. Sci. USA. 1998; 95: 388-393Crossref PubMed Scopus (444) Google Scholar, 25Geiser D.M. Dorner J.W. Horn B.W. Taylor J.W. The phylogenetics of mycotoxin and sclerotium production in Aspergillus flavus and Aspergillus oryzae.Fungal Genet. Biol. 2000; 31: 169-179Crossref PubMed Scopus (205) Google Scholar], and did not group by geography or ecology (Figure 1B). Interestingly, two A. flavus isolates (SRRC 1357 and SRRC 2112) showed closer affinity to A. oryzae than to other A. flavus isolates (Figure 1B), suggesting that A. oryzae originated from within A. flavus. One of the footprints of recent selection on the genome is the reduction in variation of regions that are close to the variants under selection [26Sabeti P.C. Schaffner S.F. Fry B. Lohmueller J. Varilly P. Shamovsky O. Palma A. Mikkelsen T.S. Altshuler D. Lander E.S. Positive natural selection in the human lineage.Science. 2006; 312: 1614-1620Crossref PubMed Scopus (808) Google Scholar]. When a beneficial allele is rapidly driven toward fixation, nearby neutral variants are likely to also become fixed as a result of the low rate of recombination between closely linked sites [27Smith J.M. Haigh J. The hitch-hiking effect of a favourable gene.Genet. Res. 1974; 23: 23-35Crossref PubMed Scopus (2218) Google Scholar]. By estimating the relative genome-wide nucleotide diversity ΘOF = log2 (ΘA. oryzae/ΘA. flavus), we identified 61 putative selective sweep regions (PSSRs) (Figures 1C and 1D; Table S3; see Supplemental Experimental Procedures). Examination of PSSR gene content indicated that the main targets of selection were genes and pathways involved in primary metabolism (PM) and secondary metabolism (SM). For example, the 148 PSSR genes were significantly overrepresented for SM (Fisher's exact test [FET], p = 0.0004), whereas five PSSRs contained SM gene clusters, including one for the biosynthesis of the tremorgenic mycotoxin aflatrem (PSSR C5-9; Figures 1C and 1D) [28Nicholson M.J. Koulman A. Monahan B.J. Pritchard B.L. Payne G.A. Scott B. Identification of two aflatrem biosynthesis gene loci in Aspergillus flavus and metabolic engineering of Penicillium paxilli to elucidate their function.Appl. Environ. Microbiol. 2009; 75: 7469-7481Crossref PubMed Scopus (105) Google Scholar]. These results were particularly noteworthy because SM gene families are thought to have expanded and to be located in unique genomic regions of the A. oryzae-A. flavus lineage compared to the far more distantly related species A. fumigatus and A. nidulans [7Machida M. Asai K. Sano M. Tanaka T. Kumagai T. Terai G. Kusumoto K. Arima T. Akita O. Kashiwagi Y. et al.Genome sequencing and analysis of Aspergillus oryzae.Nature. 2005; 438: 1157-1161Crossref PubMed Scopus (992) Google Scholar]. Furthermore, several PSSR genes are involved in protein and peptide degradation (genes in PSSRs C2-7 and C5-8) and carbohydrate metabolism (C3-5 and C5-6) (Figures 1C and 1D). One of the strongest supported PSSRs (C8-6) contained a glutaminase (Figures 1C and 1D), which catalyzes the hydrolysis of carbon-nitrogen bonds of L-glutamine to glutamic acid, a widely used food flavor enhancer found at considerable levels in sake [29Fujisawa K. Yoshino M. Formation of inosinic acid as the taste compound in the fermentation of Japanese sake.Dev. Food Sci. 1998; 40: 227-231Crossref Scopus (1) Google Scholar]. Strikingly, whereas there were six polymorphic sites within the A. oryzae isolates (two promoter and four intron), A. flavus isolates were polymorphic at 86 sites (14 synonymous, 2 nonsynonymous, 18 promoter region, and 52 intron) (Figure S1). We also examined the isolate genome data to identify differences in genome architecture between the two species (see Supplemental Experimental Procedures). Although our search identified only five genes shared uniquely by all A. oryzae isolates and none by A. flavus isolates (Table S4), it did also identify a locus that contains a nine-gene cluster in the A. oryzae genome but contains a six-gene cluster in the A. flavus NRRL 3357 genome (Figure 2A). Interestingly, the nine-gene cluster is very similar to the sesquiterpene gene cluster in Trichoderma virens [30Mukherjee M. Horwitz B.A. Sherkhane P.D. Hadar R. Mukherjee P.K. A secondary metabolite biosynthesis cluster in Trichoderma virens: evidence from analysis of genes underexpressed in a mutant defective in morphogenesis and antibiotic production.Curr. Genet. 2006; 50: 193-202Crossref PubMed Scopus (44) Google Scholar, 31Mukherjee P.K. Horwitz B.A. Kenerley C.M. Secondary metabolism in Trichoderma—a genomic perspective.Microbiology. 2012; 158: 35-45Crossref PubMed Scopus (208) Google Scholar], whose product belongs to a class of food-flavoring aromatic compounds [32Janssens L. De Pooter H.L. Schamp N.M. Vandamme E.J. Production of flavors by microorganisms.Process Biochem. 1992; 27: 195-215Crossref Scopus (235) Google Scholar], whereas the six-gene cluster comprises a terpene cyclase and GAPDH from the nine-gene cluster together with four other unrelated genes (Figure S2). Remarkably, although A. oryzae is fixed for the nine-gene cluster, A. flavus is polymorphic: three isolates contained the nine-gene cluster, whereas the other five contained the alternative six-gene cluster (Figure 2B). Furthermore, the genes contained in the two alternative cluster “alleles” at this locus have different evolutionary histories (Figure S2). Most unique genes of the nine-gene cluster group with sequences from A. clavatus and divergent fungi related to T. virens, consistent with horizontal transfer, whereas most A. flavus unique genes of the alternative cluster group with sequences from A. aculeatus, suggesting a very different history. A. oryzae has been grown continually on starch-rich substrates, such as rice and soy, for thousands of years [7Machida M. Asai K. Sano M. Tanaka T. Kumagai T. Terai G. Kusumoto K. Arima T. Akita O. Kashiwagi Y. et al.Genome sequencing and analysis of Aspergillus oryzae.Nature. 2005; 438: 1157-1161Crossref PubMed Scopus (992) Google Scholar, 14Machida M. Yamada O. Gomi K. Genomics of Aspergillus oryzae: learning from the history of Koji mold and exploration of its future.DNA Res. 2008; 15: 173-183Crossref PubMed Scopus (266) Google Scholar]. To identify functional differences and putative adaptations to this starch-rich diet, we examined the transcriptome profiles of three phylogenetically distinct isolates of sake-derived A. oryzae, as well as the proteome profiles of the reference isolate of each species, during growth on rice. Similar to the analyses of the PSSR gene content, comparison of the transcriptome and proteome profiles between A. oryzae and A. flavus identified several differentially abundant transcripts, proteins, and pathways involved in PM and SM. All A. oryzae isolates possess two or three copies of α-amylase [7Machida M. Asai K. Sano M. Tanaka T. Kumagai T. Terai G. Kusumoto K. Arima T. Akita O. Kashiwagi Y. et al.Genome sequencing and analysis of Aspergillus oryzae.Nature. 2005; 438: 1157-1161Crossref PubMed Scopus (992) Google Scholar, 21Hunter A.J. Jin B. Kelly J.M. Independent duplications of α-amylase in different strains of Aspergillus oryzae.Fungal Genet. Biol. 2011; 48: 438-444Crossref PubMed Scopus (18) Google Scholar], the enzyme that hydrolyzes the α-D-glycosidic bonds of starch to produce dextrin, compared to a single copy in A. flavus. We found that the transcript and protein abundance of α-amylase was the highest of any A. oryzae gene or protein and was significantly upregulated compared to A. flavus (gene expression: FET, p < 1 × 10−300; protein abundance: >30-fold, FET, p = 2.15 × 10−51) (Figure 3; Tables S5–S8). Several other A. oryzae upregulated genes are involved in carbohydrate PM, including the genome neighbors amylolytic transcriptional activator amyR [33Gomi K. Akeno T. Minetoki T. Ozeki K. Kumagai C. Okazaki N. Iimura Y. Molecular cloning and characterization of a transcriptional activator gene, amyR, involved in the amylolytic gene expression in Aspergillus oryzae.Biosci. Biotechnol. Biochem. 2000; 64: 816-827Crossref PubMed Scopus (96) Google Scholar] (FET, p = 1.68 × 10−97) and saccharide-metabolizing enzyme maltase glucoamylase (FET, p = 1.79 × 10−17), as well as the glucose-metabolizing enzyme sorbitol dehydrogenase (FET, p = 8.22 × 10−252) (Figure S3; Tables S6 and S8). Importantly, comparison of the transcriptional profile of the two species showed that both the upregulated and downregulated gene sets in A. oryzae were overrepresented for carbohydrate PM (FET; p = 6.24 × 10−5 and p = 4.22 × 10−12, respectively), suggesting that differential regulation of PM is a key functional difference between the two species. A. oryzae is also equipped with an arsenal of secreted enzymes that break down the proteins and complex polysaccharides of grain outer layers, providing access to the starch-rich interior layers [7Machida M. Asai K. Sano M. Tanaka T. Kumagai T. Terai G. Kusumoto K. Arima T. Akita O. Kashiwagi Y. et al.Genome sequencing and analysis of Aspergillus oryzae.Nature. 2005; 438: 1157-1161Crossref PubMed Scopus (992) Google Scholar, 13Kobayashi T. Abe K. Asai K. Gomi K. Juvvadi P.R. Kato M. Kitamoto K. Takeuchi M. Machida M. Genomics of Aspergillus oryzae.Biosci. Biotechnol. Biochem. 2007; 71: 646-670Crossref PubMed Scopus (138) Google Scholar, 16Yoshizawa K. Sake: Production and flavor.Food Rev. Int. 1999; 15: 83-107Crossref Scopus (38) Google Scholar, 34Kitamoto K. Molecular biology of the Koji molds.Adv. Appl. Microbiol. 2002; 51: 129-153Crossref PubMed Scopus (138) Google Scholar]. Several protease-encoding genes are located in PSSRs (e.g., the methionine aminopeptidase located in the PSSR C5-8), are upregulated (e.g., extracellular cellulase celA), or both (e.g., the upregulated proteinase located in PSSR C2-7) (Figures 1C and 1D; Tables S3 and S5–S8). In contrast, 16 of the 27 plant polysaccharide-degrading genes are downregulated (a few of them are also located in PSSRs, e.g., endoglucanase and feruloyl esterase in PSS C3-5 and endo-1,4-β-xylanase in PSS C5-6) (Tables S5, S7, and S8). The broad downregulation of this subset of genes likely reflects differences between A. oryzae and A. flavus. Comparison of the gene expression profiles of 610 genes in all 55 predicted SM gene clusters [35Khaldi N. Seifuddin F.T. Turner G. Haft D. Nierman W.C. Wolfe K.H. Fedorova N.D. SMURF: Genomic mapping of fungal secondary metabolite clusters.Fungal Genet. Biol. 2010; 47: 736-741Crossref PubMed Scopus (526) Google Scholar] against background genes in the two species showed that another general characteristic of the A. oryzae transcriptome during growth on rice is SM downregulation (FET, p = 7.3 × 10−10). This is consistent with the wholesale downregulation of five SM gene clusters in A. oryzae (Figure 4). Importantly, both the cyclopiazonic acid and the aflatoxin SM pathways in A. oryzae were downregulated (Figures 4A and 4B), explaining a key phenotypic difference between A. oryzae and A. flavus, the inability of the first to produce either of the two toxins [7Machida M. Asai K. Sano M. Tanaka T. Kumagai T. Terai G. Kusumoto K. Arima T. Akita O. Kashiwagi Y. et al.Genome sequencing and analysis of Aspergillus oryzae.Nature. 2005; 438: 1157-1161Crossref PubMed Scopus (992) Google Scholar, 22Kato N. Tokuoka M. Shinohara Y. Kawatani M. Uramoto M. Seshime Y. Fujii I. Kitamoto K. Takahashi T. Takahashi S. et al.Genetic safeguard against mycotoxin cyclopiazonic acid production in Aspergillus oryzae.ChemBioChem. 2011; 12: 1376-1382Crossref PubMed Scopus (25) Google Scholar, 36Rank C. Klejnstrup M. Petersen L. Kildgaard S. Frisvad J. Gotfredsen C. Larsen T. Comparative chemistry of Aspergillus oryzae (RIB40) and A. flavus (NRRL 3357).Metabolites. 2012; 2: 36-56Crossref Scopus (62) Google Scholar]. We further investigated sequence variation in the isolates using expression data with respect to five previously characterized types of mutations observed at the aflatoxin gene cluster locus: (1) transcription binding-site mutations in the aflR promoter [37Tominaga M. Lee Y.H. Hayashi R. Suzuki Y. Yamada O. Sakamoto K. Gotoh K. Akita O. Molecular analysis of an inactive aflatoxin biosynthesis gene cluster in Aspergillus oryzae RIB strains.Appl. Environ. Microbiol. 2006; 72: 484-490Crossref PubMed Scopus (102) Google Scholar], (2) an ∼250 bp 3′ deletion in the aflT coding region [37Tominaga M. Lee Y.H. Hayashi R. Suzuki Y. Yamada O. Sakamoto K. Gotoh K. Akita O. Molecular analysis of an inactive aflatoxin biosynthesis gene cluster in Aspergillus oryzae RIB strains.Appl. Environ. Microbiol. 2006; 72: 484-490Crossref PubMed Scopus (102) Google Scholar], (3) a frameshift mutation in the norA coding region [37Tominaga M. Lee Y.H. Hayashi R. Suzuki Y. Yamada O. Sakamoto K. Gotoh K. Akita O. Molecular analysis of an inactive aflatoxin biosynthesis gene cluster in Aspergillus oryzae RIB strains.Appl. Environ. Microbiol. 2006; 72: 484-490Crossref PubMed Scopus (102) Google Scholar], (4) multiple nonsynonymous mutations in the verA coding region [37Tominaga M. Lee Y.H. Hayashi R. Suzuki Y. Yamada O. Sakamoto K. Gotoh K. Akita O. Molecular analysis of an inactive aflatoxin biosynthesis gene cluster in Aspergillus oryzae RIB strains.Appl. Environ. Microbiol. 2006; 72: 484-490Crossref PubMed Scopus (102) Google Scholar], and (5) an ∼40 kb deletion spanning the genom" @default.
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• W2086867029 title "The Evolutionary Imprint of Domestication on Genome Variation and Function of the Filamentous Fungus Aspergillus oryzae" @default.
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