Trichoderma reesei meiosis generates segmentally aneuploid progeny with higher xylanase-producing capability

详细信息    查看全文

• 作者：Yu-Chien Chuang (1) (2) (3)
  Wan-Chen Li (3) (4)
  Chia-Ling Chen (3)
  Paul Wei-Che Hsu (3)
  Shu-Yun Tung (3)
  Hsiao-Che Kuo (3) (6)
  Monika Schmoll (5)
  Ting-Fang Wang (1) (3)
  
  1. Taiwan International Graduate Program in Molecular and Cellular Biology ; Academia Sinica ; Taipei ; 115 ; Taiwan
  2. Institute of Life Sciences ; National Defense Medical Center ; Taipei ; 115 ; Taiwan
  3. Institute of Molecular Biology ; Academia Sinica ; Taipei ; 115 ; Taiwan
  4. Institute of Genome Sciences ; National Yang-Ming University ; Taipei ; 112 ; Taiwan
  6. Present address ; Department of Forest Sciences ; University of Helsinki ; Helsinki ; Finland
  5. Austrian Institute of Technology ; Health and Environment Department ; Bioresources ; University and Research Center ; UFT Campus Tulln ; Tulln/Donau ; 3430 ; Austria
  
• 关键词：Trichoderma reesei ; Hypocrea jecorina ; Genome evolution ; Aneuploidy ; Sexual development ; Meiosis ; Xylanase ; Conidia pigmentation ; Lignocellulosic biomass
• 刊名：Biotechnology for Biofuels
• 出版年：2015
• 出版时间：December 2015
• 年：2015
• 卷：8
• 期：1
• 全文大小：2,070 KB
• 参考文献：1. Cole, F, Keeney, S, Jasin, M (2010) Evolutionary conservation of meiotic DSB proteins: more than just Spo11. Genes Dev. 24: pp. 1201-7 CrossRef
  2. Crown, KN, Savytskyy, OP, Malik, SB, Logsdon, J, Williams, RS, Tainer, JA (2013) A mutation in the FHA domain of Coprinus cinereus Nbs1 leads to Spo11-independent meiotic recombination and chromosome segregation. G3 (Bethesda) 3: pp. 1927-43 CrossRef
  3. Bowring, FJ, Yeadon, PJ, Catcheside, DE (2013) Residual recombination in Neurospora crassa spo11 deletion homozygotes occurs during meiosis. Mol Genet Genomics. 288: pp. 437-44 CrossRef
  4. Turner, BC, Perkins, DD (1979) Spore killer, a chromosomal factor in Neurospora that kills meiotic products not containing it. Genetics. 93: pp. 587-606
  5. Raju, NB Spore killers: meiotic drive elements that distort genetic ratios. In: Osiewacz, HD eds. (2002) Molecular biology of fungal development. Marcel Dekker, New Yorkpp. 275
  6. Harvey, AM, Rehard, DG, Groskreutz, KM, Kuntz, DR, Sharp, KJ, Shiu, PK (2014) A critical component of meiotic drive in Neurospora is located near a chromosome rearrangement. Genetics. 197: pp. 1165-74 CrossRef
  7. Goodwin, SB, M'Barek, SB, Dhillon, B, Wittenberg, AH, Crane, CF, Hane, JK (2011) Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity, and stealth pathogenesis. PLoS Genet. 7: pp. e1002070 CrossRef
  8. Wittenberg, AH, Lee, TA, Ben M'barek, S, Ware, SB, Goodwin, SB, Kilian, A (2009) Meiosis drives extraordinary genome plasticity in the haploid fungal plant pathogen Mycosphaerella graminicola. PLoS One. 4: pp. e5863 CrossRef
  9. Coleman, JJ, Rounsley, SD, Rodriguez-Carres, M, Kuo, A, Wasmann, CC, Grimwood, J (2009) The genome of Nectria haematococca: contribution of supernumerary chromosomes to gene expansion. PLoS Genet. 5: pp. e1000618 CrossRef
  10. Taga, M, Murata, M, VanEtten, HD (1999) Visualization of a conditionally dispensable chromosome in the filamentous ascomycete Nectria haematococca by fluorescence in situ hybridization. Fungal Genet Biol. 26: pp. 169-77 CrossRef
  11. Tegtmeier, KJ, VanEtten, H (1982) Genetic studies on selected traits of Nectria haematococca. Phytopathology. 72: pp. 604-7 CrossRef
  12. Ni, M, Feretzaki, M, Li, W, Floyd-Averette, A, Mieczkowski, P, Dietrich, FS (2013) Unisexual and heterosexual meiotic reproduction generate aneuploidy and phenotypic diversity de novo in the yeast Cryptococcus neoformans. PLoS Biol. 11: pp. e1001653 CrossRef
  13. Fraser, JA, Huang, JC, Pukkila-Worley, R, Alspaugh, JA, Mitchell, TG, Heitman, J (2005) Chromosomal translocation and segmental duplication in Cryptococcus neoformans. Eukaryot Cell. 4: pp. 401-6 CrossRef
  14. Zanders, SE, Eickbush, MT, Yu, JS, Kang, JW, Fowler, KR, Smith, GR (2014) Genome rearrangements and pervasive meiotic drive cause hybrid infertility in fission yeast. Elife. 3: pp. e02630 CrossRef
  15. Tang, YC, Amon, A (2013) Gene copy-number alterations: a cost-benefit analysis. Cell. 152: pp. 394-405 CrossRef
  16. Gresham, D, Desai, MM, Tucker, CM, Jenq, HT, Pai, DA, Ward, A (2008) The repertoire and dynamics of evolutionary adaptations to controlled nutrient-limited environments in yeast. PLoS Genet. 4: pp. e1000303 CrossRef
  17. Yona, AH, Manor, YS, Herbst, RH, Romano, GH, Mitchell, A, Kupiec, M (2012) Chromosomal duplication is a transient evolutionary solution to stress. Proc Natl Acad Sci U S A. 109: pp. 21010-5 CrossRef
  18. Chang, SL, Lai, HY, Tung, SY, Leu, JY (2013) Dynamic large-scale chromosomal rearrangements fuel rapid adaptation in yeast populations. PLoS Genet. 9: pp. e1003232 CrossRef
  19. Schuster, A, Schmoll, M (2010) Biology and biotechnology of Trichoderma. Appl Microbiol Biotechnol. 87: pp. 787-99 CrossRef
  20. Peterson, R, Nevalainen, H (2012) Trichoderma reesei RUT-C30 - thirty years of strain improvement. Microbiology. 158: pp. 58-68 CrossRef
  21. Montenecourt Bland, S, Eveleigh Douglas, E (1979) Selective screening methods for the isolation of high yielding cellulase mutants of Trichoderma reesei. Hydrolysis of cellulose: mechanisms of enzymatic and acid catalysis. ACS Publications, Washington, DC, pp. 289-301 CrossRef
  22. Montenecourt, BS, Eveleigh, DE (1977) Preparation of mutants of Trichoderma reesei with enhanced cellulase production. Appl Environ Microbiol. 34: pp. 777-82
  23. Mandels, M, Weber, J, Parizek, R (1971) Enhanced cellulase production by a mutant of Trichoderma viride. Applied Microbiol. 21: pp. 152-4
  24. Vitikainen, M, Arvas, M, Pakula, T, Oja, M, Penttila, M, Saloheimo, M (2010) Array comparative genomic hybridization analysis of Trichoderma reesei strains with enhanced cellulase production properties. BMC Genomics. 11: pp. 441 CrossRef
  25. Martinez, D, Berka, RM, Henrissat, B, Saloheimo, M, Arvas, M, Baker, SE (2008) Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina). Nat Biotechnol 26: pp. 553-60 CrossRef
  26. Samuels, GJ, Petrini, O, Manguin, S (1994) Morphological and macromolecular characterization of Hypocrea schweinitzii and its Trichoderma anamorph. Micologia. 86: pp. 421-35 CrossRef
  27. Seidl, V, Seibel, C, Kubicek, CP, Schmoll, M (2009) Sexual development in the industrial workhorse Trichoderma reesei. Proc Natl Acad Sci U S A. 106: pp. 13909-14 CrossRef
  28. Penttila, M, Nevalainen, H, Ratto, M, Salminen, E, Knowles, J (1987) A versatile transformation system for the cellulolytic filamentous fungus Trichoderma reesei. Gene. 61: pp. 155-64 CrossRef
  29. Herrera-Estrella, A, Goldman, GH, Montagu, M, Geremia, RA (1993) Electrophoretic karyotype and gene assignment to resolved chromosomes of Trichoderma spp. Mol Microbiol. 7: pp. 515-21 CrossRef
  30. Mantyla, AL, Rossi, KH, Vanhanen, SA, Penttila, ME, Suominen, PL, Nevalainen, KM (1992) Electrophoretic karyotyping of wild-type and mutant Trichoderma longibrachiatum (reesei) strains. Curr Genet. 21: pp. 471-7 CrossRef
  31. Jung, MK, Ovechkina, Y, Prigozhina, N, Oakley, CE, Oakley, BR (2000) The use of beta-D-glucanase as a substitute for Novozym 234 for immunofluorescence and protoplasting. Fungal Genet Newsletter. 47: pp. 65-6
  32. Deriano, L, Roth, DB (2013) Modernizing the nonhomologous end-joining repertoire: alternative and classical NHEJ share the stage. Annu Rev Gen. 47: pp. 433-55 CrossRef
  33. Steiger, MG, Vitikainen, M, Uskonen, P, Brunner, K, Adam, G, Pakula, T (2011) Transformation system for Hypocrea jecorina (Trichoderma reesei) that favors homologous integration and employs reusable bidirectionally selectable markers. Appl Environ Microbiol. 77: pp. 114-21 CrossRef
  34. Guangtao, Z, Hartl, L, Schuster, A, Polak, S, Schmoll, M, Wang, T (2009) Gene targeting in a nonhomologous end joining deficient Hypocrea jecorina. J Biotechnol. 139: pp. 146-51 CrossRef
  35. Lieckfeldt, E, Kullnig, C, Samuels, GJ, Kubicek, CP (2000) Sexually competent, sucrose- and nitrate-assimilating strains of Hypocrea jecorina (Trichoderma reesei) from South American soils. Mycologia. 92: pp. 374-80 CrossRef
  36. Mandels, M, Reese, ET (1957) Induction of cellulase in Trichoderma viride as influenced by carbon sources and metals. J Bacteriol. 73: pp. 269-78
  37. Atanasova, L, Knox, BP, Kubicek, CP, Druzhinina, IS, Baker, SE (2013) The polyketide synthase gene pks4 of Trichoderma reesei provides pigmentation and stress resistance. Eukaryot Cell. 12: pp. 1499-508 CrossRef
  38. Hakkinen, M, Arvas, M, Oja, M, Aro, N, Penttila, M, Saloheimo, M (2012) Re-annotation of the CAZy genes of Trichoderma reesei and transcription in the presence of lignocellulosic substrates. Microb Cell Fact. 11: pp. 134 CrossRef
  39. Stukenbrock, EH (2013) Evolution, selection and isolation: a genomic view of speciation in fungal plant pathogens. New Phytologist. 199: pp. 895-907 CrossRef
  40. Chen, CL, Kuo, HC, Tung, SY, Hsu, PW, Wang, CL, Seibel, C (2012) Blue light acts as a double-edged sword in regulating sexual development of Hypocrea jecorina (Trichoderma reesei). PLoS One. 7: pp. e44969 CrossRef
  41. Nordberg, H, Cantor, M, Dusheyko, S, Hua, S, Poliakov, A, Shabalov, I (2014) The genome portal of the Department of Energy Joint Genome Institute: 2014 updates. Nucleic Acid Res. 42: pp. D26-31 CrossRef
  42. Tisch, D, Kubicek, CP, Schmoll, M (2011) The phosducin-like protein PhLP1 impacts regulation of glycoside hydrolases and light response in Trichoderma reesei. BMC Genomics. 12: pp. 613 CrossRef
  
• 刊物类别：Chemistry and Materials Science
• 刊物主题：Biotechnology
  Plant Breeding/Biotechnology
  Renewable and Green Energy
  Environmental Engineering/Biotechnology
  
• 出版者：BioMed Central
• ISSN：1754-6834

文摘

Background Hypocrea jecorina is the sexual form of the industrial workhorse fungus Trichoderma reesei that secretes cellulases and hemicellulases to degrade lignocellulosic biomass into simple sugars, such as glucose and xylose. H. jecorina CBS999.97 is the only T. reesei wild isolate strain that is sexually competent in laboratory conditions. It undergoes a heterothallic reproductive cycle and generates CBS999.97(1-1) and CBS999.97(1-2) haploids with MAT1-1 and MAT1-2 mating-type loci, respectively. T. reesei QM6a and its derivatives (RUT-C30 and QM9414) all have a MAT1-2 mating type locus, but they are female sterile. Sexual crossing of CBS999.97(1-1) with either CBS999.97(1-2) or QM6a produces fruiting bodies containing asci with 16 linearly arranged ascospores (the sexual spores specific to ascomycetes). This sexual crossing approach has created new opportunities for these biotechnologically important fungi. Results Through genetic and genomic analyses, we show that the 16 ascospores are generated via meiosis followed by two rounds of postmeiotic mitosis. We also found that the haploid genomes of CBS999.97(1-2) and QM6a are similar to that of the ancestral T. reesei strain, whereas the CBS999.97(1-1) haploid genome contains a reciprocal arrangement between two scaffolds of the CBS999.97(1-2) genome. Due to sequence heterozygosity, most 16-spore asci (>90%) contain four or eight inviable ascospores and an equal number of segmentally aneuploid (SAN) ascospores. The viable SAN progeny produced higher levels of xylanases and white conidia due to segmental duplication and deletion, respectively. Moreover, they readily lost the duplicated segment approximately two weeks after germination. With better lignocellulosic biomass degradation capability, these SAN progeny gain adaptive advantages to the natural environment, especially in the early phase of colonization. Conclusions Our results have not only further elucidated T. reesei evolution and sexual development, but also provided new perspectives for improving T. reesei industrial strains.