Advertisement

The Genetic Basis of Abiotic Stress Resistance in Extremophilic Fungi: The Genes Cloning and Application

  • Shi-Hong ZhangEmail author
Chapter
Part of the Fungal Biology book series (FUNGBIO)

Abstract

In eukaryotic organisms, many genera of fungi have successfully colonized various extreme environments known on earth. For example, some species thrive in hypersaline environments and some uniquely inhabit bare rock surface niches in hot or cold deserts where other eukaryotes such as plants can hardly survive under these conditions. Therefore, extremophilic fungi are excellent models to provide understanding in the resistant mechanisms that allow higher organisms to overcome stress; these fungi present valuable resources for isolation of resistance genes to be applied in genetic engineering and biotechnology. As a model fungus, the unicellular yeast Saccharomyces cerevisiae exhibits characteristics responses to a variety of stressors, it is a practical genetic tool to identify and validate abiotic stress resistant genes. In addition, it has led to the discovery of two significant osmotic-resistance pathways: the high-osmolarity glycerol response (HOG1) pathway and calcineurin-dependent pathway. With the increasing number of fungal species being characterized and sequenced, extremophilic fungi are found to be better systems to reveal the complex extremo-resistant mechanisms, and for the isolation of abiotic stress resistance and related genes. A series of environmental stress-related genes have been investigated in diverse groups of fungi, and no doubt these specific resistance genes could be valuable for the improvement of crop tolerance to single or multiple stresses. Interestingly, several ribosomal proteins recently isolated from the extremophilic fungi have been reported to possess abiotic stress resistant functions (moonlighting functions). Collectively, a tremendous amount of tolerant genes (e.g., HOG1) cloned from extremophilic fungi appeared to be more resistant to abiotic stress than their homologs or orthologs cloned from non-extremophilic fungi, though these proteins are highly conserved and exist in a wide variety of organisms. Taking into account the special characteristics/mechanisms of genes from extremophilic fungi in stress responses, the application of these types of genes might be more valuable and reliable for biotechnological applications.

Keywords

Extremophilic fungi Abiotic stress resistance mechanisms Resistant genes to abiotic stress Application strategies 

Notes

Acknowledgments

This work was partially supported by a grant of National Natural Science Foundation of China (31171794) and a project of Ministry of Agriculture of China (2011ZX08009-001). The author is very grateful to Dr. Diane Purchase who reviewed individual sentences and gave tremendous help to the preparation of this chapter. The author also likes to express his thanks to Dr. Liu Shou-An who kindly helped to revise the manuscript of this chapter.

References

  1. Ahmadpour D, Geijer C, Tamás MJ, Lindkvist-Petersson K, Hohmann S (2014) Yeast reveals unexpected roles and regulatory features of aquaporins and aquaglyceroporins. Biochim Biophys Acta 1840:1482–1491CrossRefPubMedGoogle Scholar
  2. Albertyn J, Hohmann S, Thevelein JM, Prior BA (1994) GPD1, which encodes glycerol 3-phosphate dehydrogenase, is essential for growth under osmotic stress in Saccharomyces cerevisiae, and its expression is regulated by the high osmolarity glycerol response pathway. Mol Cell Biol 14:4135–4144CrossRefPubMedPubMedCentralGoogle Scholar
  3. Allen GJ, Sanders D (1995) Calcineurin, a type 2B protein phosphatase, modulates the calcium-permeable slow vacuolar ion channel of stomatal guard cells. Plant Cell 7:1473–1483PubMedPubMedCentralGoogle Scholar
  4. Almagro A, Prista C, Castro S, Quintas C, Madeira-Lopes A, Ramos J et al (2000) Effects of salts on Debaryomyces hansenii and Saccharomyces cerevisiae under stress conditions. Int J Food Microbiol 56:191–197CrossRefPubMedGoogle Scholar
  5. Alonso-Monge R, Navarro-García F, Román E, Negredo AI, Eisman B, Nombela C et al (2006) The Hog1 mitogen-activated protein kinase is essential in the oxidative stress response and chlamydospore formation in Candida albicans. Eukaryot Cell 2(2):351–361CrossRefGoogle Scholar
  6. Alpert P (2000) The discovery, scope, and puzzle of desiccation tolerance in plants. Plant Ecol 151:5–17CrossRefGoogle Scholar
  7. Berka RM, Grigoriev IV, Otillar R, Salamov A, Grimwood J, Reid I et al (2011) Comparative genomic analysis of the thermophilic biomass-degrading fungi Myceliophthora thermophila and Thielavia terrestris. Nat Biotechnol 29(10):922–927. doi: 10.1038/nbt.1976 CrossRefPubMedGoogle Scholar
  8. Bhatnagar-Mathur P, Vadez V, Sharma KK (2008) Transgenic approaches for abiotic stress tolerance in plants: retrospect and prospects. Plant Cell Rep 27(3):411–424CrossRefPubMedGoogle Scholar
  9. Brewster JL, de Valoir T, Dwyer ND, Winter E, Gustin MC (1993) An osmosensing signal transduction pathway in yeast. Science 259:1760–1763CrossRefPubMedGoogle Scholar
  10. Brown AD (1978) Compatible solutes and extreme water stress in eukaryotic micro-organisms. Adv Microb Physiol 17:181–242CrossRefPubMedGoogle Scholar
  11. Chen YL, Yu SJ, Huang HY, Chang YL, Lehman VN, Silao FG et al (2014) Calcineurin controls hyphal growth, virulence, and drug tolerance of Candida tropicalis. Eukaryot Cell 13(7):844–854. doi: 10.1128/EC.00302-13 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Crowe JH, Hoekstra FA, Crowe LM (1992) Anhydrobiosis. Annu Rev Physiol 54:579–599CrossRefPubMedGoogle Scholar
  13. Dana MM, Pintor-Toro JA, Cubero B (2006) Transgenic tobacco plants overexpressing chitinases of fungal origin show enhanced resistance to biotic and abiotic stress agents. Plant Physiol 142:722–730CrossRefPubMedCentralGoogle Scholar
  14. de Wit PJ (1992) Molecular characterization of gene-for-gene systems in plant-fungus interactions and the application of avirulence genes in control of plant pathogens. Annu Rev Phytopathol 30:391–418CrossRefPubMedGoogle Scholar
  15. Delgado-Jarana J, Sousa S, González F, Rey M, Llobell A (2006) ThHog1 controls the hyperosmotic stress response in Trichoderma harzianum. Microbiology 152(Pt 6):1687–1700CrossRefPubMedGoogle Scholar
  16. Dey N, Sarkar S, Acharya S, Maiti IB (2015) Synthetic promoters in planta. Planta. doi: 10.1007/s00425-015-2377-2 PubMedGoogle Scholar
  17. Dietz S, von Bülow J, Beitz E, Nehls U (2011) The aquaporin gene family of the ectomycorrhizal fungus Laccaria bicolor: lessons for symbiotic functions. New Phytol 190:927–940. doi: 10.1111/j.1469-8137.2011.03651.x CrossRefPubMedGoogle Scholar
  18. Elbein AD, Pan YT, Pastuszak I, Carroll D (2003) New insights on trehalose: a multifunctional molecule. Glycobiology 13:17R–27RCrossRefPubMedGoogle Scholar
  19. Enjalbert B, Smith DA, Cornell MJ, Alam I, Nicholls S, Brown AJP et al (2006) Role of Hog-1 stress-activated protein kinase in the global transcriptional response to stress in the fungal pathogen Candida albicans. Mol Biol Cell 17:1018–1032CrossRefPubMedPubMedCentralGoogle Scholar
  20. García-Salcedo R, Casamayor A, Ruiz A, González A, Prista C, Loureiro-Dias MC et al (2006) Heterologous expression implicates a GATA factor in regulation of nitrogen metabolic genes and ion homeostasis in the halotolerant yeast Debaryomyces hansenii. Eukaryot Cell 5(8):1388–1398CrossRefPubMedPubMedCentralGoogle Scholar
  21. Gorbushina AA (2007) Life on the rocks. Environ Microbiol 9(7):1613–1631CrossRefPubMedGoogle Scholar
  22. Gostinčar C, Turk M (2012) Extremotolerant fungi as genetic resources for biotechnology. Bioengineered 3(5):293–297. doi: 10.4161/bioe.20713 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Gray J, Shear W (1992) Early life on land. Am Sci 80:444–456Google Scholar
  24. Gupta B, Huang B (2014) Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Int J Genomics 701596. doi: 10.1155/2014/701596
  25. Hayes BME, Anderson M, Traven A, van der Weerden NL, Bleackley MR (2014) Activation of stress signalling pathways enhances tolerance of fungi to chemical fungicides and antifungal proteins. Cell Mol Life Sci 71:2651–2666CrossRefPubMedGoogle Scholar
  26. Heckman DS, Geiser DM, Eidell BR, Stauffer RL, Kardos NL, Hedges SB (2001) Molecular evidence for the early colonization of land by fungi and plants. Science 293(5532):1129–1133CrossRefPubMedGoogle Scholar
  27. Hermosa R, Botella L, Keck E, Jiménez JA, Montero-Barrientos M, Arbona V et al (2011) The overexpression in Arabidopsis sthaliana of a Trichoderma harzianum gene that modulates glucosidase activity, and enhances tolerance to salt and osmotic stresses. J Plant Physiol 168:1295–1302CrossRefPubMedGoogle Scholar
  28. Hohmann I, Bill RM, Kayingo I, Prior BA (2000) Microbial MIP channels. Trends Microbiol 8:33–38. doi: 10.1016/S0966-842X(99)01645-5 CrossRefPubMedGoogle Scholar
  29. Hohmann S, Krantz M, Nordlander B (2007) Yeast osmoregulation. Methods Enzymol 428:29–45. doi: 10.1016/S0076-6879(07)28002-4 CrossRefPubMedGoogle Scholar
  30. Horodyski RJ, Knauth LP (1994) Life on land in the precambrian. Science 263(5146):494–498CrossRefPubMedGoogle Scholar
  31. Hou Z, Xue C, Peng Y, Katan T, Kistler HC, Xu J-R (2002) A mitogen-activated protein kinase gene (MGv1) in Fusarium graminearum is required for female fertility, heterokaryon formation, and plant infection. Mol Plant Microbe Interact 15(11):1119–1127CrossRefPubMedGoogle Scholar
  32. Ikner A, Shiozaki K (2005) Yeast signalling pathways in the oxidative stress response. Mutat Res 569(1–2):13–27CrossRefPubMedGoogle Scholar
  33. Juvvadi PR, Lamoth F, Steinbach WJ (2014) Calcineurin as a multifunctional regulator: unraveling novel functions in fungal stress responses, hyphal growth, drug resistance, and pathogenesis. Fungal Biol Rev 28(2–3):56–69CrossRefPubMedPubMedCentralGoogle Scholar
  34. Kis-Papo T, Grishkan I, Oren A, Wasser SP, Nevo E (2001) Spatiotemporal diversity of filamentous fungi in the hypersaline Dead Sea. Mycol Res 105:749–756CrossRefGoogle Scholar
  35. Kraus PR, Fox DS, Cox GM, Heitman J (2003) The Cryptococcus neoformans MAP kinase Mpk1 regulates cell integrity in response to antifungal drugs and loss of calcineurin function. Mol Microbiol 48(5):1377–1387CrossRefPubMedPubMedCentralGoogle Scholar
  36. Lam HM, Xu X, Liu X, Chen W, Yang G, Wong FL et al (2010) Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nat Genet 42(12):1053–1059. doi: 10.1038/ng.715 CrossRefPubMedGoogle Scholar
  37. Levin DE (2011) Regulation of cell wall biogenesis in Saccharomyces cerevisiae: the cell wall integrity signaling pathway. Genetics 189(4):1145–1175CrossRefPubMedPubMedCentralGoogle Scholar
  38. Li T, Hu YJ, Hao ZP, Li H, Chen BD (2013) Aquaporin genes GintAQPF1and GintAQPF2 from Glomus intraradices contribute to plant drought tolerance. Plant Signal Behav 8:e24030. doi: 10.4161/psb.24030 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Liang X, Liu Y, Xie L, Liu X, Wei Y, Zhou X et al (2015) A ribosomal protein AgRPS3aE from halophilic Aspergillus glaucus confers salt tolerance in heterologous organisms. Int J Mol Sci 16(2):3058–3070. doi: 10.3390/ijms16023058 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Liu XD, Xie L, Wei Y, Zhou XY, Jia B, Liu J, Zhang SH (2014) Abiotic stress resistance, a novel moonlighting function of ribosomal protein RPL44 in the halophilic fungus Aspergillus glaucus. Appl Environ Microbiol 80(14):4294–4300. doi: 10.1128/AEM.00292-14 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Liu XD, Wei Y, Zhou XY, Pei X, Zhang SH (2015) Aspergillus glaucus aquaglyceroporin gene glpF confers high osmosis tolerance in heterologous organisms. Appl Environ Microbiol 81(19):6926–6937. doi: 10.1128/AEM.02127-15 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Luan S, Li W, Rusnak F, Assmann SM, Schreiber SL (1993) Immunosuppressants implicate protein phosphatase regulation of K + channels in guard cells. Proc Natl Acad Sci USA 90:2202–2206CrossRefPubMedPubMedCentralGoogle Scholar
  43. Luyten K, Albertyn J, Skibbe WF, Prior BA, Ramos J, Thevelein JM et al (1995) Fps1, a yeast member of the MIP family of channel proteins, is a facilitator for glycerol uptake and efflux and is inactive under osmotic stress. EMBO J 14:1360–1371PubMedPubMedCentralGoogle Scholar
  44. Martínez F, Arif A, Nebauer SG, Bueso E, Ali R, Montesinos C et al (2015) A fungal transcription factor gene is expressed in plants from its own promoter and improves drought tolerance. Planta 242(1):39–52. doi: 10.1007/s00425-015-2285-5 CrossRefPubMedGoogle Scholar
  45. Matheos DP, Kingsbury TJ, Ahsan US, Cunningham KW (1997) Tcn1p/Crz1p, a calcineurin-dependent transcription factor that differentially regulates gene expression in Saccharomyces cerevisiae. Genes Dev 11:3445–3458CrossRefPubMedPubMedCentralGoogle Scholar
  46. McHunu NP, Permaul K, Abdul Rahman AY, Saito JA, Singh S, Alam M (2013) Xylanase superproducer: genome sequence of a Ccmpost-loving thermophilic fungus, Thermomyces lanuginosus strain SSBP. Genome Announc 1(3) e00388–13. doi: 10.1128/genomeA.00388-13
  47. Mendoza I, Rubio F, Rodriguez-Navarro A, Pardo JM (1994) The protein phosphatase calcineurin is essential for NaCl tolerance of Saccharomyces cerevisiae. J Biol Chem 269:8792–8796PubMedGoogle Scholar
  48. Montañés FM, Pascual-Ahuir A, Proft M (2011) Repression of ergosterol biosynthesis is essential for stress resistance and is mediated by the Hog1 MAP kinase and the Mot3 and Rox1 transcription factors. Mol Microbiol 79(4):1008–1023CrossRefPubMedGoogle Scholar
  49. Montero-Barrientos M, Hermosa MR, Cardoza RE, Gutiérrez S, Nicolás C, Monte E (2010) Transgenic expression of the Trichoderma harzianum HSP70 gene increases Arabidopsis resistance to heat and other abiotic stresses. J Plant Physiol 167:659–665CrossRefPubMedGoogle Scholar
  50. Montero-Barrientos M, Hermosa R, Nicolás C, Cardoza RE, Gutiérrez S, Monte E (2008) Overexpression of a Trichoderma HSP70 gene increases fungalresistance to heat and other abiotic stresses. Fungal Genet Biol 45:1506–1513CrossRefPubMedGoogle Scholar
  51. Nakamura TY, Liu Y, Hirata D, Namba H, Harada S, Hirokawa T et al (1993) Protein phosphatase type 2B (calcineurin)-mediated, FK506-sensitive regulation of intracellular ions in yeast is an important determinant for adaptation to high salt stress conditions. EMBO J 12:4063–4071PubMedPubMedCentralGoogle Scholar
  52. Navarro-García F, Sánchez M, Pla J, Nombela C (1995) Functional characterization of the MKC1 gene of Candida albicans, which encodes a mitogen-activated protein kinase homolog related to cell integrity. Mol Cell Biol 15(4):2197–2206CrossRefPubMedPubMedCentralGoogle Scholar
  53. Navarro-García F, Eisman B, Fiuza SM, Nombela C, Pla J (2005) The MAP kinase Mkc1p is activated under different stress conditions in Candida albicans. Microbiology 151(8):2737–2749CrossRefPubMedGoogle Scholar
  54. Nicolás C, Hermosa R, Rubio B, Mukherjee PK, Monte E (2014) Trichoderma genes in plants for stress tolerance- status and prospects. Plant Sci 228:71–78CrossRefPubMedGoogle Scholar
  55. Oliveira R, Lages F, Silva-Graça M, Lucas C (2003) Fps1p channel is the mediator of the major part of glycerol passive diffusion in Saccharomyces cerevisiae: artefacts and re-definitions. Biochim Biophys Acta 1613:57–71. doi: 10.1016/S0005-2736(03)00138-X CrossRefPubMedGoogle Scholar
  56. Pahlman AK, Granath K, Ansell R, Hohmann S, Adler L (2001) The yeast glycerol 3-phosphatases gpp1p and gpp2p are required for glycerol biosynthesis and differentially involved in the cellular responses to osmotic, anaerobic, and oxidative stress. J Biol Chem 276:3555–3563CrossRefPubMedGoogle Scholar
  57. Panadero J, Hernández-López MJ, Prieto JA, Randez-Gil F (2007) Overexpression of the calcineurin target CRZ1 provides freeze tolerance and enhances the fermentative capacity of baker’s yeast. Appl Environ Microbiol 73(15):4824–4831CrossRefPubMedPubMedCentralGoogle Scholar
  58. Pereira I, Madeira A, Prista C, Loureiro-Dias MC, Leandro MJ (2014) Characterization of new polyol/H+ symporters in Debaryomyces hansenii. PLoS ONE 9(2):e88180. doi: 10.1371/journal.pone.0088180 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Petitjean M, Teste MA, François JM, Parrou JL (2015) Yeast tolerance to various stresses relies on the Trehalose-6P Synthase (Tps1) protein. Not on Trehalose J Biol Chem 290(26):16177–16190. doi: 10.1074/jbc.M115.653899 CrossRefPubMedGoogle Scholar
  60. Prasad AR, Maheshwari R (1978) Purification and properties of trehalase from the thermophilic fungus Humicola lanuginosa. Biochim Biophys Acta 525(1):162–170Google Scholar
  61. Prista C, Soeiro A, Vesely P, Almagro A, Ramos J, Loureiro-Dias MC (2002) Genes from Debaryomyces hansenii increase salt tolerance in Saccharomyces cerevisiae W303. FEMS Yeast Res 2:151–157PubMedGoogle Scholar
  62. Prista C, Loureiro-Dias MC, Montiel V, García R, Ramos J (2005) Mechanisms underlying the halotolerant way of Debaryomyces hansenii. FEMS Yeast Res 5(8):693–701CrossRefPubMedGoogle Scholar
  63. Redman RS, Kim YO, Woodward CJDA, Greer C, Espino L, Doty SL, Rodriguez RJ (2011) Increased fitness of rice plants to abiotic stress via habitat adapted symbiosis: a strategy for mitigating impacts of climate change. PLoS ONE 6(7):e14823. doi: 10.1371/journal.pone.0014823 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F et al (2008) Stress tolerance in plants via habitat-adapted symbiosis. ISME J 2(4):404–416. doi: 10.1038/ismej.2007.106 CrossRefPubMedGoogle Scholar
  65. Rui O, Hahn M (2007) The Slt2-type MAP kinase Bmp3 of Botrytis cinerea is required for normal saprotrophic growth, conidiation, plant surface sensing and host tissue colonization. Mol Plant Pathol. 8(2):173–184CrossRefPubMedGoogle Scholar
  66. Saito H, Posas F (2012) Response to hyperosmotic stress. Genetics 192(2):289–318CrossRefPubMedPubMedCentralGoogle Scholar
  67. San José C, Monge RA, Pérez-Díaz R, Pla J, Nombela C (1996) The mitogen-activated protein kinase homolog HOG1 gene controls glycerol accumulation in the pathogenic fungus Candida albicans. J Bacteriol 178(19):5850–5852Google Scholar
  68. Serrano R, Gaxiola R (1994) Microbial models and salt stress tolerance in plants. Crit Rev Plant Sci 13:121–138CrossRefGoogle Scholar
  69. Shoresh M, Harman GE, Mastouri F (2010) Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol 48:21–43CrossRefPubMedGoogle Scholar
  70. Singh S, Madlala AM, Prior BA (2003) Thermomyces lanuginosus: properties of strains and their hemicellulases. FEMS Microbiol Rev 27(1):3–16CrossRefPubMedGoogle Scholar
  71. Stathopoulos-Gerontides A, Guo JJ, Cyert MS (1999) Yeast calcineurin regulates nuclear localization of the Crz1p transcription factor through dephosphorylation. Genes Dev 13:798–803CrossRefPubMedPubMedCentralGoogle Scholar
  72. Tamás MJ, Luyten FC, Sutherland A, Hernandez J, Albertyn J, Valadi H et al (1999) Fps1p controls the accumulation and release of the compatible solute glycerol in yeast osmoregulation. Mol Microbiol 31:1087–1104. doi: 10.1046/j.1365-2958.1999.01248.x CrossRefPubMedGoogle Scholar
  73. Thomas E, Roman E, Claypool S, Manzoor N, Pla J, Panwar SL (2013) Mitochondria influences CDR1 efflux pump activity, Hog1-mediated oxidative stress pathway, iron homeostasis and ergosterol levels in Candida albicans. Antimicrob Agents Chemother 57(11):5580–5599CrossRefPubMedPubMedCentralGoogle Scholar
  74. Turk M, Abramović Z, Plemenitas A, Gunde-Cimerman N (2007) Salt stress and plasma-membrane fluidity in selected extremophilic yeasts and yeast-like fungi. FEMS Yeast Res 7(4):550–557CrossRefPubMedGoogle Scholar
  75. Valiante V, Heinekamp T, Jain R, Härtl A, Brakhage AA (2008) The mitogen-activated protein kinase MpkA of Aspergillus fumigatus regulates cell wall signaling and oxidative stress response. Fungal Genet Biol 45(5):618–627, 52Google Scholar
  76. Xu J-R, Staiger CJ, Hamer JE (1998) Inactivation of the mitogen-activated protein kinase Mps1 from the rice blast fungus prevents penetration of host cells but allows activation of plant defense responses. Proc Natl Acad Sci USA 95(21):12713–12718CrossRefPubMedPubMedCentralGoogle Scholar
  77. Xu H, Cooke JEK, Zwiazek JJ (2013) Phylogenetic analysis of fungal aquaporins provide insight into their possible role in water transport of mycorrhizal associations. Botany 91:495–504. doi: 10.1139/cjb-2013-0041 CrossRefGoogle Scholar
  78. Yan J, Song WN, Nevo E (2005) A MAPK gene from Dead Sea fungus confers stress tolerance to lithium salt and freezing-thawing: prospects for saline agriculture. Proc Natl Acad Sci USA 102(52):18992–18997CrossRefGoogle Scholar
  79. Zhan X, Zhu JK, Lang Z (2015) Increasing freezing tolerance: kinase regulation of ICE1. Dev Cell 32(3):257–258. doi: 10.1016/j.devcel.2015.01.004 CrossRefPubMedGoogle Scholar
  80. Zhang H, Guo J, Voegele RT, Zhang J, Duan Y, Luo H et al (2012) Functional characterization of calcineurin homologs PsCNA1/PsCNB1 in Puccinia striiformis f. sp. tritici using a host-induced RNAi system. PLoS ONE 7(11):e49262. doi: 10.1371/journal.pone.0049262 CrossRefPubMedPubMedCentralGoogle Scholar
  81. Zhang M, Liu Z, Yu Q, Mao J, Zhang B, Xing L et al (2015) Deletion of genes encoding fatty acid desaturases leads to alterations in stress sensitivity in Pichia pastoris. FEMS Yeast Res 15(4):fov020. doi: 10.1093/femsyr/fov020

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.College of Plant SciencesJilin UniversityChangchunChina

Personalised recommendations