1887

Abstract

-Arabinose, a major constituent pentose of plant cell-wall polysaccharides, has been suggested to be a less preferred carbon source for fungi but to be a potential signalling molecule that can cause distinct genome-wide transcriptional changes in fungal cells. Here, we explore the possibility that this unique pentose influences the morphological characteristics of the phytopathogenic fungus strain HITO7711. When grown on plate media under different sugar conditions, the mycelial dry weight of cultures on -arabinose was as low as that with no sugar, suggesting that -arabinose does not substantially contribute to vegetative growth. However, the intensity of conidiation on -arabinose was comparable to or even higher than that on -glucose and on -xylose, in contrast to the poor conidiation under the no-sugar condition. To explore the physiological basis of the passive growth and active conidiation on -arabinose, we next investigated cellular responses of the fungus to these sugar conditions. Transcriptional analysis of genes related to carbohydrate metabolism showed that -arabinose stimulates carbohydrate utilization through the hexose monophosphate shunt (HMP shunt), a catabolic pathway parallel to glycolysis and which participates in the generation of the reducing agent NADPH (the reduced form of nicotinamide adenine dinucleotide phosphate). Then, the HMP shunt was impaired by disrupting the related gene , which encodes glucose-6-phosphate dehydrogenase in this fungus. The resulting mutants on -arabinose showed remarkably decreased conidiation, but a conversely increased mycelial dry weight compared with the wild-type. Our study demonstrates that -arabinose acts to enhance resource allocation to asexual reproduction in HITO7711 at the cost of vegetative growth, and suggests that this is mediated by the concomitant stimulation of the HMP shunt.

Funding
This study was supported by the:
  • Sasakawa Scientific Research Grant (Award 2019-0434)
    • Principle Award Recipient: HiroshiYOSHIDA
  • Japan Society for the Promotion of Science (Award 19K06052)
    • Principle Award Recipient: ChihiroTANAKA
  • Japan Society for the Promotion of Science (Award 15H05249)
    • Principle Award Recipient: ChihiroTANAKA
  • Japan Society for the Promotion of Science (Award 15K07311)
    • Principle Award Recipient: ChihiroTANAKA
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2021-02-08
2024-05-09
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References

  1. Carpita NC, Gibeaut DM, Carpita NC, Gibeaut DM. Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 1993; 3:1–30 [View Article][PubMed]
    [Google Scholar]
  2. Biswal AK, Tan L, Atmodjo MA, DeMartini J, Gelineo-Albersheim I et al. Comparison of four glycosyl residue composition methods for effectiveness in detecting sugars from cell walls of dicot and grass tissues. Biotechnol Biofuels 2017; 10:182 [View Article][PubMed]
    [Google Scholar]
  3. Doco T, O'Neill MA, Pellerin P. Determination of the neutral and acidic glycosyl-residue compositions of plant polysaccharides by GC-EI-MS analysis of the trimethylsilyl methyl glycoside derivatives. Carbohydr Polym 2001; 46:249–259 [View Article]
    [Google Scholar]
  4. Miyamoto K, Oka M, Uheda E, Ueda J. Changes in metabolism of cell wall polysaccharides in oat leaves during senescence: relevance to the senescence-promoting effect of methyl jasmonate. Acta Physiol Plant 2013; 35:2675–2683 [View Article]
    [Google Scholar]
  5. Seiboth B, Metz B. Fungal arabinan and l-arabinose metabolism. Appl Microbiol Biotechnol 2011; 89:1665–1673 [View Article][PubMed]
    [Google Scholar]
  6. Healy RA, Horner HT, Bronson CR. Visual characterization of the extracellular matrix of Cochliobolus heterostrophus and a mutant strain with a modified matrix. Can J Bot 2004; 82:75–88 [View Article]
    [Google Scholar]
  7. Wheeler H. Ultrastructure of penetration by Helminthosporium maydis . Physiol Plant Pathol 1977; 11:171–178 [View Article]
    [Google Scholar]
  8. Bateman DF, Jones TM, Yoder OC. Degradation of corn cell walls by extracellular enzymes produced by Helminthosporium maydis race T. Phytopathology 1973; 63:1523–1529 [View Article]
    [Google Scholar]
  9. King BC, Waxman KD, Nenni NV, Walker LP, Bergstrom GC et al. Arsenal of plant cell wall degrading enzymes reflects host preference among plant pathogenic fungi. Biotechnol Biofuels 2011; 4:4 [View Article]
    [Google Scholar]
  10. Yoshida H, Tanaka C. Monitoring of in planta gene expression for xylan degradation and assimilation in the maize pathogen Bipolaris maydis . Mycoscience 2019; 60:116–124 [View Article]
    [Google Scholar]
  11. Chiang C, Knight SG. l-Arabinose metabolism by cell-free extracts of Penicillium chrysogenum . Biochim Biophys Acta 1961; 46:271–278 [View Article][PubMed]
    [Google Scholar]
  12. Witteveen CFB, Busink R, Van de Vondervoort P, Dijkema C, Swart K et al. l-Arabinose and d-xylose catabolism in Aspergillus niger . Microbiology 1989; 135:2163–2171 [View Article]
    [Google Scholar]
  13. Klaubauf S, Ribot C, Melayah D, Lagorce A, Lebrun M-H et al. The pentose catabolic pathway of the rice-blast fungus Magnaporthe oryzae involves a novel pentose reductase restricted to few fungal species. FEBS Lett 2013; 587:1346–1352 [View Article]
    [Google Scholar]
  14. Richard P, Putkonen M, Väänänen R, Londesborough J, Penttilä M. The missing link in the fungal l-arabinose catabolic pathway, identification of the l-xylulose reductase gene. Biochemistry 2002; 41:6432–6437 [View Article][PubMed]
    [Google Scholar]
  15. Li J, Lin L, Li H, Tian C, Ma Y. Transcriptional comparison of the filamentous fungus Neurospora crassa growing on three major monosaccharides d-glucose, d-xylose and l-arabinose. Biotechnol Biofuels 2014; 7:31 [View Article][PubMed]
    [Google Scholar]
  16. Abedon BG, Hatfield RD, Tracy WF. Cell wall composition in juvenile and adult leaves of maize (Zea mays L.). J Agric Food Chem 2006; 54:3896–3900 [View Article][PubMed]
    [Google Scholar]
  17. Scheller HV, Ulvskov P. Hemicelluloses. Annu Rev Plant Biol 2010; 61:263–289 [View Article]
    [Google Scholar]
  18. Smith BG, Harris PJ. The polysaccharide composition of Poales cell walls: Poaceae cell walls are not unique. Biochem Syst Ecol 1999; 27:33–53
    [Google Scholar]
  19. Tanaka C, Kubo Y, Tsuda M. Genetic analysis and characterization of Cochliobolus heterostrophus colour mutants. Mycol Res 1991; 95:49–56 [View Article]
    [Google Scholar]
  20. Smith DR, Hooker AL, Lim SM. Physiologic races of Helminthosporium maydis . Plant Dis Report 1970; 54:819–822
    [Google Scholar]
  21. Ribeiro OK. A Source Book of the Genus Phytophthora Vaduz: J. Cramer; 1978
    [Google Scholar]
  22. Leach J, Lang BR, Yoder OC. Methods for selection of mutants and in vitro culture of Cochliobolus heterostrophus . Microbiology 1982; 128:1719–1729 [View Article]
    [Google Scholar]
  23. Ohm RA, Feau N, Henrissat B, Schoch CL, Horwitz BA et al. Diverse lifestyles and strategies of plant pathogenesis encoded in the genomes of eighteen Dothideomycetes fungi. PLoS Pathog 2012; 8:e1003037 [View Article]
    [Google Scholar]
  24. Flipphi M, Sun J, Robellet X, Karaffa L, Fekete E et al. Biodiversity and evolution of primary carbon metabolism in Aspergillus nidulans and other Aspergillus spp. Fungal Genet Biol 2009; 46 (Suppl. 1):S19–S44 [View Article][PubMed]
    [Google Scholar]
  25. Stincone A, Prigione A, Cramer T, Wamelink MMC, Campbell K et al. The return of metabolism: biochemistry and physiology of the pentose phosphate pathway. Biol Rev Camb Philos Soc 2015; 90:927–963 [View Article][PubMed]
    [Google Scholar]
  26. Nordberg H, Cantor M, Dusheyko S, Hua S, Poliakov A et al. The genome portal of the Department of Energy Joint Genome Institute: 2014 updates. Nucleic Acids Res 2014; 42:D26–D31 [View Article]
    [Google Scholar]
  27. Sambrook J, Fritsch EF, Maniatis T. Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory; 1989
    [Google Scholar]
  28. Izumitsu K, Hatoh K, Sumita T, Kitade Y, Morita A et al. Rapid and simple preparation of mushroom DNA directly from colonies and fruiting bodies for PCR. Mycoscience 2012; 53:396–401 [View Article]
    [Google Scholar]
  29. Sumita T, Izumitsu K, Tanaka C. Characterization of the autophagy-related gene BmATG8 in Bipolaris maydis . Fungal Biol 2017; 121:785–797 [View Article]
    [Google Scholar]
  30. Davidson RC, Blankenship JR, Kraus PR, de Jesus Berrios M, Hull CM et al. A PCR-based strategy to generate integrative targeting alleles with large regions of homology. Microbiology 2002; 148:2607–2615 [View Article]
    [Google Scholar]
  31. Izumitsu K, Yoshimi A, Kubo D, Morita A, Saitoh Y et al. The MAPKK kinase ChSte11 regulates sexual/asexual development, melanization, pathogenicity, and adaptation to oxidative stress in Cochliobolus heterostrophus . Curr Genet 2009; 55:439–448 [View Article]
    [Google Scholar]
  32. Tanaka C, Nakada M, Tsuda M. Electrophoretic separation of chromosomes of some graminicolous fungi. Trans Mycol Soc Jpn 1992; 33:95–102
    [Google Scholar]
  33. Shimizu K, Tanaka C, Tsuda M. Cloning of Brn1, a reductase gene involved in melanin biosynthesis in Cochliobolus heterostrophus . J Gen Appl Microbiol 1997; 43:145–150 [View Article]
    [Google Scholar]
  34. Bischoff TW, Garraway MO. The effect of xylose on the growth and sporulation of an isolate of Bipolaris maydis race T and its relation to pH and ammonium levels. Phytopathology 1985; 75:138–141 [View Article]
    [Google Scholar]
  35. Cano-Domínguez N, Alvarez-Delfín K, Hansberg W, Aguirre J. NADPH oxidases NOX-1 and NOX-2 require the regulatory subunit NOR-1 to control cell differentiation and growth in Neurospora crassa . Eukaryot Cell 2008; 7:1352–1361 [View Article][PubMed]
    [Google Scholar]
  36. Egan MJ, Wang ZY, Jones MA, Smirnoff N, Talbot NJ. Generation of reactive oxygen species by fungal NADPH oxidases is required for rice blast disease. Proc Natl Acad Sci USA 2007; 104:11772–11777 [View Article]
    [Google Scholar]
  37. Minard KI, McAlister-Henn L. Sources of NADPH in yeast vary with carbon source. J Biol Chem 2005; 280:39890–39896 [View Article][PubMed]
    [Google Scholar]
  38. Battaglia E, Hansen SF, Leendertse A, Madrid S, Mulder H et al. Regulation of pentose utilisation by AraR, but not XlnR, differs in Aspergillus nidulans and Aspergillus niger . Appl Microbiol Biotechnol 2011; 91:387–397 [View Article]
    [Google Scholar]
  39. Klaubauf S, Narang HM, Post H, Zhou M, Brunner K et al. Similar is not the same: differences in the function of the (hemi-)cellulolytic regulator XlnR (Xlr1/Xyr1) in filamentous fungi. Fungal Genet Biol 2014; 72:73–81 [View Article][PubMed]
    [Google Scholar]
  40. Battaglia E, Zhou M, de Vries RP. The transcriptional activators AraR and XlnR from Aspergillus niger regulate expression of pentose catabolic and pentose phosphate pathway genes. Res Microbiol 2014; 165:531–540 [View Article]
    [Google Scholar]
  41. Klaubauf S, Zhou M, Lebrun MH, de Vries RP, Battaglia E. A novel l-arabinose-responsive regulator discovered in the rice-blast fungus Pyricularia oryzae (Magnaporthe oryzae). FEBS Lett 2016; 590:550–558 [View Article][PubMed]
    [Google Scholar]
  42. Wilson RA, Jenkinson JM, Gibson RP, Littlechild JA, Wang ZY et al. Tps1 regulates the pentose phosphate pathway, nitrogen metabolism and fungal virulence. EMBO J 2007; 26:3673–3685 [View Article][PubMed]
    [Google Scholar]
  43. Wilson RA, Gibson RP, Quispe CF, Littlechild JA, Talbot NJ. An NADPH-dependent genetic switch regulates plant infection by the rice blast fungus. Proc Natl Acad Sci USA 2010; 107:21902–21907 [View Article]
    [Google Scholar]
  44. Larochelle M, Drouin S, Robert F, Turcotte B. Oxidative stress-activated zinc cluster protein Stb5 has dual activator/repressor functions required for pentose phosphate pathway regulation and NADPH production. Mol Cell Biol 2006; 26:6690–6701 [View Article]
    [Google Scholar]
  45. Cadière A, Galeote V, Dequin S. The Saccharomyces cerevisiae zinc factor protein Stb5p is required as a basal regulator of the pentose phosphate pathway. FEMS Yeast Res 2010; 10:819–827 [View Article]
    [Google Scholar]
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