Advertisement

Indian Phytopathology

, Volume 71, Issue 2, pp 169–182 | Cite as

Understanding photoreception in fungi and its role in fungal development with focus on phytopathogenic fungi

  • Tarlochan S. Thind
  • Annemiek C. Schilder
Review Article
  • 8 Downloads

Abstract

Like other environmental factors, light can influence various developmental processes in fungal species. Most of the fungi can respond to different wavelengths of light such as blue (475 nm), near UV (300–380 nm) and red light (650 nm). Blue light has been found to be the most associated light quality with fungal development. The most commonly investigated photoregulatory receptors in fungi are the white collar complex proteins (WC-1, WC-2) in the light oxygen voltage domain which sense and regulate the effects of blue light on fungal development and reproduction. The sequencing of several fungal genomes has led to the identification of other photoreceptor genes and their products, such as phytochromes (for red light), cryptochromes (for blue light) and blue and green light absorbing rhodopsins in some ascomycetes and basidiomycetes. Although similar types of regulatory mechanisms appear to be involved in signalling light responses in fungal species, nevertheless, there may be other hitherto undiscovered mechanisms responsible for regulating light perception. It warrants further investigations on photoreception in more fungal species including plant pathogenic fungi to better understand the underlying mechanisms controlling light perception at the metabolic level. Certain circadian rhythms have been found to play crucial role in fungal perception and adaptation to light. The information has led to the use of certain photoselective materials for control of some plant diseases.

Keywords

Circadian rhythms Fungi Light signalling Photoreceptors Responses Spectral quality 

References

  1. Adams GC, Gottwald TR, Leach CM (1986) Environmental factors initiating liberation of conidia of powdery mildews. Phytopathology 76:1239–1245Google Scholar
  2. Agrios GN (2005) Plant pathology, 5th edn. Elsevier Academic Press, New YorkGoogle Scholar
  3. Alam MS, Begum MF, Sarkar MA, Islam MR, Alam MS (2001) Effect of temperature, light and media on growth, sporulation, formation of pigments and pycnidia of Botryodiplodia theobromae Pat. Pak J Biol Sci 4:1224–1227Google Scholar
  4. Atalia MM, Hassanein NM, El-Beih A, Youssef YA (2004) Effect of fluorescent and UV light on mycotoxin production under different relative humidities in wheat grains. Int J Agric Biol 6:1004–1012Google Scholar
  5. Avalos J, Schrott EL (1990) Photoinduction of carotenoid biosynthesis in Gibberella fujikuroi. FEMS Microbiol Lett 66:295–298Google Scholar
  6. Avery PB, Faull J, Simmonds MS (2004) Effect of different photoperiods on the growth, infectivity and colonization of Trinidadian strains of Paecilomyces fumosoroseus on the greenhouse white fly, Trialeurodes vaporariorum, using a glass slide bioassay. J Insect Sci 4:38PubMedPubMedCentralGoogle Scholar
  7. Babadoost M, Johnston MR (1998) Sporulation of Drechslera graminea on barley straw extract agar. Mycologia 90:63–68Google Scholar
  8. Ballario P, Vittorioso P, Magrelli A, Talora C, Cabibbo A, Macino G (1996) White collar-1, a central regulator of blue light responses in Neurospora, is a zinc finger protein. EMBO J 15:1650–1657PubMedPubMedCentralGoogle Scholar
  9. Bayram O, Biesemann C, Krappmann S, Galland P, Braus CH (2008) More than a repair enzyme: Aspergillus nidulans photolyase-like Cry-A is a regulator of sexual development. Mol Biol Cell 19:3254–3262PubMedPubMedCentralGoogle Scholar
  10. Berrocal-Tito GM, Esquivel-Naranjo EU, Horwitz BA, Herrera-Estrella A (2007) Trichoderma atroviride PHR1, a fungal photolyase responsible for DNA repair, autoregulates its own photoinduction. Eukaryot Cell 6:1682–1692PubMedPubMedCentralGoogle Scholar
  11. Betina V (1995) Photoinduced conidiation in Trichoderma viride. Folia Microbiol 40:219–224Google Scholar
  12. Bluhm BH, Dunkle LD (2008) PHL1 of Cercospora zeae-maydis encodes a member of the photolyase/cryptochrome family involved in UV protection and fungal development. Fungal Genet Biol 45:1364–1375PubMedGoogle Scholar
  13. Blumenstein A, Vienken K, Tasler R, Purschwitz J, Veith D, Frankenberg-Dinkel N, Fische R (2005) The Aspergillus nidulans phytochrome FphA represses sexual development in red light. Curr Biol 15:1833–1838PubMedGoogle Scholar
  14. Brook PJ (1969) Stimulation of ascospore release in Venturia inaequalis by far red light. Nature 222:390–392Google Scholar
  15. Brook PJ (1975) Effect of light on ascospore discharge by five fungi with bitunicate asci. New Phytol 74:84–92Google Scholar
  16. Brunner M, Kaldi K (2008) Interlocked feedback loops of the circadian clock of Neurospora crassa. Mol Microbiol 68:225–262Google Scholar
  17. Campbell MA, Medd RW, Brown JB (2003) Optimizing conditions for growth and sporulation of Pyrenophora semeniperda. Plant Pathol 52:448–454Google Scholar
  18. Canessa P, Schumacher J, Hevia MA, Tudzynski P, Larrondo LF (2013) Assessing the effects of light on differentiation and virulence of the plant pathogen Botrytis cinerea: characterization of the White Collar complex. PLoS One 8:e84223.  https://doi.org/10.1371/journal.pone.0084223 PubMedPubMedCentralGoogle Scholar
  19. Carlile MJ (1965) The photobiology of fungi. Annu Rev Plant Physiol 16:175–202Google Scholar
  20. Casas-Flores S, Rios-Momberg M, Rosales-Saavedra T, Martinez-Hernandez P, Olmedo-Monfil V, Herrera-Estrella A (2006) Cross talk between a fungal blue light perception system and cyclic AMP signalling pathway. Eukaryot Cell 5:499–506PubMedPubMedCentralGoogle Scholar
  21. Chen CH, Ringelberg CS, Gross RH, Dunlap JC, Loros JJ (2009) Genome-wide analysis of light-inducible responses reveals hierarchical light signalling in Neurospora. EMBO J 28:1029–1042PubMedPubMedCentralGoogle Scholar
  22. Cheong KK, Strub C, Montet D, Durand N, Alter P, Meile JC, Schorr-Galindo S, Fontana A (2016) Effect of different light wavelengths on the growth and ochratoxin A production in Aspergillus carbonarius and Aspergillus westerdijkiae. Fungal Biol 120:745–751PubMedGoogle Scholar
  23. Cigsar I (1996) The effect of UV-absorbing polyethylene film to the progress of fungal diseases of greenhouse tomato. Int J Food Agric Econ 9:1–2Google Scholar
  24. Cohen Y, Vaknin M, Ben-Naim Y, Rubin AE (2013) Light suppresses sporulation and epidemics of Peronospora belbahrii. PLoS ONE 8:e81282PubMedPubMedCentralGoogle Scholar
  25. Cooperman CJ, Jenkins SF (1986) Conditions influencing growth and sporulation of Cercospora asparagi and Cercospora blight development in Asparagus. Phytopathology 76:617–622Google Scholar
  26. Correa A, Lewis ZA, Greene AV, March U, Gomer RH, Bell-Pedersen D (2003) Multiple oscillators regulate circadian gene expression in Neurospora. Proc Natl Acad Sci USA 100:13597–13602PubMedGoogle Scholar
  27. Corrochano LM (2007) Fungal photoreceptors: sensory molecules for fungal development and behaviour. Photochem Photobiol Sci 6:725–736PubMedGoogle Scholar
  28. Corrochano LM (2011) Fungal photobiol: a synopsis. IMA Fungus 2:25–28Google Scholar
  29. Corrochano LM (2015) Perception in fungi sensing light and other signals. Botany 2015 (Abstract ID: 879) Google Scholar
  30. Costa HS, Robb KL, Wilen CA (2001) Increased persistence of Beuuveria bassiana spore viability under high ultraviolet-blocking greenhouse plastic. Hort Sci 36:1082–1084Google Scholar
  31. Crous P, Slippers B, Wingfield M, Rheeder J, Marasas W, Philips A, Alves A, Burgess T, Barber T, Groenewald J (2006) Phylogenetic lineages in the Botryosphaeriaceae. Stud Mycol 55:235–253PubMedPubMedCentralGoogle Scholar
  32. Dahalberg KR, Etten J (1982) Physiology and biochemistry of fungal sporulation. Ann Rev Phytopathol 20:281–301Google Scholar
  33. Daub ME, Herrero S, Chung KR (2005) Photoactivated perylenequinone toxins in fungal pathogenesis of plants. FEMS Microbiol Lett 252:197–206PubMedGoogle Scholar
  34. De Cal A, Melgarejo P (1999) Effects of long-wave UV light on Monolinia growth and identification of species. Plant Dis 83:62–65Google Scholar
  35. Devlin PF (2002) Signs of the time: environmental input to the circadian clock. J Exp Bot 53:1535–1550PubMedGoogle Scholar
  36. Diaz BM, Fereres A (2007) Ultraviolet-blocking materials as a physical barrier to control insect pests and plant pathogens in protected crops. Pest Technol 1:85–95Google Scholar
  37. Diorio LA (1996) Effect of light and glucose on the aphothecial development of Lodophanus carneus (Fungi, Ascomycotina). Rev Argent Microbiol 28:63–72PubMedGoogle Scholar
  38. Dong W, Buck JW (2011) Effect of light on in vivo urediniospores germination, lesion development and sporulation of Puccinia hemerocallidis on daylily and Puccinia pelargoniizonalis on geranium. Mycologia 103:1277–1283PubMedGoogle Scholar
  39. Dong W, Tang X, Yu Y, Nilsen R, Kim R, Griffith J, Amold J, Schuttler HB (2008) Systems biology of the clock in Neurospora crassa. PLoS ONE 3:e3105PubMedPubMedCentralGoogle Scholar
  40. Estrada AF, Avalos J (2009) Regulation and targeted mutation of opsA, coding for the NOP-1 opsin orthologue in Fusarium fujikuroi. J Mol Biol 387:59–73PubMedGoogle Scholar
  41. Friedl MA, Kubicek CB, Druzhinina IS (2008a) Carbon source dependence and photostimulation of conidiation in Hypocrea atroviridis. Appl Environ Microbiol 74:245–250PubMedGoogle Scholar
  42. Friedl MA, Schmoll M, Kubicek CB, Druzhinina IS (2008b) Photostimulation of Hypocrea atroviridis growth occurs due to a cross-talk of carbon metabolism, blue light receptors and response to oxidative stress. Microbiology 154:1229–1241PubMedGoogle Scholar
  43. Frochlich AC, Liu Y, Loros JJ, Dunlap JC (2002) White collar-1, a circadian blue light photoreceptor, binding to the frequency promoter. Science 297:815–819Google Scholar
  44. Galagan JE (2003) The genome sequence of the filamentous fungus Neurospora crassa. Nature 422:859–868PubMedGoogle Scholar
  45. Garcia-Martinez J, Brunk M, Avalos J, Terpitz U (2015) The CarO rhodopsin of the fungus Fusarium fujikuroi is a light-driven proton pump that retards spore germination. Sci Rep.  https://doi.org/10.1038/srep07798 PubMedPubMedCentralGoogle Scholar
  46. Glienke C, Pereira OL, Stringari D, Fabris J, Kawa-Cordeiro V, Galli-Terasawa L, Cannington J, Shivas RG, Groenewald JZ, Crous PW (2011) Endophytic and pathogenic Phyllosticta species, with reference to those associated with citrus black spot. Persoonia 26:47–56PubMedPubMedCentralGoogle Scholar
  47. Greene AV, Keller N, Haas H, Bell-Pedersen D (2003) A circadian oscillator in Aspergillus spp. regulates daily development and gene expression. Eukaryot Cell 2:231–237PubMedPubMedCentralGoogle Scholar
  48. Griebel T, Zeier J (2008) Light regulation and daytime dependency of inducible plant defences in Arabidopsis: phytochrome signalling controls systemic acquired resistance rather than local defence. Plant Physiol 147:790–801PubMedPubMedCentralGoogle Scholar
  49. Gunasekara TS, Paul ND, Ayers PG (1997) The effect of ultraviolet-B (UV-B :290-320 nm) radiation on blister blight disease of tea (Camellia sinensis). Plant Pathol 46:179–533Google Scholar
  50. Haggblom P, Unestam T (1979) Blue light inhibits mycotoxin production and increases total lipids and pigmentation in Alternaria alternata. Appl Environ Microbiol 38:1074–1077PubMedPubMedCentralGoogle Scholar
  51. He Q, Cheng P, Yang Y, Wang L, Gardner KH, Liu Y (2002) White collar-1, a DNA binding transcription factor and a light sensor. Science 297:840–843PubMedGoogle Scholar
  52. Heintzen C (2012) Plant and fungal photopigments. WIREs Membr Transp Signal 1:411–432Google Scholar
  53. Heintzen C, Liu Y (2007) The Neurospora crassa circadian clock. Adv Genet 58:25–66PubMedGoogle Scholar
  54. Heintzen C, Loros JJ, Dunlap JC (2001) The PAS protein VIVID defines a clock-associated feedback loop that represses light input, modulates gating, and regulates clock resetting. Cell 104:453–464PubMedGoogle Scholar
  55. Herrera-Estrella A, Horwitz BA (2007) Looking through the eyes of fungi: molecular genetics of photoreception. Mol Microbiol 64:5–15PubMedGoogle Scholar
  56. Hilderbrand PD, Sutton JC (1984) Interactive effects of the dark period, humid period, temperature, and light on sporulation of Peronospora destructor. Phytopathology 74:1444–1449Google Scholar
  57. Hillman BL, Shapira R, Nuss DL (1990) Hypovirulence-associated suppression of host functions in Cryptonectria parasitica can be partially relieved by high light intensity. Phytopathology 80:950–956Google Scholar
  58. Honda Y, Yunoki T (1977) Control of Sclerotinia disease of greenhouse eggplant and cucumber by inhibition of development of apothecia. Plant Dis Report 61:1036–1040Google Scholar
  59. Honda Y, Toki T, Yunoki T (1977) Control of gray mould of greenhouse cucumber and tomato by inhibition of sporulation. Plant Dis Report 61:1041–1044Google Scholar
  60. Hubballi M, Nakkeeran S, Raguchander T, Anand T, Samiyappan R (2010) Effect of environmental conditions on growth of Alternaria alternata causing leaf blight of Noni. World J Agric Sci 6:171–177Google Scholar
  61. Humpherson-Jones FM, Cooke RC (1977) Morphogenesis in sclerotium-forming fungi. I. Effects of light on Sclerotinia sclerotiorum, Sclerotium delphinii and S. rolfsii. New Phytol 78:171–180Google Scholar
  62. Idnurm A, Heitman J (2005) Light controls growth and development via a conserved pathway in the fungal kingdom. PLoS Biol 3:e95.  https://doi.org/10.1371/journal.pbio.0030095 PubMedPubMedCentralGoogle Scholar
  63. Idnurm A, Rodriguea-Romero J, Corrochano LM, Sanz C, Iturriaga EA, Eslava AP, Heitman J (2006) The Phycomyces madA gene encodes a blue-light photoreceptor for phototropism and other light responses. Proc Natl Acad Sci USA 103:4546–4551PubMedGoogle Scholar
  64. Idnurm A, Verma S, Corrochano LM (2010) A glimpse into the basis of vision in the kingdom Mycota. Fungal Genet Biol 47:881–892PubMedPubMedCentralGoogle Scholar
  65. Isaac S (1995) Moulds, mildews and other fungi are often found in shaded and dark situations—is their development influenced by light? Mycologist 9:41–42Google Scholar
  66. Jofffe AZ, Lisker N (1969) Effects of light, temperature, and pH value on aflatoxin production in vitro. Appl Microbiol 18:517–518Google Scholar
  67. Khan TN (1971) Effect of light on sporulation in Drechslera tritici-repentis. Trans Br Mycol Soc 56:309–311Google Scholar
  68. Komon-Zelazowska M, Neuhof T, Dieckmann R, Dohren H, Herrera-Estrella A, Kubicek CP, Druzhinina I (2007) Formation of atroviridin by Hypocrea atroviridis is conidiation associated and positively regulated by blue light and the G protein GNA3. Eukaryot Cell 6:2332–2342PubMedPubMedCentralGoogle Scholar
  69. Kritsky MS, Belozerskaya TA, Sokolovsky VY (2005) Photoreceptor apparatus for the fungus Neurospora crassa. Mol Biol 39:602–607Google Scholar
  70. Kuratani M, Tanaka K, Terashima K, Muraguchi H, Nakazawa T, Nakahori K, Kamada T (2010) The dst2 gene essential for photomorphogenesis of Coprinopsis cinerea encodes a protein with a putative FAD-binding-4 domain. Fungal Genet Biol 47:152–158PubMedGoogle Scholar
  71. Leach CM (1962) Sporulation of diverse species of fungi under near-ultraviolet radiation. Can J Bot 40:151–161Google Scholar
  72. Leach CM (1972) An action spectrum for light- induced sexual reproduction in the ascomycete fungus Leptosphaerulina trifolii. Mycologia 64:475–490Google Scholar
  73. Leach CM, Trione EJ (1966) Action spectra for light-induced sporulation of the fungi Pleospora herbarum and Alternaria dauci. Photochem Photobiol 5:621–630Google Scholar
  74. Lee K, Singh P, Chang WC, Ash J, Kim TS, Hang L, Park S (2006) Light regulation of asexual development in the rice blast fungus Magnaporthe grisea. Fungal Genet Biol 43:693–706Google Scholar
  75. Levy Y, Cohen Y (1983) Differential effect of light on spore germination of Exserohilum turcicum on corn leaves and corn leaf impressions. Phytopathology 73:249–252Google Scholar
  76. Linden H, Macino G (1997) White collar-2, a partner in blue-light signal transduction, controlling expression of light-regulated genes in Neurospora crassa. EMBO J16:98–109Google Scholar
  77. Lokhandwala J, Hopkins HC, Rodriguez-Iglesias A, Dattenbock C, Schmoil M, Zoltowski BD (2014) Structural biochemistry of a fungal LOV domain photoreceptor reveals an evolutionary conserved pathway integrating light and oxidative stress. Structure 23:116–125PubMedGoogle Scholar
  78. Lopez-Lopez A, Koller M, Herb C, Scharer H-J (2014) Influence of light management on the sporulation of downy mildew on sweet basil. Acta Hortic.  https://doi.org/10.17660/ActaHortic.2014.1041.24 Google Scholar
  79. Lucas JA, Kendrick RE, Givan CV (1975) Photocontrol of fungal spore germination. Plant Physiol 56:847–849PubMedPubMedCentralGoogle Scholar
  80. Manning WJ (1995) Climate change: potential effects of increased atmospheric carbon dioxide, ozone, and ultraviolet-B radiation on plant diseases. Environ Pollut 88:219–245PubMedGoogle Scholar
  81. Marsh PB, Taylor EE, Bassler MM (1959) A guide to the literature of certain effects of light on fungi. Plant Dis Report Suppl 261:251–312Google Scholar
  82. Miller OK (1967) The role of light in the fruiting of Punus fragilis. Can J Bot 45:1939–1943Google Scholar
  83. Moore-Lanbecker E, Shropshire W (1982) Effects of aeration and light on apothecia, sclerotia, and mycelia growth in the discomycete Pyronema domesticum. Mycologia 74:1000–1013Google Scholar
  84. Nagy P, Fischl G (2002) Effect of UV and visible light irradiation on mycelial growth and sclerotium formation of Sclerotinia sclerotiourm. Acta Phytopathol Entomol Hung 37:83–89Google Scholar
  85. Nigel DP, Rob JJ, Taylor A, Wargent JJ, Moore JP (2005) The use of wavelength-selective plastic cladding materials in horticulture: understanding the crop and fungal responses through the assessment of biological spectral weighting functions. Photochem Photobiol 81:1052–1060Google Scholar
  86. Nordskog B, Gadoury DM, Seem RC, Hermansen A (2007) Impact of diurnal periodicity, temperature and light on sporulation of Bremia lactucae. Phytopathology 97:979–986PubMedGoogle Scholar
  87. Ohmori K, Nakaiima M (1970) Effect of light on sporulation of Alternaria kikuchiana Tanaka. Ann Phytopathol Soc Jpn 36:11–16Google Scholar
  88. Onesirosan PT (1978) Factors affecting sporulation by Phomopsis pheseolorum. Mycopathologia 64:23–27Google Scholar
  89. Peries OS (1962) Studies on strawberry mildew, caused by Sphaerotheca macularis (Wallr. ex Fries) Jaczewski. Ann Appl Biol 50:211–224Google Scholar
  90. Purschwitz J, Muller S, Kastner C, Fischer R (2006) Seeing the rainbow: light sensing in fungi. Curr Opin Microbiol 9:566–571PubMedGoogle Scholar
  91. Rangel DEN (2016) Visible light during growth enhances conidial tolerance to different stress conditions in fungi. Project Report. IP&D, UNIVAP, BrazilGoogle Scholar
  92. Raymond PJ, Bockus WW, Norman BL (1985) Tan spot of winter wheat: procedures to determine host response. Phytopathology 75:686–690Google Scholar
  93. Reuveni R, Raviv M (1997) Control of downy mildew in greenhouse-grown cucumbers using blue photoselective polyethylene sheets. Plant Dis 81:999–1094Google Scholar
  94. Rockwell NC, Su YS, Lagarias JC (2006) Phytochrome structure and signaling mechanisms. Annu Rev Plant Biol 57:837–858PubMedPubMedCentralGoogle Scholar
  95. Roden LC, Ingle RA (2009) Lights, rhythms, infection: the role of light and the circadian clock in determining the outcome of plant-pathogen interactions. Plant Cell 21:2546–2552PubMedPubMedCentralGoogle Scholar
  96. Roenneberg T, Merrow M (1999) Circadian systems and metabolism. J Biol Rhythms 14:449–459PubMedGoogle Scholar
  97. Roger C, Tivoli B (1996) Effect of culture medium, light and temperature on sexual and asexual reproduction of four strains of Mycosphaerella pinodes. Mycol Res 100:304–306Google Scholar
  98. Ruger-Herreros C, Rodriguez-Romero J, Fernandez-Barranco R, Olmedo M, Fischer R, Corrochano LM, Canovas D (2011) Regulation of conidiation by light in Aspergillus nidulans. Genetics 188:809–897PubMedPubMedCentralGoogle Scholar
  99. Ruiz-Roldan MC, Garre V, Guarro J, Marine M, Roncerro MI (2008) Role of the white collar-1 photoreceptor in carotenogenesis, UV resistance, hydrophobicity, and virulence of Fusarium oxysporum. Eukaryot Cell 7:1227–1230PubMedPubMedCentralGoogle Scholar
  100. Rumbolz J, Wirtz S, Kicassemeyer H-H, Guggenheim R, Schäfer E, Büche C (2002) Sporulation of Plasmopara viticola: differentiation and light regulation. Plant Biol 4:413–422Google Scholar
  101. Sanchez-Arregui A, Perez-Martinez AS, Herrera-Estrella A (2012) Proteomic analysis of Trichoderma atroviride reveals independent roles for transcription factors BLR-1 and BLR-2 in light and darkness. Eukaryot Cell 11:30–41Google Scholar
  102. Sasaki T, Honda Y, Umekawa M, Nemoto M (1985) Control of certain diseases of greenhouse vegetables with ultraviolet-absorbing vinyl film. Plant Dis 69:530–539Google Scholar
  103. Schmoll M, Franchi L, Kubicek CP (2005) Envoy, a PAS/LOV domain protein of Hypocrea jecorina (Anamorph Trichoderma reesei), modulates cellulase gene transcription in response to light. Eukaryot Cell 4:1998–2007PubMedPubMedCentralGoogle Scholar
  104. Schuerger AC, Brown CS (1997) Spectral quality affects disease development of three pathogens on hydroponically grown plants. Hort Sci 32:96–100Google Scholar
  105. Schwerdtfeger C, Linden H (2003) VIVID is a flavoprotein and serves as a fungal blue light photoreceptor for photoadaptation. EMBO J 22:4846–4855PubMedPubMedCentralGoogle Scholar
  106. Singh UP, Singh RB (1987) Effect of light of different wavelengths on apothecium formation in Sclerotinia sclerotiorum. J Plant Dis Prot 94:500–508Google Scholar
  107. Sommer T, Chambers JA, Eberle J, Lauter FR, Russo VE (1989) Fast light regulated genes of Neurospora crassa. Nucleic Acids Res 17:5713–5723PubMedPubMedCentralGoogle Scholar
  108. Su Y-Y, Qi Y-L, Cai L (2012) Induction of sporulation in plant pathogenic fungi. Mycology 3:195–200Google Scholar
  109. Tan KK, Epton AH (1973) Effect of light on the growth and sporulation of Botrytis cinerea. Trans Br Mycol Soc 61:145–157Google Scholar
  110. Tatiana TMS, Rodrigues LA, Dhingra OD, Eduardo SGM (2010) In vitro production of conidia of Alternaria solani. Trop Plant Pathol 35:1–8Google Scholar
  111. Terashima K, Yuki K, Muraguchi H, Akiyama M, Kamada T (2005) The dst1 gene involved in mushroom photomorphogenesis of Coprinus cinereus a putative photoreceptor for blue light. Genetics 171:101–108PubMedPubMedCentralGoogle Scholar
  112. Timberlake WE (1980) Developmental gene regulation in Aspergillus nidulans. Dev Biol 8:497–510Google Scholar
  113. Tisch D, Schmoll M (2010) Light regulation of metabolic pathways in fungi. Appl Microbiol 85:1259–1277Google Scholar
  114. Toussoun TA, Weinhold AR (1967) Light requirement and light inhibition of sexual reproduction in Fusarium solani f. sp. cucurbitae race 2. Can J Bot 45:951–954Google Scholar
  115. Tudzynski B (1999) Biosynthesis of gibberellins in Gibberella fujikuroi: biomolecular aspects. Appl Microbiol Biotechnol 52:298–310PubMedGoogle Scholar
  116. Vakalounakis DJ (1991) Control of early blight of greenhouse tomato caused by Alternaria solani by inhibiting sporulation with ultraviolet-absorbing vinyl film. Plant Dis 75:795–797Google Scholar
  117. Vakalounakis DJ (1992) Control of fungal diseases of greenhouse tomato under long-wave infrared-absorbing plastic film. Plant Dis 76:43–46Google Scholar
  118. Vakalounakis DJ, Christias C (1981) Sporulation in Alternaria cichorri is controlled by a blue and near ultraviolet reversible photoreaction. Can J Bot 59:626–628Google Scholar
  119. Van der Aa HA (1973) Studies on Phyllosticta I. Stud Mycol 5:1–10Google Scholar
  120. Velmurugan P, Lee YH, Venil CK, Lakshmanaperumalsamy P, Chae J-C, Oh B-T (2010) Effect of light on growth, intracellular and extracellular pigment production by five pigment producing filamentous fungi in synthetic medium. J Biosci Bioeng 109:346–350PubMedGoogle Scholar
  121. Veluchamy S, Rollins JA (2008) A CRY-DASH type photolyase/cryptochrome from Sclerotinia sclerotiorum mediates minor UV-A specific effects on development. Fungal Genet Biol 45:1265–1276PubMedGoogle Scholar
  122. Wang A-W, Yamanouchi U, Katayose Y, Sasaki T, Yano M (2001) Expression of the Pib rice—blast-resistance gene family is up-regulated by environmental conditions favouring infection and by chemical signals that trigger secondary plant defences. Plant Mol Biol 47:653–661PubMedGoogle Scholar
  123. Wang Z, Li N, Li J, Dunlap JC, Trail F, Townsend JP (2016) The fast-evolving phy-2 gene modulates sexual development in response to light in the model fungus Neurospora crassa. mBio.  https://doi.org/10.1128/mbio.02148-15 Google Scholar
  124. Weyman PD, Pan Z, Feng Q, Gilchrist DG, Bostock RM (2006) A circadian rhythm-regulated tomato genes is induced by arachidonic acid and Phytophthora infestans infection. Plant Physiol 140:235–248PubMedPubMedCentralGoogle Scholar
  125. Willocquet L, Colombet D, Rougier M, Fargues J, Clerjeau M (1996) Effects of radiation, especially ultraviolet B, on conidial germination and mycelia growth of grape powdery mildew. Eur J Plant Pathol 102:441–449Google Scholar
  126. Wright BE (1979) Causality in biological systems. Trends Biochem Sci 4:110–111Google Scholar
  127. Xu LL, Li F, Xie HY, Liu XZ (2009) A novel method for promoting conidial production by a nematophagous fungus, Pochonia chlamydospora AS6.8. World J Microbiol Biotechnol 25:1989–1994Google Scholar
  128. Yarwood CE (1936) The diurnal cycle of powdery mildew Erysiphe polygoni. J Agric Res 52:645–657Google Scholar
  129. Yu SM, Ramkumar G, Lee YH (2013) Light quality influences the virulence and physiological responses of Colletotrichum acutatum causing anthracnose in pepper plants. J Appl Microbiol 115:509–516PubMedGoogle Scholar
  130. Zhu P, Zhang C, Xiao H, Wang Y, Toyoda H, Xu L (2013) Exploitable regulatory effects of light on growth and development of Botrytis cinerea. J Plant Pathol 95:509–517Google Scholar

Copyright information

© Indian Phytopathological Society 2018

Authors and Affiliations

  1. 1.Department of Plant, Soil and Microbial SciencesMichigan State UniversityEast LansingUSA

Personalised recommendations