New Discoveries in Agrochemicals - American Chemical Society

Chapter 6

Allelopathic Activities in Litters of Mushrooms

Downloaded by NORTH CAROLINA STATE UNIV on September 7, 2012 | http://pubs.acs.org Publication Date: November 23, 2004 | doi: 10.1021/bk-2005-0892.ch006

Hiroshi Araya Chemical Ecology Unit, Department of Biological Safety, National Institute of Agro-Environmental Sciences, 3-1-3 Kannondai, Tsukuba, Ibaraki 305-8604, Japan

I examined the influence of the mushrooms of almost 60 fungal species on the growth of lettuce (Lactuca sativa L.) seedlings. Most of the species inhibited the growth of the seedlings. The results indicate that compounds produced by mushrooms are allelopathic, and suggest that chemicals derived from certain mushrooms could be used to control weeds.

Introduction A mushroom is the fruiting body of a fungus; it typically appears above die ground and contains spores. There are at least 8000 species of mushroom in the world. Although often considered plants, fungi differfromcommon plants in that they lack chlorophyll and must rely on organic material produced by other organisms for nutrition (i). Many species influence plants directly or indirectly. Several species cause fairy rings, which form large circles in lawns (2). The ring encloses a zone of diseased or dead grass. Another zone of stimulated growth may occur inside the dead or dying zone. Nada reported that the stimulated growth of turf was caused by plant growth hormones produced by both Calocybe georgii L. and Agaricus campester Fr. (J). Other researchers have reported several plant growth inhibitors in mushrooms. These plant growth regulators can

© 2005 American Chemical Society In New Discoveries in Agrochemicals; Clark, J., et al.; ACS Symposium Series; American Chemical Society: Washington, DC, 2004.

63

64 be considered allelochemicals. However, little research on mushroom allelopathy has been reported. In this chapter, I report the allelopathic activity of almost 60 mushroom species. The possibility of allelopathic activity of mushrooms for weed control is discussed.


Allelopatic activity in mushroom In allelopathy, plant species interfere or stimulate with die germination, growth, or development of the other plant species by releasing chemical compounds. The phenomenon has been known for over 2000 years (Theophtastus, 300 B.C. (¥)). The term, derived from the two Greek words allelon ('one another') and pathos ('suffering'), was coined by Prof. Hans Molisch in 1937 to refer to biochemical interactions between plants of all kinds, including organisms which placed in the plant kingdom (4). Chemicals released from plants and having allelopathic effects are termed allelochemicals (or allelochemics). Thus, exogenous plant hormones must act as allelochemicals, and endogenous hormones may affect to other plant by release as litter. The emission of allelochemicals can occur via various routes. Possible routes are shown in Figure 1. Allelopathy plays an important role in both agroecosystem and natural ecosystem. In agroecosystems, allelopathic activities of weeds affect on crops yields. Many agronomy researchers have tried various strategies to utilize allelopathy. For example, rye (Secale céréale L.) produces allelochemicals and is used to some extent in weed management (5). On the other hand, only two studies of mushroom allelopathy have been reported. In 1937, Molisch first reported die influence of volatilesfromfruiting bodies of Agaricus campestris on vetch (Vicia sativa) (4). Fifty years later, Chamont and Simeray reported that water extracts of 114 species inhibited the growth of red radish (Raphanus sativus var. radicicola) seedlings (6). The possible emission routes of allelochemicals from mushrooms are proposed in Figure 2. Since the longevity of fruiting bodies is generally short, the main source of allelochemicals would be mycelia in soil. Mushrooms must be selected for testing on die basis of observations of allelopathy in nature. Some phenomena have been reported: for example, soil sickness caused by Matsutake (Tricholoma matsutake (S. Ito et Imai) Sing) (7); and stimulation of bamboo growth by a fungus in the Ramariaceae (8). However, wheat (Triticum aestivum (L.) Thell.) could not grow well in die field fertilizing immature compost of bed log for lacquered bracket fungus (Ganoderma

In New Discoveries in Agrochemicals; Clark, J., et al.; ACS Symposium Series; American Chemical Society: Washington, DC, 2004.

65


lucidum) (9). This may result in their pathogenicity excluding toxic compounds (10).

Figure 1. Possible Release Routes ofAllelochemicalsfromCommon Plants (See page 1 of color insert.)

Several compounds that inhibit plant growth have been isolated from mushrooms: e.g., azetidine-2-carboxylic acid from Clavaria miyabeana (11); neogrifolin and grifolin from Polyporus confluens (12); and 2-amino-3cyclopropyl-butanoie acid and 2-amino-5-chloro-4-pentenoic acidfromAmanita castanopsidis (13). In addition, the production of plant hormones has been reported: e.g. indole-3-acetic acid from Schizophyllum commune Fries (14); cytokinins from Rhizopogon roseolus (Cda.) Th. Fr* (25) and Suillus punctipes (16); and ethylene from Agaricus bisporus (Lange) Sing. (17). These are candidate allelochemicals. Allelopathy offers the opportunity for identifying new agrochemicals. Its study is therefore important.



66

Figure 2. Proposed Release Routes ofAllelochemicalsfromMushrooms (See page 1 of color insert.)

Estimation of Allelopathic Activity of Mushrooms Several bioassay methods have been used to screen allelopathic plants. Fujii demonstrated that a method using two layered agar is useful for screening of the allelopathic potential of leaf litter (18). I have been investigating the allelopathic activities in litters of mushroom fruiting bodies by application of this method (19-21). The procedure and a picture as an example are shown in Figure 3. Here I present die results of about 60 mushroom species. All die wild mushrooms were collected in Ibaraki, Tochigi, and Fukushima prefectures, Japan, except for one specimen of Morchella esculenta, which was collected and air dried in Canada. Cultivated mushrooms were obtained from Dr. A. Sekiya of which Forestry and Forest Products Research Institute, Japan. All mushrooms were lyophilized after removal of stray materials. Fragments of dried mushroom (10 mg and 50 mg) were bioassayed by standard procedures (Figure 3). Because of its sensitivity to various chemicals, lettuce (Lactuca sativa L. cv.


67 'Great Lakes 366') was used as a test plant. For the control treatment, mushrooms were not added. The lengths of die radicle and hypocotyl of lettuce seedlings were measured after incubation at 20 °C in the dark for 3 days. Efficacy of lettuce seedling growth was calculatedfromthe following formula: Efficacy (%) = 100- 100 χ sample growth / control growth.


100% means completely killed, -100% means two fold growth

Control

10 mg

50 mg

( 1 ) add 5 ml of agar (0.75 %, 40°C) (2) place fragments of mushroom (50 and 10 mg/well) on gelatinized agar (3) add 5 ml of agar (0.75 %, 40°C) (4) place lettuce seeds (Great Lakes 366) on gelatinized agar (5) incubate at 25°C in the dark for 3 days (6) measure radicle length, hypocotyl length and germination %

Figure 3. Procedure and an example for allelopathy assay for mushroom litters

Results and Discussion Most of the mushrooms inhibited the growth of lettuce seedling, as shown in Tables I and II. Several dried mushroom fruiting bodies inhibited the lettuce growth strongly: Agaricus suhrutilescens (Kauffin.) Hotson et Stuntz, Amanita cokeri (Gilb. et Ktihn.) Gilb. f. roseotincta Nagasawa et Hongo, Amanita sinensis ZL Yang, Boletus fraternus Peck, Boletus reticulates Schaeff., Coprinus comatus (Mtiller: Fr.) Pers., Cortinarius violaceus (L.: Fr.) Fr., Gymnopilus spectabilis (Fr.) Sing., Lanopila nipponica (Kawam.) Y . Kobayasi, Pleurocybella porrigens (Pers.: Fr.) Sing., Ramaria formosa (Fr.) Quel.,


68


Lyophyllum decastes (Fr.: Fr.) Sing., Morchella esculenta (L.: Fr.) Pers. var. esculenta (collected in Japan), Panellus serotinus (Pers.: Fr.) Kiihn., Pleurotus ostreatus (Jacq.: Fr.) Kummer, and Hypsizigus marmoreus (Peck) Bigelow. On the other hand, F. obliqua stimulated lettuce seedling growth. The chemicals that diffused from these mushrooms through die agar are therefore plant growth regulators and candidate allelochemicals, which could yield new herbicides. Differnt effect on two M. esculenta collected from Japan and Canada was observed. Decomposition of chemicals may have been a cause in air drying of Canadian M. esculenta. Further study is needed to verify the allelopathy.

Table I. Percent Inhibition of Lettuce Seedling Growth by Wild Mushrooms Mushrooms

Radicle Hypocotyl 10 mg 50 mg 10 mg 50 mg

Agaricus subrutilescens84.81 Albatrellus confluens 40.09 Amanita cokeri 76.45 Amanita pantherina 53.61 Amanita sinensis 88.99 Amanita vaginata 41.27 Armillariella me Ilea 71.64 Armillariella tabescens 35.23 Auricularia auricula 61.70 Boletus fratemus 74.63 Boletus griseus 53.73 Boletus pseudocalopus 72.92 Boletus regius 60.88 Boletus reticulates 78.12 Boletus sensibilis 59.94 Cantharellus cibarius 19.58 Cantharellus luteocomus 38.55 Coprinus comatu 84.65 Cortinarius purpurascens 40.54 Cortinarius violaceus 87.23 Craterellus cornucopioides 53.99 Fuscoporia obliqua -1.35

91.31 63.99 80.98 70.36 3.98 23.11 93.63 44.14 66.97 76.68 -8.60 43.74 95.71 70.07 86.30 76.01 28.17 55.90 84.22 31.08 56.18 78.16 -4.77 56.69 73.30 14.52 26.89 92.13 25.90 65.00 81.66 15.14 51.79 88.99 47.25 72.10 77.40 31.96 56.97 90.40 40.85 81.37 87.67 16.81 63.48 4.37 23.58 61.23 8.76 3.96 53.73 91.09 69.72 73.11 1.20 54.63 76.21 96.92 67.54 81.23 0.07 25.94 76.45 36.71 -50.73 -36.42

Table I. Continued on next page


69 Table I. (Continued)


Mushrooms


Gymnopilus spectabilis 76.39 Hygrophorus capreolarius 70.50 Hygrophorus fagi 51.74 lonomidotis frondosa 28.46 Lactarius volemus 38.36 Lanopila nipponica 79.34 Leatiporus sulphureus 54.13 Leccinum extremioriental 73.81 Lycoperdon perlatum 92.86 Lyophyllum sykosporum 68.93 Morchella esculenta (CAN) 54.19 Morchella esculenta (JPN) 97.12 Mycena haematopoda 76.11 Naematoloma sublateritium 49.28 Pholiota lubrica 83.52 Pleurocybella porrigens 82.41 Polyporus arcularius 72.49 Ramaria formosa 81.73 Ramaria fumigata 57.39 Russula virescens 67.64 Sarcodon imbricatus 60.25 Sarcodon scabrosus 79.32 Strobilomyces seminudus 38.78 Strobilomyces strobilaceus28.24 Tricholoma portentosum 77.08 Xanthoconium affine 80.90

90.79 29.31 70.43 79.31 19.86 36.09 66.41 -15.24 22.52 71.60 -3.99 23.41 79.53 -7.03 42.17 90.73 30.03 63.36 78.50 18.34 57.21 87.45 34.57 63.99 94.65 58.56 71.24 84.86 24.87 58.57 94.76 1.64 61.31 98.08 92.13 95.19 81.47 36.19 58.11 77.40 20.18 54.98 87.85 44.38 67.73 85.07 61.16 68.92 81.29 16.34 28.97 91.53 50.80 66.78 91.36 61.79 82.64 85.85 37.10 53.26 78.53 16.33 45.36 89.77 49.00 52.59 84.01 7.80 64.14 6.67 51.13 -30.36 87.84 24.17 52.70 89.43 48.37 64.75

The overuse of synthetic chemicals for pest control is a threat to the environment (22-23). There is a misleading tendency that compounds produced by plants are eco-friendly. In fact, many allelopathy researchers feel that allelochemicals could be ideal agrochemicals (24-33). But we must assess the safety of these products before using allelochemicals just the same way as synthetic agrochemicals.


70 Table II. Percent Inhibition of Lettuce Seedling Growth by Cultivated Mushrooms


Mushrooms


Ganoderma lucidum26.65 Grifola frondosa 68.32 Hericium erinaceum24.38 Hipsizigus marmoreus 79.44 Lentinula edodes 40.86 Lyophyllum decastes 82.39 Panellus serotinus 80.20 Pholiota nameko 58.40 Pleurotus ostreatus77.99 Pleurotus pulmonarius 73.59 Tremella fitciformis24.35

55.44 88.63 53.72 96.05 91.67 94.36 90.33 73.64 94.44 85.94 56.54

-5.98 19.91 1.97 53.63 5.25 41.31 40.23 11.12 59.60 48.85 -11.15

8.37 68.03 47.13 87.30 69.74 84.84 74.71 55.39 89.81 75.41 -1.97

Conclusion Based on this experiment, almost all mushrooms showed inhibitory activity on lettuce seedling growth. Consequently, broad leaf plant growth will be inhibited at the place after mushrooms grew, or mushroom was incorporated, if the soil did not degrade or strongly adsorb die allelochemicals or the chemicals are easily dissipated by leaching or photodegradation.

Acknowledgments I would like to express my thanks to the staff of the Chemical Ecology Unit, National Institute for Agro-Environmental Sciences, Japan, for their help and useful comments on this research work. I am also grateful to Mr. Ryuichi Koshihara, Mitsui & Co., Ltd., for his kind donation of morel (M. esculenta). I also wish to thank Dr. Atsushi Sekiya, Forestry and Forest Products Research Institute, Japan, for generous gifts of several cultivated mushrooms.


71


References 1. Lincoff, G. H.: National Audubon Society Field Guide to North American Mushrooms: Chanticleer Press Inc., New York, NY, 1981, p.11-13. 2. Smiley, R. W; Dernoeden, P. H; Clarke, Β. B.: Fairy Rings. In Compendium of Turfgrass Diseases 2nd Ed.: APS Press, Minnesota, MN, 1992, p.61-63. 3. Nada, G.: Biol. Vestn. (Ljubljana) 1975, 23, 89-96. 4. Molisch, H.: Der Einfluβ einer Pflanze auf die andere Allelopathy: Fischer, Jena, 1937. 5. Weston, L. A. Agron. J. 1996, 88, 860-866. 6. Chaumont, J. P.; Simeray, J. Rev.Écol.Biol.Sol.1985, 22, 331-339. 7. Ogawa, M. Biology of Matsutake: Tsukiji Shokan Publishing Co., Ltd., Tokyo, 1978, p.326 (Jpn). 8. Hongo, T.: Narrow Road to Mushrooms: Tombow Publishing Co., Ltd., Tokyo, 2003, p.30-31 (Jpn). 9. Araya, H., unpublished data, 2001. 10. Ariffin, D.; Idris, A. S.; Singh, G.: Status of Ganoderma in oil palm. In Ganoderma Diseases of Perennial Crops: CABI Publishing, Oxford, 2000, p.49-68. 11. Ikeda, M; Naganuma, Y.; Ohta, K.; Sassa, T; Miura, Y. Nippon Nogeikagaku Kaishi 1977, 51, 519-522. 12. Ikeda, M.; Kanou, H.; Nukina, M. Bull Yamagata Univ. Agr. Sci. 1989, 10, 849-852. 13. Yoshimura, H.; Takegami, K.; Doe, M.; Yamashita, T.; Shibata, K.; Wakabayashi, K.; Soga, K.; Kamisaka, S. Phytochemistry 1999, 52, 25-27. 14. Epstein, E.; Miles, P. G. Plant Physiol. 1967, 42, 911-914. 15. Miller, C. O. Science 1967, 157, 1055-1057. 16. Crafts, C. B.; Miller, C. O. Plant Physiol. 1974, 54, 586-588. 17. Turner, Ε. M.; Wright, M.; Osborne, D. J.; Self, R. J. Gen. Microbiol. 1975, 91, 167-176. 18. Fujii, Y. BullNatl.Inst. Agr.-Env. Sci. 1994, 10, 115-218. 19. Araya, H.; Hattori, M.; Nishihara, E.; Hiradate, S.; Fujii, Y.; Sekiya, A. Fruiting bodies of mushroom as allelopathic plants. In Third World Congress on Allelopathy - Challenge for the New Millennium, Abstracts Book2002,8,244. 20. Araya, H. Fruiting bodies of mushrooms as allelopathic plants In Allelopathy: Challenge for the New Millennium: Science Publisher, Tokyo, 2004 (in preparation). 21. Araya, H; Hiradate, S.; Fujii, Y. J. Weed Sci. Tech. 2003, 48 (sup.), 198199.



72 22. Chou, C. H.: Allelopathy and sustainable agriculture. In Allelopathy: Organisms, Processes and Applications: ACS Symposium Series 582, American Chemical Society, Washington DC, 1995, p.211-223. 23. Cutler, H. G.; Cutler, S. J.: Agrochemicals and pharmaceuticals. In Biologically Active Natural Products: Agrochemicals: CRC Press, Boca Raton, FL, USA, 1999, p.1-14. 24. Cutler, H. G. Weed Tech. 1988, 2, 525-532. 25. Cutler, H. G. Potentially useful natural product herbicides from microorganisms. In Principles and Practices in Plant Ecology: Allelochemical Interactions, CRC Press, Boca Raton, FL, USA, 1999, p.497-516. 26. Dayan, F.; Romagni, J; Tellez, M; Rimando, Α.; Duke, S. Pesticide Outlook 1999, Oct. 185-188. 27. Duke, S. O.; Abbas, Η. K.; Duke, M. V.; Lee, H. J.; Vaughn, K. C.; Amagasa, T; Tanaka, T. J. Environ. Sci. Health 1996, B31, 427-434. 28. Duke, S. O.; Abbas, Η. K.; Amagasa, T; Tanaka, T.L Phytotoxins of microbial origin with the potential for use as herbicides. In Crop Protection AgentsfromNature: Natural Products and Analogues. Critical Reviews on Applied Chemistry, Vol. 35, Society of Chemical Industry, Cambridge 1996, p.82-113. 29. Duke, S. O.; Dayan, F. E.; Romagni, J. G.; Rimando, A. M. Weed Res. 2000, 40, 99-111. 30. Hoagland, R. E.: Microbes and microbial products as herbicides: an overview. In Microbes and Microbial Products as Herbicides, ACS Symposium Series 439, American Chemical Society, Washington DC, 1990, p.2-52. 31. Hoagland, R. E.: Biochemical interactions of the microbial phytotoxin phosphinothricin and analogs with plants and animals. In Biologically Active Natural Products: Agrochemicals, CRC Press, Boca Raton, LFL, USA, 1999, p.107-125. 32. Macías, F. Α.; Molinillo, J. M. G.; Galindo, J. C. G.; Varela, R. M.; Torres, Α.; Simonet, A. M.: Terpenoids with potential use as natural herbicide templates. In Biologically Active Natural Products: Agrochemicals, CRC Press, Boca Raton, FL, USA, 1999, p.15-31. 33. Putnum, A. R. Weed Tech. 1998, 2, 510-518.


New Discoveries in Agrochemicals - American Chemical Society

Recommend Documents