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Coemansia species from the rhizospheres of wheat and barley in the United Kingdom
Mycol. Res. 103 (7) : 896–900 (1999)
896
Printed in the United Kingdom
Coemansia species from the rhizospheres of wheat and barley in the United Kingdom
H. K W A S! N A1, G. L. B A T E M A N2 A N D W. A. J. M. D A W S O N2 " Department of Forest Pathology, Agricultural University, ul. Wojska Polskiego 71c, 60-625 PoznanT , Poland # IACR-Rothamsted, Harpenden AL5 2JQ, U.K.
Coemansia aciculifera, C. scorpioidea and C. thaxteri were found in the rhizosphere of wheat and a fungus resembling C. spiralis was found in the rhizosphere of barley from two fields in eastern England when serially washed root pieces were incubated on low nutrient agar (SNA).
Since Coemansia was described by Van Tieghem & Le Monnier (1873), its representatives have been found only rarely because of their nutritional preferences. Coemansia was isolated originally mostly from the dung of small animals, especially rats and mice (Linder, 1943). The first records of its occurrence in soil appeared later but were infrequent. The species recorded most commonly in soil is C. erecta Bainier. This species was found in non-agricultural grassland in the United Kingdom, together with C. pectinata Bainier, (Warcup, 1951) and more recently with other Zygomycetes in arable soil in Spain (Cano, Fort & Guarro, 1989). Coemansia comprises a group of species characterized in general by : (i) very slow growth on culture media ; (ii) bright, yellow, abundant and high aerial mycelium ; (iii) asexual reproduction by means of elongate-cylindrical to fusiform sporangiospores formed in one-spored, rounded or sharp at the apex sporangiola borne on the lower surface of sporocladia produced on sporangiophores ; (iv) erect or ascending, highly variable in length but generally 2–3 mm long, septate, simple, regularly or irregularly branched, hyaline-yellowish to brown sporangiophores ; (v) acrogenous formation of sporocladia that are laterally disposed by continued growth of the fertile axis of the sporangiophore and are pleurogenous, stalked, elongate, nearly straight, arcuate or slightly sigmoid, septate and produce ellipsoidal to elongate-ovoid pseudophialides arranged in more or less transverse rows arising from all but one or two terminal sterile cells ; (vi) sexual reproduction by means of thick-walled, smooth, nearly hyaline zygospores formed from the fusion of small gametangia, delimited apically by two relatively short undifferentiated sexual branches or from an intercalary cell delimited in an undifferentiated sexual branch near the point of fusion of the branch with an ordinary vegetative hypha (Benjamin, 1958, 1959). During investigation of fungal communities in the rhizospheres of cereal plants, root pieces were taken in early June 1997 from wheat (Triticum aestivum L.) or barley (Hordeum
vulgare L.) grown as autumn-sown crops in two fields at Rothamsted. A total of 360 root pieces of wheat cv. Brigadier and 360 root pieces of barley cv. Pipkin, grown as second cereals on Highfield, and 1440 root pieces of wheat cv. Hereward grown as first, third or continuous wheat crops on Broadbalk field were examined. The root pieces (each 0n5 cm) were washed serially, 20 times, by shaking vigorously for 3 min in cold, sterile distilled water. They were than placed on low nutrient agar (SNA ; Nirenberg, 1976) containing penicillin, streptomycin sulphate and chloramphenicol and examined at intervals whilst incubating for 7 d at 20 mC and then up to 2 mo at 4m. After a minimum of 4 wk at the lower temperature, four Coemansia spp. previously unknown from the U.K. were identified. Subcultures were made on SNA and potato dextrose agar (PDA), although none produced cultures that contained only the Coemansia sp. These cultures are referred to below as ‘ pure mixed cultures ’ because each consisted of Coemansia and the fungi with which it was intimately associated and not removed by subculturing. Coemansia aciculifera Linder, Farlowia 1, 49–77, 1943. (Figs 1, 2, 8) In pure mixed culture the fungus grew very slowly, 8–10 mm diam. in 15 d on PDA and SNA. It produced vivid bright yellow, delicate, abundant and high aerial mycelium. Sporangiophores erect, highly variable in length, simple or branched dichotomously once or twice, mostly below or in the middle, septate, yellow-brownish, to 0n5 cm long, 10–12n5 µm broad. The upper fertile part often angled at the points of attachment of the sporocladia, becoming somewhat zig-zag. Sporocladia formed along the upper portions of the sporangiophores. The stipe of the sporocladium one-celled, 27n5–38i5–7n5 µm, often tending to proliferate and produce an additional stipe with a sporocladium or even an extra short branch. Sporocladia multi-celled, mostly nine-septate, yellow,
H. Kwas! na, G. L. Bateman and W. A. J. M. Dawson
897
Fig. 1–5. Coemansia spp. Bars l 20 µm. Fig. 1. C. aciculifera. Sporocladia on stipes which proliferate and produce an additional stipe ending with a sporocladium. Agglomeration of sporangiospores above each mature sporocladium. Fig. 2. C. aciculifera. Sporangiophores with sporocladia. Fig. 3. C. scorpioidea. Scorpioidal arrangement of sporocladia. Fig. 4. C. scorpioidea. Sporangiophore with three short branches and scorpioidally arranged sporocladia on each branch. Fig. 5. Coemansia sp. Sporangiophore and sporocladia.
Coemansia in cereal rhizospheres 36–40i9–11 µm, the terminal cell sterile, tapering, sharply recurved and beak-like. Pseudophialides ovoid to cylindrical, 5–5n5i2 µm. Sporangiospores light yellow, elongate, acicular, 12–17n5i1n5 µm, tapering to the sharply pointed ends. Coemansia aciculifera was recorded on four root pieces of wheat from Highfield. It was recorded previously on Sphagnum sp. in the U.S.A. (Linder, 1943) and, uncommonly, in soil under alder thickets in Italy (Sampo' et al., 1997) and under oak in Poland in 1998 (Kwas! na, unpublished). Coemansia scorpioidea Linder, Farlowia 1, 49–77, 1943. (Figs 3, 4, 7, 11) In pure mixed culture the fungus grew very slowly, 10–12 mm diam. in 15 d on PDA and SNA. It produced intensely yellow, delicate, abundant and high aerial mycelium. Sporangiophores erect, simple, growing from the centre of the colony, up to 1n5–2 mm in length and 8–10 µm diam., distantly septate, bearing 2–10–(12) sporocladia arranged partly in a scorpioid manner. Sporangiophores often produce 2–3 short, 15–25 µm long branches forming a whorl either terminally or subterminally. Each branch bears 2–4 sporocladia mostly arranged scorpioidally. This kind of branching of sporangiophores was not reported previously (Linder, 1943 ; Zycha, Siepmann & Linnemann, 1969). Stipe of sporocladium 1–2-septate, 19n5–21i3n5–5 µm. Sporocladia 5–9-septate, 28n5–31n3i5n5–7n5 µm. The terminal cell of the sporocladium sharply reduced in width to approximately 2 µm. Pseudophialides ovoid, tapering towards the base, 5–6i2n5–3 µm, usually arranged in pairs. Sporangiospores elongate, acicular, inequilateral, nearly straight or slightly concave on one side, tapering from the middle towards sharply pointed ends, 15–17n5i1–1n5 µm. Isolation by direct transfer of spores to PDA or SNA was unsuccessful. Growth in axenic culture was very poor. It produced only extremely slow-growing colonies, 1 mm diam. in 15 d on PDA, visible only under magnification, and formed a thallus submerged in the medium consisting of a few sterile hyphae with numerous swellings. Some Zygomycetes require the addition of biotin and thiamine to the culture medium in order to obtain appreciable axenic development (Barnett, 1970). This was not investigated for C. scorpioidea. The fungus readily produced hyaline, thick-walled zygospores, 27–44 µm diam., filled with numerous refractive globules formed by gradual coalescence of the densely granular cytoplasm. Coemansia scorpioidea was recorded on one root piece from the third wheat crop on Broadbalk field. It was found previously on duck dung (Linder, 1943). Coemansia thaxteri Linder, Farlowia 1, 49–77, 1943. (Figs 9, 10) In pure mixed culture the fungus grew very slowly, 7 mm diam. in 15 d on PDA and SNA. It produced a delicate mycelium consisting of a few long, yellow-brown sporangiophores growing from the centre of the colony. Sporangiophores erect, simple or branched dichotomously once or twice, mostly below or in the middle, septate, yellow-
898 brownish, to 0n5–1 cm long and 10–12 µm broad. Sporocladia formed along the upper portions of the sporangiophores at intervals of 100–200 µm. Stipe of sporocladium 1–2-celled, 41n5–46i6–8 µm, often tending to proliferate and produce an additional stipe with sporocladium or even an extra short branch. Sporocladia multi-celled, mostly nine-septate, yellow, 47–49n5i10–12 µm, the terminal cell sterile, tapering, sharply recurved and beak-like. Pseudophialides ovoid to cylindrical, 4n5–5i2–2n5 µm. Sporangiospores light yellow, elongate, very slender, acicular and somewhat falcate, sharply pointed at both ends, 22–23i1n5–2 µm. Apex of sporangiolum more rounded than in other species. Considering the size of the sporangiophores, sporocladial stipes, sporocladia and sporangiospores this is the largest known species in the genus. The arrangement of the sporocladia and the tendency of the sporocladial stipe to proliferate and form an additional stipe are similar to C. aciculifera. The latter, however, is a smaller species. The studied isolate of C. thaxteri produced the gangliform swellings in the vegetative mycelium that are characteristic of C. aciculifera (Linder, 1943) and that up to now have distinguished C. aciculifera from other species in the genus. Coemansia thaxteri was recorded on one root piece from the continuous wheat from Broadbalk field. It was isolated previously from dead coleopterous larvae in a moist chamber (Linder, 1943). Coemansia sp. (Figs 5, 6) In pure mixed culture the fungus grew very slowly, 4–5 mm diam. in 15 d on PDA and SNA. It produced bright yellow and delicate aerial mycelium. The sporangiophores are erect in the lower part, becoming spirally twisted towards the apex. Sporangiophores usually 1–2 mm long, 10–13 µm broad, distantly septate, simple or rarely branched near the substratum. Sporocladial stipe usually 10–12 µm long. Sporocladia 7–9-septate, 40–53i5n5–9 µm, the sterile terminal cell straight or somewhat recurved, slightly tapering to the bluntly round apex. Pseudophialides elongate-ellipsoidal to clavate. Sporangiospores hyaline to very slightly coloured, fusoid, cylindrical, 20–25i1n5–2n5 µm. The isolate conforms closely to Linder’s description of C. spiralis (Bainier) Eidam. It may, however, be different from the fungus originally described as C. spiralis by Eidam in 1887, particularly in having longer sporangiospores (Chien, 1971). The only other described species with spirally twisted sporangiophores, C. nantahalensis C. Y. Chien, differs in having shorter sporocladial stipes, sporocladia and sporangiospores (Chien, 1971). The fungus was recorded on one root piece of barley from Highfield. The similar fungus described as C. spiralis by Linder (1943) was found previously on the carcass of a horse where it grew together with Saprolegnia sp. (Linder, 1943). We thank the Committee of Scientific Researches in Poland for financing the stay of the first author at IACR-Rothamsted. The research of the other authors is funded by the Biotechnology and Biological Sciences Research Council of the United Kingdom.
H. Kwas! na, G. L. Bateman and W. A. J. M. Dawson
899
Fig. 6–11. Coemansia spp. Bars l 20 µm (Figs 6, 7, 9–11) ; 2n5 µm (Fig. 8). Fig. 6. Coemansia sp. Spirally twisted sporangiophore with sporocladia. Fig. 7. C. scorpioidea. Sporangiophore with two branches and scorpioidally arranged sporocladia. Fig. 8. C. aciculifera. Sporangiospores. Fig. 9. C. thaxteri. Branched arrangement of sporocladial stipes, stained with cotton blue. Fig. 10. C. thaxteri. Separate sporocladium with spores, stained with cotton blue. Fig. 11. C. scorpioidea. Thick-walled zygospores.
Coemansia in cereal rhizospheres REFERENCES Barnett, H. L. (1970). Nutritional requirements for axenic growth of some haustorial mycoparasites. Mycologia 62, 750–760. Benjamin, R. K. (1958). Sexuality in the Kickxellaceae. Aliso 4, 149–169. Benjamin, R. K. (1959). The merosporangiferous Mucorales. Aliso 4, 321–433. Cano, J., Fort, F. & Guarro, J. (1989). Zygomycetes from Spain I. Nova Hedwigia 49, 427–434. Chien, C.-Y. (1971). A new species of Coemansia. Mycologia 63, 1046–1050. Linder, D. H. (1943). The genera Kickxella, Martensella, and Coemansia. Farlowia 1, 49–77. Nirenberg, H. I. (1976). Untersuchungen u$ ber die morphologische und (Accepted 15 October 1998)
900 biologische Differenzierung in der Fusarium-Sektion Liseola. Mitteilungen aus der Biologischen Bundesanstalt fuW r Land- und Forstwirtschaft, Berlin-Dahlem 169, 1–117. Sampo' , S., Bergero, R., Buffa, G. & Luppi-Mosca, A. M. (1997). Soil fungal communities in a young and an old Alnus viridis coenosis. Mycologia 89, 837–845. Van Tieghem, P. & Le Monnier, G. (1873). Recherches sur les Mucorine! es. Annales des Sciences Naturelles Botanique et Biologie VeT geT tale 5, 261–399. Warcup, J. H. (1951). The ecology of soil fungi. Transaction of the British Mycological Society 34, 376–400. Zycha, H., Siepmann, R. & Linnemann, G. (1969). Mucorales. J. Cramer Verlag : Lehre.
896
Printed in the United Kingdom
Coemansia species from the rhizospheres of wheat and barley in the United Kingdom
H. K W A S! N A1, G. L. B A T E M A N2 A N D W. A. J. M. D A W S O N2 " Department of Forest Pathology, Agricultural University, ul. Wojska Polskiego 71c, 60-625 PoznanT , Poland # IACR-Rothamsted, Harpenden AL5 2JQ, U.K.
Coemansia aciculifera, C. scorpioidea and C. thaxteri were found in the rhizosphere of wheat and a fungus resembling C. spiralis was found in the rhizosphere of barley from two fields in eastern England when serially washed root pieces were incubated on low nutrient agar (SNA).
Since Coemansia was described by Van Tieghem & Le Monnier (1873), its representatives have been found only rarely because of their nutritional preferences. Coemansia was isolated originally mostly from the dung of small animals, especially rats and mice (Linder, 1943). The first records of its occurrence in soil appeared later but were infrequent. The species recorded most commonly in soil is C. erecta Bainier. This species was found in non-agricultural grassland in the United Kingdom, together with C. pectinata Bainier, (Warcup, 1951) and more recently with other Zygomycetes in arable soil in Spain (Cano, Fort & Guarro, 1989). Coemansia comprises a group of species characterized in general by : (i) very slow growth on culture media ; (ii) bright, yellow, abundant and high aerial mycelium ; (iii) asexual reproduction by means of elongate-cylindrical to fusiform sporangiospores formed in one-spored, rounded or sharp at the apex sporangiola borne on the lower surface of sporocladia produced on sporangiophores ; (iv) erect or ascending, highly variable in length but generally 2–3 mm long, septate, simple, regularly or irregularly branched, hyaline-yellowish to brown sporangiophores ; (v) acrogenous formation of sporocladia that are laterally disposed by continued growth of the fertile axis of the sporangiophore and are pleurogenous, stalked, elongate, nearly straight, arcuate or slightly sigmoid, septate and produce ellipsoidal to elongate-ovoid pseudophialides arranged in more or less transverse rows arising from all but one or two terminal sterile cells ; (vi) sexual reproduction by means of thick-walled, smooth, nearly hyaline zygospores formed from the fusion of small gametangia, delimited apically by two relatively short undifferentiated sexual branches or from an intercalary cell delimited in an undifferentiated sexual branch near the point of fusion of the branch with an ordinary vegetative hypha (Benjamin, 1958, 1959). During investigation of fungal communities in the rhizospheres of cereal plants, root pieces were taken in early June 1997 from wheat (Triticum aestivum L.) or barley (Hordeum
vulgare L.) grown as autumn-sown crops in two fields at Rothamsted. A total of 360 root pieces of wheat cv. Brigadier and 360 root pieces of barley cv. Pipkin, grown as second cereals on Highfield, and 1440 root pieces of wheat cv. Hereward grown as first, third or continuous wheat crops on Broadbalk field were examined. The root pieces (each 0n5 cm) were washed serially, 20 times, by shaking vigorously for 3 min in cold, sterile distilled water. They were than placed on low nutrient agar (SNA ; Nirenberg, 1976) containing penicillin, streptomycin sulphate and chloramphenicol and examined at intervals whilst incubating for 7 d at 20 mC and then up to 2 mo at 4m. After a minimum of 4 wk at the lower temperature, four Coemansia spp. previously unknown from the U.K. were identified. Subcultures were made on SNA and potato dextrose agar (PDA), although none produced cultures that contained only the Coemansia sp. These cultures are referred to below as ‘ pure mixed cultures ’ because each consisted of Coemansia and the fungi with which it was intimately associated and not removed by subculturing. Coemansia aciculifera Linder, Farlowia 1, 49–77, 1943. (Figs 1, 2, 8) In pure mixed culture the fungus grew very slowly, 8–10 mm diam. in 15 d on PDA and SNA. It produced vivid bright yellow, delicate, abundant and high aerial mycelium. Sporangiophores erect, highly variable in length, simple or branched dichotomously once or twice, mostly below or in the middle, septate, yellow-brownish, to 0n5 cm long, 10–12n5 µm broad. The upper fertile part often angled at the points of attachment of the sporocladia, becoming somewhat zig-zag. Sporocladia formed along the upper portions of the sporangiophores. The stipe of the sporocladium one-celled, 27n5–38i5–7n5 µm, often tending to proliferate and produce an additional stipe with a sporocladium or even an extra short branch. Sporocladia multi-celled, mostly nine-septate, yellow,
H. Kwas! na, G. L. Bateman and W. A. J. M. Dawson
897
Fig. 1–5. Coemansia spp. Bars l 20 µm. Fig. 1. C. aciculifera. Sporocladia on stipes which proliferate and produce an additional stipe ending with a sporocladium. Agglomeration of sporangiospores above each mature sporocladium. Fig. 2. C. aciculifera. Sporangiophores with sporocladia. Fig. 3. C. scorpioidea. Scorpioidal arrangement of sporocladia. Fig. 4. C. scorpioidea. Sporangiophore with three short branches and scorpioidally arranged sporocladia on each branch. Fig. 5. Coemansia sp. Sporangiophore and sporocladia.
Coemansia in cereal rhizospheres 36–40i9–11 µm, the terminal cell sterile, tapering, sharply recurved and beak-like. Pseudophialides ovoid to cylindrical, 5–5n5i2 µm. Sporangiospores light yellow, elongate, acicular, 12–17n5i1n5 µm, tapering to the sharply pointed ends. Coemansia aciculifera was recorded on four root pieces of wheat from Highfield. It was recorded previously on Sphagnum sp. in the U.S.A. (Linder, 1943) and, uncommonly, in soil under alder thickets in Italy (Sampo' et al., 1997) and under oak in Poland in 1998 (Kwas! na, unpublished). Coemansia scorpioidea Linder, Farlowia 1, 49–77, 1943. (Figs 3, 4, 7, 11) In pure mixed culture the fungus grew very slowly, 10–12 mm diam. in 15 d on PDA and SNA. It produced intensely yellow, delicate, abundant and high aerial mycelium. Sporangiophores erect, simple, growing from the centre of the colony, up to 1n5–2 mm in length and 8–10 µm diam., distantly septate, bearing 2–10–(12) sporocladia arranged partly in a scorpioid manner. Sporangiophores often produce 2–3 short, 15–25 µm long branches forming a whorl either terminally or subterminally. Each branch bears 2–4 sporocladia mostly arranged scorpioidally. This kind of branching of sporangiophores was not reported previously (Linder, 1943 ; Zycha, Siepmann & Linnemann, 1969). Stipe of sporocladium 1–2-septate, 19n5–21i3n5–5 µm. Sporocladia 5–9-septate, 28n5–31n3i5n5–7n5 µm. The terminal cell of the sporocladium sharply reduced in width to approximately 2 µm. Pseudophialides ovoid, tapering towards the base, 5–6i2n5–3 µm, usually arranged in pairs. Sporangiospores elongate, acicular, inequilateral, nearly straight or slightly concave on one side, tapering from the middle towards sharply pointed ends, 15–17n5i1–1n5 µm. Isolation by direct transfer of spores to PDA or SNA was unsuccessful. Growth in axenic culture was very poor. It produced only extremely slow-growing colonies, 1 mm diam. in 15 d on PDA, visible only under magnification, and formed a thallus submerged in the medium consisting of a few sterile hyphae with numerous swellings. Some Zygomycetes require the addition of biotin and thiamine to the culture medium in order to obtain appreciable axenic development (Barnett, 1970). This was not investigated for C. scorpioidea. The fungus readily produced hyaline, thick-walled zygospores, 27–44 µm diam., filled with numerous refractive globules formed by gradual coalescence of the densely granular cytoplasm. Coemansia scorpioidea was recorded on one root piece from the third wheat crop on Broadbalk field. It was found previously on duck dung (Linder, 1943). Coemansia thaxteri Linder, Farlowia 1, 49–77, 1943. (Figs 9, 10) In pure mixed culture the fungus grew very slowly, 7 mm diam. in 15 d on PDA and SNA. It produced a delicate mycelium consisting of a few long, yellow-brown sporangiophores growing from the centre of the colony. Sporangiophores erect, simple or branched dichotomously once or twice, mostly below or in the middle, septate, yellow-
898 brownish, to 0n5–1 cm long and 10–12 µm broad. Sporocladia formed along the upper portions of the sporangiophores at intervals of 100–200 µm. Stipe of sporocladium 1–2-celled, 41n5–46i6–8 µm, often tending to proliferate and produce an additional stipe with sporocladium or even an extra short branch. Sporocladia multi-celled, mostly nine-septate, yellow, 47–49n5i10–12 µm, the terminal cell sterile, tapering, sharply recurved and beak-like. Pseudophialides ovoid to cylindrical, 4n5–5i2–2n5 µm. Sporangiospores light yellow, elongate, very slender, acicular and somewhat falcate, sharply pointed at both ends, 22–23i1n5–2 µm. Apex of sporangiolum more rounded than in other species. Considering the size of the sporangiophores, sporocladial stipes, sporocladia and sporangiospores this is the largest known species in the genus. The arrangement of the sporocladia and the tendency of the sporocladial stipe to proliferate and form an additional stipe are similar to C. aciculifera. The latter, however, is a smaller species. The studied isolate of C. thaxteri produced the gangliform swellings in the vegetative mycelium that are characteristic of C. aciculifera (Linder, 1943) and that up to now have distinguished C. aciculifera from other species in the genus. Coemansia thaxteri was recorded on one root piece from the continuous wheat from Broadbalk field. It was isolated previously from dead coleopterous larvae in a moist chamber (Linder, 1943). Coemansia sp. (Figs 5, 6) In pure mixed culture the fungus grew very slowly, 4–5 mm diam. in 15 d on PDA and SNA. It produced bright yellow and delicate aerial mycelium. The sporangiophores are erect in the lower part, becoming spirally twisted towards the apex. Sporangiophores usually 1–2 mm long, 10–13 µm broad, distantly septate, simple or rarely branched near the substratum. Sporocladial stipe usually 10–12 µm long. Sporocladia 7–9-septate, 40–53i5n5–9 µm, the sterile terminal cell straight or somewhat recurved, slightly tapering to the bluntly round apex. Pseudophialides elongate-ellipsoidal to clavate. Sporangiospores hyaline to very slightly coloured, fusoid, cylindrical, 20–25i1n5–2n5 µm. The isolate conforms closely to Linder’s description of C. spiralis (Bainier) Eidam. It may, however, be different from the fungus originally described as C. spiralis by Eidam in 1887, particularly in having longer sporangiospores (Chien, 1971). The only other described species with spirally twisted sporangiophores, C. nantahalensis C. Y. Chien, differs in having shorter sporocladial stipes, sporocladia and sporangiospores (Chien, 1971). The fungus was recorded on one root piece of barley from Highfield. The similar fungus described as C. spiralis by Linder (1943) was found previously on the carcass of a horse where it grew together with Saprolegnia sp. (Linder, 1943). We thank the Committee of Scientific Researches in Poland for financing the stay of the first author at IACR-Rothamsted. The research of the other authors is funded by the Biotechnology and Biological Sciences Research Council of the United Kingdom.
H. Kwas! na, G. L. Bateman and W. A. J. M. Dawson
899
Fig. 6–11. Coemansia spp. Bars l 20 µm (Figs 6, 7, 9–11) ; 2n5 µm (Fig. 8). Fig. 6. Coemansia sp. Spirally twisted sporangiophore with sporocladia. Fig. 7. C. scorpioidea. Sporangiophore with two branches and scorpioidally arranged sporocladia. Fig. 8. C. aciculifera. Sporangiospores. Fig. 9. C. thaxteri. Branched arrangement of sporocladial stipes, stained with cotton blue. Fig. 10. C. thaxteri. Separate sporocladium with spores, stained with cotton blue. Fig. 11. C. scorpioidea. Thick-walled zygospores.
Coemansia in cereal rhizospheres REFERENCES Barnett, H. L. (1970). Nutritional requirements for axenic growth of some haustorial mycoparasites. Mycologia 62, 750–760. Benjamin, R. K. (1958). Sexuality in the Kickxellaceae. Aliso 4, 149–169. Benjamin, R. K. (1959). The merosporangiferous Mucorales. Aliso 4, 321–433. Cano, J., Fort, F. & Guarro, J. (1989). Zygomycetes from Spain I. Nova Hedwigia 49, 427–434. Chien, C.-Y. (1971). A new species of Coemansia. Mycologia 63, 1046–1050. Linder, D. H. (1943). The genera Kickxella, Martensella, and Coemansia. Farlowia 1, 49–77. Nirenberg, H. I. (1976). Untersuchungen u$ ber die morphologische und (Accepted 15 October 1998)
900 biologische Differenzierung in der Fusarium-Sektion Liseola. Mitteilungen aus der Biologischen Bundesanstalt fuW r Land- und Forstwirtschaft, Berlin-Dahlem 169, 1–117. Sampo' , S., Bergero, R., Buffa, G. & Luppi-Mosca, A. M. (1997). Soil fungal communities in a young and an old Alnus viridis coenosis. Mycologia 89, 837–845. Van Tieghem, P. & Le Monnier, G. (1873). Recherches sur les Mucorine! es. Annales des Sciences Naturelles Botanique et Biologie VeT geT tale 5, 261–399. Warcup, J. H. (1951). The ecology of soil fungi. Transaction of the British Mycological Society 34, 376–400. Zycha, H., Siepmann, R. & Linnemann, G. (1969). Mucorales. J. Cramer Verlag : Lehre.