Taxonomic Studies of Choanephoraceae in India

TAXONOMIC STUDIES OF CHOANEPHORACEAE IN INDIA

B. S. I~{EHROTRA and M. D. MEHROTRA (Botany Department, University o~ Allahabad, India)

(with 8 pIates)

(24.VI.1963)

INTRODUCTION The family Choanephoraceae was first established by FITZPAT- t~ICK (1930) and later it was amended by NAu~ov (1939). It has both typical asexual and sexual characteristics. Its type genus, Choanephora, was first reported by CIZRRE¥ (1873). He had previously named it Cunninghamia, after D. D. CVNNINGt~AM, on whose material he had based his description, but later he changed it to the present name because the earlier named genus already existed in the conifers. The type species, previously named, was Cunninghamia in/undibuli/era but was later changed by him to Choanephora cunninghamiana, thus changing the specific epithet as well. This was later corrected by SACCARDO (1891) who was, therefore, the first to use the combination Choanephora in/undibuli/era, now recognized as the type species of the genus. The principal asexual characters of the species were described to be the presence of sporangia with appendaged sporangiospores and conidia borne on vesicular swelling at the apex of a conidiophore; the latter type of spores being non-appendaged. The sexual spore, the zygospore, was found to be produced between the tips of entwining branches. A number of species have since been included in the genus Choane- phora. Out of these HESSELTI~E (1953), in his review of the family, recognized four species, viz., Choan@hora in/undibuli/era, C. cucurbitarum, C. con]uncta and C. ~ersicaria; and placed Choanephora sim- sonii among the doubtful species. Recently C. persicaria has been transferred by him (t{ESSELTINE, 1960) to a new genus, Gilbertella. This species produces only sporangia with the appendaged sporangiospores, characteristic of the family Choanephoraceae. But it has been shown by him to produce Mucor type zygospores, a character which justifies its inclusion in a new genus and a probable place in ~ t3. S. MI~ttI~OTRA ~ M. D, MEI-IROTRA the Mucoraceae, after broadening the concept of the family to include forms with appendaged sporangiospores. In India a new variety of this species has been found to be quite common on fading flowers of Thevetia nerri/olia JlJss and in garden soil. A morphological and physiological study of this variety, G. ~ersicaria var. indica MEt~ROTRA and MEI-IROTRA, has been reported in an earlier communication from this laboratory (MEHROTRA & MEm~OTRA, 1962). In the year 1914, THAXTER added a second genus to the family, viz., BlakesZea with the type species Blakeslea trispora. This species lacked conidia but instead, it developed few-spored sporangiola on sporangioliferous heads. Later SINHA (1940) demonstrated the production of single spored sporangiola by this fungus, when it was grown on a starvation medium. From this he concluded that the monosporous sporangiola of BZakeslea tri@ora were identical with the conidia of Choanephora. He suggested that the generic name Blakeslea must be considered as a synonym of Choanephora. Recent- ly POITRAS (1955) also observed, on a medium of low nutritional level, that there is a definite tendency in Blakeslea trispora with respect to the reduction in the content and size of sporangia and sporangiola. He also found in this species, under abnormal nutritional conditions, true monosporous sporangiola on the sporangioliferous heads, besides the normal few-spored sporangiola. The significant finding of POITRAS (1955) was with regard to the nature of conidia borne on the conidiophores of Choan@hora, a feature regarded as the chief characteristic, distinguishing that genus from Blakeslea. He subjected the conidia of Choanephora to various treatments and concluded that the conidia are in fact monosporous sporangiola. He demonstrated that there is an outer wall of the sporangium and a separate coloured inner wall of the endospore. In few of the germinating conidia he observed that the outer thin sporangiolic membrane was drawn out for a short distance with the germ tube, indicating thereby that the inner spore wall is separate from the outer sporangiolic membrane. Also conidia exhibiting empty spaces within the sporangiolic membrane at both the basal and apical ends of the endospore were frequently observed. POITRAS (1955) pointed out that the correct epithet for the species having multi-spored (usually 3--5) sporangiola is Choanephora trispora (THAXTER) SIN- ~IA. In 1955 NAGANISflI & KAWAKAMI placed a second species, Bla- keslea circinans in the genus. This species produced only multi- spored columellate sporangia with appendaged sporangiospores but lacked sporangiola or conidia. HESSELTINE & BENJAMIN (1957) studied the mating reaction of this species and found that the zygospores were similar to other species of Choanephora. They, therefore, transferred this species to the genus Choanephora. The correct epithet for this species now stands as Choanephora circinans (NAGA- NISHI and I{AWAKAMI) HESSELTINE and BENJAMIN. No systematic study of the Choanephoraceae has been made in India, since the publication of SIN~A's (i940) paper. The present TAXONOMY OF INDIAN CHOANNPHORACEAE 23 study deals with an attempt at a taxonomic treatment of the family based on isolations made in India.

MATERIALS AND METHODS Collections were made during a period of three years from varied sources including fading flowers of Lu//a aegyptiaca MILL., Lagenaria vulgaris SER., Cucurbita pepo L., Momordica charantia L., Solarium melongena L., Hibiscus esculentus L., Sida acula L., Scrophularia sp., Thevetia nerri/olia Juss, Capsicum annuum L., Hibiscus rosa sinensis L., Zinnia sp. and other plants; decomposing leaves of Colocasia antiquorum SCHOTT, Zinnia sp., Hibiscus esculentus L. and other plants; decomposing fruits of Lu//a aegyptiaca MILL., Momordica charantia L., Lyc@ersicum esculentum MILL. and soils of the different gardens and orchards of Atlahabad. The media used for the isolation and identification of the cultures were potato dextrose agar 1, syn- thetic Mueor-agar z, and hay infusion agar ~.

TAXONOMIC CONSIDERATIONS All the recognized species of the family have been isolated, besides a new species from a dead insect earlier described as Choanephora hetero@ora (MEHROTRA & MEHROTRA, 1961). This species is a significant addition to the genus. The conidiophores bearing conidia, which so far have been known to be simple or slightly branched at the apex, have been found to show true fertile branches. We have also observed such branching in Choanephora conjuncta and occa- sional branching of the sporangiophores bearing multi-spored sporangia in Choanephora circinans. In the latter species some of the sporangiophores develop peculiar proliferating sporangia. The unbranched sporangiophore may end in a vesicle (sterile sporangium) from which proliferate out sterile hyphae or fertile sporangiophores which bear secondary sporangia, or may remain sterile and may further proliferate to give rise to sporangiophores terminating into tertiary sporangia. The heterosporous sporangium in C. heterospora and the numerous appendages on the surface of the sporangiospores are features in which this species stands out of all other species of the genus. The family Choanephoraceae, as it stands today, is characterized by the normal production of two types of sporophores -- one producing terminally multi-spored, columellate sporangium and another producing conidia or few-spored sporangiola on primary or secondary vesicles at its apex. Besides, under poor nutritional conditions the reduction in size and content of the sporangia and sporangiola are

1) Potato, 200 g; dextrose, 20 g; dist. water, 1000 mL 3) Dextrose, 40 g; asparagine, 2 g; IKH3PO ~, 0.5 g; MgSOa. 7H20, 0.25 g; thiami- ne hydrochloride, 0.5 rag; agar agar, 20 g; dist. water, 1000 ml. 3) Decomposing hay, 50 g; KH~]PO4, 2.0 g, agar agar, 15.0 g, dist. water, 1000 ml. 24 B. S. MI~HROTRA ~ M. D. MEHROTRA also observed. The sporangiospores from sporangium or from few- spored sporangiola are always appendaged while the conidia are devoid of appendages. The family Choanephoraceae should include two genera, viz., Choanephora and Blakeslea. The authors agree with HESSELTINE (Personal communication, 1963) that the retention of the genus BlakesIea seems appropriate from the practical stand point. It is true that few-spored sporangiola normally seen in Blakeslea are ho- mologous with conidia, but the two can easily be distinguished from each other irrespective of the fact that under certain abnormal conditions (e.g., poor nutritional conditions) the unispored sporangiola may also be produced in Blakeslea tri@ora. While studying the isolates of Choanephora as found in natural habitats, it has been observed that they are of two types with respect to the secondary vesicles on heads bearing conidia. In some of them the secondary vesicles persist as funnel-shaped structures after the conidia are detached and in others the vesicles remain unaffected even after the fail of conidia. In the former category of species are found two types of isolates, one having ovoid to ellipsoid conidia which are characteristics of most species of Choanephora where they are known, another having typically obovate eonidia on the heads. The former type of isolates are generally recognized to belong to the species Choanephora in/undibuli/era and the latter to C. conjuncta. However, doubts have been expressed (PoITRAS, 1955; HESSELTINE, 1962) about the reliability of such characters as striations on the spore wall of the monosporous sporangiola and funnel-shaped vesicles. We feel that at present we do not possess enough data to ex- press a definite opinion regarding the correct taxonomic position of the two species, viz., C. con1"uncta and C. in/undibuli/era. These two species are, therefore, being retained, distinguishing them on the basis of characters currently recognized.

DIAGNOSES A description of the family, its two genera and the isolates of the different species excluding C, heterospora MEI~ROTRA & MEH- ROTRA is given below. Choanephoraceae FITZPATRICK, Lower Fungi 258. 1930, emend. NAUMOV, C16s des Mucorin6es, 97. 1939. Mycetium hyaline, much branched; multi-spored, columellate sporangia; reduced sporangia with one or more sporangiospores in each; few-spored sporangiola or conidia on a primary vesicle or secondary vesicles at the tip of an usually unbranched sporangiophore. Sporangiospores from sporangia or few-spored sporangiola possess fine radiating appendages and conidia without appendages. Zygo- spores produced between the tips of entwining branches. TASKONOMY OF INDIAN CHOANEPHORACEAI~; 25

Plate I. Figs. 1--1~2. Blakeslea trispora. 1. A sporangiophore with a primary vesicle bearing few-spored sporangiola. 2. A sporangiophore with bifurcation of the apex, each branch bearing a vesicle at its tip. 3. A sporangiophore showing secondary vesicles borne on diehotomously branched stalks. 4. Two nmlti-spored sporangia borne on the circinate sporangiophores. 5. One sporangiospore from a few spored sporangiolum showing appendages at either end. 6. Two few-spored sporangiola. 7. A sporangiophore with one monosporons and two few-spored sporangiola borne on primary vesicle. 8. Two few-spored sporangia. 9. A number of columellae showing the range in size and shape. I0. Four sporangiospores from a multi-spored sporangium showing appendages at either end. 11. An enlarged sporangiospore from a multi-spored sporangium showing appendages at either end. I2. tlyphae showing chlamydospores. 26 B.s. MEI-IROTRA ~C 1V2. D. MJiilil~OTR~-

Key to Genera A. Columellate few-spored to multi-spored sporangium and few-spored sporangiola on the sporangiotiferous heads present; conidiophores with conidia absent -- Blakeslea. AA. Columellate few-spored to multi-spored sporangium and conidiophores with conidia on vesicles present; few-spored sporangiola on the sporangioliferous heads absent -- Cho- anephora. Blakeslea THAXTER, Bot. Gaz. 58: 353, 1914. Multi-spored, columellate sporangia oil unbranched sporangiophores; reduced sporangia with one or more sporangiospores in each; sporangiola without columellae, borne on small vesicular sterigmata which are in turn attached to sporangioliferous heads; sporangiospores from both sporangia and sporangiola striate and appendaged, conidia absent. Zygospores formed between suspensors. Only species, Blakeslea trispora THAXTER. Blakeslea trispora TIIAXTER, Bot. Gaz. 58: 353. Pls. 26, 27, and figs. 1--18. 1914. (PLATES I & VI) 1923. Choanephora dichotoma GA~'DRUP, Besoek, Proefsta~. Medel. 3:5 (Nomen nudnm according to WEBER and W~OLF). 1940. Choa~¢ephora trispora (T~tAXTER) SIXHA, Proc. Indian Acad. Sci. ]3. 11: 167. Colony cottony, white when young becoming yellowish on aging, growing rapidly; hyphae non-septate, granular upto 13 # in width, showing tight twisted knots of mycelium; sporangiophores of sporangia arising from surface hyphae, unbranched, often bent or circinate below the sporangium quite variable in length; sporangia at first white and later becoming brownish black, spherical, or slightly flattened, 20--160 ~; wall hyaline, persistent, tuberculate breaking open to give two halves; reduced sporangia borne on smaller sporangiophores, generally few-spored, rarely one-spored sporangia also seen; cotumellae elongate, oval to pyriform, with a collar, 45--120 X 14--59 }~; sporangioliferous sporangiophores may end into a primary vesicle which directly bears typically 3 spored sporangiola, rarely 1 or 4 spored sporangiola also produced, primary vesicle may be absent and the sporangiophore may bifurcate at its apex giving rise to secondary vesicles, at times the stalks may branch dichoto- mousty, the ultimate branches terminate into sporangioia bearing vesicles; sporangiola oval, 12--15 × 11--13/~, mostly 3 spored, rarely 1 or 4 spored borne on rounded sterigmata on the vesicles; sporangiospores like those of sporangia, 8--15× 4--8.5 #; chlamydospores oval or fusiform, 11--20 × 13 ~, usually present in old cultures, solitary or in chains; zygospores not seen. Isolated from decomposing leaves of Colocasia antiquorum SCHOTT, flowers of Thevetia nerri/olia Jvss and soils collected from various parts of India, viz., Calcutta, Amarkantak (M.P.), Suhagi TAXONOMY OF INDIAN CHOANEPHORACEA~ 27

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15 '30 1 Plate II. Figs 1--13. Choanephora cucurbitarum. 1 & 2. Two conidiophores with primary and secondary vesicles. 3. A conidiophore with primary vesicle from the surface of which arise simple or dichotomously branched stalks, l. A conidiophore with a bifurcated primary vesicle. 5. Two sporangia borne on circinate sporangiophores. 6. Conidia, three of them showing empty spaces. 7. A conidiophore with two of the vesicles bearing conidia. 8. A number of columellae showing the extent of variation in size and shape. 9. Three few-spored sporangia. 10. Some sporangiospores from a sporangium showing appendages at two to four points. 11. Three germinating sporangiospores. 12. Hyphae showing chlamydospores. I3. Two zygospores borne between the tips of the entx~4ning branches. 28 B. S, MEHROTRA ~ M. D. MEHROTRA

(M.P.), Mysore and Hardwar. Culture No. MX--10 on which the above description is based has been deposited in culture collection, Botany Department, University of Allahabad, Allahabad. Choanephora CURREY, J. Linn. Soc. Bot. 13: 578. 1873. 1873. Cunninghamia C~IRR~Y, J. Linn. Soc. Bot. 13:334. 1904. Choanephorella VUILLEMIN, Bull. Soc. lV[ycol. Fr. 20:28. (N~omen nudum.) Multi-spored, columellate sporangia usually on unbranched sporangiophores; reduced sporangia with one or more sporangiospores in each; sporangiospores striate and appendaged; conidia on a primary or secondary vesicle at the tip of an usually unbranched conidiophore; conidia faintly or distinctly striate and non-appendaged. Zygospores produced between the tips of the entwining branches. Type species -- Choanephora in/undibuli/era (CURRE¥) SACCARDO.

Key to Species of Choanephora A. Sporangia (few to many-spored) and conidia both present B B. Sporangiospores in sporangia of an uniform size range, not heterosporous ...... C C. Secondary vesicles not persistent on funnel- shaped structures; sporangiospores mostly ellipsoidal ...... C. cucurbitarum CC. Secondary vesicles persistent as funnel shaped structures ...... D D. Conidia mostly ellipsoidal and distinctly striate ...... C. in/undibuli/era DD. Conidia mostly ovoid and faintly striate C. con/uncta BB. Sporangiospores in sporangia usually heterosporous C. heterospora AA. Sporangia (few-to many-spored) present; conidia absent C. circinans Choanephora cucurbitarum (BEt~I~. and RAy.) TnAXTER. Rhodora 5: 102. P1. 46, figs. 1--6. 1903. [PLATES Ii & iv] 1875. Rhopalomyces cucurbitarum BERXBL~¥ and t;IAVEXEL, Gravillea 3: 109. i893. Rhopalomyces elegans COXDA vat. cucurbitarum 3/J[ARCEAL, Rev. MycoL 15: 11. 1901. Choanephora americana MOELLE~, Phycomyceten und Ascomyceten 393. 1915. Cun- ninghamella mandshurica SAITO and N&GANISI~I, t3ot. Miag. Tokyo 29: 285. 1934. Choanephora manshurica (S~-Iiro and NAGA~'ISI~II) TAI, Sinensia 4: 219. (Fide Zycha). Colony colourless when young becoming slightly yellowish at maturity, growing rapidly; hyphae non-septate, 5.0--13.6 # in width, branching irregularly; sporangiophores arising from surface hyphae, unbranched, often bent or circinate below the sporangium, hyaline; sporangia sphericaI to slightly flattened, at first white later brownish black, 23.5--170 ~u ill diam. mostly 80--115#; wall persistent, tuberculate, breaking from above to base to give two equal halves, TAXONOMY OF INDIAN CHOANEPHORACEAE 29

Plate III, Figs. 1---13. Choavzephovain/undibuli/era. I. A conidiophore with primary vesicle from the surface of which arise simple or dichotomonsly branched stalks. 2 & 3. Two conidiophores each with a bifurcated primary vesicle from the surface of which arise stalked secondary vesicIes. 4. Two multi-spored sporangia borne on the circinate sporangiophores, g. Five conidia, one of which showing empty spaces. 6. Showing the attachment of the secondary funnel-shaped vesicle. 7. One funnel-shaped secondary vesicle. 8. A number of columellae showing the extent of variation in size and shape. 9. Three, one to few-spored sporangia, i0. Three sporangiospores showing appendages at either end. 11. tIyphae showing chlamydospores. 12. Two zygospores borne between the tips of the entwining branches. I3. Two germinating sporangiospores. 30 B S.xMtgHROTRA (~)/[. D. M/~;HROTRA reduced sporangia borne on smaller, sporangiophores, globular generally few-spored, rarely one-spored sporangia also seen; columellae pyriform to globose, with a collar, upto 136 × 98.5 # mostly 35-- 98.8× 30---69.8 #; sporangiospores light coloured, often granular, ellipsoid to almost triangular, striations seen under high magnification, with hair-like appendages, 1 to 1.5 times as long as the sporangiospores, 16--26×8--14.5 ~ mostly 18--24×11--12.75 /~, germinating usually by one or two germ tubes; conidiophores, erect nonseptate, hyaline, 15--40 ,u in diam. upto 3.8 mm in length; may end into a primary vesicle which bears conidia, primary vesicle may give rise to stalks terminating into secondary vesicles bearing coni- dis, primary vesicle may be absent and the conidiophore may bifurcate at its apex giving rise to secondary vesicles, at times the stalk may branch dichotomously, the ultimate branches end into conidia bearing vesicles; conidia brown, ovoid to ellipsoid, 13.5--20 × 8.5-- 12 ft, longitudinally striate, with a papilla at one end; chlamydospores oval or globose, 12.5-.--16 x 12.6 x 36 #, usually present in old cultures, solitary or in chains; heterothallic: zygospores dark brown, 50--90/~. Isolated from the decomposing leaves of Psidium guajava L., Carica papaya L. and Colocasia antiquorum Sc~oTT, flowers of Hi- biscus esculentus L., Momordica charantia L., Hibiscus rosa sinensis L., Solanum mdongena L., Capsicum annuum L., and various garden soils. Culture No. MX--11, deposited in culture collection, Botany Department, University of Allahabad, Allahabad.

Choanephora in/undibuli/era (CuRl~:Y) SACCARDO, Syll. Fung. 9: 339. 1891. [PLATES III & IV] 1873. Cunninghamia i~z/undibuti/era CURR~Y, J. Linn. Soc. Bot. 13: 334. 1873. Choanephora cunninghamiana Cul~Ian-z, J. Linn. Soc. Bot. 13: 578. Colony colourless when young becoming yellowish on aging, growing rapidly; hyphae non-septate, 4.5--14.5 ,u in width, branching irregularly; sporangiophores arising from surface hyphae, unbranched, often bent or circinate below the sporangium, hyaline, usually shorter than the conidiophores; sporangia mostly spherical but sometimes flattened, at first white later brownish black, 35-- 160 }~ in diam., mostly 62.5---135 #; wall persistent, hyaline, tuberculate, rupturing vertically; reduced sporangia borne on smaller sporangiophores, generally few-spored, rarely one-spored sporangia also seen; columellae pyriform to globose, with a collar upto 124.5 x 90 ,u, mostly 45--105 × 35--75 #; sporangiospores deep brown, ovoid to ellipsoid, sometimes irregular, longitudinally, striate, striations seen usually under high magnification, appendaged at either end, 22.6--14 X 8--14.5/~, germinating mostly by one or two germ. tubes; conidiophores, erect non-septate, hyaline, 18---38.6 # in diam., upto 3.5 mm in length, may end into a primary vesicle which directly bears conidia, primary vesicle may give rise to stalks terminating TAXONOMY OF INDIAN CHOANEPHORACEAE 31

Plate IV. Figs, 1--°~3. Choanephora cucurbitar~,~m. 1. A young bi%rcated conidiophore ~dth two vesicles bearing young conidia, X 550. 2. A mature conidiophore with secondary vesicles and mature conidia, x 500. 3. A magnified conidium showing striations, X 2000. Figs. 4 & 5. Choanephora i@undibuli/era. 4. Two funnel-shaped secondary vesicles, × 130. 5. A conidium showing striations, × 1500. 32 B, S. NIEIKROTRA ~5 I~. D, MEH2ROTRA into secondarv vesicles bearing conidia, primary vesicle may be absent and the conidiophore may bifurcate at its apex giving rise to secondary vesicles, the stalks at times may branch dichotomously, the ultimate branches end into conidia bearing vesicles; on collapsing give a characteristic funnel-shaped appearance; conidia brown, o- void to ellipsoid, 12--17.6 × 8.5--i0.6 #, longitudinally striate, with a papilla at one end; chlamydospores oval or fusiform, 11.6-- 11.6--17 × 16--34.4 #, usually present in old cultures, solitary, also in chains; heterothallic, zygospores deep brown, 45.5-76 #, suspen- sots tong-like, wall striate. Isolated from the decomposing leaves of Zinnia sp., Colocasia antiquorum SCHOTT and Sida acuta L., flowers of Zinnia sp., Scro- phularia sp., Thevetia nerri/olia Jvss, Lagenaria vuZagris Ser., Cu- curbita pepo L. and fruits of Coccinia indica W. & A. and various garden soils. Culture No. MX--8 on which the above description is based, has been deposited in culture collection, Botany Depart- ment, University of Allahabad, Allahabad. Choan@hora con]uncta COUCH, J. Elisha Mitchell Sci. Soc. 41 : 143, 1925. [PLATES V & VI] Colony colourless when young becoming yellowish on aging, growing rapidly; hyphae non-septate, 4.5--1.4 # in width, branching irregularly; sporangiophores arising from surface hyphae, unbranched, often bent or circinate below the sporangium, hyaline usually shorter than tile conidiophores; sporangia at first white later becoming brownish black, globose to dorsiventrally flattened, 30-- 130 # in diam., mostly 45--90 t,; wall persistent, tuberculate, hyaline, rupturing vertically; reduced sporangia borne on smaller sporangiophores, generally" few-spored, rarely one-spored sporangia also seen; columetlae pyriform to globose, with a collar, 20--84× 16--- 62.6 #; sporangiospores brown, ovoid to ellipsoid, appendaged at either end, longitudinally striate, striations seen under high magnification, 6--15 × 11--23.5 #, germinating mostly by one or two germ tubes; conidiophores erect, non-septate, hyaline, 12--36.5 # in diam., upto 4.8 mm in length, mostly unbranched, may end into a primary vesicle which directly bears conidia, primary vesicle may be absent and the conidiophore may bifurcate at its apex giving rise to secondary vesicles, the stalks at times may branch dichotomously, the ultimate branches end into conidia bearing vesicles; vesicles on collapsing give a characteristic funnel-shaped appearance; conidia brown typically obovate, striations not so distinct as in other species, with a papilla at one end, 12--16.6 X 8--16.6 #, mostly 13--16.6 × 9.9-- 13 #t; chtamydospores oval or fusiform, 13--18.6 x 24--30.6 tt solitary, also in chains, usually present in old cultures; heterothallic; zygospores 30--67 # in diam., brown in colour. Isolated from decomposing flowers of Thevetia nerri/olia Jvss, Scrophularia sp., and shrivelled seedlings, and various garden soils. TAXONOMY OF INDIAN CHOANEPHORACEAE 33

Plate V. Figs. 1--13. Choan~phora conjuncta, l. A conidiophore with few secondary vesicles. 2. A conidiophore showing a number of stalked secondary vesicles. 3. A conidiophore showing three stalked secondary vesicles, one of which bearing conidia. 4. A conidiophore with two branches, arising much below the apex. 5. A truncate secondary vesicle showing attachment of conidia. 6, A few conidia, three of which show empty spaces. 7. Two multi-spored sporangia borne on the circinate sporangiophores. 8, A number of colnmellae showing the extent of variation in size and shape. 9. Two few-spored sporangia. I0. Three sporangiospores from a sporangium bearing appendages at either end, II. Hyphae showing chlamydospores. 12. Two zygospores borne between the tips of the entwining branches. I3. Two germinating sporangiospores. Mycopathol. et Mycol. AppL XXII, 1. 3 ~4 B. S, MEttROTRA C~ M, D. MEHROTRA

Culture No MX--7 on which the above description is based, has been deposited in culture collection, Botany Department, University of Allahabad, Allahabad. Choan@hora circinans (NAGANISHI and KAWAKAMI) HESSELTINE and BENJASIIN var. proli/era MEttROTRA and MEIIROTRA var. nov. [PLATES VII & VIII~ Coloniae albae, lente crescentes, marginibus irregularibus, hyphis aereis laxis et intermixtis, paupercule sporas ferentibus; sporangiophori supportantes sporangia vulgo furcati, non septati, colorati fere usque ad sporangium; nonnulli sporangiophori monstrant sporangia peregrina proliferantia, sporangiophori desinere posunt in vesiculam (sporangium sterile) ex qua emergunt hyphae steriles vel fertiles sporangiophori, qui supportant sporangia secundaria quae nonnumquam sterilia manere possunt atque iterum proliferant ad producendos sporangiophoros qui desinunt in sporangia tertiaria. Sporangia primo alba, turn luteola, tandem brunneo-nigra, globosa vei paulum complanata, 22.5--225 ~ diam, parietibus purpureis, superficie granulari; parietes in frustula rumpuntur, collari lato ad basim relicto; columellae parietibus levibus, tenuiter brunneae, ovales vel pyriformes, semper longiores quam latae, earum vero largio- res semper pyriformes, 23.6--114 × 16--75 #; sporangia deminuta insidznt,~a sporangiophoris minoribus, vutgo rarispora, nonnumquam etiam sporangia unispora evoluta; sporangiosporae forms irregulares vulgo ovales, striatae, striis sub potenti microscopio distinguendis, vel bino germinationis poro. Conidia nulla. Chlamydosporae vulgo hyalinae, appendiculatae, 4--16 × 3.3--7.0 #, germinates vulgo uno solitariae, 8--17 × 18--30.6 ,u, Zygosporae haud visae. Typus M-68 tectus ex solo in horto, positus in colIectione cultu- rarum in sectione botanica universitatis allahabadensis atque in NURD Peoria, Illinois in U.S.A. sub numero A-11764. Colony white, growing slowly, with irregular margin, aerial my- celia made up of tax and tangled hyphae, sporulating poorly; sporangiophores bearing conidia absent; sporangiophores bearing sporangia mostly unbranched, non-septate, coloured upto a short length below sporangium; some of the sporangiophores showing peculiar proliferating sporangia, the sporangiophores may end in a vesicle (sterile sporangium) from which proliferate out sterile hyphae or fertile sporangiophores which bear secondary sporangia which at times may remain sterile and further proliferate to give rise to sporangiophores terminating into tertiary sporangia; sporangia at first white then yellowish and finally brownish black, globose or slightly flattened, 22.5--225 # in diam., sporangial wall purplish in colour, with surface smooth; wall breaking into pieces leaving a distinct broad collar at the base; columellae smooth-walled, faintly brown in colour, oval to pyriform, always longer than broad and the larger ones al- always pyriform, 23.6--114× 16--75 # in size; reduced sporangia borne on smaller sporangiophores, generally few-spored, rarely one- TAXONOMY OF INDIAN CHOANEPHORACEAE 35

Plate VI. Figs. 1--3. Choanephora con]uncla. I. An enlarged conidiophore with truncate funnel-shaped vesicles, × 750. 2. A conidiophore showing branching much betow the apex, × 160. 3. Conidiamnchenlarged, × 3600. Fig. 4. Blakeslea triapora. 4. Sporangioliferons head with two few-spored sporangiola and one ~ni- spored sporangiolum (faintly seen), X 2000.

3* 36 B.S. ~E~ROTRA & M. D. M~HROTRA

11 ,oo - // 2

Plate VII. Figs. 1---14. Choanephora circinans var. protifera. 1. A sporangiophore bearing a sporangi~tm at its tip. 2. A broken mllltispored sporangium showing pieces of the sporangial wall and a number of sporangiospores. 3. A sporangiophore terminating into a vesicle (sterile sporangium) from which proliferating out two sporangiophores terminating into sporangia. 4. A sporangiophore terminating into a vesicle (sterile sporangium) from which proliferating out sterile hyphae and sporangiophores terminating into secondary vesicles (sterile secondary ,sporangia). From these secondary vesicles arising a number of sterile hyphae and sporangiophores terminating into sporangia. 5. A number of few-spored sporangia. ~3. A number of columellae showing the extent of variation in size and shape. 7---9. Three swollen sporangiophores showing columellae with inflated collars. 10. A branched sporangiophore each branch showing coIumella with inflated collar. 11. A number of sporangiospores from a sporangium. 19,. Three entarged sporangiospores from a sporangium showing appendages at either end. 13. Hyphae with ehIamydospores. 14. Two germinating sporangiospores. TAXONOMY OF INDIAN CHOANEPHORACEAE 37

Plate VIII. Figs. 1 & 2. Choanephom circina~zs var. protifera. I. Showing sporangiophores ending into sterile vesicles from which are proliferating fertile sporangiophores, X 60. 2. A portion of (1) magnified, X 130. 3~ B. s, M~HROTRA ~C M, D. MEIIROTRA spored sporangia also developed; sporangiospores irregular in shape, mostly oval, striate, striations visible at high magnifications, hyaline, appendaged, 4--16 × 3.3 × 7.0/4 germinating mostly by one or two germ tubes; chlamydospores usually solitary, 8 × 17 × 18--30.6 #; zygospores not seen. Isolated from various soils collected from Amarkantak (M.P.), Suhagi (M.P.), Mirzapur (U.P.), Calcutta. Culture No. 68 on which the above description is based has been deposited in culture collection, Botany Department, University of Allahabad and at NURD, Peoria, Illinois, U.S.A. under No. A-11764. The above isolate resembles Choanephora circinans in all essential characters but differs in the presence of proliferating vesicular apices of the sporangiophores, Such characters are frequently seen in this isolate. They have never been reported in C,~oanephora circinans nor have they been found by the authors in the isolate NRRL 2546 sent by Dr. C.W. HESSELTI~E.

Summary A taxonomic study of the members of the family Choanephoraceae was undertaken. Almost all the species of the family have been isolated from various sources in India. Two genera, viz., Blakeslea and Choanephora have been recognized and a key to the genera has been given. The genus Blakeslea includes only one species B. trisflora and the genus Choan@hora five species. A key to the species has also been given. A new variety of Choanephora circinans, viz., C. circinans var. pro/i/era MEHROTRA and MEHROTRA based on the proliferating vesicular apices of the sporangiophores has been described.

Acknowledgements The authors are grateful to Dr. C. W. HESSELTINE for reviewing the paper and for many helpful suggestions. Thanks are also due to Dr. H. SANTAPAU for the Latin translation of the new variety and Dr. R. N. TANDON for the laboratory facilities.

Literature cited CIJRREY, F. 1873. On a new genus in the order Mueedines, J. Linn. Soc. Bot. 13: 333: 334, 578. FITZPATRICK, H. ~{. 1930. The Lower Fungi. Phycomycetes. HESSELTINE, C. \V. 1953, A revision of the Choanephoraceae. Amer. Midland Nat. 50: 248--256. HRSSnLTINE, C. W. I960. Gilbertella gen. nov. (IVlucorales) Bull. Torrey Bot. Club. 87: 21--30. HnSS~LTIN:~, C. W. 1962. Personal communication. HESS~LTINE, C. ~V. & C. ]~. BENJAMIN. 1957. Notes on the Choanephoraceae. Nfyco- logia. XLIX: 723--733. MEHROTRA, B. S. • M. D, MEttROTRA. 1961. A new species of Choanephora from India. Mycologia LII: 464--470. MEHROTRA, t3. S. & ?d. D. ME~InOTRA. 1962. A morphological and physiological study TAXONOMY OF INDIAN CHO&N~PHORACEAE ~9

of Gilbertella in India. Accepted for publication in Mycologia. N&GANIS~II, H. & N. I~AWAKAMI. 1955. On Blakeslea Thaxter in Japan. (II) Bl. cir¢i- hans sp. nov. Bull. Fac. Eng. Hiroshima Univ. 4: 183--187. NAuNov, •. A. 1939. CI~s des Mucorin6es. Encyclopgdie 2¢iycoI. 9: 1-137. POITRaS, A. ~. 1955, Observations on asexual reproductive structures of the Choa- nephoraceae. Mycologia 47: 702---713. SACC~a~DO, P. A. 1891. Sylloge Fungorum. 9: 339. SIN~A, A. 1940. A wet rot of leaves of Colocasia antiquor~tm due to secondary infec- tion by Choa~ephora cucurbitam~m Thaxter and Choa~eph.ora trispora Thaxter sp. (Blakeslea lrispora Thaxter), Proc. Indian Acad. Sci. ]3. 11 : 167--176. T~AXTXR, R. 1914. New or Peculiar Zygomycetes. Blc~kestea, D~ssophorc*, Hc~plo- spo~angium, ~ova genera. Bot. Oaz. 58: 353---366. '~¢VAKSMAN, S. A. 1931. Principles of Soil Microbiology. Bailleire Tindall & Co. London. 本文献由“学霸图书馆-文献云下载”收集自网络，仅供学习交流使用。

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