Additions and corrections to names published in Cercospora in Iran

INTRODUCTION

Cercospora Fresen. is one of the largest genera among cercosporoid fungi and its species are associated with leaf spots and considered as important pathogens on various host plants. (Crous & Braun 2003). Chupp (1954), who adopted a broad generic concept listed over 1800 species. By careful morphological examination of Cercospora and similar taxa, Deighton (1973, 1976) segregated and introduced new genera. Crous & Braun (2003) published an annotated list of Cercospora and Passalora names with more than 5700 taxa. Recently, Ershad (2009) corrected 59 names in Cercospora previously published from Iran, but he did not follow to synonymize morphologically indistinguishable taxa in Cercospora apii s. lat. Study on Cercospora and allied genera is more considered in recent years in Iran. Pirnia et al. (2012 a, b, c, d) identified new species of cercosporoids from the north of Iran. Hesami et al. (2011, 2012) introduced new Cercospora and Cercospora-like species from Guilan province. Recently, Bicharanlou et al (2013 a, b, c) and Behrooz et al. (2015) reported new cercosporoid species from Mazandaran and Kohgiluyeh and Boyer-Ahmad provinces, respectively.

MATERIALS AND METHODS

Specimens from the north of Iran (Guilan, Mazandaran, Golestan and Ardabil provinces) and all specimens belonging to Cercospora deposited in fungal reference collection of Ministry of Jihad-e-Agriculture “IRAN” in Iranian Research Institute of Plant Protection were morphologically re-examined. Microscopic slides were prepared from stromata, conidiophores and conidia in 25% lactic acid. Characters such as pigmentation, shape and dimension of conidia and conidiophores and thickness and darkness of conidial scars and hila were studied. Drawings were made using a drawing-tube attached to an Olympus BH2 microscope.

RESULTS AND DISCUSSION

According to Crous & Braun (2003), some taxa in the genus Cercospora on various host plants are morphologically indistinguishable. Therefore, they proposed Cercospora apii s. lat. for those taxa and linked 83 host genera to the latter species. Pirnia et al. (2010) and Bicharanlou et al. (2013a) followed Crous & Braun (2003) and linked 19 hosts with C. apii s. lat. based on Braun's idea this proposal is a temporary solution for Cercospora apii species complex and new molecular evidences are needed to confirm it, therefore previous valid names are acceptable as separate species. In this research, the taxa which previously placed in Cercospora apii s. lat. were re-examined and segregated on various hosts based on morphological characters. Cercospora species on Abelia grandiflora L. (C. deutziae Ellis & Everh.), Erythrina crista-galli L. (C. erythrinicola Tharp), Euphorbia heterophylla L. (C. pulcherrimae Tharp) and Zanthedeschia aethiopica (L.) Spreng. (C. richardiicola G.F. Atk.) are new records for mycobiota of Iran. Cercospora althaeina Sacc. (on Gossypium hirsutum Cav.), C. avicennae Chupp (on Abutioln theophrasti Medic.), C. beticola Sacc. (on Beta vulgaris L.), C. bizzozeriana Sacc. & Berl. (on Cardaria draba (L.) Desv.), C. brunkii Ellis & Galloway (on Pelargonium zonale (L.) L Her. ex Ait), C. canescens Ellis & G. Martin (on Vigna sinensis (L.) Endl.), C. caricis Oudem. (on Carex orbicularis Boott.), C. gerberae Chupp & Viegas (on Gerbera jamesonii Hook), C. hydrangeae Ellis & Everh. (on Hydrangea macrophylla (Thunb.) Ser.), C. lactucae-sativae Sawada (on Lactuca serriola L.), C. peckiana Chupp (on Rumex crispus L., R. sanguineus L.), C. physalidis Ellis (on Lycopersicon esculentum Mill.), C. sonchi Chupp (on Sonchus arvensis L.), C. zebrina Pass. (on Medicago sp.) and C. zonata G. Winter (on Vicia faba L.) were identified on the specimens collected from the northern provinces of Iran. Other morphologically similar Cercospora species listed by Ershad (2009) on Gerbera jamesonii (C. gerberae), Glycine max L. (C. kikuchii T. Matsumoto & Tomoy.), Hibiscus esculentus L. (C. malayensis Stev. & Solh.), Hydrangea hortensia L. (C. hydrangeae), Impatiens balsamina L. (C. fukushiana (Mat.) Yam.), Medicago sp. (C. medicaginis Ellis & Everh.), Petunia hybrida Wilm.(C. physalidis Ellis) and Vigna sinensis (C. canescens) proved to be the correct names according to morphological descriptions provided in Chupp (1954). Cercospora iridis which was previously reported from Iran (Pirnia et al. 2010), probably belongs to the genus Passalora, but the amount of the specimen was not sufficient for the exact identification. All specimens are deposited in “IRAN”.

Key to Cercospora species reported from Iran

1. Species occurs on Compositae…………………..10

2. Species occurs on Leguminosae………………...15

3. Species occurs on Cruciferae…………………...21

4. Species occurs on Malvaceae…………………...23

5. Species occurs on Euphorbiaceae………………25

6. Species occurs on Polygonaceae………………..27

7. Species occurs on Solanaceae…………………..29

8. Species occurs on Amaranthaceae……………...30

9. Species occurs on other plant families………….31

10a. Length of conidiophores up to 150 µm, length of conidia up to 200 µm…………………………..11

b. Length of conidiophores up to 125 µm, length of conidia up to 150 µm…………………………..12

11a. On Xanthium………………………C. xanthiicola

b. On Sonchus and Taraxacum……………….C. sonchi

12a. Conidiophores branched, on Zinnia……C. zinnia

b. Conidiophores unbranched, on other hosts……...13

13a. Conidiophores tortuous to multi-geniculate, on Helianthus………………………….C. helianthiicola

b. Conidiophores sinuous or 1-3 geniculate, on Gerbera………………………………………...14

14a. Tip of conidia subacute, on Lactuca...................................C. lactucae-sativae

b. Tip of conidia acute, on Gerbera………C. gerberae

15a. Maximum length of conidia less than 150 µm..16

b. Maximum length of conidia more than 150 µm...18

16a. Conidia acicular, on Medicago and Trifolium…………………………………..C. zebrina

b. Conidia cylindric to cylindro-obclavate………...17

17a. Conidial scars terminal, on Trigonella……………………………..C. traversiana

b. Conidial scars terminal and lateral, on Vicia…………………………………………C. zonata

18a. Length of conidiophores up to 175 µm……….19

b. Length of conidiophores up to 250 µm……….…20

19a. Conidiophores uniform in color and width, on Medicago……………………………..C. medicaginis

b. Conidiophores paler and narrower towards the tip, on Vigna………………………………...C. canescens

20a. Length of conidia up to 200 µm, on Erythrina…………………………….C. erythrinicola

b. Length of conidia up to 300 µm or more, on Glycin……………………………………...C. kikuchii

21a. Conidia acicular, on Raphanus……………………………C. cruciferarum

b. Conidia cylindrical to cylindro-obclavate……….22

22a. Tip of conidia bluntly rounded, on Cardaria……………………………..C. bizzozeriana

b. Tip of conidia subobtuse, on Cheiranthus……………………………C. cheiranthi

23a. Conidiophores up to 100 µm, conidia mostly cylindric, on Althaea and Gossypium……………………………….C. althaeina

b. Conidiophores up to 250 µm, conidia acicular….24

24a. Length of conidia up to 150 µm, on Hibiscus………………………………..C. malayensis

b. Length of conidia up to 200 µm, on Abutilon…………………………………C. avicennae

25a. Conidiophores 0-septate, branched in the upper part, on Mercurialis………………….C. mercurialis

b. Conidiophores septate, not branched……………26

26a. Length of conidiophores up to 150 µm or longer, on Euphorbia………………………C. pulcherrimae

b. Length of conidiophores up to 100 µm, on Ricinus…………………………………….C. ricinella

27a. Length of conidiophores and conidia up to 250 µm or longer, on Rumex……………………...C. apii

b. Length of conidiophores mostly up to 100 µm, conidia shorter………………………………….28

28a. Stromata present, 50–75 µm in diam., fascicles dense to very dense……………………..C. peckiana

b. Stromata lacking or composed of few cells, fascicles not dense………………………..C. rumicis

29a. Length of conidiophores and conidia up to 100 and 150 µm respectively, on Daturea…………………………………C. daturicola

b. Length of conidiophores and conidia up to 250 µm, on Lycopersicon and Petunia………..C. physalidis

30a. Fascicles compact, length of conidiophores and conidia up to 100 µm, on Amaranthus...C. acnidae

b. Fascicles divergent, length of conidiophores and conidia up to 200 µm, on Amaranthus……………………………..C. brachiata

31a. Maximum Length of conidiophores mostly up to 100 µm, sometimes up to 150 µm……………...32

b. Maximum length of conidiophores more than 150 µm……………………………………………...41

32a. Conidia cylindro-obclavate…………….…......33

b. Conidia acicular…………………………………34

33a. Fascicles compact in basal part, conidiophores unicellular; on Datisca………………C. datiscicola

b. Fascicles divergent, conidiophores rarely septate, on Carex…………………………………….C. caricis

34a. Length of conidia up to 200, on Beta and Spinacia…………………………………...C. beticola

b. Length of conidia mostly up to 150 µm or shorter…………………………………………35

35a. Stromata distinct……….……………………..36

b. Stromata lacking or small, composed of few cells……………………….……………………37

36a. Conidiophores uniform in width and color; on Hosta………………………………………...C. hostae

b. Conidiophores slightly paler and narrow towards the tip, on Sorghum ……………………….C. sorghi

37a. Conidiophores uniform in color and width, on Hydrangea……………………………C. hydrangeae

b. Conidiophores paler and fairly narrower towards the tip…………………………………………...38

38a. Conidial scars numerous, terminal and lateral..39

b. Conidial scars infrequent, mostly terminal……...40

39a. Conidiophores sub-hyaline to very pale olivaceous brown, on Plantago…….C. pantoleuca

b. Conidiophores brown in basal part, paler towards the tip, on Viola…………………………….C. violae

40a. Stromata black to dark brown, conidiophores not branched, on Fraxinus…………………..C. texensis

b. Stromata, brown, conidiophores rarely branched, on Elaeagnus………………………....C. elaeagni

41a. Conidiophores not geniculate or rarely geniculate, on Pelargonium……………..C. brunkii

b. Conidiophores geniculate to sinuous……………42

42a. Maximum length of conidia up to 150 µm…...43

b. Maximum length of conidia more than 150 µm...45

43a. Conidia obclavate, tip of conidia bluntly rounded, on Heliotropium………………..C. taurica

b. Conidia acicular…………………………………44

44a. Tip of conidia acute, on Phytolacca…………………………......C. flagellaris

b. Tip of conidia subobtuse, on Abelia….C. deutziae

45a. Length of conidia up to 200 µm, on Cucurbita………………………………..C. citrullina

b. Length of conidia up to 300 µm, on Zanthedeschia………………………C. richardiicola

Cercospora deutziae Ellis & Everh. J. Mycol. 4: 5 (1888)

Leaf spots circular, center greyish-white, 1.5–4.5 mm in diameter; stromata lacking or composed of a few brown cells, 20–30 µm wide; caespituli epiphyllous; conidiophores in small fascicles, medium dark brown, uniform in color, not branched, septate, 30–200 × 3–5 µm; conidialscars conspicuous, thickened and darkened, terminal and lateral; conidia hyaline, acicular to cylindrical, multiseptate, base truncate, tip subobtuse, 30–125 × 2.5–5 µm; hilum thickened and darkened (Fig. 1).

Specimen examined: Iran, Mazandaran Province, Nowshahr, on Abelia grandiflora, 29 Oct. 2012, B. Bicharanlou (IRAN 16192 F).

Note: This specimen was previously reported as C. apii by Bicharanlou et al. (2013b). Morphology of the specimen examined agrees with description of C. deutziae provided by Chupp (1954). The species is distinguished from C. apii s. lat. by having moderately shorter conidiophores and conidia.

Fig. 1. Cercospora deutziae on Abelia grandiflora. (A) Conidiophores, (B) Conidia, (C) Symptoms on leaf, scale bar = 50 µm.

Cercospora erythrinicola Tharp, Mycologia 9: 109 (1917)

Leaf spots circular to subcircular, greyish white, 1–3 mm in diameter; stromata lacking or composed of a few brown cells, 30–50 µm wide; caespituli amphigenous, mostly epiphyllous; conidiophores pale brown, paler and narrower towards the tip, not branched, septate, 20–125 × 3–5 µm; conidial scars conspicuous, thickened and darkened, terminal and lateral; conidia hyaline, acicular, straight to curved, multiseptate, base truncate, tip acute to subacute, 40–175 × 3–4 µm; hilum thickened and darkened (Fig. 2).

Specimens examined: Iran, Mazandaran Province, Nowshahr, on Erythrina crista-galli, 9 Oct. 2012, B. Bicharanlou (IRAN 16197 F).

Note: Specimen on above mentioned host was previously reported as C. apii by Bicharanlou et al. (2013b). In this species, fascicles were moderately dense and some conidiophores were sparingly sinuous to 1-3 geniculate and conidia were moderately shorter than 150 µm. These characters distinguish the species from C. apii s. lat. and fit well with description of C. erythrinicola in Chupp (1954).

Cercospora pulcherrimae Tharp, Mycologia 9: 114 (1917)

Leaf spots circular to subcircular, 1–3 mm in diameter; stromata composed of a few brown cells, 30–40 µm wide; caespituli amphigenous, mostly epiphyllous; conidiophores olivaceous brown, paler and narrower towards the tip, not branched, septate, 20–150 × 4–6 µm; conidialscars conspicuous, thickened and darkened, terminal and lateral; conidia hyaline, acicular, straight to curved, multiseptate, base truncate, tip subacute, 40–125 × 2.5–4 µm; hilum thickened and darkened (Fig. 3).

Specimens examined: Iran, Golestan Province, Gorgan, on Euphorbia heterophylla, 10 Nov. 2010, M. Pirnia & R. Zare (IRAN 15018 F).

Note: This specimen was previously reported as C. apii by Pirnia et al. (2010). Moderately short conidiophores and conidia separate the species from C. apii s. lat., and hyaline acicular conidia separate C. pulcherrimae from the others on Euphorbia (Chupp 1954).

Fig. 2. Cercospora erythrinicola on Erythrina crista-galli. (A) Conidiophores, (B) Conidia, (C) Symptoms on leaf, scale bar = 50 µm.

Fig. 3. Cercospora pulcherrimae on Euphorbia heterophylla. (A) Conidiophores, (B) Conidia, scale bar = 50 µm. 

Cercospora richardiicola G.F.Atk. (richardiaecola), J. Elisha Mitchell Sci. Soc. 8: 51. (1892)

Leaf spots circular to subcircular, center greyish white, with narrow dark brown margin, 1–12 mm. in diameter; stromata present, small to moderately developed, 25–40 µm wide, brown; caespituli amphigenous, mostly hypophyllous, punctiform, conidiophores in small fascicles, arising from stromata, pale to olivaceous brown, paler towards the tip, erect, geniculate to sinuous in the upper part, not branched, 77–130 × 4–7 µm, septate; conidiogenous cellsintegrated, terminal; conidial scars conspicuous, thickened and darkened, terminal and lateral; conidia hyaline, acicular, straight to curve, multiseptate, 8–12 transverse septa, 95–160 × (2.5-)3–4 µm, base truncate, tip acute; hilum thickened and darkened (Fig. 4).

Specimen examined: Iran, Guilan Province, Some'e-Sara, on Zanthedeschia aethiopica, 15 July. 2007, A. Khodaparast (IRAN 14807 F).

Note: This specimen was previously reported as C. apii by Pirnia et al. (2010). Morphology of the specimen agrees with the description of C. richardiaecola given by Chupp (1954). The species was originally published as C. richardiaecola, which is corrected to C. richardiicola in this study, according to Crous & Braun (2003). The species is somehow morphologically close to C. callae, but the latter species can be distinguished by its obclavate, shorter and wider conidia.

Cercospora bizzozeriana Sacc. & Berl., Malpighia 2: 248. (1888)

Specimens examined: Iran, Yazd Province, Taft, on Cardaria draba, 8 May 2010. Khorramnejad (IRAN 15488 F); Northern-Khorasan Province, Shirvan, 3 July 2011. B. Bicharanlou (IRAN 15489 F).

Note: The species is characterized by having obclavate to cylindrical conidia and moderately short conidiophores, which was listed by Pirnia et al. (2012a) for the first time from Iran.

Cercospora caricis Oudem., Nederl. Kruidk. Arch. II, 6: 59. (1892)

Specimen examined: Iran, Ardabil Province, Neur Lake, on Carex orbicularis, 22 May 2011. Javadi-Estahbanati (IRAN 15490 F).

Note: Chupp (1954) introduced Cercospora caricis on various species of the genus Carex. The species is characterized by having short conidiophores and acicular to cylindro-obclavate conidia, and was listed by Pirnia et al. (2012a) for the first time from Iran.

Fig. 4. Cercospora richardiicola on Zanthedeschia aethiopica. (A) Conidiophores, (B) Conidia, (C) Symptoms on leaf, scale bar = 50 µm.