Acta Sci. Pol., Hortorum Cultus 10(2) 2011, 213-224 CHARACTERISTICS AND OCCURRENCE OF Phoma spp. ON HERBS FROM THE FAMILY Lamiaceae Beata Zimowska University of Life Sciences in Lublin Abstract. Fungi belonging to Phoma spp. commonly occur on herbaceous plants, including herbal ones. In the years 2004–2006 isolates belonging to genus Phoma which were differentiated in morphological respects were obtained from herbs belonging to family Lamiaceae. Basing on constant morphological feature observed in vitro in the cultures developing on standard media, isolates of Phoma spp. were included within the proper section, and next the species were identified. P. exiqua var. exiqua was isolated from all parts of the examined plants. P. nepeticola cultures were obtained from the leaves and stems of motherwort, whereas isolates of P. nemophilae were from the roots. Apart from the above mentioned species, P. capitulum, P. labilis, P. pereupyrena, P. subglomerata and P. septicidalis were also isolated. Key words: fungi, herbaceous plants, Phoma spp., motherwort, sage, savory INTRODUCTION Fungi of the genus Phoma are at present one of the more widespread ones in respect of their geography and they consist of a large number of species which one can find in varied ecological niches. From among 3000 taxa described so far, 110 are pathogenic species often infecting those plant parts that are important from the economic point of view [Aveskamp et al. 2008]. Some of them are included within a quarantine, because they cause serious problems for organizations creating legal settlements concerning plant quarantine [Miric et al. 1999, Mendes et al. 2006]. Herbs belong to plants that are frequently colonized by fungal species from the genus Phoma. Phoma dictamnicola, P. glaucii and P. multirostrata var. microspora were isolated from the leaves and stems of thyme [Machowicz-Stefaniak et al. 2002]. Cultures of P. exiqua var. exiqua, P. capitulum and P. glomerata were obtained from the roots, stems and leaves of thyme, lemon balm and St. John's wort [MachowiczStefaniak et al. 2002, Zimowska and Machowicz-Stefaniak 2004, Machowicz-Stefaniak Corresponding author – Adres do korespondencji: Beata Zimowska, Department of Plant Pathology and Mycology, University of Life Sciences in Lublin, Leszczyskiego 7, 20-069 Lublin, e-mail:beata.zimowska@up.lublin.pl 214 B. Zimowska et al. 2004]. P. strasseri was isolated from the stems and rhizomes of peppermint with the symptoms of the black stem rot [Zimowska and Machowicz-Stefaniak 2005, Zimowska 2007a]. The author’s own studies conducted in the years 2004–2009 on diseases of so far not studied species of herbs from the family Lamiaceae extended the collection of cultures of the Department of Plant Pathology and Mycology, University of Life Sciences in Lublin with the new isolates of Phoma spp. The present work relates to the occurrence and characteristics of Phoma spp., with special regard to the species described in the literature as pathogenic. MATERIAL AND METHODS The studies conducted in 2004–2006 concerned three plantations of motherwort (Leonurus cardiaca L.) and sage (Salvia officinalis L.) in the second year of cultivation, and in 2007–2009 three 1-year-old plantations of savory (Satureja hortensis L.). The plantations were situated in the communes of Fejsawice, Dziecinin and Suchodoy in the Lublin province. The procedure of taking plants for investigations and isolating the fungi was already described in detail by Zimowska [2008a]. The obtained isolates of Phoma spp. were identified after making single-spore cultures on standard media. The keys considering the current principles of the taxonomy of fungi from genus Phoma were used for identification [Boerema et al. 2004, De Gruyter and Noordeloos 1992]. Isolates: L 121 obtained from the roots of motherwort, S 458 from the stems of sage and Sh 6002 isolated from the roots of savory were chosen from the population of P. exiqua var. exiqua for further studies. Isolates L 284, L 291 and L 302 obtained from the leaves of motherwort represents the population of P. nepeticola and three isolates of P. nemophilae L 171, L 205 and L 248 from the roots of motherwort. The randomly chosen isolates were grown on the standard media MA (malt agar), OA (oatmeal agar) and CA (cheery agar) [De Gruyter and Noordeloos 1992]. The cultures were incubated during the first week in a thermostat without access of light at the temperature of 22C, and for the next 13 hours in UV light and 11 hours in darkness. After this time measurements of the diameter of the colonies were done and also colour of the avers and the reverse, character of growth of the edge of the colony and character of growth of hyphae of the air mycelium were evaluated. After 14 days of keeping the cultures in the thermostat, the same features were described as after 7 days. Aditionaly on OA medium colour of the cultures after their reaction with 2–3 drops of 1N NaOH was studied. Moreover, the arrangement of the pycnidia was defined on OA medium. Shape of the pycnidia, character of the ostioles, colour of the conidial exudates and structure of the pycnidial wall surface were studied. After 2 weeks of the growth of the cultures on OA medium, the measurements of 300 conidia (3 isolates × 100 conidia) and 150 pycnidia (3 isolates × 50 pycnidia) were done for every species. Attention was also paid to presence of chlamydospores. _____________________________________________________________________________________________________________________________________________ Acta Sci. Pol. Characteristics and occurrence of Phoma spp. on herbs from the family Lamiaceae 215 RESULTS The present investigations showed that all organs of the analysed plant species were infected by P. exiqua var. exiqua, section Phyllostictoides (tab. 1). The cultures of this species were most frequently obtained from the roots showing the symptoms of necrosis and the set-back of the growth and from the bottom parts of stems with the symptoms of necrosis. Etiological signs in the form of pycnidia and conidia with the features typical for the above species were found on the infected organs. The isolated species from plants of motherwort, sage and savory was P. glomerata belonging to the section Peyronellea (tab. 1). The cultures of P. nepeticola from the section Phyllostictoides were received from the leaves and the stems of motherwort showing the symptoms in the form of regular, necrotic spots. Besides the characteristic symptoms, pycnidia were found on these organs, and in them conidia with the typical features of the Phoma genus. The isolates of P. nemophilae, species also belonging to the section Phyllostictoides, were obtained only from the roots of motherwort (tab. 1). Moreover, the isolates of P. labilis from the section Phoma were isolated from the roots and stems of motherwort and sage. Cultures of P. septicidalis from the section Paraphoma, were obtained only from the stems and roots of motherwort , while P. subglomerata, species belonging to the section Peyronellea, was also isolated from sage plants (tab. 1). Table 1. Occurrence of Phoma spp. on herbs from Lamiaceae family in 2004–2009 Tabela 1. Wystpowanie Phoma spp. na zioach z rodziny Lamiaceae w latach 2004–2009 Plant species – Gatunki rolin Phoma spp. Section Sekcja Leonurus cardiaca L. Salvia officinalis L. a b c Phoma capitulum Phoma labilis Phoma Phoma exigua var. exigua + + Phyllostictioides Peyronellaea Phoma subglomerata Phoma septicidalis c + Paraphoma + + ++ ++ Satureja hortensis a b c + + + + + + + + + + + + + + Phoma nepeticola Phoma glomerata b + Phoma pereupyrena Phoma nemophilae a + + + + + + + + + + + + + – frequency up to 5% – czstotliwo do 5% ++ – frequency from 5 to 10% – czstotliwo od 5 do 10% The investigations concern the growth of chosen isolates of P. exiqua var. exiqua on standard media showed that cultures of the fungus on MA medium after 7 days were characterized by brown-olive, flocky aerial hyphae of the air mycelium with a white edge (photo 1). The reverse of the colony was olive-grey. The character of the growth of _____________________________________________________________________________________________________________________________________________ Hortorum Cultus 10(2) 2011 Table 2. Characteristics of pycnidia and conidia of Phoma exigua var. exigua, Phoma nepeticola and Phoma nemophilae (mean for 3 isolates) Tabela 2. Charakterystyka piknidiów i konidiów Phoma exigua var. exigua, Phoma nepeticola oraz Phoma nemophilae (rednia dla 3 izolatów ) Author Autor a Globose with usually one ostiole, Own data 74.2 × 195 Badania Okrge, wasne najczciej z 1 ujciem, 74,2 × 195 P. exigua var. exigua Pycnidia Piknidia b On the agar, but partly submerged in the agar, glabrous but often with soft hyphal, outgrowts Na powierzchni podo a lub czciowo zagbione w podo e, gadkie lub czsto z delikatnymi utworami strzpkowymi Conidia Konidia c Subglobose, ellipsoidal to oblong. Conidia aseptate 3.7–7.2 × 2.2–3.5, septate 6.9–9.5 × 2.1–3.2, Prawie okrge, elipsoidalne do podu nych. Konidia bez przegród 3,7–7,2 × 2,2–3,5. Konidia z przegrod 6,9–9,5 × 2,1–3,2 Variable in shape and dimension. Globose to Conidia aseptate subglobose with 4–7(–12) × 2.5–3.5, usually 1–2 Solitary or septate Boerema ostioles, 75–200 confluent glabrous 7–10(–13) × 2.5–3.5 et. al 2004 Okrge do Pojedyncze lub Zró nicowane Boerema prawie okrgzebrane w grupy, w ksztacie i i in. 2004 ych najczciej gadkie rozmiarze. Konidia z 1 do 2 uj, bez przegród 75–200 4–7(–12) × 2,5–3,5, z przegrod 7–10(–13) × 2,5–3,5 a P. nepeticola Pycnidia Piknidia b Conidia Konidia c a P. nemophilae Pycnidia Piknidia b Conidia Konidia c Conidia hyaline, oval to On the agar or ellipsoidal. submerged, Conidia aseptate glabrous or 6.2 × 2.9, septate sparsely covered 12.1 × 3.2, by mycelial hairs Konidia Na powierzchni bezbarwne, podo a lub owalne do zagbione, elipsoidalnych. gadkie lub Konidia bez pokryte przegród delikatnymi 6,2 × 2,9. strzpkami Konidia z przegrod 12,1 × 3,2 Globose to irregular with 1–3 sometimes elongated ostioles 63 × 257 Okrge do nieregularnych, ujcia od 1 do 3, czasami wydu one Submerged in the agar, glabrous or covered by mycelial outgrowts Zagbione w podo u, gadkie lub pokryte strzpkami Subglobose to ellipsoidal, conidia aseptate Glabrous or Globose with 5–7 × 2.5 septate usually 1 ostiole sparsly covered 9.5–14.5 × 2.5–5. by mycelial hairs 70 × 240 Prawie okrge Gadkie lub Okrge, do elipsoidalpokryte najczciej nych, konidia bez delikatnymi z 1 ujciem przegród strzpkami 70 × 240 5–7 × 2,5, z przegrod 9,5–14,5 × 2,5–5. Globose to irregular with 1–5 usually ostides later developing to an elongated neck, 60 × 260 Okrge do nieregularnych z 1–5 ujciami z czasem w ksztacie wycignitej szyjki, 60 × 260 Cylindrical allantoid, aseptate Glabrous or with 4–9.5 × 1.5–2.5, septate conidia some mycelial outgrowths 12 × 3.5. Gadkie lub z Cylindryczne allantoidalne, nielicznymi bez przegród wyrostkami strzpkowymi 4–9,5 × 1,5–2,5 z przegrod 12 × 3,5 Globose with 1 ostiole 75 × 230 Okrge z 1 ujciem a – shape and dimension in m – ksztat i wymiary w m, b – arrangement and structure of wall surface – rozmieszczenie i struktura powierzchni ciany, c – shape and dimension in m – ksztat i wymiary w m. Ellipsoidal to cylindrical mainly aseptate 6.3 × 1.5 septate 11.8 × 3 Elipsoidalne do cylindrycznych, gównie bez przegród 6,3 × 1,5, konidia z przegrod 11,8 × 3,2 Characteristics and occurrence of Phoma spp. on herbs from the family Lamiaceae 217 the colony and the colour of the averse and the reverse were similar on OA and CA media. The edge of the colony on all media was irregular, lightly sliced (photo 1). After 14 days the colour of the hyphae was more intensive. The diameter of the colony after 7 days ranged from 27 to 39 mm, and after 14 days from 60 to 78 mm on OA and CA media and from 40 to 45 on MA medium. The pycnidia formed on OA medium in great Phot. 1. 14-day old colonies of P. exiqua var. exiqua (L 121) on malt agar. Photo E. Zalewska Fot. 1. 14-dniowe kolonie P. exiqua var. exiqua (L 121) na po ywce maltozowej. Fot. E. Zalewska Phot. 2. Pycnidia of P. exiqua var. exiqua (L 121) – × 125 (a) – photo E. Zalewska; SEM – × 790 (b); Pycnidium and fragments of mycelium hyphae – photo M. Wróbel Fot. 2. Piknidia P. exiqua var. exiqua (L 121) – × 125 (a) – fot. E. Zalewska; SEM – × 790 (b); Piknidium i fragmenty strzpek grzybni – fot. M. Wróbel _____________________________________________________________________________________________________________________________________________ Hortorum Cultus 10(2) 2011 218 B. Zimowska Phot. 3. Conidia of P. exiqua var. exiqua (L 121) – × 500 (a) – photo E. Zalewska; SEM × 6500 (b) – photo M. Wróbel Fot. 3. Konidia P. exiqua var. exiqua (L 121) – × 500 (a) – fot. E. Zalewska; SEM × 6500 (b) – fot. M. Wróbel Phot. 4. 14-day old colonies of P. nepeticola (L 284) on malt agar. Photo E. Zalewska Fot. 4. 14-dniowe kolonie P. nepeticola (L 284) na po ywce maltozowej. Fot. E. Zalewska number were scattered over the whole surface of the colony in an irregular way, and they were partly sunken in agar. The pycnidia had a round shape and one ostiole from which creamy white drops of the conidial exudate flowed out (tab. 2). The walls of the pycnidia were generally smooth, with delicate hyphal outgrowths sometimes visible (photo 2). The size of the pycnidia ranged from 74.2 to 195.5 m (tab. 2). The conidia _____________________________________________________________________________________________________________________________________________ Acta Sci. Pol. Characteristics and occurrence of Phoma spp. on herbs from the family Lamiaceae 219 of the studied isolates of P. exiqua var. exiqua were differentiated in shape and size, most frequently being oval, elliptic or round, with single drops of fat on the poles, without secondary septum or rarely with one septum (photo 3). The dimensions of 1-cell spores – 3.5–7.2 × 2.2–3.5 m, and 2-cell 6.9–9.5 × 2.1–3.2 m (tab. 2). The test with 1 N NaOH showed the positive reaction. The change of the tinge of agar was observed in all studied isolates around the colony from green to red. Chlamydospores were not observed. Phot. 5. Pycnidia of P. nepeticola (L 284) – × 125 (a) – photo E. Zalewska; SEM × 2400 (b); Ostiole of pycnidium and fragments of mycelium hyphae – photo M. Wróbel Fot. 5. Piknidia P. nepeticola (L 284) – × 125 (a) – fot. E. Zalewska; SEM × 2400 (b); Ujcie piknidium i fragmenty strzpek – fot. M. Wróbel Phot. 6. Conidia of P. nepeticola (L 284) – × 500 (a) – photo E. Zalewska; SEM × 9900 (b); Conidia and fragments of mycelium hyphae – photo M. Wróbel Fot. 6. Konidia P. nepeticola (L 284) – × 500 (a) – fot. E. Zalewska; SEM × 9900 (b); Konidia i fragmenty strzpek grzybni – fot. M. Wróbel Isolates of P. nepeticola on MA medium after 7 days of the growth were characterized by quite compact hyphae of the air mycelium of the grey-olive colour. After 14 days on the same medium, the hyphae of the air mycelium produced a flocculent struc_____________________________________________________________________________________________________________________________________________ Hortorum Cultus 10(2) 2011 220 B. Zimowska Phot. 7. 14-day old colonies of P. nemophilae (L 205) on malt agar. Photo E. Zalewska Fot. 7. 14-dniowe kolonie P. nemophilae (L 205) na po ywce maltozowej. Fot. E. Zalewska ture in the central part of the colony and they were of the white-cream colour (photo 4). The reverse was olive-green. Similar features were shown by the colonies growing on OA and CA media. The edge of the colony was slightly irregular. The isolates growing on OA medium reached the largest diameter and after 7 the days of growth it ranged from 40 to 43 mm. The diameter of the colonies was a little smaller on OA and CA media and it ranged from 35 to 38 mm. After 14 days on OA medium the diameter of the colony ranged from 74 to 76 mm while on CA from 45 to 49 mm. Numerous pycnidia formed on OA medium were round, smooth or covered with delicate hyphal outgrowths (photo 5). They were formed singly or in small aggregates. Drops of the conidial exudate of cream-salmon pink to pink colour went out from the ostioles. The size of the pycnidia ranged from 75 to 230 m (tab. 2). The conidia were hyaline, oval to ellipsoidal, usually with several small drops of fat (photo 6). One-cell conidia with the mean dimensions of 6.2 × 2.9 m predominated, two-cell ones occurred rarely and their size was on an average 12.1 × 3.2 m (tab. 2). The reaction of the cultures of P. nepeticola with 1 N NaOH was negative; moreover, none of the isolates of the fungus formed chlamydospores. The isolates of P. nemophilae formed after 7 days of growth on standard media a dark olive air mycelium with a similar reverse. After 14 days the colour of the air mycelium became brown-olive tinge, and the hyphae of the air mycelium produced a flocculent structure. In the central part of the colony delicate, white hyphae of the air _____________________________________________________________________________________________________________________________________________ Acta Sci. Pol. Characteristics and occurrence of Phoma spp. on herbs from the family Lamiaceae 221 Phot. 8. Pycnidia of P. nemophilae (L 205) – × 160 (a) – photo E. Zalewska; SEM × 790 (b) – photo M. Wróbel Fot. 8. Piknidia P. nemophilae (L 205) – × 160 (a) – fot. E. Zalewska; SEM × 790 (b) – fot. M. Wróbel Phot. 9. Conidia of P. nemophilae (L 205) – × 500 (a) – photo E. Zalewska; SEM × 6500 (b); Conidia and fragments of mycelium hyphae – photo M. Wróbel Fot. 9. Konidia P. nemophilae (L 205) – × 500 (a) – fot. E. Zalewska; SEM × 6500 (b) Konidia i fragmenty strzpek grzybni – fot. M. Wróbel mycelium were seen around the point of transfer. The edge of the colony was regular (photo 7). The diameter of the colony after 7 days of growth on all three media was similar and ranged from 65 to 73 mm, while after 14 days from 80 to 88 mm. The pycnidia formed in small aggregates were the most often round or slightly elongated. They were partly sunken in agar (photo 8). They had one to three elongated ostioles, which were surrounded by hyphal outgrowths. Drops of conidial exudate of creamywhite colour got out through the pycnidial ostioles. The conidia were hyaline, ellipsoidal to cylindrical with several small drops of fat on the poles (photo 9). One-cell conidia with the dimension 6.3 × 1.5 m predominated. Two-cell conidia occurred rarely, and their dimension was, on an average, 11.8 × 3.2 m (tab. 2). The reaction with 1 N NaOH on MA and OA media for all studied isolates of P. nemophilae was positive. The change of the tinge of agar was observed around the colony, initially into the green colour which changed in red. Chlamydospores were not observed. _____________________________________________________________________________________________________________________________________________ Hortorum Cultus 10(2) 2011 222 B. Zimowska DISCUSSION The present studies showed that despite herbaceous plants produce substances of bacteriostatic and fungistatic properties [Kozowska et al. 2010, Tajkarimi et al. 2010], they are commonly colonized and infected by fungi, including those belonging to Phoma. The diversity of species of the genus Phoma occurring on the herbs from family Lamiaceae which was proved in the present paper confirms the information from the literature on their frequent occurrence, especially on herbal plants, including herbaceous ones [Aveskamp et al. 2008]. Saprobes commonly developing on different substrates include the species also isolated in the present studies: P. capitulum, P. labilis, P. pereupyrena, P. subglomerata and P. septicidalis, with the possibility that the latter species can cause necrosis of plants from family Gramineae [De Gruyter and Boerema 2002, Zimowska 2007b, 2008b ]. The fact of obtaining isolates of P. exiqua var. exiqua from all the studied plants confirms the information in the literature that this species is one of the most frequently occurring of Phoma in the world [Aveskamp et al. 2008]. Isolates of this fungus have been so far obtained from over 200 genera of plants [Boerema et al. 2004], and results of these studies enrich the collection with successive hosts. P. exiqua var. exiqua, as a facultative pathogen can cause different disease symptoms, e.g. necrosis of the leaves and the stems, root rot or seedling blight [Van Der et al. 2000, Machowicz-Stefaniak et al. 2008]. Isolation of the fungus cultures from the studied plants showing symptoms of necrosis and growth inhibition of the root system, together with the presence of etiological signs on them can indicate that P. exiqua var. exiqua caused such symptoms. Infection of leaves and stems by the fungus should be assessed negatively. Due to the facultative character of the fungus parasitism, infection of these organs can occur through the injuries caused by cultivation, different weather conditions or interaction with other organisms. P. nepeticola is described in the literature as a commonly occurring pathogen of catnip (Nepeta cataria) and other plants from family Lamiaceae. The list of host plants that can infect P. nepeticola includes Leonurus cardiaca and Mentha spp. [De Gruyter et al. 2002, Zimowska 2008b]. Isolation of this fungus cultures from the leaves and stems of motherwort showing symptoms of small necrotic spots, together with the presence of etiological signs on them may suggest that they were caused by the fungus species under discussion. P. nemophilae is a pathogen known both in Europe and the United States to cause seedling blight and stem decay of plants from genus Nemophila [De Gruyter et al. 2002]. The fact of obtaining fungus isolates from motherwort roots can point to the role of this fungus species in causing disease symptoms on motherwort plants. However, in order to confirm the pathogenic abilities of the enumerated species of Phoma spp. it is necessary to conduct infection studies according to Koch’s postulates. Studies conducted on the morphology of the examined isolates confirmed the assumption put forward in the 1930’s and 1940’s by Wollenweber, Hochaphel and Dennis, and later continued by Boerema et al. They proved that establishing taxa within Phoma spp. is possible only on the basis of constant morphological features observed in vitro in cultures developing in standard conditions. It is only such a procedure that en_____________________________________________________________________________________________________________________________________________ Acta Sci. Pol. Characteristics and occurrence of Phoma spp. on herbs from the family Lamiaceae 223 abled to qualify differentiated isolates obtained from motherwort plants, sage and savory within the proper section, and next, within the section, to the species. REFERENCES Aveskamp M. M., De Gruyter J., Crous P.W., 2008. Biology and recent developments in the systematics of Phoma, a complex genus of major quarantine significance. Fungal Diversity, 31, 1–18. Boerema G.H., De Gruyter J., Noordeloos M.E., Hamers M.E.C., 2004. Phoma identification manual. Differentiation of specific and infra-specific taxa in culture. 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Charakterystyka izolatów Phoma strasseri nie notowanego w Polsce patogenu mity pieprzowej (Mentha piperita L.). Acta Agrobot., 58 (2), 151–162. Van Der Aa., Boerema G.H., De Gruyter J., 2000. Contributions towards a monograph of Phoma (Coelomycetes) VI-1. Section Phyllostictoides: Characteristics and nomenclature of its type species Phoma exiqua. Persoonia, 17, 435–456. CHARAKTERYSTYKA I WYSTĉPOWANIE Phoma spp. NA ZIOàACH Z RODZINY Lamiaceae Streszczenie. Gatunki nale ce do rodzaju Phoma powszechnie wystpuj na rolinach zielnych, w tym równie zielarskich. W latach 2004–2006 z zió z rodziny Lamiaceae otrzymano zró nicowane pod wzgldem morfologicznym izolaty nale ce do rodzaju Phoma. Na podstawie obserwacji staych cech morfologicznych, przeprowadzonych in vitro w kulturach rozwijajcych si na standardowych podo ach zakwalifikowano poszczególne izolaty Phoma spp. do odpowiedniej sekcji, a nastpnie do gatunku. Ze wszystkich organów badanych rolin izolowano gatunek P. exiqua var. exiqua. Kultury P. nepeticola otrzymano z lici i odyg serdecznika pospolitego, a z korzeni uzyskano izolaty P. nemophilae. Oprócz wy ej wymienionych gatunków wyizolowano równie P. capitulum, P. labilis, P. pereupyrena, P. subglomerata oraz P. septicidalis. Sáowa kluczowe: grzyby, roliny zielarskie, Phoma spp., serdecznik pospolity, szawia lekarska, czber ogrodowy Accepted for print – Zaakceptowano do druku: 29.03.2011 _____________________________________________________________________________________________________________________________________________ Acta Sci. Pol.