Volume 11
Issue 1
Horticulture
JOURNAL OF
POLISH
AGRICULTURAL
UNIVERSITIES
Available Online: http://www.ejpau.media.pl/volume11/issue1/art-21.html
BIODIVERSITY OF FUNGI COLONIZING DIFFERENT PARTS OF CARAWAY (CARUM CARVI L.)
Zofia Machowicz-Stefaniak, Ewa Zalewska
Department of Plant Pathology,
Agricultural University in Lublin, Poland
The present paper determined the occurrence and harmfulness of fungi, especially Septoria carvi, towards different cultivars of caraway Carum carvi L. in the climatic conditions of the Lublin region. The studies were conducted in the years 2001-2004 on the plots sown with schizocarps of the cultivars Arterner, Niederdeutscher, Record and Konczewicki. The percentage of plants with disease symptoms on the aboveground parts and the percentage of leaves and umbels with the symptoms of septoriosis were determined in the second years of caraway cultivation. The fungi were identified on the basis of etiological symptoms visible on the infected plant parts and on the basis of the mycological analysis by the method of artificial cultures. The major pathogen to caraway in the examined conditions was fungus Septoria carvi, causing necrosis of the leaves, leaf petioles, stems, umbels and schizocarps. In the conditions which were favourable to the development of S. carvi, all the tested cultivars, and especially Niederdeutscher, were highly susceptible to this pathogen. A complex of other fungi species, including Botrytis cinerea, Rhizoctonia solani, Colletotrichum gleosporioides and toxin-forming species from the genera of Fusarium and Altenaria were isolated from the aboveground parts of caraway every year. Sclerotinia sclerotiorum occurred on the roots and the stem base of the examined cultivars in 2004.
Key words: caraway, fungi, diseases.
INTRODUCTION
Caraway is one of the oldest spice and medicinal plants. The quality and quantity of the herbal raw material are decreased by pathogenic factors from different taxonomic units, e.g. viruses, phytoplasms, bacteria and fungi [2,6,8,14]. A significant role in causing herb diseases is ascribed to fungi. They infect the roots and the stem base, which causes rapid inhibition of growth and the decay of plants [4,5,6,11,22]. Necrosis of the aboveground parts of caraway is caused by Phomopsis diachenii, Botrytis cinerea, Mycocentrospora acerina, Septoria carvi and numerous toxin-forming species of fungi from the genera of Altenaria and Fusarium [1,4,5,16,20]. Plasmopara nivea, causing downy mildew, and Erysiphe umbelliferarum f. carvi, causing powdery mildew, among obligatory pathogens, may occur on caraway [7,18]. In the years 2001-2002 the occurrence of pathogenic fungi was found in the vicinity of Chełm on caraway plants cultivar Konczewicki [10]. The obtained results inspired the studies on their biodiversity and harmfulness, especially of S. carvi towards different cultivars in the climatic conditions of the Lublin region.
MATERIAL AND METHODS
Observations were performed in the years 2001-2004 on cultivar plots of caraway, established at Motycz near Lublin, by the method of random blocks. This plant had not been earlier cultivated in the studied area. The plots were set up every year after potato cultivation on the soil of II valuation class with pH 5.0-5.5. Schizocarps of Arterner, Niederdeutscher, Record and Konczewicki cultivars obtained in the original form from BA f. Züchtungsforschung an Kulturpflanzen Inst. F. Resistenzforschung und Pathogendiagnose in Aschersleben, and schizocarps of Konczewicki cv. from reproduction in Poland were used. Caraway schizocarps were sown in the years 2001-2003 in the period between the 18th and the 30th April. Every year 32 schizocarps were sown in two rows for each cultivar, 16 schizocarps in each row. In the second year of cultivation, i.e. in the years 2002-2004, the healthiness of caraway was observed, establishing the percentage of plants with necrotic symptoms on the aboveground parts and the percentage of leaves and umbels with the symptoms of septoriosis. The data obtained from 32 plants of each cultivar were submitted to statistical analysis, using SAS program. The occurrence of fungi was determined on the basis of etiological symptoms occurring on the infected parts of plants and on the basis of mycological analysis. The plant material for mycological examinations was taken each time from 5 plants of particular cultivars at anthesis and in the period of maturation. The stems and leaves were analyzed at the first date, while the stems, umbels and schizocarps – in the other. The mycological analysis of the plant material, which had been previously disinfected, was conducted by the method of artificial cultures, using maltose medium [14]. In 2004, at the end of the harvest, a mycological analysis was made of the roots and the stem base of caraway in connection with the occurrence of disease symptoms that had not been earlier observed on those organs.
RESULTS
In the first year of the cultivation of the studied cultivars of caraway no visible disease symptoms were macroscopically found on the plants. The healthiness of the aboveground plant parts considerably decreased after wintering. At the beginning of the vegetation period, i.e. in the second half of May of 2002, 2003 and 2004, all plants of Niederdeutscher and Arterner cultivars as well as 40% of plants of the other cultivars showed the symptoms of spots on the aboveground parts. On the other hand, disease symptoms occurred on all plants of the studied cultivars in the period of maturation. Those were necrotic spots of the diameter ranging from 0.3 to 3.0 mm, brown in colour, with a clearly marked edge. They were numerous on the leaves, the petioles, the stems and the umbels. At anthesis the percentage of leaves with spots was, depending on the years and the cultivars, from 5.19 to 70.06 (Table 1). In the years 2003 and 2004 leaf infection was significantly higher than in 2002. The percentage of infected leaves was the highest, i.e. ranging from 64.69 to 70.06, in 2003 and 2004 in cv. Niederdeutscher. There were numerous pycnidia on the leaves, the petioles and the stems with the exudation of conidial spores with the features typical of genus Septoria. Strongly infected leaves and stems gradually yellowed and decayed (Photo 1). The percentage of leaves with the symptoms of septoriosis considerably increased, ranging from 61.50 to 92.93, in the period of maturation, i.e. in the years 2002 and 2003, in the first 10 days of July, while in 2004 – in the first half of June (Table 1). Leaf infection of cv. Niederdeutscher was significantly higher in all studied years than on the leaves of the other cultivars (Table 1). The leaves were completely dried up, black, they often fell on the ground (Photo 2) and dark sporulating fungi from the genera of Altenaria, Cladosporium and Mucor developed on their surface. At that time the symptoms of septoriosis also commonly occurred in the stems, the umbels and the schizocarps (Photo 3). The mean percentage of infected umbels, depending on the cultivar and the studied year, ranged from 9.78 to 40.31 (Table 1). The umbels of cv. Niederdeutscher were always significantly more infected than the umbels of the other cultivars (Table 1). Not numerous, deformed schizocarps with numerous pycnidia of the pathogen on the surface were formed on the infected umbels (Photo 3). In the years 2002 and 2003, which were characterized by quite a high temperature in summer months, the occurrence of septoriosis was common (Tables 1, 2).
Table 1. Mean percentage of caraway studied organs Carum carvi L. with symptoms of septoriosis in second year of cultivation |
Cultivars |
2002 |
2003 |
2004 |
Mean |
|
Leaves – anthesis |
Record |
5.19 a |
44.50 c |
54.37 f |
34.64 a |
Arterner |
6.94 a |
53.62 f |
52.13 ef |
37.57 b |
|
Konczewicki N |
6.87 a |
47.44 cd |
47.06 cd |
33.79 a |
|
Konczewicki |
6.43 a |
49.47 de |
53.78 f |
36.56 b |
|
Niederdeutscher |
11.15 b |
70.06 h |
64.69 g |
48.69 c |
|
NIR = 4.0860 |
NIR = 1.8949 |
||||
Mean |
7.35 a |
53.02 b |
54.38 c |
||
NIR = 1.2602 |
|||||
Leaves – maturation of plants |
Record |
67.53 bc |
68.56 bc |
67.71 bc |
67.94 a |
Arterner |
70.06 bc |
68.94 bc |
71.34 c |
70.13 ab |
|
Konczewicki N |
78.87 d |
61.50 a |
65.56 ab |
68.65 a |
|
Konczewicki |
76.81 d |
70.21 bc |
70.59 bc |
72.54 b |
|
Niederdeutscher |
92.06 e |
90.16 e |
92.93 e |
91.72 c |
|
NIR = 5.3270 |
NIR = 2.4701 |
||||
Mean |
77.07 c |
71.87 a |
73.64 b |
||
NIR = 1.6427 |
|||||
Umbels |
Record |
9.78 a |
14.25 abcd |
16.53 bcd |
13.52 a |
Arterner |
12.31 ab |
12.97 abc |
13.28 abc |
12.85 a |
|
Konczewicki N |
15.81 bcd |
19.53 de |
24.53 e |
19.96 c |
|
Konczewicki |
16.18 bcd |
17.03 bcd |
18.43 cd |
17.22 b |
|
Niederdeutscher |
38.00 f |
37.15 f |
40.31 f |
38.49 d |
|
NIR = 5.6950 |
NIR = 2.6408 |
||||
Mean |
18.42 a |
20.19 b |
22.62 c |
||
NIR = 1.7563 |
Table 2. Air temperature, rainfall and relative air humidity in the years 2002-2004 |
Month |
Mean for the years |
Difference of air temperatures in comparison with means for the years |
Percentage of the rainfall |
|||||
air temperature |
rainfall |
2002 |
2003 |
2004 |
2002 |
2003 |
2004 |
|
March |
1.1 |
25.8 |
3.7 |
0.6 |
0.9 |
12.8 |
25.5 |
33.9 |
April |
8.2 |
41.2 |
0.1 |
-1.8* |
0.3 |
43.6 |
98.7 |
38.1 |
May |
13.1 |
35.6 |
3.4 |
3.1 |
-1.4* |
87.0 |
200.0 |
38.0 |
June |
16.5 |
76.7 |
0.2 |
1.1 |
-0.9* |
138.2 |
51.6 |
49.9 |
July |
20.3 |
75.2 |
0.3 |
-0.7* |
-0.1* |
95.7 |
134.0 |
90.5 |
August |
19.1 |
51.9 |
0.7 |
-0.3* |
0.8 |
65.5 |
52.0 |
48.5 |
September |
12.5 |
73.4 |
0.3 |
0.9 |
-0.4* |
51.7 |
39.5 |
14.2 |
October |
7.9 |
40.3 |
-1.1* |
-2.6* |
1.9 |
124.3 |
124.3 |
26.1 |
November |
2.5 |
39.1 |
2.2 |
2.4 |
0.3 |
58.5 |
43.4 |
65.5 |
* values lower than mean for the years |
Table 3. Fungi isolated from aboveground organs of caraway Carum carvi L. in the second year of cultivation in the years 2002-2004 |
Species of fungi |
Number of isolates |
Total |
Total |
||||||||||||||||||||||
Arterner |
Niederdeutscher |
Record |
Konczewicki N |
Konczewicki |
|||||||||||||||||||||
l |
st |
u |
sc |
l |
st |
u |
sc |
l |
st |
u |
sc |
l |
st |
u |
sc |
l |
st |
u |
sc |
l |
st |
u |
sc |
||
Alternaria spp. |
40 |
28 |
43 |
70 |
66 |
40 |
65 |
80 |
91 |
28 |
46 |
63 |
41 |
27 |
69 |
77 |
59 |
36 |
48 |
58 |
297 |
159 |
271 |
348 |
1075 (63.9) |
Botrytis cinerea Pers. |
1 |
1 |
1 |
1 |
13 |
5 |
1 |
3 |
8 |
1 |
10 |
8 |
13 |
4 |
35 (2.0) |
||||||||||
Chaetomium spinosum Chiv. |
9 |
9 |
9 (0.5) |
||||||||||||||||||||||
Chaetomium trilaterale Chiv. |
2 |
2 |
2 (0.1) |
||||||||||||||||||||||
Cladosporium cladosporioides (Fres.) de Vries |
9 |
2 |
14 |
9 |
6 |
32 |
6 |
2 |
40 (2.3) |
||||||||||||||||
Colletotrichum gloeosporioides (Penz.) Sacc. |
4 |
3 |
1 |
7 |
14 |
1 |
15 (0.8) |
||||||||||||||||||
Epicoccum purpurascens Ehrenberg |
5 |
1 |
5 |
4 |
7 |
4 |
2 |
3 |
1 |
7 |
6 |
5 |
2 |
16 |
22 |
45 (2.6) |
|||||||||
Fusarium spp. |
11 |
- |
1 |
1 |
6 |
- |
8 |
4 |
3 |
11 |
- |
5 |
26 |
- |
4 |
7 |
4 |
- |
15 |
3 |
50 |
11 |
28 |
20 |
109 (6.4) |
Phoma exigua Desm. var. exigua |
1 |
1 |
6 |
1 |
1 |
1 |
1 |
3 |
3 |
15 |
2 |
1 |
5 |
13 |
19 |
9 |
41 (2.4) |
||||||||
Rhizoctonia solani Kühn |
11 |
1 |
4 |
11 |
6 |
33 |
33 (1.9) |
||||||||||||||||||
Saccharomyces spp. |
2 |
2 |
2 (0.1) |
||||||||||||||||||||||
Sclerotinia sclerotiorum (Lib.) de Bary |
2 |
2 |
2 (0.1) |
||||||||||||||||||||||
Septoria carvi Syd. |
42 |
11 |
8 |
15 |
40 |
12 |
10 |
10 |
28 |
3 |
5 |
20 |
9 |
3 |
21 |
3 |
2 |
22 |
151 |
38 |
23 |
52 |
264 (15.6) |
||
Ulocladium botrytis Preuss |
4 |
4 |
4 (0.2) |
||||||||||||||||||||||
Dark, not sporulating mycelium |
1 |
2 |
5 |
5 |
8 |
5 |
13 (0.7) |
||||||||||||||||||
Total |
133 |
41 |
57 |
95 |
134 |
53 |
83 |
103 |
133 |
44 |
63 |
80 |
122 |
59 |
76 |
88 |
104 |
49 |
77 |
95 |
626 |
246 |
356 |
461 |
1689 (100) |
Explanation: l – leaves, st – stems, u – umbels, sc – schizocarps |
Table 4. Species of fungi from genera Alternaria and Fusarium obtained from aboveground organs of caraway in the second year of cultivation in the years 2002-2004 |
Genus |
Species |
Alternaria |
A. alternata (Fr.) KeisslerA. radicina Meier A. raphani Groves et Skolko |
Fusarium |
F. avenaceum (Fr.) Sacc.F. culmorum (W.G.Sm.) Sacc. F. equiseti (Corda) F. oxysporum Schlecht F. sporotrichioides Sherb. |
Table 5. Fungi isolated from caraway roots and a base of stems Carum carvi L. in the time of harvest (23.07.2004) |
Fungi |
Number of isolates |
Total |
Total |
|||||||||||
Arterner |
Niederdeutscher |
Record |
Konczewicki N |
Konczewicki |
||||||||||
r |
bst |
r |
bst |
r |
bst |
r |
bst |
r |
bst |
r |
bst |
number |
% |
|
Alternaria alternata (Fr. Keissler) |
- |
3 |
2 |
- |
- |
30 |
6 |
3 |
- |
3 |
8 |
39 |
47 |
8.5 |
Fusarium solani (Mart.)Appel et Wollenw. emend. Snyd et Hans. |
2 |
2 |
3 |
- |
- |
- |
- |
3 |
1 |
3 |
6 |
8 |
14 |
2.5 |
Fusarium sporotrichioides Sherb. |
17 |
6 |
- |
19 |
- |
- |
- |
7 |
- |
- |
17 |
32 |
49 |
9.0 |
Penicillium spp. |
- |
- |
- |
- |
- |
- |
- |
- |
16 |
- |
16 |
- |
16 |
3.0 |
Rhizoctonia solani Kühn |
- |
14 |
- |
10 |
12 |
- |
- |
- |
- |
- |
12 |
24 |
36 |
6.5 |
Sclerotinia sclerotiorum (Lib.) de Bary |
39 |
33 |
52 |
30 |
35 |
30 |
29 |
40 |
12 |
48 |
167 |
181 |
348 |
63.0 |
Trichoderma koningii Oud. |
- |
- |
- |
- |
8 |
- |
25 |
3 |
- |
6 |
33 |
9 |
42 |
8.0 |
Total |
58 |
58 |
57 |
59 |
55 |
60 |
60 |
56 |
31 |
60 |
259 |
293 |
552 |
100 |
Explanation: r – roots, bst – base of stem |
Photo 1. Necrosis of caraway leaves caused by S. carvi (a), pycnidia of fungus on the leaf petiole (b) and the stem (c) (photo by E. Zalewska) |
![]() |
Photo 2. Severe symptoms of septoriosis on Record cultivars of caraway caused by S. carvi (photo by E. Zalewska) |
![]() |
Photo 3. Necrosis of caraway umbels caused by S. carvi (photo by E. Zalewska) |
![]() |
Photo 4. White mould of caraway caused by S. sclerotiorum (photo by E. Zalewska) |
![]() |
The mycological analysis of caraway confirmed the common colonization of plants by Septoria carvi. The fungus was isolated from all aboveground organs – totally, 264 cultures, i.e. 15.6% of all isolations (Table 3). The fungus cultures obtained at anthesis from 2-year-old plants constituted 24.1% of all isolated obtained at that time, whereas in the period of maturation it was 9.3%. Cultures of Botrytiis cinerea, constituting 2.0% of all isolations, were obtained from the leaves, the stems, the umbels and the schizocarps (Table 3). Rhizoctonia solani were obtained from all cultivars at the first date of studies. Fungi from genus Fusarium were isolated from all aboveground parts, at both dates of studies, and their cultures constituted 6.4% of all isolations (Table 3). Colletotrichum gloeosporoides were found on the leaves and the stems of some cultivars at the first date of studies. All caraway organs were colonized most numerously by the species from genus Altenaria, constituting 63.9%, including A. alternata, A. radicina and A. raphani (Table 4). The species that was found not earlier than in the third year of studies was Sclerotinia sclerotiorum, and singular cultures of the fungus were observed on schizocarps in the period of their maturation (Tables 3 and 5). Massive occurrence of caraway rot was found on the roots and the stem base at the end of the harvest in 2004. The disease was shown in extensive necrosis of the roots and the stem base, with the softening of tissues, and numerous sclerotia of S. sclerotiorum visible on the enumerated parts of plants (Photo 4). The mycological analysis of the roots and the lower part of stems gave a lot of isolates of fungi belonging to 7 species, including the isolates of S. sclerotiorum constituting 63% (Table 5).
DISCUSSION
The obtained results proved that the main pathogen towards caraway in the studied conditions was fungus Septoria carvi, which was shown by the characteristic disease symptoms on the aboveground parts of plants, microscopic examinations of etiological symptoms and fungus isolation on artificial medium. The common occurrence of septoriosis on caraway in the studies area was probably possible thanks to favourable thermal and humidity conditions for the pathogen, whose thermal optimum ranges from 25 to 28°C (unpublished). The favourable conditions for the development of S. carvi are testified to by an intensive secretion of spores from the pycnidia on the surface of the infected organs. In the examined conditions septoriosis caused by Septoria carvi should be considered as a dangerous disease of all aboveground parts of caraway, i.e. leaves, stems, umbels and schizocarps, while since 1998 the main cause of the dying out of caraway stems and umbels in Germany has been regarded to be Phomopsis diachenii [5]. In recent years S. carvi was found on caraway cultivated in the Czech Republic and Austria [1,19]. The isolation of S. carvi from plants is possible in the initial period of the development of the disease, before other accompanying fungi species appear on plants. The studies showed that in the conditions favouring the development of S. carvi all the tested cultivars, especially Niederdeutscher, were highly susceptible to the pathogen. The aboveground parts of caraway were colonized by a complex of other fast growing fungi species, capable of infecting plants. They included Botrytis cinerea, Rhizoctonia solani, Colletotrichum gloeosporioides and Fusarium spp., causing diseases of different herb species [3,4,5,6,14,15]. What should be regarded as dangerous is frequent colonization of caraway by a toxin-forming fungus F. sporotrichioides, producing not only strongly toxic trichotecenes but monilioformin as well [9]. F. equiseti, isolated in the present studies, was considered in Israel as the cause of massive dying out of the seedlings and adult plants of caraway [21]. Determination of pathogenicity of the obtained isolates of F. oxysporum requires additional studies because a special form of this fungus is already known for caraway [20]. Fairly frequent isolation of P. exigua var. exigua from different caraway parts and the harmfulness of the fungus to the sprouts and seedlings of lemon balm, thyme and dill [11,13] suggest that it can make the healthiness of different herb species worse. The fungi causing microbiological contamination of caraway aboveground parts include the species of genus Altenaria, commonly isolated in the present studies. These are saprotrophic of occasionaly parasites, which – due to the fact that they produce secondary metabolites and cause spots on the plants green parts, considerably lower the quality of the herb material [15,17]. The occurrence of white mould Sclerotinia sclerotiorum on plants in 2004 proved to be damaging to caraway. The consequence of the infection of the roots and the stem base by the pathogen is dying out of the lower parts of plants, which progresses upwards, as different from septoriosis, which begins with the upper parts of plants. Frequent colonization of caraway schizocarps by different fungi species observed in the present studies points out that they can be the source of the primary infection of a new generation of plants [12,15].
CONCLUSIONS
The main pathogen to caraway in the climatic conditions of the Lublin region was S. carvi.
In the conditions favouring the development of S. carvi the tested cultivars, especially Niederdeutscher, were susceptible to the pathogen.
The fungi lowering the quality of the raw material also include Botrytis cinerea, Rhizoctonia solani spp. and Altenaria spp.
ACKNOWLEDGEMENT
We would like to thank Jutty Gabler, Ph.D., from BA f. Züchtungsforschung an Kulturpflanzen Inst. F. Resistenzforschung und Pathogendiagnose in Aschersleben for the sowing material of four caraway cultivars.
REFERENCES
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Accepted for print: 10.03.2008
Zofia Machowicz-Stefaniak
Department of Plant Pathology,
Agricultural University in Lublin, Poland
Kr. Leszczyńskiego 7, 20-069 Lublin, Poland
Phone: (+48 81) 532-30-47 ext. 133
email: zofia.machowicz@ar.lublin.pl
Ewa Zalewska
Department of Plant Pathology,
Agricultural University in Lublin, Poland
Kr. Leszczyńskiego 7, 20-069 Lublin, Poland
Phone: (+48 81) 532-30-47 ext. 142
email: ewa.zalewska@ar.lublin.pl
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