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Mycologia, 94(5), 2002, pp. 856-861.
© 2002 by The Mycological Society of America

Intraspecific variation in Heterobasidion annosum for mortality rate on Pinus sylvestris and Picea abies seedlings grown in pure culture


Antoni Werner 1

     Department of Phytopathology, Institute of Dendrology, Polish Academy of Sciences, Parkowa 5, 62-035 Kórnik, Poland

Piotr Lakomy

     Department of Forest Pathology, August Cieszkowski University of Agriculture, Wojska Polskiego 71c, 60-625, Poznan, Poland

   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 

One-month-old Scots pine (Pinus sylvestris) and Norway spruce (Picea abies) seedlings were inoculated in vitro with Heterobasidion annosum strains, four each of the P-, S- and F-intersterility groups. Variation among strains and between the IS groups in virulence, expressed in mortality rate, was detected during twelve months after inoculation. Most of the strains were more virulent on spruce than on pine, and mortality of spruce seedlings was significantly higher. The P strains displayed similar virulence on both hosts, while S strains caused higher mortality of spruce seedlings and significantly lower mortality of pine seedlings. Strains of the F group were less virulent, but killed significantly (P < 0.05) more spruce than pine seedlings. In the interspecific analyses with two hosts, the isolates and IS groups accounted for most of the explained variation in the host mortality

Key words: Heterobasidion annosum, intersterility groups, mortality rate in vitro, Norway spruce, Scots pine


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Heterobasidion annosum (Fr.) Bref. is one of the most important specialized, root-inhabiting pathogens of the temperate and boreal regions of the world, causing great losses to the production of timber, primarily in managed coniferous forests. It consists of three intersterility (IS) groups showing different preferences for host trees (Korhonen 1978Citation, Capretti et al 1990Citation). The S-group is common on Norway spruce (Picea abies (L.) Karst.) and only occasionally infects other trees in most parts of Europe, North America, and Asia (Dai and Korhonen 1999Citation, Morrison and Johnson 1999Citation). In Europe, the main host of the P-group is Pinus sylvestris L. of all ages, but it also inhabits a variety of other plants including Norway spruce. The F-group was mainly found on Abies species in southern and central Europe (Capretti et al 1990Citation, Korhonen and Piri 1994, Korhonen et al 1998Citation, Lakomy 1996Citation, Kowalski and Lakomy 1998Citation, Lakomy et al 2000Citation). Although in Europe the distribution areas of the three IS groups overlap, in nature they are genetically isolated, and only a few natural intergroup hybrids have been reported (Garbelotto et al 1996Citation). In the laboratory, however, they show some degree of sexual compatibility (Korhonen 1978Citation, Capretti et al 1990Citation, Goggioli et al 1998Citation). A high degree of interfertility has been found between Italian isolates of IS group F and Finnish isolates of IS group S (Capretti et al 1990Citation). Compatible mating has also been described between isolates of IS group S and P (Korhonen 1978Citation, Stenlid and Karlsson 1991Citation).

In contrast to field studies (Kaufmann et al 1980Citation), several greenhouse experiments provided strong evidence for host preference, similar to that observed in nature. In the study by Kuhlman (1970)Citation, variation in host susceptibility due to host, isolate, and host x isolate interaction were significant at the 1% level. A significant interaction between pine and Douglas-fir isolates (ascribed later to the North American P- and S-IS groups by Harrington et al 1989Citation) and Pinus ponderosa and Abies concolor was showed by Worrall et al (1983)Citation. Intraspecific variation in H. annosum growth in Picea abies and Pinus sylvestris sapwood was studied by Stenlid and Swedjemark (1988)Citation. In greenhouse conditions S-group isolates easily infected spruce but showed limited growth on pine, whereas P isolates aggressively attacked both hosts. Spruce was more susceptible than pine. Also, in the study by Swedjemark et al (1999)Citation, the P-group isolates were more virulent on pine than the S-group isolates. In spruce, P isolates were also more virulent, but the difference between isolates of the both IS groups was not statistically significant.

Since the host specialization of the IS groups seems not to be strict due to their ability to occur on the same host species, especially when colonizing dead wood, and the fungal growth in stems after wounding may be so highly altered by the host response that the measured virulence may be an artifact of the inoculation experiment (Delatour 1982Citation), an in vitro system was developed to test virulence, expressed in mortality of intact plants after inoculation with the fungus under uniform conditions.

The objectives of the study were (i) to assess variation in virulence among isolates and between three IS groups of H. annosum on Pinus sylvestris and Picea abies seedlings grown in vitro over a period of one year after inoculation; (ii) to estimate how much the pathogen and host plant contribute to variation in host mortality in tests with two hosts by twelve isolates and the three IS groups


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
Plant material – The plant material consisted of Pinus sylvestris L. seedlings representing the provenance of Bolewice (52°28'N and 16°03'E) and Picea abies (L.) Karst. (Sniezka Forest District, 50°55'N and 15°46'E; altitude : 400–600 m).

Heterobasidion annosum strain – Twelve strains of H. annosum were selected for the study. Periodic passages on host plants grown in vitro enable maintenance of constant growth character, aggressiveness, and pathogenicity of the fungi. Details of origin of the strains are listed in Table I. The fungal strains were grouped to IS groups (P, S, and F) according to their ability to heterokaryotize homokaryotic tester mycelia (Korhonen 1978Citation). Each isolate was paired with homokaryotic tester strains. Three P, seven S, and ten F testers were used. The P testers originated from Poland (Oborniki—94149, Podanin—97064, 97066), the S testers from Estonia (Saaremaa—91109/1, Hiiumaa—93102/2, Vormsi—93142/2), Finland (Kirkkonummi—92044/5, 93254/2), Italy (Vicenza 87075/2) and Slovenia (Hotedersica—9211/1.3), and the F testers from France (Grande Chartreuse—92144/1, Lyon—92169/2), Greece (Parnon mountain—HL-2.1, Menalon Mt.—93315), Italy (Firenze—91280/11, 930912/1.3.1, Pistoia—930920/3.2.2, Potenza—92179/2), and Slovenia (Lovrenc na Pohorju—9210/4.2, Krekovse—92192).


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  		TABLE I. Origin of strains

 
Growth conditions and inoculation procedures – Pine and spruce seeds were soaked in water, sterilized superficially with 2% HgCl2 for 4 min and washed three times (15 min each) in sterile distilled water. Seeds were germinated on 0.6% agar (w/v) medium, in the dark at 24 C. Subsequently, they were aseptically transferred to 300 x 30 mm test tubes containing 100 mL of medium composed of a modified Ingestad's nutrient solution (Ingestad 1979Citation) [1.8 mM NH4NO3, 2 mM CaCl2, 0.03 mM FeCl3, 0.6 mM MgSO4 x 7 H2O, 0.6 mM KCl, 0.6 mM KH2PO4, 3.0 µM MnCl2 x H2O, 6.6 µM MnSO4, 3.0 µM ZnCl2, 0.0003 µM CuCl2 x 2 H2O, 0.3 µM NaMoO4 x 2 H2O, 0.15 µM thiamine-HCl and 15 g Bacto-Agar (DIFCO)] in 1 L of distilled water.

The seedlings were incubated in a growth room under fluorescent tubes (Osram L36/W77 Flora) (100 µEm-2s-1) light 18 h per day, 75% RH at 24:20 C day : night temperatures. Seedlings contaminated with bacteria and/or saprobic fungi were excluded. After one month an inoculum disc (5 mm in diam) of a 2-wk-old mycelial mat of H. annosum was placed on the agar close to the seedling. Altogether 803 pine and 706 spruce seedlings were inoculated with the strains of the pathogen. As controls 50 non-inoculated seedlings each of pine and spruce were grown in the same conditions. They remained alive and uncontaminated until the end of the experiment. During next 12 mo the number of dead seedlings was counted in each host/pathogen strain combination. Root pieces of the dead seedlings were incubated on malt-agar in Petri dishes at 24 C for 2 wk and then checked for Spiniger meineckellus (Olson) Stalpers conidial stage, used as a positive indicator of H. annosum infection. The experiment was repeated twice and the plants were totally randomized once a month. Seedling mortality was expressed as percentage of dead plants in total number of inoculated plants in each replication.

Statistical analysis – Analysis of variance (Anova/Manova), Tukey's HSD test, and Student's test were conducted using statistical analysis software Statistica PL 1997 (StatSoft Polska Inc., USA). Data in % were transformed before the analysis according to formula of C. I. Bliss (Snedecor and Cochran 1976Citation) of the form: arcsin .


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
None of the non-inoculated seedlings grown in vitro died before the end of the experiment. All strains of the IS groups were more virulent on spruce than on pine, and consequently the mortality of spruce seedlings was significantly higher at the 5% level (Fig. 1A). Mean mortality in spruce was 53.91% and in pine 38.43%.



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  		 FIG. 1. Mean mortality of Scots pine and Norway spruce seedlings inoculated in vitro with P, S, and F strains of Heterobasidion annosum (A), mean mortality caused by individual strains on pine and spruce seedlings (B), host preference of the P-, S- and F-IS groups on pine (C) and spruce (D) and on both hosts (E). Bars represent standart error for each group. Means designed by the same letter did not differ significantly at the 5% level using Tukey's HSD test. * = P < 0.05 according to Student's test.

 
Variation in mortality rate among all strains of H. annosum and three IS groups was highly statistically significant when tested on two hosts (Tables II and III) and on pine and spruce seedlings separately. There was no statistically significant difference between replications (P = 0.5875), and the host x strain and host x IS group factors were significant. The components of variance in Table II show that much of the variance in seedling mortality was attributable to the strain effect. Of the explained variance (i.e., non-error variance), 59.80% came from strain. Of the remaining explained variance, more than twice as much was from the host x strain interaction term (27.96%), as from host-plant (12.24%). Just as in the interspecific test of two hosts by twelve isolates, the isolates split up by IS groups accounted for most of the explained variance (47.57%) (Table III). The larger component of variance explained by strain effect, when compared with IS-group effect, indicated that the differences between strains within each of the IS groups were smaller.


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  		TABLE II. Analysis of variance of mortality for host-intraspecific specialization by twelve strains of Heterobasidion annosum representing P, S, and F intersterility groups on pine and spruce in pure culture

 

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  		TABLE III. Analysis of variance of mortality for host-intraspecific specialization by three intersterility groups of Heterobasidion annosum on pine and spruce in pure culture

 
In the intraspecific analyses, the between-strain variation was similar for both hosts (P < 0.00001), whereas the between-IS group-within-pine variation was far more statistically significant (P < 0.0001) compared to that within spruce (P < 0.05). The P-group isolates did not differ significantly on pine, whereas the differences among the S and F isolates were significant at the 5% level. On spruce, S isolates varied at the 5% and the P, and F isolates at the 1% level.

From among isolates of the P group, two of them (P-Kl and P-95107) caused higher mortality of pine seedlings (49.09 and 80.0%, respectively) in comparison with spruce (33.75 and 55.0%), whereas strain P-Bor killed more spruces (88.0%) than pines (57.95%) (Fig. 1B). Generally, the P-group isolates displayed similar mortality rate on both pine and spruce seedlings (Figs. 1C and D). Corresponding frequencies were 61.45 and 59.95%, respectively, and the differences were not statistically significant. All strains of the S group caused significantly higher mortality of spruce seedlings (66.76%) (Fig. 1D) and significantly (P < 0.0002) lower mortality of pine seedlings (26.04%) (Fig. 1C).

Comparing the strain effect of the F group, except of F-96067, which showed high mortality rate on pine and spruce (54.0 and 62.04%, respectively), the rest of the F-group isolates were less virulent (Fig. 1B). Generally they killed, however, significantly more (P < 0.05) spruces than pines. On pine, their effect did not vary from that caused by the S-group isolates (Fig. 1C). In contrast to similar and low mortality of the S- and F-IS groups on pine, the P isolates were more virulent on spruce than F-group (Figs. 1D and E).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
Seedlings of conifers have seldom been used to test aggressiveness and pathogenicity of H. annosum. Fine, non-suberized and suberized roots are, however, considered to be a useful model for studying resistance mechanisms (Johansson and Asiegbu 1994Citation), and consequently were used to study infection process, host-pathogen interaction, and host resistance (Werner 1990Citation, 1991aCitation, b, CitationAsiegbu et al 1993Citation, 1994Citation, 1995Citation, Heneen et al 1994aCitation, bCitation, Werner and Idzikowska 2001Citation).

In spite of in vitro conditions, the study provided strong evidence for the occurrence of intraspecific variation in the host preference, similar to that observed in nature, which is interpreted as an early step towards species differentiation in H. annosum complex (Korhonen 1978Citation), and showed that using pine and spruce seedlings grown in vitro to test virulence and host preference is an alternative method to measurement of fungal spread in sapwood of seedlings or long-term infection experiments on standing trees. Moreover, since, contrary to other artificial infection experiments, the final outcome of host-pathogen interactions was largely dependent on host and pathogen genotypes, these results can contribute to better understanding the nature of host preference. The host preference was the most distinct among S isolates to spruce. They killed 66.75% of spruce seedlings and only 26.04% of pine seedlings, whereas there was almost no difference in mortality rate between S and P strains on spruce, as corresponding frequencies were 66.75 and 59.95%, respectively. These results correspond with previous studies on infection frequency and mortality of 4-yr-old Norway spruce and Scots pine trees inoculated with S and P isolates (Stenlid and Swedjemark 1988Citation, Swedjemark at al 1999Citation).

Statistically non-significant differences between effects of S and F groups on pine and P and F groups on spruce may indicate lack of preference to non-host plants. In spite of higher mortality of spruce seedlings inoculated with F isolates, compared to pine, there was no significant host-F-group isolates interaction factor (P = 0.07103), therefore in the absence of fir seedlings in the experiment, it may be only related to higher susceptibility of spruce. Recently however, molecular analyses of the H. annosum complex have shown that IS groups S and F are more closely related to each other than to IS group P (Kasuga et al 1993Citation, LaPorta et al 1993Citation, Otrosina et al 1993Citation, Müller et al 1995Citation, Karjalainen 1996Citation).

Since all the F isolates originated from one locality, but only the most virulent (F-96067) was isolated from a dead tree, a relatively low virulence of the other F isolates may be related to their saprobic properties (Capretti et al 1990Citation, Lakomy 1996Citation). Large between-strain-within-P, and S group variation might have been also explained in terms of the strain origin and differences in their pathogenic and saprobic potential. Some strains isolated from dead trees (i.e., P-Bor, P-95107, F-96067) were stronger pathogens than those isolated from stumps and logs; however, in studies by Swedjemark et al (1999)Citation, the assumption of faster sapwood growth among isolates originating from trees was not confirmed experimentally. In spite of the small number of isolates representing each of the IS groups, their very different geographical origins may also explain the large genetic variation, which is most probably larger than if they originated from a spatially limited populations, as was the case of S isolates from trees and stumps and tested by Swedjemark et al (1999)Citation.


   ACKNOWLEDGMENTS
 
This study was financially supported by the Polish Academy of Sciences and the Polish Committee for Scientific Research, grant No 5 P06H 004 15. The tester strains were kindly provided by Drs. Kari Korhonen from Finland, Paola Capretti from Italy, Panagihiotis Tsopelas from Greece, and Alenka Munda from Slovenia. We also wish to thank Mrs. Anna Blaszkowiak for her skillful technical assistance.


   FOOTNOTES
 
1 Corresponding author, Email: aswerner{at}rose.man.poznan.pl Back

Accepted for publication February 27, 2002.


   LITERATURE CITED
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
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