183

Gunilla SWEDJEMARK1 and Jan STENLID2

"The Forestry Research Institute of Sweden, Uppsala Science Park, S-751 83 Uppsala, Sweden.#Department of Forest Mycology and Pathology, Swedish University of Agricultural Sciences, Box 7026, S-750 07 Uppsala, Sweden.

Received 10 February 2000 ; accepted 16 June 2000.

The wood of one Picea abies stump, including its roots (1±3 m in length), was sliced into 2 cm thick discs. The stump originated from

a thinning conducted 7 yr prior to the investigation in a 30 yr old spruce stand planted on previous farmland that became

heavily infected by Heterobasidion annosum. After incubation of the wood discs, interaction zones were observed on the surfaces and

H. annosum was isolated from the areas between the zones and from the zone lines, resulting in 296 isolates. The isolates were

tested with somatic incompatibility to detect 35 different genets. Of the 27 genets colonising the upper part of the stump (excluding

the roots), 12 had proceeded into the roots. Seven genets found in the roots were not found in the upper part of the stump and one

genet isolated from an interaction zone on the top of the stump was not found elsewhere in the stump or in the roots. Two of the

genets had grown into root contact with other trees.

INTRODUCTION

Heterobasidion annosum is a serious pathogen on conifers

throughout the boreal and temperate zones of the Northern

Hemisphere. Trunks of infected Norway spruce trees can be

decayed up to 12 m height (Stenlid & Wa$ sterlund 1986). Since

the pathogen is a poor interspecific competitor (Rishbeth

1950, Capretti & Mugnai 1989, Holmer & Stenlid 1994)

spores can only successfully germinate on uncolonised wood

such as freshly cut stumps. The fungus colonises the stump

and is then able to spread vegetatively to adjacent trees via

root contacts. Stumps left after thinning or clear-cuttings may

act as substrate for the fungus for at least 30 years (Greig &

Pratt 1976, Stenlid 1987). The lateral spread from the primary

infection centre varies between 0±1 and 2 m per year (Fowler

1962, Hodges 1969, Swedjemark & Stenlid 1993). The growth

rate of H. annosum is higher in dead than in live wood (Bendz-

Hellgren et al. 1999).

In Scandinavia, H. annosum consists of two intersterility

groups (IS groups). The S group is mainly confined to Norway

spruce while the P group is most often found on Scots pine,

but also on other coniferous and broadleaf trees (Korhonen

1978, Capretti, Goggioli & Mugnai 1994, Swedjemark &

Stenlid 1995). Two groups are identified by their ability to

heterokaryotize homokaryotic tester strains of known IS

group (Korhonen 1978). The intersterility is not complete and

some mycelia are able to mate with both IS groups (Korhonen,

Stenlid & Capretti 1998).

A basidiomycete population is composed of genetically

different individuals which are able to recognise self and non-

self through a system called somatic incompatibility (Todd &

Rayner 1980, Stenlid 1985, Rayner & Boddy 1988, Hansen,

Stenlid & Johansson 1993a, b). In H. annosum this is a

polygenic system where differences at one or more loci result

in an incompatibility reaction (Hansen et al. 1993a, b). Brasier

& Rayner (1987) proposed that the term ‘genet ’ should

describe all parts of a vegetative mycelium that have the same

set of somatic incompatibility genes.

In zones of somatic incompatibility between two hetero-

karyotic strains, new combinations of the four nuclei involved

can occur (Hansen et al. 1993a). Such new combinations are

normally short-lived and confined to small areas between the

interacting mycelia. Hypothetically, they could escape away

from the progenitors when growing in wood by entering into

new wood cells not colonised by other mycelia.

The silvicultural treatment, age and history of a stand are

important factors for the size and number of fungal genets in

a forest area (Dahlberg & Stenlid 1990, Smith, Bruhn &

Anderson 1992, Swedjemark & Stenlid 1993). The population

density of H. annosum varied between 25 and 4800 genets per

hectare (Stenlid 1985, 1987, Piri, Korhonen & Sairanen 1990,

Swedjemark & Stenlid 1993, Garbelotto, Cobb & Bruns 1994,

Morrison & Pellow 1994, Mokritsky 1994), where the dense

populations with relatively small genets were the result of

strong disturbance through forestry and the sparse populations

with large genets were found at sites with a long forest

history of relatively extensive forestry. Swedjemark & Stenlid

(1993) found that 31% of the thinning-stumps in the

Mycol. Res. 105 (2) : 183–189 (February 2001). Printed in the United Kingdom.

A highly diverse population of Heterobasidion annosum in asingle stump of Picea abies

A diverse Heterobasidion annosum population 184

investigated stand contained more than one genet of H.

annosum. The maximum number of genets obtained from the

top of one stump was 13, while from trees nearby only one

genet was obtained. The analysed stump in the present

investigation originated from this stand.

The purpose of this study was to analyse the distribution

and development of H. annosum genets in a population

colonising a single stump 7 years after infection.

MATERIAL AND METHODS

Stand description and history

The stand was situated at Siaro$ , an island in the archipelago

on the Swedish east coast, 50 km north of Stockholm

(Swedjemark & Stenlid 1993). Norway spruce was planted at

a 1±5 m spacing on 7±5 ha abandoned farmland during

1961}62. No silvicultural operations were carried out until

1982. A thinning was then made during July and August.

Sixty percent of the stems were left, which corresponds to a

basal area of 35±5 m# ha−". No signs of decay were found in

the stumps at the time of thinning, and since no heavy

machinery was allowed in the stand the remaining trees were

free from logging and extraction damage.

Disease pattern in the stand

By 1968}87 some trees had died and resin flow was present

on several stems. In 1989, parts of the stand were surveyed for

Fig. 1. Norway spruce stump created at a thinning containing several different genets of H. annosum. Each genet occupies a distinct

sector.

disease and mortality (Swedjemark & Stenlid 1993). Decay

was then detected in 63% of the analysed stems and in 70%

of the stumps (Fig. 1) left after the thinning (thinning stump).

Between 1982 and 1990, 4.5% of the trees had died, mainly

caused by H. annosum infection. Infected thinning-stumps

contained between one (36% of the infected stumps) and 13

fungal genets at the level 0–5 cm from the stump top, while

the trees contained only one genet each. Ninety-five percent

of the collected isolates were assigned to the S group, 2% to

the P group, and 3% could not be classified. S and P isolates

coexisted on stumps but only S isolates were found in the

trees. The smallest genets were confined to one stump while

the largest genet encompassed one stump and two trees and

measured 5 m laterally from the stump to the most distant tree

(Swedjemark & Stenlid 1993). After clear cutting 1993, all

stumps were screened for visible signs of decay. About 85%

of the stumps showed decay.

Sample collection

A stump analysed in the study in 1989, that in the top 5 cm

contained 10 different genets of both the S and P IS groups,

was chosen for the detailed stump study. The stump, including

about 1±3 m of all its major roots, was dug up in spring

1991 and transported to the laboratory. The surrounding trees

and stumps were carefully mapped (ca 5 m from the stump)

and contacts between roots from the stump and other tree or

stump roots were marked.

The complete stump was consecutively cut into 2 cm thick

G. Swedjemark and J. Stenlid 185

Fig. 2. Norway spruce stump, including its roots, colonised by H.

annosum. The stump was cut into 2 cm thick discs, H. annosum was

collected from each sector and tested for somatic incompatibility to

detect single genets.

discs (Fig. 2). All discs were numbered and incubated under

humid conditions in 20 °C for 7 d. Colonies of H. annosum

were recognised from their conidial stage. Any distinct

interaction zone visible on the discs, was identified and

numbered. Corresponding areas on the following discs were

numbered according to previous discs even if the interaction

zones were less distinct. For all discs originating from roots,

the distance to the stump was noted. Distinct areas bordered

by interaction zones from the upper surface from all 4 discs

Fig. 3. Stump discs after sampling. Drawings of the distinct areas bordered by interaction zones from the upper surface of all 4 discs

(I–IV) from the investigated stump, excluding the roots. Any distinct area between interaction zones visible on the discs, was identified

and lettered. In disc I and II, corresponding areas were lettered according to the previous disc. On disc III and IV each isolate has a new

identity due to difficulties to interpret the interaction zones. Dark areas represent wood that did not show signs of decay. (Isolates

sampled from the bottom surface of the discs are not documented in this figure.)

from the stump (excluding the roots) were documented

(Fig. 3).

Isolations were made under a dissecting microscope. A

sterilised needle, slightly touching the conidiophores, was used

to transfer conidia to an Hagem agar (HA) plate (Swedjemark

& Stenlid 1993). Isolations were made from both sides on all

discs from all distinct areas and areas which possibly could

contain a fungal genet. Isolations from all contact points

between the stump roots and other roots were also performed.

The interaction zones were studied under the dissecting

microscope and when conidiophores were observed on the

zones, isolates from those were made separately.

Somatic incompatibility tests

Isolates were paired by placing 3¬3 mm inocula 2–3 cm

apart on HA plates. The morphology of the interaction was

studied 4–5 weeks later after incubation in 20 °C. A compatible

reaction shows a continuous mycelial matt when isolates of

the same genetical origin were paired. When genetically

different isolates were paired a zone with sparse mycelial

growth is observed between the two isolates (incompatible

reaction). Isolates of different intersterility groups create a

morphologically different pigmented zone between them

when paired (Stenlid 1985). Somatic incompatibility was

studied between isolates as follows :

A diverse Heterobasidion annosum population 186

(A) Among all isolates in the upper part of the stump (discs

1–4, including the tap-root).

(B) Among all isolates within the same root.

(C) Between isolates originating from the stump and

isolates originating from the roots.

(D) Between isolates from other roots in contact with the

investigated stump and isolates from the contacted root

originating from the stump.

(E) Between isolates from interaction zones and all isolates

from the stump, roots and root contacts.

(F) Between the isolates sampled in 1989 and all isolates

from the stump, the roots, the contacts and the reaction zones

(3 isolates sampled in 1989 were lost due to contamination

during storage, leaving 7 isolates for somatic incompatibility

tests).

Approximately 6500 pairings were made.

Intersterility group studies

Isolates were assigned to IS group according to their ability to

heterokaryotize homokaryotic known test strains (Korhonen

1978, Stenlid & Karlsson 1991).

RESULTS

The stump was 22 cm diam and about 25 cm high with ten

roots, diameters ranging between 2 cm and 11 cm at the root

base. The tap-root was heavily decayed, which explains why

only the top 5 cm could be recovered. The longest root

obtained was 125 cm. Sampled root contacts were between

25 cm and 125 cm away from the stump.

None of the isolates obtained in 1989 from this stump was

found in any tree in the stand. From decayed trees within 5 m

from this stump only H. annosum genets with known

origin from other stumps were isolated

Table 1. Details of the distribution of isolates of Heterobasidion annosum and genets, determined from somatic incompatibility, at various levels in the

examined stump. The (1 P) indicates that one of the genets in this category is of the P intersterility group. Three of the isolates sampled in 1989 were

lost due to contamination during storage, leaving 7 isolates for somatic incompatibility tests.

Origin of

isolate

Total

No. of

isolates

No. of genets

after

confrontation

within the

unit

No. of genets

that were not

found in the

wood of the

upper part of

the stump in

1990

No. of genets

found in the

upper part of

the stump in

1990 and

elsewhere

Stump}root

diam at

the root base

and at the

root end (cm)

Root

length

(cm)

Upper part of

the stump

62 24 (1 P) — 12 22 —

Root 1 65 5 3 2 10–2 56

Root 2 17 1 1 — 4–0±5 40

Root 3 75 3 0 3 7–0±8 54

Root 4 24 2 0 2 11–2 20

Root 5 15 3 3 — 3–1±5 20

Root 6 1 1 0 1 4–3 20

Root 7 2 1 0 1 2–1 35

Root 8 3 1 0 1 3–1 20

Root contacts 14 2 0 2 — 125

Reaction zones 8 3 1 2 — —

Genets isolated

in 1989

10(7) 10(7) 3 (1 P) 7 — —

Total 296 56 11 — — —

On the top and the second disc of the stump 14 distinct

interaction zones were observed similar to those described by

Swedjemark & Stenlid (1993). On the 3rd disc 13 and on the

4th disc, 16 distinctly separated areas were noted (Fig. 3). On

most root discs, a similar pattern of interaction zone-bordered

sections were noted. Two roots, 4 and 2±5 cm diam, were free

from conidiophores. No root grafts were observed at points

of contact between the roots. Of 23 analysed root contacts,

14 developed conidiophores of H. annosum following

incubation.

From the complete stump, a total of 296 successful isolates

were made. Of those, 62 isolates were from the upper part of

the stump (disc 1–4 including about 5 cm of the tap-root), 217

from the roots, 14 from root contacts and 8 isolates were

collected from interaction zones (one of those originated from

a root). From the investigation in 1989, 7 genets were

included (Table 1).

In a few cases it was difficult to interpret somatic

incompatibility tests, but it eventually proved possible to

classify a majority of these after repeated confrontation. Only

two isolates in root 1 did not form the typical self or non-self

morphology when confronted with other mycelia. Absence of

clamp connections suggested that these isolates were

homokaryotic.

After confrontations within each unit (stump or root) a total

of 49 genets were noted. In the upper part of the stump 27

genets were identified and in the roots and interaction zones

19 and 3 genets were identified, respectively (Table 1). Of the

27 genets colonising the upper part of the stump, 12 had

proceeded into the roots. On one root two different genets

were present on the same disc. Of the genets from roots and

interaction zones, seven and one, respectively, were distinct

from the ones in the upper part of the stump. From the isolates

sampled in 1989, three genets were not identical with stump-

isolates from 1991 (Table 1). Following confrontations among

G. Swedjemark and J. Stenlid 187

Table 2. Distribution of genets within the stump at different levels after

somatic incompatibility tests. Isolates sampled from the bottom surfaces of

the discs are not included in this Table (3 separate genets from bottom

surfaces on discs III and IV, respectively).

Disc I Disc II Disc III Disc IV

AI¯A

IIA

II¯A

Iab¯ ED

I1, 14¯GJ

II

BI¯B

IIB

II¯B

Ic¯ F

I2¯ 2

CI¯C

IIC

II¯C

Idefhkm¯ JKLN

I3¯ 3

EDI¯ ED

IIED

II¯ ED

Igi¯M

I4-, 5¯B

I

FI¯ F

IIFII

¯ FI

j¯BI

6¯ 6

GI¯H

IIGJ

II¯ 1, 14

IVl¯ 1 7, 8¯A

I

HI¯H

IH

II¯G

I9, 12, 15¯ L

II

II¯ I

IIIII

¯ II

11¯ 11

JKLNI¯K

IIK

II¯ JKLN

I13¯ JKLN

I

MI¯ gi

IIILII

¯ 12IV

16¯ ED

MII

¯MII

17¯ 17

NII

¯NII

isolates from different parts of the stump, altogether 35

distinct genets of the fungus were detected in the stump

(Tables 1–2, Figs 3–4).

Two genets of the P intersterility group were found, one

among the genets isolated in 1989 and one among the isolates

in the stump from 1991. In roots 1 and 4, one genet in each

root could not be assigned to either group based on the

macroscopic morphology of the interaction zone.

Fig. 4. Stump discs after sampling and somatic incompatibility tests. Isolates within circles all represent separate fungal individuals. A *

indicates that the isolate was also identified in a root or a root contact. On disc III isolate d, e, f, h, m and k belong to the same genet

which is indicated by a line between circles. The same applies for isolate 9, 12 and 15 on disc IV. Isolates sampled from the bottom

surfaces of the discs are not included in this figure (3 separate genets from bottom surfaces on discs III and IV, respectively). Details

about the relationship between fungal individuals on different levels in the stump are presented in Table 2.

DISCUSSION

The size of a mycelium will influence the amount of resources

produced and hence its potential to produce fruiting bodies

and spores. The probability of transferring the genes of a

mycelium into future populations increases with the number

of viable spores produced (Rayner & Boddy 1988). Since

Heterobasidium annosum may complete its life-cycle both on

dead and live wood (Swedjemark & Stenlid 1993), the fungus

has a large supply of substrate. Intraspecific competition in the

saprotrophic phase in a stump containing several genets, may

reduce the production of fruit-bodies and the ability of the

fungus to spread to adjacent trees. None of the genets from

the stump in the present investigation were found in any of

the trees in the stand even though two of the genets were

found at root contacts. The strongest selective forces therefore

seem to be connected with the transition from a saprotrophic

to a parasitic life-form in H. annosum. Support for this

conclusionwas also obtained from a second stump investigated

in less detail from the same stand, where only one genet out

of seven at the stump surface had successfully invaded a

nearby tree (data not shown).

The three genets of H. annosum that were not recovered in

1991 probably represent shallow mycelia that were cut off the

stump when sampled in 1989. Most of the genets found in

1991 were recovered from several wood discs at different

A diverse Heterobasidion annosum population 188

depths in the stump. Interaction zones at this stump age are

not fully reflecting the distribution of fungal genets. For

example, sectors D and E at the level of disc I (Fig. 4) were

both inhabited by the same genet, seven years after felling.

One possible explanation for this could be that one genet had

invaded and taken over the domain of a second one that

subsequently became excluded from the stump. Support for

this interpretation also comes from a previous investigation

in the same geographical area, indicating that the number of

genets at the stump surfaces is reduced with time (Swedjemark

& Stenlid 1993).

It is interesting to speculate on the origin of the genets that

were only found in the roots and interaction zones away from

the surface of the stumps. Several possibilities exist. One

possible scenario is that all 35 genets established more or less

simultaneously from 70 individual spores with distinct nuclei

at the time of thinning in 1982. Based on dissimilar growth

rates they would subsequently have spread out at different

depths in the stump, possibly also dying back in the older

parts of the mycelium, and by radial expansion covered large

parts of each section. However, theoretically, only 9 different

spores with dissimilar nuclei would be needed to form 35

distinct dikaryotic mycelia. Since mycelia sharing one of their

mating types have previously been reported from the same

stump (Chase & Ullrich 1983), it seems likely that not all

genets have established from two spores, different from all

others. Furthermore, the positioning of some of the genets

away from direct contact with any airborne inocula in the

interaction zone between two other genets is hard to explain

with the 70 spores scenario. The spatial positioning of the 35

genets in the stump and its roots, which are sometimes non-

matching, is also hard to explain from a simultaneous

establishment at the stump surface.

Another possibility is that some of the genets established

from spores had been washed down through the soil and onto

the surface of the roots. Following the dying off of the stump

roots, the spores may have germinated and mycelia established

in the roots. This is a distinct possibility and some authors

have also described viable spores washed through sand (Molin

1957), and successful inoculations of H. annosum spores onto

weakened roots (Kuhlman 1969). However, the root infections

would not explain the higher diversity of genets in the upper

part of the stump or the presence of small distinct genets in

interaction zones.

To get a full understanding of the origin of genets we need

to consider the possibility of multiple mating among

established mycelia and reassortment of nuclei in interaction

zones between somatically incompatible heterokaryons. One

homokaryotic mycelium can, for example, mate with several

other mycelia that establish in its vicinity, thereby creating

different genets that share one of their nuclei. The other

possibility of reassorting nuclei between already established

heterokaryons was proposed by Hansen et al. (1993a) and has

some support from our finding that distinct genets were

detected inside the stump in the interaction zone between two

other genets. Both these possibilities would extend the

distribution of one nucleotype outside the extension of one

genet, and open up novel prospects when defining selection

pressures on a population.

ACKNOWLEDGEMENT

We would like to thank Karin Grip for technical assistance and the Swedish

Council of Forestry and Agricultural Research for financial support.

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Corresponding Editor : D. J. Bond