Variation in growth of Heterobasidion parviporum in a full-sib family of Picea abies

Abstract

Heterobasidion parviporum (Fr.) Niemelä & Korhonen and Heterobasidion annosum (Fr.) Bref. sensu lato are some of the major forest pathogens in the northern hemisphere causing root and butt rot to conifers. The relative susceptibility to H. parviporum was investigated in a full-sib family of Norway spruce [Picea abies (L.) Karst.] by inoculating a set of 252 cloned progenies from a controlled cross. Four ramets of each progeny were used and the 2-year-old rooted cuttings were incubated for 6 weeks under greenhouse conditions. The condition of the cuttings was assessed visually and all the plants were in excellent vigour with no mortality recorded during the experiment. To score the relative susceptibility, lesion length in the inner bark and fungal growth in the sapwood were measured. Among the progenies, significant differences were found for fungal growth in the sapwood (p<0.0005). There was no significant difference for lesion length; however, there was a significant positive correlation between fungal growth and lesion length. The broad-sense heritability was 0.11 for fungal growth. This shows that the genetic component for susceptibility to H. parviporum can be detected even within a full-sib family of Norway spruce and that there is a potential for mapping quantitative trait loci for this trait in Norway spruce.     

Susceptibility to Heterobasidion parviporum in Picea abies clones grown in different environments

Thirty-five Norway spruce, Picea abies, clones from Sweden were tested for resistance to Heterobasidion parviporum. Rooted cuttings of the clones were planted in Italy and Greece and cultivated for two growing seasons before inoculation with H. parviporum. Extent of infection was determined 6 weeks later. The results were compared to those of earlier inoculations in Sweden. Plant growth traits were under strong genetic control in all locations with broad sense heritability estimates between 0.14 and 0.54. Lesion and fungal extension heritabilities were moderate, H² ranged from 0.09 to 0.20, and exhibited rather large genetic variation. There was significant genotypic correlation between Italy and Greece with respect to both lesions and fungal extension. No such correlations were found between Sweden and the two other countries. The lack of repeatability in testing susceptibility is unsatisfactory. It could be explained by C-effects associated with propagation of the host plants. Height growth correlated significantly and positively among all countries.     

Effect of Thinning and Phlebiopsis gigantea Stump Treatment on the Growth of Heterobasidion parviporum Inoculated in Picea abies

The spread of Heterobasidion parviporum Niemelä & Korhonen in roots of Norway spruce was studied in three unthinned first rotation stands of Norway spruce [Picea abies (L.) Karst.] on former agricultural land in south-western Sweden. Heterobasidion parviporum was inoculated at stump height into the trunk of 135 standing trees in a randomized block design. One year after inoculation, two-thirds of the trees were thinned out and one-third was left standing. Half of the stumps left by thinning were treated with spores of Phlebiopsis gigantea (Fr.) Jül and half were left untreated. The spread of H. parviporum was examined both 3 and 5 yrs after inoculation. The rate of spread of H. parviporum and the proportion of infected roots were found to be significantly higher in the root systems of the stumps than in those of the standing trees. Treatment with P. gigantea had no significant effect on the development of H. parviporum in the stumps. There was a tendency 5 yrs after inoculation, however, for a lower proportion of H. parviporum-infected roots in the stumps treated with P. gigantea than in the untreated stumps. In conclusion, thinning of infected Norway spruce was found to increase the rate of spread of H. parviporum in the root systems of the infected trees, which could increase the risk of a rapid build-up of infection in the remaining stand.     

Mycelial growth and exclusion of Heterobasidion parviporum inoculated in branches of 15‐year‐old Picea abies clones

Twigs of 22 clones of 15‐year‐old Picea abies grafts were inoculated with Heterobasidion parviporum in July and in September 2003. Fungal growth varied between clones and exclusion of the pathogen varied significantly among clones inoculated in July. The results indicate that twigs exhibit the same infection pattern as cuttings when inoculated with H. parviporum and that exclusion of the pathogen in twigs is a clone‐dependent character that occurs during the vegetation period.     

Growth rates of Heterobasidion annosum s.s. and H. parviporum in functional sapwood of Pinus sylvestris and Picea abies

Growth rates of H. annosum s.s. and H. parviporum were investigated in the functional sapwood of young Pinus sylvestris and Picea abies plants as an indicator of the relative susceptibilities of the hosts to these pathogens. The stems of 520 five‐year‐old P. abies and 321 four‐year‐old P. sylvestris plants were inoculated and the extent of infection determined 16 weeks later. H. annosum s.s. grew further than H. parviporum in P. sylvestris sapwood, while in P. abies, no differences between the two Heterobasidion spp. were found. Both H. annosum s.s. and H. parviporum spread faster in the sapwood of P. abies than in P. sylvestris. There was high within‐host species variation in growth rates for both P. sylvestris and P. abies suggesting it may be possible to identify tree genotypes with lower susceptibility.     

Infection studies with Heterobasidion annosum on young trees of Picea abies

Infection studies with Heterobasidion annosum were carried out on 15-year-old, cloned spruces between 1971 and 1978. The inoculum was introduced into the sapwood of the test plants at the base of the stem. All inoculations, conducted at different times of the year, were uniformly successful. The pathogen spread through the xylem tissue rapidly during the vegetation period, but from early autumn onwards gradually disappeared over the following two years. After this period, the fungus could no longer be detected.     

New records of Heterobasidion parviporum in China

Twenty‐one basidiocarp specimens of Heterobasidion annosum s.l. were collected in six forest areas in western and central China, from host trees Picea schrenkiana, Abies fabri, Abies fargesii and Larix griffithii. Single‐spore cultures were isolated from the basidiocarps and identified by mating tests. All the specimens proved to belong to the species Heterobasidion parviporum. The results show that this fungus has a wide distribution in China. It seems to be a less aggressive pathogen in China than in Europe, although reliable data on the occurrence of Heterobasidion root rot in coniferous forests of China are so far lacking.     

Stump treatment against Heterobasidion with Phlebiopsis gigantea and some chemicals in Picea abies stands in the western Alps

The effectiveness against Heterobasidion natural airborne infections on Norway spruce stumps was tested for six treatments: aqueous suspension of Phlebiopsis gigantea oidiospores, 10%, 20% and 30% aqueous urea solutions, 4% copper oxychloride aqueous solution, and borax powder. The experiment was carried out in four naturally regenerated forests in the western Alps, each characterized by a different airborne inoculum potential. Within each stand, all treatments, with the exception of urea 10%, were effective and resulted in colonized areas of stumps significantly lower than controls. The effect of ambient spore loads on the stump colonization is discussed.     

Transfer of the P-type of Heterobasidion annosum from old-growth stumps of Picea abies to Picea abies and Larix×eurolepis

The infection of Picea abies and Larix x eurolepis by Heterobasidion annosum was studied in felled trees in Sweden. Thinnings were carried out in two stands of L. x eurolepis, 15 and 20 years old, and in a 25-year-old stand of P. abies, established on a site heavily infected by H. annosum. The 15- and 20-year-old L. x eurolepis stands exhibited the greatest incidence of butt rot with infections amounting to 38 and 57%, respectively, of removed trees. The incidence of butt rot in the P. abies stand was only 5%. Heterobasidion annosum was the main butt rot causing fungus. All isolates of H. annosum were of the P-intersterility group. Transfer of H. annosum from old-growth P. abies stumps to trees felled in the thinning of the next generation was demonstrated by somatic incompatibility tests. However, the majority of infections could not be connected with decay already established in the previous generation. In L. c eurolepis, rot columns were frequent, including also several genotypes in the same stem, and typically positioned in the inner sapwood. The few infections of P. abies were situated in the heartwood.     

Heterobasidion annosum infection of Picea abies following manual or mechanized stump treatment

Heterobasidion annosum (Fr.) Bref. s. l. colonization following thinning was studied in 1246 stumps of Picea abies (L.) Karst. trees from 14 previously unthinned stands in Sweden. Treatments included mechanized and manual application of (1) 35% urea solution, (2) Phlebiopsis gigantea (Fr.) Jül. spores, and (3) 5% solution of disodium octaborate tetrahydrate (DOT), and untreated stumps, cut in the summer and winter. Compared with untreated stumps cut in the summer, all stump treatments and winter cuttings significantly reduced the colonized stump area 6–7 weeks after thinning by 88–99%. Mechanized stump treatment provided as good protection as manual treatment against H. annosum infections. The probability of spore infection (p _ij ) was reduced by 53–83% in mechanized treatment and 79–98% in manual treatment compared with untreated summer thinning. In terms of p _ij , urea had significantly higher control efficacy than P. gigantea and manual treatment performed better than mechanized treatment.     

Infection of roots of Norway spruce (Picea abies) by Heterobasidion annosum

Wounding of excised roots of Norway spruce [Picea abies (L.) Karst.] caused a rapid accumulation of phenolic compounds, decrease of starch content and of certain enzyme activities in the ray cells. Infection of the wounds by Heterobasidion annosum (Fr.) Bref. intensified these processes, caused oxidation of the phenols, and induced activity of acid phosphatase and β-glucosidase in the ray cells of the infected area. The reactions were oxygen-dependent. Intra- and extracellular enzymes were detected in the wood-infecting hyphae. Other wood-growing fungi caused similar reactions in the wood as H. annosum.     

Intraspecific variation in Heterobasidion annosum for growth in sapwood of Picea abies and Pinus sylvestris

Two greenhouse experiments were conducted to study intraspecific variation in growth of the root rot fungus Heterobasidion annosum in living host sapwood. In experiment 1, Scots pine (Pinus sylvestris) and Norway spruce (Picea abies) seedlings were inoculated with H. annosum isolates, 14 each of the S-and P-intersterility groups, collected from various parts of Sweden. In pine, the P-group isolates were more virulent than the S-group isolates both in terms of infection frequency, induced mortality rate (p < 0.05), and fungal growth in sapwood (p < 0.05). In spruce, the P-group isolates were also more virulent on average, but the difference was not statistically significant. Both S and P isolates had a higher infection frequency and a significantly longer sapwood growth on spruce than on pine. The P-group caused higher mortality on pine than on spruce. The length of the lesion in the inner bark was strongly correlated with fungal growth in spruce, but not in pine where the lesions were short or absent. In experiment 2, ten Norway spruce clones were inoculated with 18 S-isolates, originating from nine live-decayed trees and from nine spore-infected stumps in a single Norway spruce stand. The objective was to test whether any selection for growth rate in sapwood was detectable among individuals of H. annosum originating either from stumps or trees. The results gave no support for such selection since no difference in sapwood growth between the two groups of isolates was found.     

Resistance of Picea abies seedlings to infection by Heterobasidion annosum in relation to drought stress

Norway spruce (Picea abies) seedlings, 2–4 years old, were subjected to different degrees of stress. Drought stress affected the predisposition to infection by Heterobasidion annosum in the same way in root wood, stem wood and stem bark. At high water potentials (?3 to ?5 bar) resistance was high, at intermediate levels (- 5 to - 15 bar) it was low but increased again at water potentials below - 8 to - 15 bar. Neither light nor oxygen deficiencies appeared to have adverse effects on resistance. Total length of unsuberized roots was a sensitive indication of strain on the seedlings.     

Terpene response of Picea abies and Abies alba to infection with Heterobasidion s.l.

The monoterpene composition of Picea abies and Abies alba resin was analysed in relation to growth by Heterobasidion spp. Fifteen‐year‐old P. abies and A. alba trees were inoculated on branches with three species of Heterobasidion annosum s.l. After 4 months of incubation, each host was colonized to a significantly greater degree by the pathogen specific to that host (H. parviporum on P. abies, H. abietinum on A. alba) than by the other fungi. Analysis of the enantiomeric monoterpene profiles in the spruce and fir showed that the response in terms of the relative proportions of the monoterpene compounds in the resin differed between tree species. Following challenge with Heterobasidion spp., A. alba trees did not show changes in monoterpene composition in addition to those in the wounding response (increase in (−)‐α‐pinene and (−)‐camphene, and decrease in β‐phellandrene). In P.abies, (−)‐α‐pinene, (+)‐α‐pinene and δ‐3‐carene increased following Heterobasidion attack but not after wounding alone.     

Variation in growth of Heterobasidion annosum among clones of Picea abies incubated for different periods of time

Thirty‐seven 4‐year‐old clones of Picea abies were inoculated with one isolate of the S intersterility group of Heterobasidion annosum in a greenhouse. The dehardened cuttings were organized in three different groups with four to six ramets in each group. All groups were inoculated on the same day shortly after shoot elongation. The groups were sampled for H. annosum growth after 34 (group 1), 83 (group 2) and 182 days (group 3), respectively. Measured parameters were cutting height and diameter, vigour index of the cuttings, infection incidence, mortality rate and fungal growth in the stem. The height of the cuttings was almost constant during the 6 months of incubation, whereas the diameter increased by about 10% during the same period. The proportion of living cuttings containing H. annosum decreased with time (99.5, 93 and 67% infection in groups 1, 2 and 3, respectively) and differed significantly among clones in group 3. Mortality rate increased with time (0.5, 22 and 37% mortality in groups 1, 2 and 3, respectively) and differed significantly among clones in groups 2 and 3; the same clones being most susceptible for both times. Mean fungal growth into the wood was significantly different among groups and among clones within each group. The ranking position for fungal growth was similar in the three groups. The results indicate that frequency of infection success, mortality rate and fungal growth are clone‐dependent factors. Broad sense heritability varied between 0.08 and 0.25 for fungal growth and lesion length at the three incubation periods. Infection success frequency was initially not different among clones but in the longer incubation periods there were significant differences among clones, indicating differences in resistance. Fungal growth in wood differed among separate host clones irrespectively of the length of inoculation period. The vigour of the cuttings seem to influence the length of fungal extension only in the initial stage of the infection.     

Spore deposition of Heterobasidion annosum coll. in Picea abies stands of North Karelia,eastern Finland

Spore deposition of Heterobasidion annosum coll.was measured with the wood disc method in 20 Norway spruce stands in June, July and September 1999 in North Karelia, eastern Finland. The study area crossed the presently known northern boundary of the distribution area of H. annosum (62°45′N). The spore deposition rate decreased northwards and in the northernmost parts of the study area, deposition was detected only in September. On average 71% of the spore deposition consisted of intersterility group P and 29% of intersterility group S. The proportion of S‐type in the deposition increased northwards. Most of the isolated colonies were homokaryons, but the proportion of heterokaryons increased with increasing deposition rate.     

Heterobasidion annosum root rot in Picea abies: Modelling economic outcomes of stump treatment in Scandinavian coniferous forests

Abstract

The economic outcomes of stump treatment against spore infections of the root rot pathogen Heterobasiodion annosum s. l. were analysed based on simulations in four stands typical of Swedish forestry and forest management: (A) Norway spruce [Picea abies (L.) Karst.] stand on former agricultural soil (SI?=?32), (B) Norway spruce stand (SI?=?26) on forest land; (C) Mixed stand of Norway spruce and Scots pine (Pinus sylvestris L.) (SI?=?24) with only H. parviporum present, i.e. no infection of Scots pine and no possibility of interspecies spread of disease between hosts; and (D) same as C, but H. annosum s. str. (Fr.) Bref and H. parviporum Niemelä & Korhonen present, i.e. interspecies spread of disease possible. Models for disease development, growth and yield and cross-cutting were used in the simulations. The simulated decay frequency in Norway spruce trees ranged between 2 and 90%. Stump treatment at the previous final felling and in all thinning operations was profitable at interest rates 1 and 3% in stands A, B and D, but not in stand C. In stand C, no stump treatment at all or treatment in thinnings only gave the highest net future value. Implications for stump treatment in practical forestry are discussed.     

Stilbenes and resin acids in relation to the penetration of Heterobasidion annosum through the bark of Picea abies

Concentrations of the stilbene glucosides astringin and isorhapontin, which ranged from 5 to 50 mg/g fresh weight in Picea abies bark, decreased in response to in vivo infection with the root-rot fungus Heterobasidion annosum. The initial concentration of the stilbene astringin was negatively correlated with the depth of hyphal penetration. Resin acid contents increased following infec-tion, but were not correlated with the depth of hyphal penetration. The spatial distribution of stilbene glucosides in spruce stem, root collar and root bark, and the seasonal variations in con-centration, were estimated.     

Genotypic variation in natural infection frequency of Heterobasidion spp. in a Picea abies clone trial in southern Sweden

Abstract

Natural root and butt rot infection with Heterobasidion spp. was recorded on three occasions in trees from a 20-year-old Norway spruce [Picea abies (L.) Karst.] clone trial. In the first assessment, carried out when the trial had been running for 15 years, 29.5% of the trees felled were infected with Heterobasidion spp., but no statistically significant differences were found between the different clones. In the second assessment, also at 15 years, bore cores were taken from 595 trees. Of these cores, 16.5% were infected, but again no statistically significant differences were found between the different clones. Combining the two first assessments also revealed no significant differences. The discrepancy in rot incidence between the two assessments was explained by the inaccuracy of the bore core method. The third assessment was carried out after the trial had been running for 20 years. At that time, 424 trees of 50 clones were felled and sampled. Visible infection was recorded in 46.5% of the trees. The differences between clones were statistically significant and the broad-sense heritability estimate was 0.18. There were no significant genotypic correlations between tree size and rot infection; this is important for the Norway spruce breeding strategy. Calculations show that economic viability would increase by 0.28 SEK per plant for every 10% decrease in root rot frequency at final felling.     

Optimizing the Management of a Butt-rotted Picea abies Stand Infected by Heterobasidion annosum from the Previous Rotation

There are no instructions on the management of stands of Norway spruce [ Picea abies (L.) Karst.] in which butt rot caused by Heterobasidion annosum coll. (Fr.) Bref. was not discovered until the time of first thinning. A stochastic simulation model describing the spread of butt rot in a stand of Norway spruce was used with a new submodel describing the butt rot of young trees. Non-linear stochastic optimization was used to determine the most profitable management schedule of a young Norway spruce stand with butt rot. If the initial level of butt rot was 5% or 10%, or the stand was thinned in summer with stump treatment, one thinning with a rotation of 55 yrs was optimal. Two winter thinnings with a rotation of 61 yrs was optimal in an initially healthy stand. Optimizations indicated that silvicultural measures that decrease the transfer of H. annosum to next generation at clear-cuttings could be economically fulfilled.