Rosellinia necatrix is responsible for what is sometimes called white root rot, or "pourridié laineux" in Francophone literature. Its infections on poplars has so far been confined to rather limited areas. Nevertheless, since the parasite is common on other arboreous and herbaceous plants - which are possible source of inoculum - and some current trends, mainly concerning cultural practices, could be favourable to it, special measures should thus be taken to prevent its appearance in till now free regions.
1.1.1.1. Symptoms and the damage caused - In poplar growing, substantial attacks by R. necatrix was only reported in intensive plantations under warm-temperate or sub-tropical climates, especially in those placed on soils with a fluctuating water table or which are anyhow conditioned by an irregular supply of water. Young trees until the second year after planting out and mature or senescent trees are most vulnerable, but infection of seedlings and saplings sometimes occurs too.
When saplings are planted out, the parasite is often already present in the soil as a saprophyte, usually as a carry-over on wood residues left when a previous plantation was felled. Infection by such a dense inoculum is highly probable, since the host is in a state of crisis owing to the transplanting and its roots are small, rich in reserve substances and devoid of protective tissues. The most serious effects appear within 3 or 4 years and often result in the apoplectic death of the entire tree.
During a subsequent phase of the plantation, colonisation and degradation of root cortical tissues by the fungus is usually asymptomatic. This stage may last for several years in chronologically intermediate stands in full vegetative vigour, since their trees manage to circumscribe and/or tolerate the infections by forming reaction tissues and putting out new healthy roots near the uninfected areas of the collar.
When a plantation comes to maturity, which is negatively conditioned by the reduced spacing of trees through an increasing competition for nutrients on the part of their extended and interwoven roots, their ability to regenerate tissues diminishes. Therefore, invasion of ever larger parts of the root system makes itself evident in the form of stunted vegetation and increasingly extensive yellowing of large sectors of the crown; leaves eventually wither and fall off. The terminal stage of the disease is marked by the death of the main branches dependent on the infected roots and, not rarely, the entire tree is often killed. This gradual decline as opposed to sudden death, however, is also observed in the case of young trees, especially if they belong to clones with good rhizogenic capabilities enabling them to get through the vulnerable stage after planting out and then conquer the disease, at least in appearance.
These epigeal symptoms are non-specific in themselves; they are similar, for example, to those caused by Armillaria mellea (Vahl: Fr.) Kummer, though this usually attacks senescent plants and in different growing conditions. Infections by R. necatrix almost never proceeds beyond the collar, therefore they can be reliably diagnosed by exposing the hypogeal part and looking for a loose, filamentous and embracing mycelium with sections organised in cords or interrupted by plates; it is whitish at first and turns to brown as the rot proceeds. It is composed of bundles of interwoven cylindrical hyphae with diagnostically significant piriform swellings near septa.
The damage is evidently quantitative, since wood growth is stunted as a result of decline and entire trees are lost in young plantations. In some Indians regions, nursery mortality rates of 10-30% were recently reported, whereas fairly recent estimates in Italy have shown on a local scale mortality of as much as 10%, with a loss of almost 1% of the national production.
1.1.1.2. The pathogen - R. necatrix Prill., long cited as R. necatrix (Hart.) Berl., is a member of the fam. Xylariaceae (ord. Xylariales, phylum Ascomycota) which is able to parasitize hypogeal organs of many herbaceous plants, shrubs and trees, including vine, beet, avocado, various ornamental flowers, broom, elder, walnut, olive, plane, fruit trees, oak, eucalyptus, willow, poplar etc.
Its pathogenic activity on poplars is most marked in Italy, where it has been present for a long time, with an high incidence in areas bounding Po river and near its delta. Here, it was one the main factors that limited poplar growing in the first decades of this century and then, after a period of stasis, in the second half of the 1980s. Considerable attacks have been described during the latest years in Portugal and southern Africa, as well as in India, where are mostly observed in the nursery.
Although all poplar groups are susceptible, certain P. deltoides and P. × euramericana clones seem less affected by infections, not so much because they mount a true resistance reaction as because their tolerance is respectively enhanced by a lower predisposition to water stresses or by a better rhizogenic capacity.
In Italy, other species were occasionally reported on poplar roots in the past, i.e. R. aquila (Fr.: Fr.) De Not. (= Sphaeria aquila Fr.) and R. desmazieresii (Berk. et Br.) Sacc. (= R. quercina Hart.)4, both of negligible importance on Salicaceae. More recent findings are R. corticium (Schw.: Fr.) Sacc. in France (on branches) and R. subsimilis Karst. et Starb. in Switzerland (on P. tremula branches).
1.1.1.3. Biology and predisposing factors - The teleomorph of R. necatrix is very rarely found at the base of dead or totally impaired plants. It is characterised by globose stromata (Ø = 1.2-2.0 mm) rising from a short stipe, at first reddish brown to dark brown and then black at maturity, single or in clumps, which erupt from the host cortical tissues. Stromata are initially covered by a felty or woolly mycelial matrix (subiculum) of a similar colour, but then gradually emerge until they are mostly exposed to the air, whereas the subiculum remains as a basal layer of mycelium. Each stroma has an ostiole and contains a single perithecial ascoma (Ø = 1.0-1.5 mm) that opens in ripening to release brownish, one-celled ellipsoid or fusiform ascospores (35.5-40.5 × 6.1-6.9 µm), which are then dispersed by the wind and by insects.
The anamorph, Dematophora necatrix Hart. (= Graphium desmazieresii Sacc.), is much more frequent since it appears, besides on subicula of the teleomorph, on the surface of infected roots. It is composed of flocky synnematal conidiomata, formed by united brown to reddish hyphae (0.5-1.5 mm long) arising from a common base and with dusty hyaline tips due to the formation of conidiophores. These are divergent, light brown, frequently di- and trichotomously branched, and produce light brown globose or ellipsoid conidia (3-5 × 2.5-3 µm).
Propagation of the fungus in poplar plantations, however, seems less dependent on ascospores and conidia than on mycelial fragments installed on woody or herbaceous plant residues, and than on the mycelial cords (similar to true rhizomorphs5) that run through the soil from the inoculum sources to susceptible hosts. This usually occurs in spring and autumn, when adequate precipitations and ideal temperatures allow the fungus to spread vigorously as a saprophyte, while its dispersion may be further assisted by local flooding, since the mycelium attached to infected debris can survive for several weeks in running water.
Penetration into the host requires breaches in the bark, which are however numerous in the lower part of the trunk and on the delicate root system of recently outplanted saplings, rich in parenchyma and devoid of protective tissues. The main root near the collar and the more superficial lateral ones are usually the first to be attacked, then the deeper sectors too are gradually involved. When the infection is established, further colonisation is favoured by debilitation of the host, which in warm-temperate areas has often already been caused by a lack of water and sometimes aggravated by epidemics of Marssonina brunnea, a leaf pathogen very active in the summer (see § 1.4.2).
This ability of R. necatrix to propagate as a saphrophyte in wet periods and to invade trees as a parasite in dry periods makes it very insidious when poplars are grown on marginal lands, with coarse soil and a fluctuating water table and often situated near a watercourse, while its remarkable ability of passive survival in adverse conditions is sometimes aided by the organisation of its mycelium into roundish (Ø = 3-4 mm), brown-blackish sclerotia.
1.1.1.4. Control strategies - As in the case of all broadly polyphagous facultative parasites, ad hoc genetic selection of poplar clones resistant to R. necatrix is impracticable. Nevertheless, it is possible to look for genotypes endowed with a rhizogenic capacity enabling them to tolerate the presence of root rot during the critical post-transplant stage, when the death of plants is more likely.
Priority, however, must be assigned to the adoption of cultivation practices that minimise the probability of attacks, which would not only damage the current plantation, but also those in the future in a dangerous cumulative fashion, since the parasite can survive on the wood debris left on the ground. Since it is not economically feasible to remove all the roots when a plantation is felled, it is right at least to grub up the stumps and take them away without shredding them on the spot, as is often done today in many cultivation districts. As many as possible of the wood residues should also be brought to the surface so that the dry air can impair the survival of the parasite, and the soil should be treated with ammoniacal nitrogen to speed up their biodegradation. Before beginning a new production cycle, the soil needs to be left free from poplars through at least one or two years; in the meanwhile, it is advisable to grow herbaceous plants, e.g. maize, which help in decomposing the biological substrate of R. necatrix if they are appropriately fertilised with nitrogen. This cultivation system considerably reduces the aggressiveness of the parasite, though it extends the woody production cycle. The new plantation should be composed of clones with a good epigeal/hypogeal growth ratio, which react to R. necatrix more strongly. During the cultivation, stressful situations, such as overcrowding, water shortages and leaf diseases, must also be avoided as far as possible, both in the field and obviously in the establishment of a new nursery.
Attempts to treat an already clear attack almost always fail and are only truly beneficial in young plantations, in the case that the distribution of rots is still limited. The most infected trees can be uprooted and the roots of the others can be partly bared to expose the fungus to an unfavourable environment. The initial infection sources can be extinguished by spraying the ground with benomyl suspensions (50 g/plant a.i.) or triforine suspensions (30 g/plant a.i.), in either one or two treatments.
Biological control has nothing concrete to offer at the moment.
R. necatrix is the only root rot agent capable of attacking young intensive poplar plantations and impairing the growth and often the survival of plants for much of the cultivation period. Other root parasites are mostly sporadic, though sometimes are endemic in limited regions. They appear in nurseries, plantations, quick-rotation coppices and natural formations; in the last three cases, however, they only infect mature or senescent trees ready for felling and rarely cause substantial damage.
1.1.2.1. Root and butt rots caused by Armillaria spp. - The genus Armillaria (Fr.: Fr.) Staude (fam. Tricholomataceae, ord. Agaricales, class Basidiomycetes) includes several species variously pathogenic for herbaceous plants and both conifers and broad-leaved trees.
The most widespread and most pathogenic agent is A. mellea (Vahl: Fr.) Kummer, long cited as A. mellea (Vahl) Quél. [= Armillariella mellea (Vahl: Fr.) Karst. = Clitocybe mellea Vahl], a parasite of prime importance on vines, fruit trees and numerous forest broad-leaved trees growing in many parts of the world. In Europe, its distribution can be called Atlantic-Mediterranean, since it is not found beyond Denmark to the north and increases in frequency in areas influenced by the Atlantic ocean and even more so in those influenced by the Mediterranean sea, whereas it is rare in Central and Eastern Europe under continental climates, though it was observed in Georgia and southern Russia. The fungus was also found in Syria and North Africa, and there are reports from the tropical Africa too (Kenya, Tanzania, Zaire). In North America, it is confined to the U.S.A., where is found on both the western (California) and the eastern side, while it becomes less frequent in the interior.
Its areale, that is fairly thermophilous, and its predilection for compact, fundamentally asphyxiating soils partly explain its limited incidence on genus Populus utilised in intensive plantations, which are characterised by a short cycle and in preference grow on loose and well-aired soils. Both in natural and natural-like forests its presence on over-mature plants, or on those weakened by adverse environmental conditions, is more common, although always sporadic. In Europe, Euramerican poplars close to maturity are sometimes attacked in some parts of France as well as in the centre and south of Italy, always on soils conditioned by water stagnation.
Although the epigeal symptoms are similar to those caused by R. necatrix (decline of sectors of the crown, stunted vegetation etc.), examination of the lower part of the trunk and of the roots next to the collar enables A. mellea to be identified from the presence of crimson, palmate, subcortical mycelial plates, often accompanied by typical flat black rhizomorphs (2-8 mm wide). The parasite can also climb up under bark tissues of the trunk to more than a metre from the collar, as well as penetrate the wood via the medullary rays causing fibrous decay. The typical fruiting bodies (basidiomata) of the fungus can form at the base of the most debilitated plants. They have a honey-yellow to brownish pileus (cap) (Ø = 3-10 cm), sprinkled with small transient scales that become fewer towards the edge, and with many lamellae (gills), whitish at first then reddish at maturity, decurrent along the stipe (stalk); this is fibrous, circular (Ø = 1-3 cm), 5-12 cm long and darker in its lower part, characterised by an armilla (ring) with yellowish stripes on its under surface.
The hyaline, ellipsoid basidiospores (7-10 × 5-7 µm) are of little account in the propagation of the fungus, which is mainly entrusted to root-to-root contacts with neighbouring plants and to the possibility of vegetating in the soil through the colonisation of organic debris. In the case of A. mellea, which is more pathogenic than saprophytic, rhizomorphs running in the soil have a limited growth capacity and hence are of little consequence as propagation and/or resistance organs; they are primarily active structures for the infection of roots not too distant from the starting substrate. Since it is a weakness parasite, albeit endowed with considerable pathogenic potential, A. mellea afflicts plants suffering from some form of stress. In poplar growing, this stress is generated by the excessive reciprocal competition for nutrients in crowded mature plantations and by recurrent leaf diseases.
As regards other Armillariae on poplars, in Europe the sole A. gallica Marx. et Romagn. [= A. bulbosa (Barla) Kile] was very sporadically reported in the United Kingdom and France, but it is generally much less pathogenic.
Some species have been found in association with dead or greatly debilitated plants in the north-eastern U.S.A., though the extent to which each of them is really parasite or saprophyte is still uncertain. A. ostoyae (Romagn.) Herink [= A. obscura (Schaeffer) Herink], which primarily attacks conifers, has been found on trees and suckers of P. tremuloides and P. grandidentata Michx., where it is thought to be an active root rot agent. A. gallica, probably as a secondary parasite or saprophyte, and A. sinapina Bérubé et Dessur., a species with greater pathogenicity, were also found on the aforesaid hosts. A. nabsnona Volk et Burdsall ranges from California to British Columbia and Alaska; it is a recently established species that was reported on P. trichocarpa T. et G.
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Mention can also be made of other sporadic root rot agents on poplars:
- Heterobasidion annosum (Fr.: Fr.) Bref. [= Fomes annosus (Fr.) Cke.; fam. Coriolaceae, ord. Poriales, class Basidiomycetes] parasite of primary importance on conifers, which was also found on declined P. tremula stands in Scandinavia and Poland;
- Ganoderma lipsiense (Batsch.) Atk. [= G. applanatum (Pers.: Wallr.) Pat.; fam. Ganodermataceae, ord. Ganodermatales, class Basidiomycetes], a common pathogen on various forest plants and often found on tree-lined avenues; in the Rocky Mountains, it is sometimes responsible for root decay in P. tremuloides, and infected trees are likely to be blown down by the wind;
- Botryodiplodia palmarum (Cke.) Petr., a mitosporic fungus responsible for so-called "set rot" in nurseries of P. yunnanensis Dode, P. ciliata Royle, P. deltoides and P. × euramericana in some regions of India, which sometimes reaches incidences of the order of 20-50%; the syndrome is also observable in 1-2 year-old plantations associated with sugar cane.
4 R. amphisphaerioides Sacc. et Speg. was also found on poplar roots in Italy, but afterwards it was excluded from genus Rosellinia De Not. and renamed Amphisphaerella dispersella (Nyl.) O. Eriks. [= A. amphisphaerioides (Sacc. et Speg.) Kirschst].
5 The term "rhizomorph" refers to an agglomeration of hyphae, often divided into a rigid outer layer of small dark cells and a central part with elongated hyaline cells, with structure resembling that of a root and with a distinct apical growth zone.
