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1.4. Diseases of leaves and young shoots

1.4.1. Rusts caused by Melampsora spp.

Leaf parasite fungi belonging to genus Melampsora Cast., now recognised as the only member of the fam. Melampsoraceae (ord. Uredinales, class Teliomycetes, phylum Basidiomycota), are solely responsible for all poplar rusts.

Over the last twenty years, the leaf diseases known as rusts have been increasingly limiting poplar culture in countries such as Belgium, France and Italy, where it has long been established, and have hampered its further expansion in those where it has been recently introduced, such as Australia, New Zealand, southern Africa and Argentina. At the world level, they are one of the poplar's main enemies and as such cannot be overlooked by the researcher in his selection of clones and choice of control strategies, nor by the grower in the establishment and management of his plantations.

1.4.1.1. Symptoms and the damage caused - The presence of a rust agent is solely determined by the extent to which its host is genetically susceptible.

This description of rust symptoms mostly refer to intensively cultivated black and hybrid poplars belonging to the Aigeiros section but, with some variations, they are equally applicable to most rusts infesting poplars of the other sections.

First attacks in the plantation take place from early to late summer, depending on the geographic region, and a little earlier in the nursery, where its beginning is accelerated by high humidity and crowding of the saplings.

On susceptible plants, the first signs are minute roundish chlorotic spots with indistinct edges, randomly spread over the leaf abaxial side, which gradually become more evident and circumscribed while others continue to appear. After 2-3 days, the more developed spots give rise to small yellow to orange pustules (depending on the agent involved), that over the course of a few hours grow into irregular shapes after lacerating the leaf cuticle. These powdery formations, called uredinia, represent one of the anamorphs of the pathogen and are composed of masses of urediniospores, which are able to reinfect distant plants since they are readily dispersed by light breezes and, probably, also by the bodies of some insects. Very young and very old leaves are less susceptible than those of middle age, therefore uredinia are usually first noted at a certain distance from the apical leaflets, and then spread to the leaves close to them. As the growing season proceeds, repeated infections on the same plants result in thick uredinia over most leaves, which are thus sprinkled with a fine yellowish-orange powder that is the typical symptom of the disease.

In this stage, extensive portions of the leaf blade parch, owing to the confluence of the small necrotic areas around uredinia, or show conspicuous yellowing. This helps in sharpening the distress of the plant, which is also caused by excessive transpiration via the lacerated leaf cuticle and by a general weakness due to consumption of nutrients by the parasite. Precocious defoliation during the summer weakens the shoots and makes them unable to withstand the rigours of winter. It has also been shown that the marked decline exposes the hosts to attacks of weakness parasites in the following year, especially on the part of the bark pathogen Discosporium populeum.

In autumn, on the portions of the axial and/or abaxial side - depending on the species of Melampsora - of the senescent or already fallen leaves originally occupied by the uredinia, irregular blackish crusts (up to 1 mm), named telia, develop and remain in the litter throughout the winter. Telia, which secure the survival of the parasite till the next growing season, are seen as the teleomorph of rust agents.

Such heavy levels of attacks are mostly encountered in nurseries, where the tips of the saplings may even die, and quantitative damage in terms of impaired growth may thus be converted into total loss of the production because it is not up to commercial standards. In plantations - except the thick mini-rotations for the production of biomass in semiarid areas (such as the Near East) - the disease rarely proceeds further than moderate defoliation, because the microclimatic conditions are less favourable and leaf formation slows down in the height of summer. Even so, the cumulative effect of attacks during several growing seasons may lead to a substantial loss of woody growth and predisposition to drought stress, due to insufficient root development.

1.4.1.2. Life cycle - The Melampsorae are obligate parasites that draw nutrients from live plant tissues in every stage of their life cycle. This includes several types of anamorphs and spores, each with a well-defined reproductive role, and also requires for its completion the passage of some stages on other hosts, named secondary hosts, which may be arboreal or herbaceous depending on the rust species and are not taxonomically related to Populus.

Briefly, a typical life cycle develops as follow. Telia, that form in the autumn on senescent and fallen leaves, are aggregations of elongated spores, arranged like a palisade and known as teliospores, which remain dormant during the winter. In spring, when suitable conditions of temperature and humidity take place, each teliospore emits a short germ tube on which basidiospores, derived from the conclusion of the sexual process, are formed. Basidiospores cannot reinfect the poplar, but need to pass to a secondary host and infect its green tissues. The first, not every evident, anamorph fructifications, called spermogonia or pycnia, appear about ten days later; their task is to produce tiny gamete-like propagules, called spermatia, in a sticky sugar-rich substance, and to capture, by means of receptive hyphae, spermatia of the opposite mating type brought by raindrops and some insects from other pycnia. The true fecundation takes place at the base of the pycnia and leads to the formation of a second type of anamorph fructifications , the aecia. These elongated, yellowish, powdery masses, that burst out of the cuticle of herbaceous tissues or of needles (in case the host is a conifer), are long chains of aeciospores, which are easily airborne and have a durable viability. Aeciospores are able to reinfect poplar, i.e. the primary host, through entering leaf stomata. Uredinia are then formed on the leaf abaxial side throughout the remainder of the growing season, owing to the production of at least two or three urediniospore generations. In autumn, the overwintering telia differentiate on senescent or fallen leaves.

Teliospores are of great biological significance, since they are the scene of the conclusion of the sexual process, i.e. the modifications of the genetic complement that will be transmitted to basidiospores and perpetuated through the next cycle.

In many areas both in and outside Europe, some poplar Melampsorae resume their production of urediniospores in the next vegetative season without passing to the secondary host, because they overwinter either as mycelia close to the dormant buds or, in small percentage and in places where the winter is not too cold, as urediniospores that remain attached to the dry fallen leaves. When designing a plantation, a grower must none the less have a sufficient knowledge of the secondary hosts and of their proximity to the land he intends to use, since their presence favours genetic recombination of the parasite, which can only take place if its cycle is completed, and hence the probable propagation of new pathogenic strains.

1.4.1.3. The pathogens - Many Melampsora species, whose taxonomy is the subject of current discussion, can infect Populus (Table 3), though only a few are of phytopathological significance. Rusts on black and hybrid poplars belonging to the Aigeiros section (P. nigra, P. deltoides, P. euramericana) are of prime concern on account of the economic damage they are now causing to intensive cultivations on the world scale as well as of the risk associated, even in the short term, with their proven genetic dynamism, which raises serious strategic problems for the selector of clones. Three species, with different degrees of aggressiveness against currently employed clones, are responsible: M. allii-populina Kleb., M. larici-populina Kleb. and M. medusae Thm.

M. allii-populina is relatively thermophilous and covers a large areale that once extended from northern Africa to western Asia and much of south-central Europe, but now embraces southern Africa as well. It produces telia on the leaf abaxial side and uredinia usually dark orange. Even though it can perpetuate infections on poplar (paracycle), it completes its life cycle on herbaceous plants of the Allium L., Arum L. and Muscari Mill. genera. Two formae speciales were recently stated: f. sp. allii-populina, pathogenic on various Allium and Arum species, and f. sp. muscaridis-populina Vien., found solely on M. comosum (L.) Mill.

M. larici-populina is probably the most cosmopolitan, since it occurs wherever poplars are grown. Initially confined to Eurasia, it spread to South Africa, Australia and New Zealand in the 1970s and to Washington, Oregon and California over the last ten years; it was also reported in Argentina. In the latest years, it is responsible for repeated epidemics on European and Australian intensive cultivations of Aigeiros species, and has also been observed both in the U.S.A. and Europe on species from other sections, e.g. P. trichocarpa or P. interamericana, which are widely planted in regions of the northern hemisphere under continental climates. In addition to producing its telia on the leaf adaxial side, it is distinguishable from M. allii-populina through some microscopic characters (Table 4). Its secondary hosts are some larch species, though in the U.S.A. it was recently found on Pinus ponderosa and P. contorta too; like M. allii-populina, it can perpetuate on poplar in the uredinial stage.

M. medusae, original of North America, is now widespread in Argentina, South Africa, India, Japan, south-eastern Australia and New Zealand too, whereas in Europe it is currently confined to Spain, Portugal and south-western France. By contrast with the aforesaid species, it needs to complete its life cycle on secondary hosts, these being almost solely North American species of Pinus, Larix, Pseudotsuga, Tsuga, Abies and Picea. Morphological, biological and epidemiological identities led to the synonymy of M. albertensis Arth. and, according to the latest interpretations, of M. abietis-canadensis (Farl.) C.A. Ludwig with M. medusae. In addition to Aigeiros poplars, where it is active as f. sp. deltoidae Shain, it is able to infect P. tremuloides and P. grandidentata (as f. sp. tremuloidae Shain) as well as several Tacamahaca poplars and intersectional hybrids (e.g. P. interamericana). M. medusae produces its telia both on the leaf adaxial and abaxial side.

Mention may also be made of M. medusae-populina Spiers, a new species recently discovered on black poplars in New Zealand, with a middle morphology between M. medusae and M. larici-populina.

M. occidentalis Jacks., a species currently confined to the U.S.A. and Canada, is very morphologically and symptomatologically similar to M. larici-populina, but it has a much broader spectrum of secondary hosts. Its phyopathological importance, however, is negligible.

Leuce poplars are not often cultivated intensively and hence their rusts are of minor economic significance. In Europe, the main species found on Albidae and Trepidae are M. pinitorqua Rostr., M. larici-tremulae Kleb. and M. rostrupii Wagn. Some authors still refer to them as the M. populnea complex on account of their similar characters and the same primary hosts (P. alba, P.tremula, P. canescens).

In north-central China, M. rostrupii and M. magnusiana Wagn.8 are responsible for heavy nursery losses, especially at the expense of P. tomentosa Carr.

1.4.1.4. Relations with the host - Like all the rust agents, the Melampsorae are obligate parasites of living tissues; therefore, they do not kill the cells they colonise, but absorb some of their substances, particularly certain sugars and aminoacids. The parasitic association is very complex, and the extremely specific compatibility between the parasite and the host stems from reciprocal recognition on the part of the former's genetic sequences and their complementary sequences of the latter. This recognition underlies the existence of what are known as physiologic races, differing solely in their range of susceptible clones but morphologically identical, which are responsible for the recent increase in Europe of the severity and spread of attacks by M. larici-populina, now virulent on previously resistant clones. Five races have been reported in about ten years, while the presence of others is suspected, even in places such as the western U.S.A., where the parasite has only spread recently. M. allii-populina and M. medusae too seem involved by this phenomenon, whereas in this connection little is known of rust agents reported on the other poplar sections, one reason being their minor economic importance.

1.4.1.5. Control strategies - A balanced, effective protection against Melampsorae, as far as possible, must be primarily sought through quarantining and the search for resistant clones and, subordinately, through growing practices and a limited use of fungicides.

A close check must be kept on the international exchange of plant materials, since the recent spread of various rust agents to new regions has been partly due to ill-advised importations. Nevertheless, these provisions are not absolutely reliable, since independent dispersion of rust fungi over long distances is always possible.

Satisfactory short-term results can be obtained through the selection of resistant or tolerant clones capable of withstanding other adversities, adaptable to various environments and sufficiently productive. For example, many P. deltoides clones are resistant to M. larici-populina and M. allii-populina, whereas in P. euramericana different reactions are showed according to the various genotypes. Unfortunately, in the long term the emergence of new physiologic races, able to attack clones previously shown to be resistant, may well stultify the selector's efforts (e.g. M. larici-populina race E3 to the detriment of "Luisa Avanzo" Euramerican clone).

Appropriate growing practices are thus indispensable, especially in nurseries and mini-rotations for the production of biomass. They range from eradication of the secondary hosts (sound practice for M. allii-populina) in areas near the plantation, to covering of propagule-bearing leaf residues with earth to a sufficient spacing of cuttings to reduce the excessive dampness of the microclimate.

In epidemic areas, the aforesaid practices can be integrated with fungicides treatments at fortnightly intervals from the appearance of the first uredinia, though not more than 2-3 times in a single growing season. Good experimental results were achieved with suspensions containing organic nitrogen compounds, benzimidazoles and ergosterol biosynthesis inhibitors; myclobutanyl, triadimenol, tebuconazole and cyproconazole are among the most effective active principles.

Biological control through the use of micro-organisms naturally present on poplar leaves also furnished interesting experimental results. Cladosporium Link spp., Alternaria alternata (Fr.) Keissler, Sphaerellopsis filum (Biv.-Bern.: Fr.) Sutton etc. demonstrated a certain ability to inhibit the sporulation of rusts.

Table 3 - Melampsora species found on Populus, their distribution and their poplar and secondary hosts (in bold character the currently recognised species).

species

distribution

poplar hosts

secondary hosts

M. larici-populina Kleb.
[= M. cylindrica (Str.) Rostr.]

Europe
Asia
South Africa
U.S.A
South America
Australia
New Zealand

sec. Aigeiros Duby:
P. nigra L.
P. deltoides Bartr.
P. fremontii S. Watson
P. euramericana (Dode) Guinier

sec. Tacamahaca Spach:
P. maximowiczii A. Henry
P. ciliata Royle
P. koreana Rehder
P. laurifolia Ledebour
P. suaveolens Fischer
P. simonii Carr.
P. trichocarpa T. et G.
P. interamericana Broek.
P. angustifolia James
P. balsamifera L.

sec. Leucoides Spach:
P. lasiocarpa Oliv.
P. wilsonii Schneider

Larix decidua Mill.
L. gmelini Litv.
L. kaempferi (Lamb.) Carr.
L. occidentalis Nutt.
L. laricina (DuRoi) K. Koch
L. sibirica Led.
Pinus ponderosa Laws.
Pinus contorta Dougl.

M. medusae Thm.
[= M. albertensis Arth.
= M. abietis-canadensis (Farl.) C.A. Ludwig]

Argentina
North America
South Africa
India, Japan
Australia
New Zealand
Spain, Portugal
France

sec. Aigeiros:
P. nigra
P. deltoides
P. euramericana

sec. Tacamahaca:
P. maximowiczii
P. simonii
P. trichocarpa
P. interamericana

sec. Populus Ecken.:
P. tremuloides Michx.
P. grandidentata Michx.

Abies canadensis Michx.
A. concolor Hoopes
A. grandis (Dougl.) Lindl.
A. lasiocarpa (Hook) Nutt.
Larix decidua
L. kaempferi
L. occidentalis
L. laricina
Picea sitkensis (Bong.) Carr.
Pseudotsuga menziesii (Mirb.) Franco
P. taxifolia (Lamb.) Britt.
Tsuga canadensis (L.) Carr.
T. mertensiana (Bong.) Carr.
Pinus banksiana Lamb.
Pinus ponderosa
Pinus contorta
Pinus lambertiana Dougl.
Pinus radiata Don
Pinus sylvestris L.

M. medusae-populina Spiers

New Zealand
Australia?

P. deltoides P. yunnanensis
P. deltoides P. nigra

Larix decidua?

M. allii-populina Kleb.

southern Europe
Russia
northern Africa
southern Africa

sec. Aigeiros:
P. nigra
P. deltoides
P. fremontii
P. euramericana

sec. Tacamahaca
:

P. maximowiczii
P. laurifolia
P. suaveolens
P. trichocarpa
P. balsamifera

sec. Populus
:
P. tremula L.

Allium cepa L.
A. ascalonicum L.
A. carinatum L.
A. oleraceum L.
A. sativum L.
A. schoenoprasum L.
A. sphaerocephalum L.
A. ursinum L.
A. vineale L.
Arum maculatum L.
Arum orientale M.B.
Muscari comosum (L.) Mill.

M. larici-tremulae Kleb. (= M. laricis Hart.)

Europe
ex-U.S.S.R.
Japan
U.S.A.

sec. Tacamahaca:
P. balsamifera

sec. Populus :
P. tremula
P. alba
P. canescens (Ait.) Sm.
P. davidiana (Dode) Schn.
P. tomentosa Carr.

L. decidua
L. kaempferi
L. sibirica

M. magnusiana Wagn. (= M. klebahni Bub.)

Norway
eastern Europe
ex-U.S.S.R.
Korea, China
Japan
Canada, U.S.A.

sec. Aigeiros:
P. nigra

sec. Tacamahaca
:
P. suaveolens
P. trichocarpa

sec. Populus
:
P. alba
P. tremula
P. canescens
P. grandidentata
P. davidiana
P. sieboldii
P. tomentosa

Chelidonium majus L.
Corydalis ambigua
Ch. et Schl.
C. bracteata L.
C. bulbosa D.C.
C. cava (Mill.) Schw. et K.
C. digitata Pers.
C. fabacea Pers.
C. laxa Fr.
C. nobilis (L.) Pers.
C. pumila (Host.) Rchb.
C. remota Fisch.
C. solida (L.) Sw.
Fumaria officinalis L.
Papaver dubium L.

M. pinitorqua Rostr. (= M. pruinosae Tranz.)

Europe
ex-U.S.S.R.
Japan

sec. Tacamahaca:
P. balsamifera

sec. Populus :
P. alba
P. tremula
P. canescens

sec. Turanga Bunge
:

P. pruinosa Schrenk

Pinus sylvestris
Pinus pinaster Ait.
Pinus pinea L.
Pinus halepensis Mill.
Pinus mugo Turra
Pinus nigra Arn.
Pinus laricio Poiret
Pinus ponderosa

M. rostrupii Wagn.
[= M. pulcherrima Maire = M. aecidioides (D.C.) Schroet.]

Europe
ex-U.S.S.R.
India, China
U.S.A

sec. Aigeiros:
P. nigra

sec. Tacamahaca:
P. balsamifera

sec. Populus
:
P. alba
P. tremula
P. canescens
P. tomentosa

sec. Turanga
:
P. euphratica Oliv.

Mercurialis perennis L.
M. annua L.

M. osmaniensis Bagyan. et Ram.

Germany

P. sieboldii Miq.

?

M. microspora Tranz. et Eremeeva

ex-U.S.S.R.
Iran

P. nigra

?

M. ciliata Barcl.

India

P. ciliata

?

M. abietis-populi Imai

Japan

sec. Aigeiros:
P. nigra
P. euramericana

sec. Tacamahaca:
P. maximowiczii
P. koreana
P. simonii

Abies firma Sieb. et Zucc.
A. homolepis Sieb. et Zucc.
A. sachalinensis Mast.
A. veitchii Lindl.

M. occidentalis Jacks.

U.S.A.
Canada

sec. Aigeiros:
P. nigra
P. fremontii

sec. Tacamahaca:
P. trichocarpa
P. angustifolia
P. balsamifera

sec. Populus :
P. alba

Abies concolor
Larix kaempferi
L. occidentalis
Picea sitkensis
Pseudotsuga menziesii
Pinus ponderosa
Pinus contorta
Pinus lambertiana
Pinus radiata
Pinus monticola Dougl.

M. cumminsii Bagyan. et Ram.

U.S.A

Populus sp.

?

Table 4 - Macroscopic and microscopic characters of uredinial and telial stages of the most important Melampsorae found on intensive poplar cultivations (in bold the characters of diagnostic value for similar species).

species

uredinia

urediniospores

telia

teliospores

M. larici-populina

- hypophyllous

- subepidermal

- yellow to orange-yellow

- 0.5-1 mm

- paraphyses clavate to capitate (80 15-20 m), apically thickened

- ellipsoid or oblong

- 30-50 15-22 m

- spore wall equatorially thickened up to 7 m

- apex not echinulate

- epiphyllous

- subepidermal

- blackish-brown

- aggregated in small groups

- up to 1 mm

- prismatic, rounded at both ends

- 40-70 6-10 m

- apically thickened up to 3 m

- brown

M. medusae

- mostly hypophyllous

- subepidermal

- yellow to orange-yellow

- 0.3-0.5 mm

- paraphyses capitate (65 13-25 m)

- ovate to ellipsoid

- 23-35 15-23 m

- spore wall equatorially thickened up to 10 m

- equatorial zone not echinulate

- amphigenous

- subepidermal

- reddish-brown

- scattered or aggregated

- up to 0.5 mm

- prismatic

- 20-45 10-15 m

- cinnamon brown

M. medusae-populina

- mostly hypophyllous

- subepidermal

- yellow to orange-yellow

- 0.15-0.5 mm

- paraphyses clavate to capitate (18-50 8-16 m), apically thickened

- clavate to broadly ellipsoid to ovate

- 25-50 12-25 m

- spore wall equatorially thickened up to 10 m

- not echinulate areas on or near the apex and around the centre

- mostly epiphyllous

- subepidermal

- blackish-brown

- often aggregated

- up to 1 mm

- prismatic

- 20-50 6-16 m

- light brown

M. allii-populina

- mostly hypophyllous

- subepidermal

- orange to red-orange

- about 1 mm

- paraphyses capitate (50-60 16-20 m)

- elongated, ellipsoid to ovate

- 28-40 15-20 m

- spore wall not equatorially thickened

- apex not echinulate

- mostly hypophyllous

- subepidermal

- dark brown

- often aggregated

- 0.2-1 mm

- prismatic, rounded at both ends

- 35-60 6-12 m

- light brown

1.4.2. Leaf spots caused by Marssonina spp.

The form-genus Marssonina Magnus include the anamorphs of those agents of pathological phylloptoses whose teleomorphs - in the case of poplar pathogens - are ascribed to Drepanopeziza (Kleb.) Hhn. (fam. Dermateaceae, ord. Leotiales, phylum Ascomycota).

With regard to M. brunnea, their most important pathogen, these phylloptoses offer an illuminating example, dramatic for the poplar growers, of how the absence of phytosanitary checks on exchanged plant material can be the initial cause of severe epidemics affecting entire continents, Europe in the case in point, caused by parasites existing in a relative phytopathological equilibrium in their original areale.

1.4.2.1. Symptoms and the damage caused - The Marssoninae are able to attack healthy plants. Symptoms vary in function of the parasite species and the host.

On Aigeiros poplars, M. brunnea, by contrast with the Melampsorae, is mainly active in plantations and preferably attacks young leaves and shoots still in the herbaceous state. Leaves starting from the stage of development just prior to extension and for about 10 days are particularly receptive, whereas a refractivity to infection hardens as the tissues mature; nevertheless, senescent leaves reacquire a certain degree of susceptibility, especially in late summer. In spring, brownish spots ( _ 1-2 mm), paler in the centre, appear on both sides of the leaf, scattered at first, but soon confluent owing to their thickening. The surrounding leaf tissues turns yellow, then brown, thus leaves as a whole acquire a bronzed appearance that is typical of the disease and usually the prelude to their early falling off. On vascular bundles, petioles and other green parts of the plant (vegetative tips, current year branchlets, inflorescences and then infructescences), similar spots - though a little larger and elongated - now appear, within which the parasite produces a large number of conidia inside fruiting bodies known as acervular conidiomata, that are visible to the naked eye as whitish waxy lumps. As already stated, the main attacks occur in plantations where, starting from the lowest branches, the typical bronzing of the foliage is soon followed by a more or less marked early phylloptosis, though the apical portion of the foliage is spared. Appearance of the disease in the nursery is less common, especially in the first year.

M. tremulae, now more correctly transferred to M. brunnea f. sp. trepidae, is responsible for similar symptoms on P. tremula and P. tremuloides. Rather larger brownish spots ( = 2-3 mm) appear, usually on the leaf abaxial side, and then join together to cause large tissue necrosis. However, the ensuing phylloptosis is usually rather late and confined to the lower branches and the suckers.

The syndrome caused by M. populi takes the form of much larger roundish spots ( _ 4-5 mm), mainly on the leaf adaxial side, with an outline that is distinct on the Euramerican hybrids, frayed on P. nigra. These blotches extend over much of the leaf through confluence, whereas large lozenge-shaped lesions appear on the still green shoots. The attacks of this species are almost never of any epidemiological importance.

M. castagnei causes spots on P. alba that are similar in size to those induced by M. populi, though their edges are never frayed. These too are usually found on the leaf adaxial side, since their appearance is hindered on the abaxial side by its thick tomentum. With a shape that is often irregular, they are greyish-white in the centre and, at a certain stage, sprinkled with tiny waxy protuberances, i.e. the fruiting bodies of the parasite. On the petiole smaller spots elongated in the direction of its axis often appear, whereas traces of infections are rare on shoots. The disease causes marked yellowing, especially of the lower branches, followed by early phylloptosis.

Repeated attacks by M. brunnea on intensively cultivated sensitive Euramerican clones lead to gradual impairment of their annual wood production, and also make them predisposed to infections by weakness parasites, agents of bark necroses, and to the so-called "brown spots" coming from physiological stresses. Death of the trees belonging to the more susceptible clones is exceptionally reported.

1.4.2.2. The pathogens - According to the latest taxonomic revision, Populus is attacked by four Marssonina species, differing in their natural hosts and in some features of their conidia (Table 5).

M. brunnea (Ell. et Ev.) P. Magn. (= M. populicola Miura) is by far the most important in both phytopathological and economic terms. Of little consequence until the end of the 1950s and endemic in well-delimited areas of the U.S.A., it since spread first to Japan, then to Italy and most of the rest of Europe, where it caused ruinous epidemics on plantations still in full expansion, and subsequently to other Asian countries, New Zealand (1976) and Argentina (1990). Today it is present with varying degrees of incidence wherever poplars are grown, with the sole exception of Africa. Spiers (1984) recently distinguished two formae speciales with different hosts: f. sp. brunnea, which attacks P. nigra, P. deltoides and above all P. euramericana, but not P. tremula and P. tremuloides; f. sp. trepidae Spiers (= M. tremulae Kleb.), which is only pathogenic on the last two species. Even so, f. sp. brunnea is also able to infect members of the Tacamahaca section (P. trichocarpa, P. simonii Carr.) and the intersectional hybrid P. interamericana (north-western U.S.A.). According to what was stated for the anamorph, Spiers & Hopcroft (1998) for reasons of precedence transferred to Drepanopeziza tremulae Rimpau D. punctiformis Gremmen, the ascomycete that was previously described as the teleomorph of M. brunnea.

M. populi (Lib.) P. Magn. (= M. populi-nigrae Kleb.), whose teleomorph is D. populorum (Desm.) Hhn., is found throughout Europe and in Russia, China and North America, but is of limited phytopathological importance. It is more active on P. nigra (particularly on Lombardy poplar) and some P euramericana clones little used for intensive cultivation than on P. deltoides and other hybrids; besides, it can infect P. tacamahaca and some Aigeiros Tacamahaca hybrids. It differs from M. brunnea in the symptoms induced on the host and in having curved, pear-shaped conidia.

M. castagnei (Desm. et. Mont.) P. Magn. (= M. populi-albae Kleb.), with teleomorph D. populi-albae (Kleb.) Nannf., was widespread throughout Europe, the Middle East and America before being reported in Australia and New Zealand in the mid-1980s. By comparison with other countries, in New Zealand it has displayed a certain degree of aggressiveness and triggered by no means negligible epidemics on the "silver poplar" cultivar of P. alba, widely used locally for soil conservation. In addition to this species, which is virtually its only host in nature, it can infect some Albidae Trepidae intrasectional hybrids as well as Leuce Aigeiros and Leuce Tacamahaca intersectional hybrids, but curiously it is not reported on Trepidae poplars.

M. balsamiferae Y. Hirats., the most recently described species, was only reported in 1984 on three herbarium specimens of P. balsamifera collected in Canada (Manitoba and Ontario). Its curved conidia with pointed tips quite distinguish it from the other three species and are more reminiscent of Neomarssoniella U. Braun.

1.4.2.3. Life cycle and relations with the host - The Marssoninae are leaf parasites like the rust agents but, unlike them, they kill and degrade the tissues they colonise through a proper enzymatic action. This means that their relationship with the host does not reach the levels of specificity displayed by the Melampsorae, since the metabolic recognitions with the host living cells and the close relations between portions of its genetic material and those of the parasite are lacking. This behaviour may also explain why no physiological races have yet been identified within Marssonina species, although proper studies were made.

Acervular conidiomata, representing the anamorph of the fungus, are differentiated in the centre of the spots from 7 to 10 days after inoculation on susceptible clones and in optimum atmospheric conditions, i.e. rain and/or occult precipitations and temperatures between 17 C and 22 C. Those of M. brunnea and M. castagnei are always intraepidermal, those of M. populi can also be subcuticular. Each conidioma ( = 200-400 m) is composed of a rather slack hyphal matrix supporting a layer of short conidiophores, which produce two-celled hyaline conidia whose shape vary from one species to another (Table 5), and whose common feature is the proximal cell (corresponding to the insertion on the conidiophore) smaller than the distal one. After rupture of the overlying epidermal wall and/or the cuticle of the host, the conidia are released in bulk in a mucilaginous substance and dispersed mainly by rain or dew, which dilute them into an aqueous suspension, and by the wind to considerable distances.

On coming into contact with susceptible green tissues and favoured by a film of water, the conidia germinate. The germ tubes, which may originate from either cell, are able to directly perforate the epidermis and to colonise the mesophyll cells without needing to pass through the stomata.

Table 5 - Different morphological and morphometric characters of the Marssoninae reported on poplars.*

species

symptoms on leaves

conidia

ascomata

ascospores

M. brunnea (Ell. et Ev.) P. Magn.

(tel.: D. tremulae Rimpau)

- f. sp. brunnea:

    brownish spots on both leaf sides

    ( _ 1-2 mm)

- f. sp. trepidae

    Spiers:

    brownish spots usually hypophyllous

    ( = 2-3 mm)

hyaline, clavate, two-celled

(12-19 4-7 m), with the upper cell about twice longer than the lower

sessile, lenticular

(100-200 70-100 m);

asci measuring 90-115 11-14 m

hyaline, ellipsoid, one-celled

(9-14 3-7 m)

M. populi (Lib.) P. Magn.

[tel.: D. populorum (Desm.) Hhn.]

large brownish blotches, mainly epiphyllous, dendritic on P. nigra ( _ 4-5 mm)

hyaline, clavate, two-celled

(17-25 6-11 m),

with the upper cell bigger than the lower

sessile, lenticular

( = 130-260 m);

asci measuring 80-100 13-14 m

hyaline, ellipsoid, one-celled

(10-16 5-9 m)

M. castagnei (Desm. et Mont.) P. Magn.

[tel.: D. populi-albae (Kleb.) Nannf.]

large circular to irregular blotches, greyish-white in the centre ( _ 4-5 mm)

hyaline, obovate, straight or not much curved, two-celled

(17-23 7-10 m), with the upper cell bigger than the lower

sessile, lenticular

( = 210-320 m);

asci measuring 80-100 13-14 m

hyaline, ellipsoid, one-celled

(14-18 7-9 m)

M. balsamiferae Y. Hirats.

(teleomorph not known)

brown to reddish-brown spots, mainly hypophyllous

( _ 5 mm)

hyaline, curved, two-celled

(18-21 4-6 m), upper cell larger with pointed end

-

-

* The characters of acervular conidiomata are not reported owing to their relative uniformity.

If the weather is favourable, during a vegetative season the succession of some peaks of conidium production result in one infection cycle after another. When autumn approaches, the usual conidia are accompanied by ellipsoid one-celled microconidia that probably serve as spermatia for differentiation of the teleomorph. The non-finding of the latter in New Zealand, even though M. brunnea and M. castagnei made remarkable inroads in recent years and despite the presence of their microconidia, suggests that each fungus is heterothallic and that in this country one mating type is absent.

Formation of the teleomorph fruiting bodies begins in autumn on the fallen leaves, when portions of mycelium clump together in the mesophyll to build the ascomata. At the start of the following spring, the ascomata, now in an advanced stage of maturation, burst from the tegument in response to progressive pressure to take on the typical lenticular shape of apothecial ascomata with no stalk (measuring 100-300 m depending on the species). The fertile layer, exposed to the outside in a stage of full maturation, is composed of paraphyses and asci, which are elongated sack-like cells each containing eight hyaline, one-celled, ellipsoid ascospores (10-16 3-9 m depending on the species).

By contrast with the conidia, the ascospores are chiefly dispersed by currents of air and are responsible for primary infections when the vegetative season recommences. Their real epidemiological importance, however, is determined by both the geographic region and its climate: for example, in north-central Europe they seem usually determinant, whereas in southern Europe their role is totally secondary by comparison with the copious attacks resulting from conidia, which are more favoured by the milder climate and thus already in progress before the ascospores are dispersed. This pattern stems from the fact that the parasite is able to overwinter in the forms of stromata (i.e. compact masses of vegetative hyphae), particularly in the cortical tissues of already infected branchlets, which produce new conidia infecting the sprouting leaves when growth recommences.

1.4.2.4. Control strategies - Being stated that the exchange of biological material between one country and another must be strictly supervised by appropriate quarantining, to prevent or at least delay the further spread of the parasite, as in the case of the agents of other specific diseases resistant clones must be selected and employed.

Genetic improvement and the selection of clones have so far been favoured by the continuing absence in the Marssoninae of physiologic races. This type of control, however, must also take account of the resistance to other diseases and the adaptability to the environment of genetic material previously obtained in the absence of Marssonina. For example, the resistance of several P. deltoides clones to M. brunnea is opposed by their susceptibility to the poplar mosaic virus and their vulnerability to wind damage; that of some highly productive Euramerican selections by their predisposition to physiological stress and hence to the appearance of "brown spots", or by their susceptibility to Pollaccia elegans (see 1.4.3) and to Melampsorae. The same can be said for some P. interamericana selections, whereas other new clones, some of them intersectional too, seem to offer better prospects of success.

Among indirect measures, though almost never resolutive, correct cultivation practices are advisable, especially during the parasite's winter quiescence, to reduce the mass of inoculum and hence the heaviness of the subsequent attacks. The maturing ascomata and stromata hibernating in the fallen leaves can be dug in, those hibernating in the bark of the branchlets can be destroyed by pruning and burning. Resistance can also be raised, within certain limits, by the application of potassium and nitrogenous fertilisers.

Increasing awareness of ecological repercussions of the use of chemicals has placed a brake on this form of control. Nevertheless, In European and North American plantations susceptible to M. brunnea and in Oceanian plantations susceptible to M. castagnei as well, it may be necessary to employ fungicides systematically. Attention is primarily directed to preventive treatments with dithiocarbamates, i.e. maneb or mancozeb (200 g/hL a.i.). Curative treatments, however, are also possible using fungicides with systemic action, such as triforine (60 g/hL a.i.), dodine (70 g/hL a.i.) and triadimenol (10 g/hL a.i.). To be effective, these treatments must be performed in spring starting from the leaf sprouting time (no more than two or three treatments at monthly intervals), and applied with either land-based nebulizers or atomisers mounted on fixed-wing aircraft or helicopters, which ensure the maximum promptness and effectiveness on large areas.

1.4.3. Leaf scab and blight caused by Pollaccia spp.

The form-genus Pollaccia Bald. et Cif. - taxonomically revised on several occasions in recent years - includes the anamorphs of parasites on poplar leaves and shoots whose teleomorphs, only occasionally observed in nature, are ascribed to Venturia Sacc. (fam. Venturiaceae, ord. Dothideales, phylum Ascomycota).

The main pathogens are P. elegans, the subject of particular attention owing to its renewed aggressiveness on black and euramerican poplars cultivated in some European and North American areas, and P. radiosa, which attacks many Leuce poplars in several continents. This section is also infected by P. borealis and P. populi-albae on a more local scale. Finally, P. mandshurica is currently endemic in China on some members of various sections.

1.4.3.1. Symptoms and the damage caused - Healthy plants from susceptible clones, in cool stands, are attacked by these pathogens at the beginning of the spring.

P. elegans is primarily active in the plantation against Aigeiros poplars; its targets are the first leaves sprouting from dormant buds and the shoots of the current year. On leaves, it causes brown-yellowish lesions irregular in shape, though mostly rhombic, that usually are placed along the main bundles. Confluence of these lesions results in extensive necrosis and turns the leaf blackish. A few days after the appearance of the first symptoms, an olive bloom, due to the mass production of conidia, thicken on the dead leaf tissues. Almost at the same time, the still herbaceous shoots display depressions and necroses, often located at their base owing to the passage of the parasite through petioles. The distal tissues gradually lose their turgor, bend into a hook shape, dry out and eventually split. In more resistant clones, reddenings and swellings form around the infection sites and block any further colonisation. Widespread and intensive attacks can impair all the leafage put out at the beginning of the vegetative season, but the host is able to activate the buds below the necrotised sprouts and thus to form a new crown, that is not usually stricken by new infections. Woody growth is only impaired in the event of repeated severe attacks during some years.

The symptoms caused by P. radiosa and P. populi-albae on Leuce poplars are much the same, though the leaf lesions are more numerous, less extensive and irregularly roundish. Their colour ranges from olive to brown with a darker border, and changes to reddish-brown in the centre at the time of sporulation.

P. borealis has been recently been reported on Populus tremuloides. By contrast with those of P. radiosa, the lesions it induces are brown-purple, limited in size ( _ 0.5 cm) but confluent, surrounded by a dark brown ring that is more evident on the leaf abaxial side, the only place where sporulation occur. The leaves of some clones are pierced by holes which are distinctly smaller than ordinary necroses and have a thickened inner rim. They can readily be mistaken for the work of insects. By contrast with the attacks of other species, petioles and shoots show no sign of infection.

P. mandshurica is the agent of the syndrome known in China as "grey spot disease". Primarily serious in the nursery and on young trees up to 5 or 6 years old in the plantation, it causes lesions similar to those provoked by P. radiosa, except that their inner part is silver grey and bounded by a dark brown edge.

1.4.3.2. The pathogens - The Pollacciae found on poplars differ in their elective hosts, and also in some morphological and morphometric features of their fruiting bodies and propagules (Table 6). Many disputes have arisen concerning the species which prefer the Leuce section.

P. elegans Serv. [teleomorph: Venturia populina (Vuill.) Fabr.] is widespread in Eurasia on Aigeiros and Tacamahaca poplars, in North America only on Tacamahaca (P. trichocarpa and P. balsamifera in the North West Territories and in Alaska) and P. trichocarpa P. deltoides hybrids. It is currently present in a latent form in Europe, where it causes sporadic infections in very damp springs, but retains a core of higher aggressiveness in the Alps and subalpine regions (at 200-800 m above sea level) and in the eastern Po Valley. In this zone, the use of Euramerican clones selected from "Canadian" genotypes, in its turn imposed by repeated attacks of Marssonina brunnea on the established clones, has been responsible for a certain recrudescence in recent years (1990-1993).

P. radiosa (Lib.) Bald. et Cif. (teleomorph: V. tremulae Aderh.) was divided by Morelet, as accepted here, into two varieties that differ in their micromorphology and (partially) in their hosts, but that induce virtually identical symptoms:

- var. radiosa (teleomorph: V. tremulae Aderh. var. tremulae), which is spread in Eurasia and North America on Populus tremula, P. tremuloides, P. canescens, P. alba and various intrasectional hybrids;

- var. letifera (Peck in Sacc.) Morelet (= P. americana Ondrej), whose teleomorph is V. tremulae Aderh. var. grandidentatae Morelet, spread in Canada and U.S.A. on Populus grandidentata, P. tremuloides, P. alba and various intrasectional hybrids.

P. radiosa was once thought to be the anamorph of V. macularis (Fr.: Fr.) Mller et v. Arx, but the latter is actually a saprophyte fungus (like V. viennotii Morelet) of no phytopathological importance, whose anamorph is for the present unknown, found on dead leaves and petioles of Populus grandidentata, P. tremuloides, P. tremula and P. canescens.

P. populi-albae (Morelet) Rulamort [= P. ramulosa (Desm.) Ondrej], whose teleomorph is V. tremulae Aderh. var. populi-albae Morelet, attacks P. alba only both in Europe and North Africa.

P. borealis Funk differs from P. radiosa in the appearance and course of the lesions it causes on leaves, as already mentioned, and in some micromorphological characters. Its areale includes parts of British Columbia far from the Pacific coast, the North West Territories and Yukon, where it is responsible for substantial epidemics on P. tremuloides. The teleomorph V. borealis Funk was obtained on artificial medium, but has not yet been observed in nature.

P. mandshurica Morelet (teleomorph: V. mandshurica Morelet) is endemic in north-eastern China in the region once called Manchuria, where it induces a syndrome first recognised in the early 1960s, though the fungus was not described and identified as the pathogen until the 1990s (owing to constant confusion with the bark parasite Coryneum populinum Bres. and with Mycosphaerella mandshurica Miura in the case of its anamorph and teleomorph respectively). Populus simonii, P. nigra, P. davidiana and various P. simonii P. nigra hybrids are susceptible to its infections, whereas P. alba, P. trichocarpa, P. deltoides and P. euramericana hybrids are resistant.

Table 6 - Different morphological and morphometric characters of the Pollacciae reported on poplars.

species

symptoms

conidio-phores

conidia

ascomata

ascospores

P. elegans Serv.

[tel.: V. populina (Vuill.) Fabr.

extensive, brown-yellowish irregular lesions on leaves; necroses of herbaceous shoots

short

(4-6 5-6 m)

fusiform, light olive, 3-celled or sometimes 2-celled

(24.5-30.5 9-11 m)

globose, brown

( = 150-180 m);

asci: 130-150 15-20 m

ovoid, yellow-green, 2-celled with the upper cell larger than the other (22-25 10-14 m)

P. radiosa (Lib.) Bald. et Cif. var. radiosa

(tel.: V. tremulae Aderh. var. tremulae)

irregularly roundish lesions, olive-brown with a darker border, turnig to reddish-brown; necroses of herbaceous shoots

cylindric

(10-14 3-4 m)

ellipsoid or obclavate, yellow to light brown, mainly 3-celled or often 2-celled, rarely 1-celled

(16-26.6 5.3-8 m)

globose, brown to reddish-brown

( = 95-183 m);

asci: 59-88 12-16 m

ovoid, light yellow, 2-celled with the upper cell larger than the other (16-19.9 8-10.6 m)

P. radiosa (Lib.) Bald. et Cif. var. letifera (Peck in Sacc.) Morelet

(tel.: V. tremulae Aderh. var. grandidentatae Morelet)

very similar to those caused by P. radiosa var. radiosa

cylindric

(8-12 4-6 m)

curved, yellow to light brown, mainly 2-celled or often 3-celled, rarely 1-celled

(17.3-27.9 6.6-9.3 m)

globose, brown to reddish-brown

( = 95-183 m);

asci: 59-88 12-16 m

ovoid, light yellow, 2-celled with the upper cell larger than the other (13.3-17.3 6.7-9.3 m)

P. populi-albae (Morelet) Rulamort

(tel.: V. tremulae Aderh. var. populi-albae Morelet)

very similar to those caused by P. radiosa var. radiosa

cylindric

(6-10 6-7 m)

ellipsoid or obclavate, yellow to light brown, mainly 2-celled, more often 1-celled than 3-celled

(16-25.3 8-10.6 m)

globose, brown

( = 95-183 m);

asci: 59-88 12-16 m

ovoid, light yellow, 2-celled with the upper cell larger than the other (14.6-18.6 6.7-9.3 m)

P. borealis Funk

(tel.: V. borealis Funk)

two different types on leaves only:

a) brown-purple confluent lesions ( _ 0.5 cm)

b) holes with a thickened inner rim

cylindric

(-)

solitary or in chains of two, cylindric, truncate at the base, light brown,

1-celled only

(15-22 4-5 m)

globose, dark brown

( = 200-250 m);

asci: not seen

fusiform, greenish to light brown, 2-celled with the upper cell larger than the other (16-19 5-6 m)

P. mandshurica Morelet

(tel.: V. mandshurica Morelet)

irregular, coalescent blotches, silver grey in their inner part, bounded by a dark brown edge; necroses of herbaceous shoots

cylindric

(up to 17 m long)

fusiform, often curved,

tapered towards the apex,

light brown, mainly

4-celled

(24-39 6.6-9.9 m)

globose, brown

(-);

asci: 84-120 16.6-18.5 m

broadly ellipsoid, pale yellow, 2-celled with the upper cell larger than the other (18-22 9-11 m)

1.4.3.3. Life cycle and relations with the host - The Pollacciae are favoured by falls in temperature following the vegetative restarting of buds in the presence of moderate precipitations and high humidity, a common situation in early spring, both because they are fungi that vegetate well at quite low temperatures (the optimum range is 15-20 C) and because the susceptibility of the shoots is enhanced in these atmospheric conditions. P. mandshurica alone mainly infects during the summer; in north-eastern China, in fact, concentration of the rainfall in temperate summers favours later attacks.

Primary infections are carried out by ascospores. They are two-celled, yellow-greenish (22-25 10-14 m), released from typical pseudothecial ascomata that, in the case of V. populina, are differentiated in particular on the dried tissues of necrotised shoots bordering the still vital parts, and also on infected leaves that have fallen to the ground in the case of V. tremulae and V. mandshurica. At least in European poplar districts, infections on the part of the conidia released from stromata formed by the hibernating mycelium in the necrotised tissues, mainly inside the shoots killed the previous year, appears to be more important for the initial propagation of the disease, whereas the role of ascospores seems less important on account of their late maturation.

Subsequent infections are performed by conidia released from new typical cushion-like structures known as sporodochial conidiomata, which are composed of short hyphae and differentiated on the leaf necroses.

They continue to originate new infections as long as the favourable weather lasts (some workers maintain that there may be as many as five P. radiosa generations, each lasting two weeks, throughout the vegetative season), but usually their production ceases during the summer, thus the disease regresses. Resumptions in the autumn, when the optimum temperature and humidity values are re-established, are completely a matter of chance.

As in the case of the Marssoninae, no populations with different pathogenicity have yet been observed within the single Pollaccia species.

1.4.3.4. Control strategies - Particular attention must be directed to the selection and use of resistant clones. This has already led to lasting results and offered good incremental and technological parameters of the wood. In north-central Europe, for example, the preference for interamerican hybrids and P. deltoides clones as opposed to the euramericans limited the spread of P. elegans, despite the ideal climate. Care, however, must be taken to ensure that the clones selected are equally resistant to pathogens such as the Melampsorae, the Marssoninae, Discosporium populeum, Xanthomonas populi that are currently a major threat to poplar growing. Now that so much is known about the ease with which diseases can spread, the misfortunes that might arise from the imposition of a single resistance would be less excusable than in the past.

Cultivation practices able to reduce the incidence of the disease by removing the overwintering inoculum (pseudothecial ascomata and conidiogenous stromata), such as destruction of the infected shoots or turning over the soil to bury the fallen leaves, are costly measures and not always economically justifiable.

Systemic and contact fungicides too have failed to provide satisfactory practical results, not because their active ingredients are ineffective, but because treatments are rendered difficult by uncertain prediction of the time when the conditions favouring an attack are likely to occur. They are also very expensive and impose a heavy environmental burden if repeated.

1.4.4. Other leaf diseases

1.4.4.1. Yellow blister of leaves and amenta caused by Taphrina spp. - The syndromes attributable to some members of Taphrina Fr. (fam. Taphrinaceae, ord. Taphrinales, phylum Ascomycota), while encountered world-wide, are rarely the cause of substantial economic damage to poplars and are primarily known for their unmistakable characteristics.

The Taphrinae are obligate parasites of living tissues, hence do not kill the mesophyll cells or other green tissues before establishing the parasitic relationship, but they do not display a specificity comparable with that of the Melampsorae. To reproduce, they require a temperature of not more than 15-20 C and high atmospheric humidity, thus their attacks mainly occur in spring.

The Taphrinae on leaves, while also found on adult poplars, are only a cause for concern in the nursery, where they take advantage of the closeness of the saplings and the particular microclimate to which this gives rise.

The most important species is T. populina (Fr.: Fr.) Fr. [= T. aurea (Pers.) Fr.], widespread in Eurasia, southern Africa, North America and South America (Argentina, Chile), also reported on willows. In the early days of poplar cultivation, the fungus had a certain impact in some European zones (e.g. in northern Italy) on black Eurasian poplars not yet selected for their disease resistance. It was soon brought back within latency level, however, through improved cultivation practices and empirical exclusion of the phenotypes that proved most sensitive. It is still quite common, especially in east-central Europe. The Aigeiros section is primarily affected (P. nigra and Euramerican hybrids, some of whose clones are anyhow poorly susceptible, such as "Robusta", or resistant, such as "I-214") and the Tacamahaca poplars are also attacked, though to a lesser extent.

Infections results in the appearance of blisters on the leaf blade, concave towards the abaxial side, isolated at first then confluent, up to 3 cm in diameter. The leaf adaxial side remains green for a long time, whereas the areas of the abaxial side corresponding to the concavities, derived from deformations of the mesophyll connected with hormonal disorders, turn bright yellow and then orange. This colour change is consequent to the reproduction stage of the parasite, provided by the formation of bare cylindrical asci (50-112 15-40 m), arranged in a layer outside the leaf and supported by basal cells differentiated in the host's epidermal cells. Even before they mature, these asci contain droplets of a golden lipid substance whose mass gives its colour to the underlying areas of the leaf blade. The one-celled ascospores ( = 4-6 m) are short-lived and generate many blastospores ( = 2-3 m) by budding inside the asci, which eventually break open. The release of blastospores may be followed either by infections through development of subcuticular mycelium, or by direct production of other blastospores, which are then dispersed in the environment by the rain and the wind. At a late stage of the disease, large portions of the leaf necrotise and dry out, and holes are formed at the blisters. The fungus overwinters both inside the preformed leaflets of poplar buds in a mycelial state, and outside them as adherent blastospores with a thickened cell wall.

Another more localised leaf parasite is T. populi-salicis Mix, which is found in North America on willows and poplars (P. nigra, P. trichocarpa).

T. johansonii Sadeb. and T. rhizophora Johans. attack amenta at the ovaries and cause large, bright yellow swellings (hypertrophies). The first has been reported in Europe (mainly east-central Europe), Japan and North America on various members of Leuce and Aigeiros sections, the second only on P. alba in east-central Europe and Australia. The two species are distinguished by the length of their asci (more than 120 m long in T. rhizophora).

1.4.4.2. Powdery mildews - For this group of diseases are responsible various members of the fam. Erysiphaceae (ord. Erysiphales, phylum Ascomycota). By contrast with forest nurseries and fruit-growing, they almost never cause serious damage in poplar cultivation.

The best known agent is Uncinula adunca (Wallr.: Fr.) Lv. [= U. salicis (DC) Wint.], widespread in Eurasia and North America on many Leuce, Aigeiros and Tacamahaca species, and also established on willows. The other agents reported on poplar are:

- U. populi Sharma, recently described on P. nigra in India;

- Phyllactinia guttata (Fr.) Lv. [= P. suffulta (Reb.) Sacc. = P. corylea (Pers.) Karst.], a cosmopolitan species found on numerous broad-leaved trees, but only reported on Euramerican poplars in southern Asia (Pakistan, India, China, Korea);

- Erysiphe horridula (Wallr.) Lv., observed in 1960 in Italian nurseries of P. nigra.

The powdery mildews are obligate leaf parasites like the Taphrinae, but are much less dependent on humidity and their attacks are thus more frequent in summer. A white mat of mycelium appears on the leaf adaxial side (and also the abaxial one in the case of P. guttata) which produces the typical conidia of the anamorph, responsible for the secondary infections, throughout the vegetative season. Leaves gradually curl up because the parasitised cells in the upper epidermis stop dividing, whereas those in the lower one continue to grow and divide. On the approach of the adverse season, globose corpuscles, known as cleistothecial ascomata, are seen for the first time on the white powdery mat. Yellow at first, then reddish and finally black as their maturation proceeds, they constitute the teleomorph of the parasite and contain many asci (in the case of species active on poplars). In the temperate regions, they are the form that overwinters on fallen leaves, while they also ensure the fungus dissemination by means of variously shaped external appendages which have a specific function of active transport (e.g. for P. guttata) or of attachment to the host surface (e.g. for U. adunca and U. populi).

The current incidence of the Erysiphaceae in poplar growing is too low to justify a special genetic selection of resistant clones or fungicide treatments.

1.4.4.3. Leaf blotch caused by Septotinia podophyllina - This pathogen (fam. Sclerotiniaceae, ord. Leotiales, phylum Ascomycota) was often referred to in the past as a poplar-specific species called S. populiperda Waterman et Cash, but later it was shown to be substantially coincident with the type-species S. podophyllina Whetzel, which has precedence and is also found on Podophyllum spp. and Prunus serotina Ehrh. It is thought to originate from North America, and has since been reported in some European countries (France, Holland, Jugoslavia, ex-Czechoslovakia, Russia) as well as in Korea and Japan. In the 1950s-1970s, it was the subject of a certain interest on account of its sporadic and occasionally serious recurrence in nurseries, where it damaged the production of cuttings (mainly in France), and in young plantations in the north-central U.S.A. There have been no subsequent reports about its activity.

The parasite is able to infect poplars of the three main sections (Leuce, Aigeiros, Tacamahaca), though with differences of clonal susceptibility. The disease appears in spring on young leaves as grey-brown spots, often placed on their edges or near insect punctures, that gradually expand following the mycelial growth when the humidity is high. Eventually each blotch reaches a remarkable size (up to 5 mm in diameter) and displays a distinct though irregular border, surrounding concentric light and dark bands corresponding to growth and static, low-humidity periods respectively, when leaf tissues react with a local accumulation of tannic compounds. On these blotches, which are readily visible on the leaf adaxial side, groups of whitish sporodochial conidiomata ( = 120-250 m) produce fusiform, one- to five-celled hyaline conidia (18-45 5-8 m) ascribed to the anamorph Septotis podophyllina (Ell. et Ev.) v. Arx. During the vegetative season, the blotches can converge and kill large portions of the leaf blade, causing precocious defoliation in serious infections. The parasite can also reach shoots via the petioles and induce dark, sometimes encircling lesions.

The teleomorph appears in winter, on fallen leaves, in the form of black circular or elongated sclerotia(3-5 1-2 mm), on which arise groups of cup-shaped apothecial ascomata ( = 2-7 mm) with long stipes and a greyish hymenium. Overwintering is ensured both by the hyaline ovoid ascospores (10-13 4-5 m) and by conidia supported by sclerotia or produced in the lesions on shoots. Nevertheless, the real weight of these components in primary infections is a controversial question.

1.4.4.4. Leaf blight caused by Linospora spp. - Two species of Linospora Fuckel (fam. Valsaceae, ord. Diaporthales, phylum Ascomycota) are of a certain importance on poplar:

- L. ceuthocarpa (Fr.) Munk ex Morelet (= L. tremulae Morth.), spread in Eurasia, but also reported several times in the east-central U.S.A., agent of mild epidemics in France in the 1970s, and now with a purely secondary incidence;

- L. tetraspora Thompson, a northern species spread throughout Canada and increasingly in recent years, though still sporadically, in the northern U.S.A. too.

Besides having different areales, the two pathogens also have different hosts. L. tetraspora only attacks some Tacamahaca and Aigeiros American poplars (primarily P. balsamifera, followed by P. deltoides and P. trichocarpa P. deltoides), whereas L. ceuthocarpa mainly invades Leuce species (P. alba, P. tremula, P. tremuloides, P. grandidentata), though it is occasionally found in nature on P. deltoides, P. euramericana, P. trichocarpa and on intersectional hybrids (P. deltoides P. trichocarpa, P. tacamahaca P. deltoides).

At the height of summer, infections of Leuce poplars by L. ceuthocarpa cause grey-violet leaf spots visible on both sides, each measuring a few mm. Their further progression depends on the rainfall during the season: if this keep quite high, the spots expand rapidly at the end of August and the beginning of September in west-central Europe. They gradually become whitish in the centre, but remain dark on the edges, while their shape becomes circular or elliptical with wavy borders, often elongating at a main vascular bundle. There are rarely more than two or three blots per leaf, though the size they reach (as many as several cm) means that much of the same is involved, while its unaffected parts turn yellow. Brownish spots (1-2 mm) are sometimes observed on the petioles as well. Intensive attacks are rare; their immediate effect is early defoliation.

Black subcuticular acervular conidiomata ( = 100-350 m) are soon differentiated in the whitish centre of the blots. When these mature, they lacerate the cuticle and release, in mucilaginous little masses, fusiform or sometimes curved hyaline conidia (7-24 2-3 m), usually one-celled, often bound together by short lateral anastomoses. This is the anamorph, indicated as Titaeosporina tremulae (Lib.) v. Luik [= Gloeosporium tremulae (Lib.) Pass. = G. populi-albae Desm.]. The teleomorph appears at the end of the spring on dead leaves from the previous year, in the form of ovoid perithecial ascomata (average 400 140 m) inserted between two parallel pseudostromatic laminae, visible to the naked eye as black, jagged notches, from which only the long necks of the ascomata protrude. The yellowish, filiform ascospores (100-130 1.9-2.7 m), subdivided by 2 to 5 septa, are arranged in the asci in coiled bundles and are responsible for the primary infections.

Very similar symptoms are induced by L. tetraspora, with single blots that sometimes involve the entire leaf. Its ascomata, on the other hand, are smaller (175-270 110-175 m) than those of the other species, and its ascospores are longer (175-225 2.5-3 m) and have more septa (6-8).

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Lastly, mention may be made of a number of poplar leaf parasites whose attacks are sometimes the cause of concern on a local scale or in particular contexts:

- Ciborinia whetzelii (Seaver) Seaver (fam. Sclerotiniaceae, ord. Leotiales, phylum Ascomycota), agent of the ink-spot disease mainly in young stands of P. tremuloides, sporadic throughout Canada and the northern U.S.A., which is so-called owing to the conspicuous black sclerotia formed on leaves; attacks on P. grandidentata, P. balsamifera and P. deltoides are rare;

- Glomerella cingulata (Ston.) Spauld. et H. Schrenk (fam. Phyllachoraceae, ord. Phyllachorales, phylum Ascomycota), with anamorph Colletotrichum gloeosporioides (Penz.) Penz. et Sacc. in Penz. (= Gloeosporium fructigenum Berk.), a polyphagous species responsible on poplar for moderate leaf and shoot blights, mainly in plantations of north-western America and Indian nurseries, reported in France as agent of brown necroses on one-year branchlets;

- Sphaceloma populi (Sacc.) Jenkins (= Hadotrichum populi Sacc.), the anamorph of Elsino populi Jenkins (fam. Elsinoaceae, ord. Dothideales, phylum Ascomycota), an agent of anthracnoses on Aigeiros and Tacamahaca poplars in conditions of high humidity, mainly active in India but also reported in Europe, Japan and Argentina;

- Alternaria alternata (Fr.) Keissler (= A. tenuis Nees), a cosmopolitan mitosporic fungus very common on poplar as a component of its epiphytic mycoflora, which occasionally occurs as the agent of leaf blight in hot and very humid stands (especially in India and China);

- some species of Phyllosticta Pers. (Mitosporic Fungi), reported in Europe (e.g. P. populina Sacc.), Argentina, southern Australia, Japan and (as P. adjuncta Bub. et Serebr.) above all in India, which cause leaf spots on poplars rendered more vulnerable by particular growing conditions (e.g. very humid nurseries) or other diseases;

- two species of Phoma Sacc. (Mitosporic Fungi): Phoma exigua Desm.9, reported in New Zealand as a leaf blotch agent on one-year-old seedlings of P. alba, and Phoma macrostoma Mont., a polyphagous parasite that in India is sporadically responsible for leaf spots in nurseries and young plantations of P. deltoides;

- Phaeoramularia maculicola (Rom. et Sacc.) Sutton (= Torula maculicola Rom. et Sacc. = Cladosporium subsessile Ell. et Barth.), a mitosporic fungus which is agent of leaf spots on Aigeiros, Tacamahaca and above all Leuce poplars in North America and Scandinavia, as well as India, where its attacks have become increasingly frequent during the last twenty years;

- Cladosporium humile J.J. Davis, a mitosporic fungus responsible for severe phylloptoses in nurseries and plantations in various regions of India, especially on the indigenous P. ciliata, on which it is a pathogen of primary importance;

- Cercospora populina (Ell. et Ev.) Deighton, a mitosporic fungus that is found in India, where it gives rise to leaf blotch epidemics of a certain importance both in nurseries and plantations of P. deltoides, causing precocious defoliation in the older ones;

- Rhizoctonia solani Khn., the anamorph of Thanatephorus cucumeris (Frank) Donk (fam. Ceratobasidiaceae, ord. Ceratobasidiales, cl. Basidiomycetes), an extremely polyphagous species with a wide variety of manifestations that on poplar causes a syndrome, known as leaf web blight, which reaches a high incidence in nurseries and young plantations in various regions of India subjected to heavy monsoon rains, thus requiring special cultural practices and fungicide treatments; its main symptom is a web of hyphae that is well visible on infected leaves like a cobweb and often stretches from one leaf to another.;

- Drechslera maydis (Nisikado) Subram. et Jain [= Bipolaris maydis (Nisikado et Miyake) Shoem.], the anamorph of Cochliobolus heterostrophus (Drechsler) Drechsler (fam. Pleosporaceae, ord. Dothideales, phylum Ascomycota), long known as an important leaf parasite on maize, recently observed in India (isolates designated "T race") on some clones - mainly male of Texan origin - of P. deltoides, where it is responsible for a leaf blight of very high incidence; on the contrary, tests showed that P. nigra and P. ciliata are totally resistant.

8 According to the most recent taxonomic revision of Melampsora species found on poplars (Bagyanarayana, 1998), which here is followed in part, the collective species M. populnea (Pers.: Pers.) Karst. [= M. populina (Pers.) Lv.] should include the former M. larici-tremulae, M. magnusiana, M. pinitorqua and M. rostrupii, together with M. allii-populina, as formae speciales: f. sp. laricis (Hart.) Boer. et Verh., f. sp. magnusiana (Wagn.) Bagyanarayana, f. sp. pinitorqua (Hart.) Boer. et Verh., f. sp. rostrupii (Wagn.: Kleb.) Boer. et Verh. and f. sp. allii-populina (Kleb.) Bagyanarayana respectively. This was suggested because these taxa do not differ essentially in morphology, but only in their aecial [secondary] hosts (ibidem).


9 It is distinct from Phoma exigua Desm. var. populi de Gruyter et Scheer, a sporadic agent of bark necrosis that was previously mentioned.

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