10.6092/issn.2531-7342/6151
Molti sono i caratteri di Ailanthus altissima (Mill.) Swingle (noto come “Albero del paradiso”, Simaroubaceae) che lo rendono un albero invasivo che provoca gravi problemi in tutte le aree ove è stato introdotto e si è naturalizzato: velocità di accrescimento, abbondante fruttificazione e capacità di riproduzione vegetativa, facilità di germinazione dei semi e presenza di apparato radicale irruente, proprietà allelopatiche, resistenza all’erbivoria combinata a straordinaria capacità di tolleranza nei confronti di situazioni ambientali estreme. Dopo una breve descrizione delle difficoltà insite nelle campagne di eradicazione basate sul taglio meccanico seguito da trattamenti erbicidi, la nota illustra il possibile ruolo, come micoerbicida,o di un agente patogeno tracheomicotico (Verticillium nonalfalfae H.W. Platt, R.M. Bostock, R.M. Davis &amp; Subbarao) recentemente descritto negli Stati Uniti e segnalato anche in Austria.
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2531-7342
6151
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Giacomo Lorenzini
Italian Journal of Mycology
wilt disease
Will a fungus save us from the <em>Ailanthus</em> invasion?
Text.Serial.Journal
https://italianmycology.unibo.it/
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Articles
2016-05-10
2016-05-10
2016-04-21
2018-08-20
13-18
Ital J Mycol
Giacomo Lorenzini
2016/05/10
10.6092/issn.2531-7342/6151
13
University of Pisa
2531-7342
wilt disease
en
18
Will a fungus save us from the <em>Ailanthus</em> invasion?
https://italianmycology.unibo.it/article/download/6151/5925
45
G. Lorenzini                                              Italian Journal of Mycology vol. 45 (2016) ISSN 2531-7342
DOI: 10.6092/issn.2531-7342/6151



 Short communication

 Will a fungus save us from the Ailanthus invasion?
 ________________________________________________________________________________

                                            Giacomo Lorenzini

 Department of Agriculture, Food and Environment of the University of Pisa

 Corresponding author e-mail: giacomo.lorenzini@unipi.it

 Abstract

    Rapid growth rate, prolific fruiting and vegetative reproduction from root sprouts, ready germination and
    extended root system, allelopathic effects, resistance to herbivory combined to tolerance to environmentally
    stressful conditions such as infertile sites, make Ailanthus altissima (Mill.) Swingle (also known as Heaven
    tree, Simaroubaceae) a noxious and highly invasive tree in all countries where it has been introduced and is
    become naturalized. After a brief historical trait of the importance of the presence of this plant and the
    complexity of eradication campaigns based on manual cutting and herbicide treatments, the note illustrates the
    possible role as a candidate mycoherbicide of a soilborne fungal wilt agent (Verticillium nonalfalfae H.W.
    Platt, R.M. Bostock, R.M. Davis & Subbarao) recently described in the USA and also reported from Austria.


    Keywords: Verticillium nonalfalfae; mycoherbicide; biocontrol; Ailanthus altissima; tree-of-heaven; wilt
    disease.


 Riassunto

    Molti sono i caratteri di Ailanthus altissima (Mill.) Swingle (noto come “Albero del paradiso”, Simaroubaceae)
    che lo rendono un albero invasivo che provoca gravi problemi in tutte le aree ove è stato introdotto e si è
    naturalizzato: velocità di accrescimento, abbondante fruttificazione e capacità di riproduzione vegetativa,
    facilità di germinazione dei semi e presenza di apparato radicale irruente, proprietà allelopatiche, resistenza
    all’erbivoria combinata a straordinaria capacità di tolleranza nei confronti di situazioni ambientali estreme.
    Dopo una breve descrizione delle difficoltà insite nelle campagne di eradicazione basate sul taglio meccanico
    seguito da trattamenti erbicidi, la nota illustra il possibile ruolo, come micoerbicida,o di un agente patogeno
    tracheomicotico (Verticillium nonalfalfae H.W. Platt, R.M. Bostock, R.M. Davis & Subbarao) recentemente
    descritto negli Stati Uniti e segnalato anche in Austria.

    Parole chiave: Verticillium; micoerbicida; difesa biologica; Ailanthus altissima; tracheomicosi.

 Imagine everything happened merely because of a mistake when (around 1750) the French clergyman Pierre
 d’Incarville brought to Paris from faraway China a stock of seeds that he thought were those of the prized
 lacquer tree [Rhus verniciflua, Sin. Toxicodendron vernicifluum (Stokes) F. Barkley] but were instead
 ailanthus seeds [Ailanthus altissima (Mill.) Swingle, sin. A. glandulosa, also known as Heaven tree,
 Simaroubaceae] (FERET, 1985). Thus begins one of the most important biological invasions of the plant

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DOI: 10.6092/issn.2531-7342/6151



 world in the modern times. This neophyte was valued in Europe for its beautiful appearance (it can reach
 over 20-25 m in height with an elegant straight habit, and a trunk diameter of more than 1 m; its foliage is
 pleasing to the eye and is reminiscent of walnut and ash trees). Its hardiness is incomparable (it has no
 acclimatization problems as regards climate and edaphic factors). It is easy to cultivate and grows
 exceptionally fast. It is perfect for beautifying streets and parks, reinforcing slopes, and colonizing difficult,
 unstable terrain. One episode that contributed to its quick dissemination was when the breeding of the
 classical silk worm (Bombyx mori L.) underwent a severe health crisis and another lepidopteran was
 introduced from the East by the zoologist Paolo Savi in Pisa in 1856: the ailanthus silkworm, Samia cynthia
 Drury, which indeed feeds on the ailanthus. Thus, an alternative sericulture industrial chain was set up, with
 this tree becoming even more popular. In Florence, a “Società Ailantina Italiana” was set up to encourage the
 spread of this tree species (RIDOLFI, 1861). However, this situation did not last for long. While Louis Pasteur
 solved in 1864 the Bombyx infection problem – which was pebrine, a disease caused by the protozoan
 Nosema bombycis Nageli – the industrial quality of the cocoons produced by the Samia butterfly was quite
 scarce. However, by then ailanthus had established itself and conquered ever more new areas. In the
 meanwhile, it had also reached the USA (starting from Pennsylvania in 1784 – KASSON et al., 2013),
 imported by English settlers and even there it was appreciated. A second line of introduction also occurred in
 California in the mid-19th century at the hands of the Chinese who emigrated to work on the transcontinental
 railway (but also to search gold!). The ailanthus tree is a true cult for the Chinese, who use almost all its parts
 in their traditional medicine. The list of health problems that find a speedy and satisfying solution in extracts
 of its bark, leaves, fruit, and wood is endless (KUNDU and LASCAR, 2010). Strangely enough, this topic has
 never been tackled in real terms elsewhere on the planet even if by now the complex pool of secondary
 metabolites present in the various organs of the plant is well characterized. Within a few decades, this
 species has been naturalized on all the continents, and become a problem everywhere (KOWARICK and
 SAUMEL, 2007). Its favorite habitat is represented by such open areas as railway lines and communication
 routes, abandoned settings, and marginal stations with a high anthropic disturbance.
 A complete description of the botanical and ecological features and distinguishing characters of the ailanthus
 is readily available (e.g. http://www.cabi.org/isc/datasheet/3889; HU, 1979). Ailanthus is a wonderful
 biological machine and by no means a “banal” tree, which exhibits rapid establishment and growth, with a
 high rate of sexual reproduction. The tree bears unisexual flowers on different trees, and a single female
 plant can produce up to 1 million wind-dispersed seeds in a year. Its true peculiarity lies in the capacity to
 grow side-shoots and root-suckers. Starting from the trunk, surface roots, sometimes tens of meters long, are
 differentiated and from them suckers easily branch off. Removing the trunk just triggers quick and stubborn
 differentiation reactions of buds from the stump and roots so that, due to the ability to resprout rapidly and
 form clonal stands after disturbance, paradoxically, “the more it is cut back, the more the production of new
 biomass is stimulated”. The average lifespan is estimated at a hundred years maximum but, due to its
 capability to propagate via underground stems, suckers or stolons, it may be considered “immortal” in the
 sense that its vitality does not end with the death of the original trunk, as it has yielded a pure clonal colony
 that, if undisturbed, can even cover a 4,000 square meter area. It has a marked allelopathic activity, which
 grants it further advantages as regards competition. In can be found at a range of altitudes up to 2400 m. Its
 hardiness is proverbial, making use of an exceptional phenotypic plasticity that lets it adapt to a wide range
 of thermal and water regimes. It is a perfect example of a “water saving mechanism”, through modifications
 of water conductance of the root system and evapotranspiration processes (TRIFILO’ et al., 2004). It easily
 deals with critical situations, such as those of simple cracks in stone materials. It can easily grow in extreme
 environmental conditions (Fig. 1), and is viewed by many as a symbol of dereliction and abandonment. It is
 resistant to urban environment and to herbivores and is actually free from attacks by pests, at least in Europe

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G. Lorenzini                                                 Italian Journal of Mycology vol. 45 (2016) ISSN 2531-7342
DOI: 10.6092/issn.2531-7342/6151



 (the above-mentioned lepidopteran Samia cynthia has been a mere scientific curiosity for some time, a real
 “prize” for photo-naturalists).




 Fig. 1. Severe colonization of ailanthus saplings in the Old English Cemetery of Livorno
        Grave colonizzazione di giovani piante di ailanto nell’Antico cimitero degli Inglesi di Livorno

 All these characteristics could make ailanthus an interesting candidate for the remediation of marginal and
 degraded areas. But, like few others, this is an invasive pioneer plant (it successfully rivals with black locust,
 Robinia pseudo-acacia L.). Not accepted by ungulates, it threatens the biodiversity of natural and
 anthropized ecosystems, easily establishing mono-specific plant formations. Once introduced into
 environments with a high natural importance (e.g. the Isle of Montecristo), it rapidly replaces the indigenous
 flora, jeopardizing the conservation of native biocenoses, and forcing difficult (and usually useless)
 eradication campaigns. The presence of stands along traffic routes and transportation corridors is
 unacceptable because of the problems linked to the reduced visibility and the invasiveness of the foliage and
 roots that damage road surfaces. It also poses human health problems, causing contact dermatitis and
 possibly immunoallergic respiratory issues and myocarditis. In Tuscany, the Regional Law 56/2000 forbids
 the use of this species for reforestation, re-vegetation, and reinforcement works.
 Researchers have focused attention on finding strategies to counter the growth of this invasive plant in such
 sensitive areas as archeological sites, railway lines, roadways, natural parks, and urban settlements. There are
 ecological, economic, and cultural reasons urging the adoption of effective measures of eradication. But how

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G. Lorenzini                                             Italian Journal of Mycology vol. 45 (2016) ISSN 2531-7342
DOI: 10.6092/issn.2531-7342/6151



 can it be done? Some key points: the ailanthus is like an iceberg, since most of the problem is underground!
 A simple (manual) eradication and/or a mechanical cut at the base of the trunk or girdling are totally
 ineffective (even if they are useful for neutralizing highly prolific seed-bearing mother plants). On the
 contrary, they stimulate the tree to rapidly produce an abundance of vigorous and aggressive young runners
 and suckers. The above-mentioned actions must be accompanied by the periodical use of systemic (and
 nonselective) herbicides that can be transported to the root system and compromise (but usually only partly)
 future vegetative renewal (DITOMASO and KYSER, 2007). However, recent regulatory measures have made
 these interventions almost impossible. On the one hand, the Tuscan Region (Resolution 821 of August 4,
 2015) has forbidden all non-agricultural uses of crop protection agents based on glyphosate, the universally
 acknowledged active ingredient indicated as the most suitable for such weed killer treatments. On the other,
 the National Action Plan for the sustainable use of plant protection products (D.M. January 22, 2014) is
 leading to serious limitations in the use of chemical pesticides on roads (Action A.5.5) and in population
 centers (Action A.5.6); more specifically, Point A.5.6.1 (Use of herbicide products) says that “weed-killer
 treatments are banned and have to be replaced with alternative methods in population centers… in the case of
 exemptions plant-protection products cannot be used if the label bears the following expressions of risk …
 R41” (i.e., risk of severe eye lesions, precisely the one referring to glyphosate). What can be done, then?
 A careful examination of the abundant literature on this subject points out an interesting novelty. In the USA,
 for some years now, a case of the ailanthus naturally decline and dying-off has been under investigation (tens
 of thousands of dead trees in Pennsylvania and in some neighboring States). It has been attributed to the
 attacks of a soilborne microfungus, new to the sciences, and described as an (almost) host-specific strain of
 Verticillium nonalfalfae (INDERBITZIN et al., 2011), originally referred to V. albo-atrum Reinke & Berthold
 (SCHALL and DAVIS, 2009). This pathogen is a wilt agent, able to move within the vascular system to reach
 the suckers and to transfer from an infected individual to a nearby healthy one by intraspecific root grafting
 (O’NEAL and DAVIS, 2015a) and is specialized on the ailanthus, causing little or no adverse effects on non-
 target forest species (KASSON et al., 2014). It leads to the rapid death of the affected trees and seems a
 perfect mycoherbicide candidate. In vitro culturing techniques and artificial inoculation protocols based on
 an efficient and stable form of V. nonalfalfae are now ready (O’NEAL and DAVIS, 2015b). Following
 seedling artificial inoculations, the first visible symptom is wilt of leaflets, commonly followed by chlorosis
 and/or necrosis of the leaflets, or proceeding directly into defoliation, and eventually death of the plant in 9-
 11 weeks (SNYDER et al., 2014) (Fig. 2a, b). Once the Verticillium infections have spread in a stand, the
 disease can progress independently, starting from the inoculation produced by diseased plants. Since
 Verticillium-resting structures can remain dormant for years in soil depending on conditions, new ailanthus
 seedling and sprouts could eventually succumb to the resting pathogen. This would potentially allow the sites
 to be free from ailanthus reintrusion for years and allow native plants to begin re-establishment (SNYDER et
 al., 2014). An important role of insects in the spread of propagules has been verified. Recently, KASSON et
 al. (2015) tested 71 woody species for their susceptibility to V. nonalfalfae infection and found that only
 Aralia spinosa L. (devil’s walkingstick) and Acer pennsylvanicum L. (striped maple) acquired infections
 through natural spread from infected Ailanthus altissima. When purposefully injected with V. nonalfalfae,
 numerous woody species showed minor wilting and the fungus was able to be reisolated from the woody
 tissue; however, these other species were able to survive the infection after six years. This research confirms
 that V. nonalfalfae is host adapted to tree of heaven and that other woody species are tolerant of the fungus.
 Recently (MASCHEK and HALMSCHLAGER, 2016) this pathogen has been recorded in Austria causing typical
 symptoms on ailanthus.




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G. Lorenzini                                               Italian Journal of Mycology vol. 45 (2016) ISSN 2531-7342
DOI: 10.6092/issn.2531-7342/6151




 Fig. 2 (Photos courtesy of Prof. Donald D. Davis, The Pennsylvania State University).
         a: on the left, ailanthus healthy plant (control); on the right: ailanthus plant artificially inoculated with
         Verticillium nonalfalfae. b: wilting of a twig of an ailanthus tree naturally infected by the pathogen.

        a: a sinistra: pianta di ailanto sana (controllo); a destra: pianta di ailanto inoculata artificialmente con
        Verticillium nonalfalfae. b: avvizzimento di un rametto di una pianta di ailanto infettata naturalmente dal
        patogeno.

 It is easy to dream about the possibility of actively introducing this microorganism and using it for effective,
 economical, and eco-sustainable actions to finally counter the ailanthus’s otherwise unrestrainable advance.
 The idea of using plant pathogens as contrast agents of infesting and invasive plants is as old as the science
 of plant pathology itself (WILSON, 1969). Unfortunately, practical applications are rather limited, given the
 remarkable difficulties that the technique entails. Obviously, a rigorous risk assessment would be
 indispensable, aimed first of all at ensuring that the pathogen does not also infect the non-target plants.
 However, have we perhaps found a solution?

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G. Lorenzini                                          Italian Journal of Mycology vol. 45 (2016) ISSN 2531-7342
DOI: 10.6092/issn.2531-7342/6151



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