SEMPERVIVOPHILIA : Fungal diseases

Mycoses or fungal diseases, i.e. conditions induced by fungi, are extremely frequent in higher plants, bacterial infections being relatively rare. This is the inverse of that is observed in higher animals, in which infectious pathology of bacterial origin predominates (while putting aside those infections a little special that are viroses). The study of mycoses is all the more important because it is among fungi that one finds the most interesting parasite of the genus Sempervivum, and the only one that is specific to it.

1. Endophyllum sempervivi

The monomaniac lovers of the genus Sempervivum are not recruited exclusively in the human species, here's the proof:

A modest fungus basidiomycete is also an exclusive enthusiast of these plants... It deserves that one grants it some interest, less for its damages, that, in cultivation, remain generally moderate, than for its original and interesting physiology.

1.1. Endophyllum and its host

This fungus belongs to the genus Endophyllum, a genus that includes several other species, each one being linked to a very precise host-plant. Let's notice that no relation of close relationship exists between the host-plants of the various species of Endophyllum (Crassulaceae, Euphorbiaceae...). Endophyllum sempervivi (Albertini & Schweinitz) De Barry, as its name indicates, is a specific and exclusive parasite of sempervivums, no other host having, it seems, been noted, at least in the natural situation.

It should be noted that this parasite affects as well Sempervivum s.s and Jovibarba (the mentions for Jovibarba are few but this fact has been noted personally, cf. photo). Besides, the very characteristic symptoms of the infection by Endophyllum are strictly identical in these two groups. However, these visible symptoms are essentially the reflection of the host's reaction and not the direct effects of the presence of the parasite, as one will see lower. This fact is important because it demonstrates again the close relationship between these two "genera".

It would be however interesting to know if the strains of the fungi infecting Sempervivum are able to infect Jovibarba, and reciprocally, therefore if they are or not two distinct "physiological races" of this fungus. The case is actually very frequent in fungal plant pathology, that a precise race of a parasite apparently with multiple hosts corresponds to each host. These various races can be differentiated only experimentally by their specificity to a given host (this specificity corresponds, in fact, to some subtle adaptive nuances in the enzymatic equipment of the parasite). Some complementary studies about this topic would be therefore welcome in Sempervivum and Jovibarba.

About the linking with Sempervivum, let's notice however that an author also mentions it in Echeveria [ Huber H., 1963 in Hegi, Ill. Fl. MittelEur. ed.2, IV-2 ]. Echeveria is also a genus belonging to Crassulaceae but related to another systematic group (the subfamily Echeverioideae sensu Berger, a subfamily with rather blurred limits but nevertheless distinctly from the Sempervivoideae // or group "Acre" sensu t'Hart, a group with larger limits but distinct of the "Leucosedum-Aeonium-Sempervivum" group that integrates the Sempervivoideae sensu Berger). Besides, the genus Echeveria is localized exclusively in Central America, which makes doubtful this indication (artifact of cultivation? vicariance of the parasite? identification error?). More information about what is likely an error would be necessary.

As its generic name specifies it ("endo" = inside", "phyllum" = "leaf"), it is an endoparasite, that means Endophyllum develops its mycelium (vegetative filaments of the fungus) inside its host's tissues, contrary to other ectoparasitic fungi that remains on the surface of their host and content themselves to plunge some suckers inside it (the vast group of oidiums for example).

Endophyllum is related to the vast group of the "rusts" (Uredineae), and more precisely to the family of Pucciniaceae which also groups together all the rusts of cereals. It is sometimes named "Sempervivum rust" but, just this once, its scientific name Endophyllum is more known and of more commun use than its vulgar appellation.

1.2. Symptomatology and life cycle

Once in place, Endophyllum develops its mycelium inside the foliar tissues without producing necroses of these, and without showing any visible effect at first time. Nevertheless, more or less quickly, the infected leaf, arrived at adult state or nearly, continues or starts again to grow, and that in an immoderate manner. This excess growth doesn't occur in every direction, but practically only in length. Thus, this infected leaf will reach quickly two, three or four times the normal size for the species, or even more...

What has happened? No, you have not just discovered a new variety "longifolium". Simply, Endophyllum stimulated in a particularly active manner the growth of its leaf-meat-safe. By what mechanism? It would seem that it is hormonal and that Endophyllum is able to increase the content in auxine (AIA = Acid Indol-Acetic) in the infected leaf. [ See about this topic: Pilet P.E. & Gaspar Th., Le catabolisme auxinique, Masson ed. : 110-114 (1968) ; Pilet P.E. ; Problème hormonal concernant l'Endophyllum sempervivi, in Bull. Soc. Bot. Suisse 62(269): (1952) ]. Although the hyperauxiny seems have been demonstrated, one cannot stop from questioning the possible action (or more probably the synergy) of other regulating substances, in particular the cytokinines. Adult leaf tissues are actually normally insensible to auxine whereas some cytokinines can experimentally make the elongation of this type of cells to start again.

The increase in concentration of the plant growth regulation hormone that AIA is will restart the multiplication and especially the cell growth (the elongation) of the tissues of it host-leaf. This tenant acts therefore a little as every good gardener feeding its vegetables with fertilizer before eating them!

N.B. This kind of adaptation is not however unique and is met in a few other parasitic inferior fungi. Thus, Gibberella fujikuroi (=Fusarium heterosporum) induces also a gigantism in rice, while secreting a substance analogous to another natural plant growth regulator, and that has by this way been put in evidence and named according to it: Gibberelline.

The mechanism of the accumulation of AIA is probably a reduction of its degradation, by inhibition of the enzymatic system of AIA-oxydases in infected tissues. This system needs intervention of some peroxydases; some mechanisms of photo-oxidization of auxine also exist. This makes this a rather unstable compound and not accumulating therefore normally in physiological conditions (those among its synthetic derivatives that are stable behave as weed-killers at strong doses...).

This hypertrophied leaf remains green a long time, although of a more lucid tonality than a normal leaf (cf. photo). The chloroplasts stock of the cells doesn't apparently follow the considerable growth of the size of these. The host-leaf preserves therefore its chlorophyllian function while increasing its receiving surface to solar rays. It can therefore photosynthesize abundantly the necessary sugars to feed its host, which, replete, will soon think about perpetuating the species. This is how, at the end of the cycle of these gigantic leaves, one sees some small whitish then yellowish pocks appearing just under the epidermis. These protuberances are bags stuffed full of spores and are the fruiting organs of the fungus, and its only visible organs to the naked eye.

These pocks will be prompt to pierce themselves by a punctiform opening, thus forming a way of umbilicus freeing a vivid orange dust constituted by the spores of dissemination of Endophyllum sempervivi, from that its common name of "rust".

It is necessary to note that the life span of an infected leaf is only little shortened in comparison with a healthy leaf. This parasite being specific and well adapted doesn't kill its host, and makes only its general growth to slightly slow down (i.e the growth of the rosette, not that of its leaves!). If this fungus by himself, as an organism, remains inconspicuous, the consequences of its presence can, on the other hand, with difficulty go unnoticed: an infected rosette will present a very characteristic and spectacular "daisy-like" aspect (cf. photo), will only produce few or no stolons, and won't bloom generally. This last affirmation is bound to the relative rarity of the observation in situ of infected floral stems. It is therefore likely that the blooming and infected rosettes are the consequence of a subsequent infection to the floral induction.

The first signs of the leaf hypergrowth appear precociously, since the starting of vegetation of its Sempervivum host. The features are at their apogee in the spring in cultivation and at the beginning of summer in situ. To note that some forerunner signs can sometimes be observed in the heart of winter, at least in the snug conditions of cultivation. These forerunners are some central or median leaves that, although again at normal size, show a beginning of asymmetric growth compared to their neighbors and that are often more light. It seems therefore that Endophyllum cannot fructify the very year of the infection and begins to make it only during the following year.

Once all spores are scattered, then the death by drying up of the gigantic leaves, Endophyllum becomes again undetectable, and the rosette continues its growing season in a quite normal way. The fungus remains present however at the level of the stump at quiescent state. It is then impossible to differentiate an infected rostte from a healthy one. In the following spring, Endophyllum will reinfest a crown of leaves for a new cycle and so forth.

1.3. About host-parasite relations

One is not then very far from a relation of symbiosis, that means of a mutual association of two organisms. However, it is at the present time very difficult to find an any advantage that Sempervivum could get from this association. It would be therefore surely excessive and premature to define Endophyllum sempervivi as an endosymbiote, like it would be reducing to consider it as a simple opportunist parasite.

In fact, the couple Sempervivum/Endophyllum poses an interesting problem of coevolution, that means of evolutionary interaction between a host and its parasite. Coevolution is defined like this:

In this case, it is evidently a coevolution of antagonistic type, that means that the evolutionary mechanisms occur on a system that balances itself by two opposite tendencies: on the one hand the capacity of the parasite to become implanted on its host and to consume the resources of it, on the other hand the host's capacity to oppose this implantation and to preserve its own resources.

Every modification of this host-parasite balance, whatever its sense, is damaging to the parasite and this one should adjust to it quickly (or to benefit from the host's adaptive reaction) or disappear. All increase of the host's resistance would risk to entail the quick disappearance of the parasite since its host is unique. In the same way, every increase of the pathogenicity of the parasite, that would risk to kill its host or to decrease its growth or its multiplication, would decrease the global selective competitiveness of this one and therefore its strengths, which would have the effect of decreasing those of its parasite too.

The result of these two contradictory tendencies succeeds to a subtle balance between the pathogenicity of the parasite and its host's reactivity. It is besides possible to observe objectively that the low prejudice for the host, produced by the presence of the parasite, is really the result of a dynamic balance host/parasite and not a static state directly linked either to the absolute host sensitivity, or to the absolute parasite aggressiveness, or to the simple adding/juxtaposition of these two capacities. One notes actually that the infection by Endophyllum of rosettes in bad physiological state (more or less etiolated, feeding defaulting, etc.) succeeds often to their death (all leaves are touched and the vegetative point is destroyed). The infection by Endophyllum is therefore potentially lethal for its host. To the opposite, one notes that an adequate cultivation of infected rosettes in conditions of oceanic climate (therefore different from natural conditions) entails often the disappearance of the parasite or its change to a permanent quiescent state. Sempervivum can therefore neutralize potentially its parasite once this one is installed in its tissues. In both these cases the result is the same: the parasite will disappear with the rosette that carries it because without host, no parasite! Rigorously, it would be therefore false to say that Endophyllum is a little aggressive parasite as it would be false to say that Sempervivum tolerates well the attacks of Endophyllum, these two antagonistic characters (parasite pathogenicity / host resistance) are inseparable and are obviously the result of a Sempervivum/Endophyllum coevolution.

1.4. Associated pathology

One often observes that these infected and hypertrophied leaves are distinctly more subject to infestation by aphids that the healthy leaves. It is a possibility that these benefit indirectly from the enzymatic equipment of the fungus and the increased dissociation of macromolecules that this one produces. However, the explanation is maybe simply a thinner epidermis for these leaves with excessive and sudden growth.

1.5. Natural distribution

This parasite is very frequent on wild Houseleeks, especially in some dry regions (but not all of them). It seems a lot rarer, or even absent, in those with more elevated hygrometry. Is it only an impression, without any report or numbering to support it.

It is possibly linked to the absence of a necessary intermediate host for the parasite cycle? (a cycle with two often very botanically distant hosts, is a frequent if not usual case in this fungi group). This impression is reinforced again by the observation that in these dry zones, this parasite is more abundant nevertheless in the biotopes with sufficiently humid microclimate, indicating by that a logically easier dissemination with a sufficient hygrometry (necessary to the germination of the spores). I didn't find mention nowhere of this very hypothetical intermediate xerophilous host, and I don't have any mycological expertise to argue its existence. Besides Endophyllum sempervivi is reputed to loop its cycle on only one host, what would not be surprising according to the extreme adaptation of this parasite to its host.

In fact, maybe it is not an intermediate host which is necessary to this fungus but more simply a vector insect of its spores. Actually, this mode of transportation is used by a close species, Endophyllum euphorbiae-sylvaticae, the attractive factor of spores for the vector insect, of which species is not specified, being the odour [ cf. Ainsworth 1966, The Fungi ]. It doesn't appear documented for Endophyllum sempervivi.

Praeger [Acc. Semp. Group: 21 (1932)] notices E. sempervivi as more abundant at high altitudes, it could be exact if one considers the global populations of sempervivums, that means while integrating those in more or less naturalized situation, but demands ampler observation if one only considers the only natural populations, because it is easy to find some populations at low altitude particularly infested (in Massif Central for example).

The global distribution area of Endophyllum sempervivi is likely superimposable to that of its host-genus, because it is mentionnned in the reports of specialized literature, at least punctually, from France as far as Turkey and into Russia, while passing by central Europe. Although not noted for the Apennines (Italy), it is there however abundant in the Tuscan-Emilian Apennine. Although it doesn't seem noted either in non Pyrenean Spain, one can observe it there in the Cantabrian region (but in a very localized manner, it seems), as well as in Sierra Nevada and in Sierra de Gredos. It should be noted that in the central massif of this last zone, of more arid aspect than most other big center-Spain Sierras, Houseleeks nest preferentially in sheltered and shaded sites and therefore more humid ones than the ambient environment, which seems to confirm the hypothesis already formulated of the obvious preference of this parasite for the Houseleeks occupying the most humid biotopes of the globally driest regions.

1.6. Endophyllum sempervivi in cultivation

Endophyllum sempervivi est généralement introduit en culture par une rosette prélevée dans la nature et déjà infectée sans que cela soit encore visible. En effet, il peut s'écouler, du moins en culture, plusieurs mois entre l'infection et les premières manifestations visibles.

As in the wild, Endophyllum seems to prefer, to maintain itself in cultivation, sufficiently dry conditions because it tends to disappear by itself in a humid zone or at least remain in a quiescent and non detectable state. Under a pure oceanic climate, its maintaining from one year to the other is difficult or even exceptional, and this possibility seems linked to the particular sensitivity of some clones. Even in the case of maintaining, its contagiousness in such conditions remains low or null, at least as long as the plants are in good physiological conditions. In the contrary case (weakened plants), Endophyllum can entail a loss of some rosettes, because there is then rupture of the dynamic balance mentionned higher. However, its damages remain, at worst, extremely limited.

The classic and safest treatment (provided that a treatment is necessary...) consists in eliminating all affected rosettes, but, in case of low virulence and only in this case, one can try to limit to leaf removal that often entails the apparent recovery of the rosette. In fact, the leaf removal only prevents the fruition of the fungus and avoiding a contamination therefore by the spores, but some quiescent mycelium will remain present in the stem.

When one comes to have interest in cultivation of a type of plant whatever it is, the tendency is frequent to consider all pathogenic organisms for this one as scourges and calamities: some "bugs" to which one didn't ask for anything and which don't have another reason apparently to be on the planet than to come specially to spoil your pleasure! As such, Endophyllum sempervivi is therefore a "bug" indeed... It is however a point of view too frequently adopted by the Houseleeks growers. And yet, how can one not be full of admiration in the face of such an evolutionary process and the fine adaptation of this organism, that succeeded in diverting the mechanisms of growth regulation of its host to take control of them for its own profit, while taking great care to preserve its host! Besides, visiting some wild populations of Sempervivum is sufficient to note how commonplace and without any damaging consequence the presence of Endophyllum is. The most resplendent populations are often the most infected! One comes then quickly to consider that Endophyllum sempervivi is inseparable from Sempervivum and that one cannot really appreciate one without appreciating the other. As challenging as it can appear, it is not excessive to say that a moderate presence of Endophyllum is one of the signs of a well managed cultivation of Sempervivum!

Thus, before tempting to eradicate Endophyllum sempervivi out of your cultivation, take the time to observe it and to have a liking for it, it too deserves that!

2. Rhizoctonia solani

To date, this affliction seems have been authenticated on Sempervivum only in USA on cultivated plants. The following information is therefore mainly extracted from Russell H.C., Rhizoctonia solanii, a fungus infection affecting Sempervivums, in Sempervivum Fanciers Association Newsletter, USA, 9(1): 2 (1983).

However, it seems that in Europe also some damages can be assigned to it. This fungus is characterized indeed by a humid rot and heaps of external mycelium filaments, in particular on the substratum and under the low leaves. Some cases of rot from the basal leaves with a neat conglomeration of leaves by mycelium are probably to connect to this agent.

As it has been described on Houseleeks in cultivation in USA, the affection appears to start from a leaf and propagates to the whole rosette in one week. The contamination continues step by step while destroying completely the rosettes that soften without showing other visible signs of fungal attack . The damages can be important.

This affection requires continuous hot and damp conditions to appear and to develop. Such climatic conditions are unknown or fleeting in the natural habitats of Sempervivum, and very rare in cultivation. However, this fungus being polyphagous and very common as the agent of rot of roots and collar of various cultivated plants (Begonia, Euphorbia, Tulipa, Dianthus, Brassica, Lactuca, etc. ) it is preferable to keep it in mind and to consider it like a potential danger. One can see there a supplementary reason not to let some Houseleeks lying about in a badly aerated greenhouse!

As curative measures, except a modification of the cultivation conditions, which is not always possible, the good old oxyquinoleine in soil watering (1/4000) is revealed efficient.

3. Colletotrichum gloeosporioides

The fungi of the genus Colletotrichum are the agents of various "anthracnoses", i.e dry rots in blackish circular spots. Thus, Colletotrichum gloeosporioides is known as an agent responsible for anthracnoses on Araceae, Orchids, etc. Being a localized and rather slow-diffusing infection, its treatment consists in ablation of the parts affected, chemical treatment is based on dichlofluanide and has only a preventive action.

Without personal experience of this parasite (at least without having identified it positively as such) the following information is extracted from Chase A.R., Leaf rot of four species of Crassulaceae caused by Colletotrichum gloeosporioides, in Plant Pathology, 32(3): 351-352 (1983).

This fungus is frequently met in commercial cultivation in Florida (USA) on various Crassulaceae among which Sempervivum. It entails there average losses of 10% of the production. The contamination seems to be only possible by a traumatism of tissues, that can be however minimal.

Colletotrichum gloeosporioides entails a black rot of the leaves contaminated, of rather slow evolution (in two weeks after contamination). Rot can scatter then to the rest of the plant or the more often remain localized to the contaminated leaves.

4. "Translucent" rot

This infection, of which the precise identity of the responsible organism(s) (probably Phytophthora sp.) is uncertain, poses a real problem at the time of the wintering in damp conditions. The adult leaves become dull and yellowish, then translucent, and at the end brownish with a covering , if rain doesn't wash them out, of a whitish beige veil. The attack is progressive and starts from adult or intermediate leaves, young leaves generally resisting well and a long time to the infestation. This one passes on from leaf to leaf, but affects more rarely, and often very partially, the stump. However, some sorts are more sensitive than other ones and their rosettes can rot fully and quickly at the least attack.

Preventively and curatively, it is advised to remove a maximum of these rotting leaves, because it limits (a few) the direct contamination and (especially) airs the rosette while facilitating their drying. One won't forget to protect from slugs the stumps thus denuded by this peeling, if not the remedy risks to be worse than the illness!

This infection transforms in winter a beautiful tuft of Houseleeks to a set of cores where only a few skinny terminal vegetative points remain, and makes often some rosettes to disappear. It is not generally catastrophic because the main part of the reserves necessary for the starting again of growth is stocked in the stumps and the roots, and damages are quickly repaired in spring. Nevertheless, the aesthetic result is pitiable and all sorts don't overcome this trial as well.

This kind of rot is the main limiting factor in Houseleeks cultivation. It forbids for some of them a wintering out of shelter in regions with high pluviometry and hygrometry. Even under shelter, it is difficult for some of them to avoid it at the time of humid winters, especially if the plants have been sheltered with their humid clod or if the ventilation is insufficient. Even during summer, some natural clones can suffer from it, according to their sensitivity, under oceanic climate. This type of rot can also follow the damages due to hail, the succulent structure of their leaves making Houseleeks rather vulnerable to injuries that it entails, especially in spring, a period during which it is impossible in plain for them to avoid a relative level of etiolation and therefore of mechanical fragility.

As chemical struggle one can find advised as fungicides against Pythium and Phytophthora on Sempervivum fosetyl (Aliette®) and metalaxyl.

5. Botrytis cinerea

Let's note that the very well-known gray rot produced by this ubiquitous and polyphage fungus is surprinsingly named in France "Pourriture noble (noble rot)" when it affects the grape, whereas some other much less honorary names are prefered when it honours the other plants...

This affection can be observed on Houseleeks as on a lot of other plants in damp conditions. Suddenly, a rosette takes a dark color and softens then becomes covered in a few days by a powdery gray down. The rosette is lost irreparably because its stump is destroyed at the same time as the leaves, but the attack is generally limited to only one rosette that it is necessary to hurry then to remove (without too sprinkling the neighbours with spores...). The sensitivity is very variable according to species, which are generally much more affected than cultivars, especially at young seedling state.

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Fungal diseases

1. Endophyllum sempervivi

1.1. Endophyllum and its host

1.2. Symptomatology and life cycle

1.3. About host-parasite relations

1.4. Associated pathology

1.5. Natural distribution

1.6. Endophyllum sempervivi in cultivation

2. Rhizoctonia solani

3. Colletotrichum gloeosporioides

4. "Translucent" rot

5. Botrytis cinerea