Soil Fungi As a Biotic Factor Affecting on the Plants

SOIL FUNGI AS A BIOTIC FACTOR AFFECTING ON THE PLANTS

propahul [Methodological approaches of plant sort of cucumber sorts and hybrids in agrophytocenoses]. evaluation using of resistance to plant fungal patho- Extended abstract of Candidate′s thesis. Kyiv [in gens]. Ahroekolohichnyi zhurnal — Ahroecological Ukrainian]. journal, 3, 90–93 [in Ukrainian]. 21. Beznosko, I.V. (2013). Rol’ askorbinovoyi kysloty i 16. Parfenyuk, A.Í. (2009). Sorti síl’s’kogospodars’kikh tsukriv u vzayemodiyi sortiv pertsyu solodkoho ta kul’tur, yak faktor bíokontrolyu fítopatogennikh mikromitsetu Alternaria solani (Ell. et Mart.) [The míkroorganízmív v agrofítotsenozakh [Sorts of crops role of ascorbic acid and sugar in interaction of sweet as factor of biocontrol of pathogenic microorga - pepper sorts and micromycete Alternaria solani (Ell. nisms in agrophytocenoses]. Ahroekolohichnyi zhur- et Mart.)]. Ahroekolohichnyi zhurnal — Ahroecologi- nal — Ahroecological journal, Special Issue, 248–250 cal journal, 4, 130–132 [in Ukrainian]. [in Ukrainian]. 22. Blahinina, A.A. Ekolohichni osoblyvosti vzayemo - 17. Parfenyuk, A.Í., Kulinich, V.M., Krut’, V.Í. (2009). diyi henotypiv pshenytsi ta patotypiv fitopato- Sorti buryaka stolovogo, yak faktor bíokontrolyu henykh hrybiv [Ecological features of wheat geno- fítopatogennikh míkroorganízmív [Sorts of red beet type interaction with pathogenic types of fungi]. as a factor of biocontrol of pathogenic microorgan- Extended abstract of Candidate′s thesis. Kyiv [in isms] Ahroekolohichnyi zhurnal — Ahroecological Ukrainian]. journal, Special Issue, 251–253 [in Ukrainian]. 23. Blahinina, A.A., Parfenyuk, A.I. (2013). Vplyv me- 18. Parfenyuk, A.Í., Chmíl’, O.M., Pasinok, Í.V. (2009). tabolitiv roslyn riznykh sortiv pshenytsi ozymoyi na Chisel’níst’ fítopatogennikh gribív na líníyakh ta intensyvnist’ propahuloutvorennya hrybiv Fusarium gíbridakh ogírka [Number of plant pathogenic fungi oxysporum Schlecgt. ta Alternaria tenuis Ness.Ness. etet Fr.Fr. on lines and hybrids of cucumber]. Ahroekolohich- [The influence of metabolites of different sorts of nyi zhurnal — Ahroecological journal, Special Issue, winter wheat on intensity of sporulation of Fusarium 254–255 [in Ukrainian]. oxysporum Schlecgt. and Alternaria tenuis Ness. et 19. Parfenyuk, A.Í., Beznosko, Í.V., Gorgan, M.D. (2012). Fr.]. Ahroekolohichnyi zhurnal — Ahroecological jour- Vpliv sortív í gíbridív pertsyu solodkogo na ínten- nal, 2, 87–90 [in Ukrainian]. sivníst’ sporoutvorennya fítopatogennikh gribív 24. Parfenyuk, A., Sterlikova, O., Beznosko, I., Krut′, V. rodu Fusarium [The influence of sorts and hybrids (2014). Osobluvosti vzaemodii bakterialnogo of sweet pepper on intensity of spore reproduction of shtamy Micrococcus luteus LBK1 z roslynamy sor- plant pathogenic fungi from genus Fusarium]. Nau- tiv/hibrydiv ohirka ta pertsyu solodkoho ta hrybom kovyy visnyk NUBiP — Scientific Journal of NULAS, Fusarium oxysporum Scelecht [Features of interac- 178, 59–64 [in Ukrainian]. tion of bacterial strain Micrococcus luteus LBK1 20. Sterlikova, O.M. (2013). Formuvannya populya- with sorts/hybrids of cucumber and sweet pepper tsiy fitopatohennykh hrybiv pid vplyvom sortiv ta and fungus Fusarium oxysporum Scelecht]. Mikro- hibrydiv ohirka v ahrofitotsenozakh [Formation of biolohichnyy zhurnal — Microbiological journal, 1, plant pathogenic fungi populations under influence 33–37 [in Ukrainian].

УДК 631.466 SOIL FUNGI AS A BIOTIC FACTOR AFFECTING ON THE PLANTS E. Kopylov, O. Nadkernichna Інститут сільськогосподарської мікробіології та агропромислового виробництва НААН Наведено сучасні погляди на роль ґрунтових грибів у мікробно-рослинній взаємодії. Визначення взаємовідносин грибів з рослинами можуть бути науковим підґрунтям для розробки засад оптимізації функціонування симбіозів і асоціацій мікроорганізмів з рослинами, що відкривають шлях як до створення нових екологічно безпечних мікробних препаратів, так і для їх практичного використання у рослинництві. Ключові слова: ґрунтові гриби, симбіоз, ендофітна асоціація, мікориза, фітогормони, фітотоксичні речовини.

Soil fungi are presented by different taxo- mental groups which differ by feeding type nomic units belonging to certain environ- and interaction with other organisms. Among them saprophytes destroying plant and ani- © E. Kopylov, O. Nadkernichna, 2017 mal residues, facultative and obligate plants

2017 • № 2 • АГРОЕКОЛОГІЧНИЙ ЖУРНАЛ 163 E. KOPYLOV, O. NADKERNICHNA parasites, mycorhiza-forming and predator parasites change over to the resting stage. The fungi occur. Soil fungi are presented by all main feature of saprophytic fungi that rapidly mentioned classes: Phycomycetes, Ascomyce- appropriate readily accessible carbohydrates tes, Basidiomycetes, Deuteromycetes. is active mycelia growth, rapid spores’ germi- Fungi play an important role in organic nation and dormant forms in the presence of compounds transformation, first of all — cel- a suitable substrate. In the first place these lulose, lignin and pectin. Also they have sig- fungi include class Zygomycetes, generally nificant role in nitrogen cycle, particularly Mucorales molds, and some types of imperfect ammonification processes, making conditions fungi, particularly Penicillium, Aspergillus aandnd for development of other microorganisms. other genus. Many of them are characterized Besides, the soil fungi are able to produce by the ability to form antibiotics and toxic different biological active substances: amino substances, which creates more opportunities acids, enzymes, lipids, polysaccharides, anti- to fight for nutritional resources [1]. biotics, plant growth stimulants, vitamins and Cellulose decomposing fungi grow slower toxic substances. and cannot compete with fungi that rapidly The soil fungi have an adsorptive type of assimilate easily available carbohydrates. This nutrition; therefore they are closely associated group includes members of ascomycetes and with the substrate and have a large absorption imperfect fungi. The most active cellulose surface. Fungi are characterized by their fila- destroyers are Ascomycetes and Deyteromi- mentous structure, rapid growth of mycelium cetes. Among them there are Fusarium, As- apex at length and active metabolism. This pergillus, Penicillium, Stachybotrys, Trichode- promotes for fast substrate colonization, and rma, Cladosporium genus. For the most fungi possibility for producing antibiotic and toxic hyphal growth is one from many examples of substances increases their competitiveness morphological structure adaptation to the according to substrate adaptation. Using sub- substrate conformation. Basidiomycetes be- strate fungi metabolism is decelerating and long to the group destroying lignin. They chlamydospores, sclerotiums or another dwell grow slowly and begin to develop when all structures are formed. Spores can be easily come-at-able carbohydrates are used. There transferred from one to another substrate, is an evidence that some types of deytero- which provides high adaptability of fungi for micetes are also able to decompose lignin. environmental conditions. There are Trichoderma, Fusarium, Aspergillus, Depending on substrate decomposition Penicillium among them. As far as plant pick- a succession of fungi species is taking place ings being destroyed fungi utilizing specific presented by facultative parasites (fungi pen- humus substances begin to develop. Usually etrating in plant roots), saprophytic fungi they don’t require a large amount of nutrients (which absorb readily available substances: [2, 3]. sugars, starch, hemicellulose) and fungi that Fungi distribution on the root surface (in destroy cellulose and lignin. rhyzoplana) is not only the result of substrate Facultative parasites penetrating in plants specificity, but it also depends on fungi com- roots proceed to exist there for some time petitive abilities. The roots surface contains after the root death. Their parasitism lies in both saprophytic fungi and facultative para- the verge of saprophytic existence, and they sites. They grow rapidly, form extracellular are mainly presented by fungi of the genus enzymes actively, destroy the host plant cells Fusarium, Pythium, Corticium, as well as some penetrating into them, but they may change types of Cladosporium. Their mycelium grows a type of nutrition to saprophytic. They are on root surface and opens the way for inva- also considered as soil fungi, although many sion by saprophytic fungi which absorb read- of them can be found as soil dormant stage ily accessible substances and rapidly take over and germinate only under the influence of the space among the dead plant residues. Be- root exudates. In plant rhizosphere, where ing unable to compete with them, facultative favorable conditions for the most plants and

164 AGROECOLOGICAL JOURNAL • No. 2 • 2017 SOIL FUNGI AS A BIOTIC FACTOR AFFECTING ON THE PLANTS microorganisms are created thanks to ek- synthesis, pigments formation, biosynthesis of zosmos the content of fungi is much greater metabolites and plant resistance to environ- than in soil without plants. The specificity of mental stress factors. The greatest biological root secretions determines the composition of activity has indolyl-3-acetic acid (IAA). Also rhizosphere fungi species. Fungal communities there are another compounds with auxin ac- depend on physiologically active substances tivity which are indoles in most cases and secreted by the root cells. Rhizosphere micro- similar to the IAA by chemical structure. organisms, in turn, affect the plant through These indole compounds can be the precur- the root system, producing growthregulated sors of indolyl-3-acetic acid, or the products substances. of its further transformation. 1. Phytohormonal impact of fungi on Molds of genus Fusarium, Rhizoctonia, plants. Rhizopus, Absidia, Aspergillus, Penicillium, It used to suppose that coordination of Monilia, Phoma, Pythium, Trichoderma, Ac- regulation system, the processes of growth tinomucor, Amanita can produce auxins, such integration and development of plants is ef- as indolyl-3-acetic acid. The ability to syn- fected by means of plant hormones, which thesize IAA is inherent for many pathogenic are synthesized by specialized plants tissues fungi genus such as Taphrina, Phytophtora, and operate in extremely small doses. Later it Ustilago, Alternaria, Fusarium, Plasmodiopho- was proved that many microorganisms which ra, Colletotrichum, Phymatotrichum, Lentinus, closely interact with plants are also capable to Sclerotium, Monilia, Rhizoctonia. Mycorrhizal synthesize phytohormones. For today phyto- fungi of genus Laccaria, Pisolithus, Amanita, hormones are considered to be specific media- Rhizopogon, Paxillus, Hebelota also synthesize tors of communication between host plants IAA [7–12]. and microflora associated with it [4, 5]. Despite the fact that plants and microor- Synthesis of phytohormones is inherent to ganisms are able to synthesize IAA, different rhizosphere, epiphytic and symbiotic micro- ways of its formation exist. Thus, in plant cells organisms stimulating and improving plant IAA is generated de novo from tryptophan growth and development. At the same time by oxidative deamination through indolyl-3- phytohormones are synthesized also by patho- pyruvic acid and indole-3-acetaldehyde, or by genic microorganisms, whereby in amounts generation of an intermediate product — tryp- that greatly exceed plant needs. This type of tamine through indole-3-acetaldehyde [13]. phytohormones hypersynthesys by pathogens Microorganisms have 5 different ways of unbalances plant hormonal system and be- IAA biosynthesis, and only three of them in- comes a factor of many diseases [6–8]. herent to fungi. Thus, the majority of Fusari- It is known that higher plants contain sev- um, Rhizoctonia and Colletotrichum phytopath- eral important classes of hormones: auxins, ogenic molds have the most common way of gibberellins, cytokinins, abscisic acid and ethy- IAA formation through indolyl-3-pyruvic acid lene. Recently brasin (brassinosteroid) and and indole-3-acetaldehyde. For unidentified jasmon acid are included to them. Conven- fungi forming mycorrhiza with orchids is typi- tionally, auxins, gibberellins cytokininsand cal alternative way of IAA synthesis via tryp- partly brasinscan be attributed to the stimu- tamyne. Some pathogenic fungi of genus Col- lating substances, while abscisic acid, ethy- letotrichum have biosynthesis of IAA occuring lene and zhasmon acid are the inhibitors. via indolyl-3-acetamide [5, 6, 10, 11]. Auxins are the first phytohormones that In plants IAA is bound with sugars, amino were investigated. Auxins are responsible for acids and proteins making inactive (reserve) the plant cells and tissues division and dif- forms. If necessary, phytohormones release ferentiation. They stimulate seeds and tubers and regain their physiological activity. Some germination, accelerate root-made processes fungi (Pisolithus iutinctorius aandnd Paxillus invo- and coordinate vegetative growth, tropisms lutus) are also able to produce bound forms of and fruitification. They influence on photo- indolyl-3-acetic acid [5, 14].

2017 • № 2 • АГРОЕКОЛОГІЧНИЙ ЖУРНАЛ 165 E. KOPYLOV, O. NADKERNICHNA

A lot of fungi are characterized by presence commune also capable to produce gibberellins. of several ways auxin biosynthesis expanding Active producers of gibberellins occur among their ecological abilities in formation of asso- pathogenic fungi: Ustilago mayis, Sphacelo- ciations and symbioses with plants. Epiphytic ma manihoticola, Cercospora rosicola, Bot- and rhizosphere molds have the leading role ryodiplodia theobromae, Fusarium semitectum, in conversion of tryptophan, which is con- F. acuminatum, F. anguioides, F. avenaceum, tained in plants’ exudates to indolyl-3-acetic F. chlamydosporum, F. equiseti, F. osysporum, acid. Adding the tryptophan into the medium F. moniliforme. Some different gibberellic ac- where molds being grown can increase bio- ids (HK3, HK7, HK4, HK13) were found in synthesis of auxins in ten times. The ability conidias of F. graminearum straight after 2:00 to produce IAA actively is a strain feature of hours of spores incubation [5, 16]. the microorganisms. Investigations of gibberellins production Among fungi within the same genus and among plants and molds indicate that during even species high activity strains and strains the evolution plants and molds being formed with law activity of indolyl-3-acetic acid bio- the independent biosynthetic routes of phy- synthesis occurred, and also can happen the tohormones of this group. strains which do not generate the IAA. Cytokinins are the adenine derivative by Auxins make a stimulating effect on growth their chemical structure. Physiological activ- and development not for only plants but also ity of cytokinins differs depending on struc- for microorganisms. First of all, this is nitro- ture of molecule purine ring. This explains the gen-fixing bacteria of Rhizobium, Azotobacter, fact that cytokinins regulate various physio- Azospirillum and Bacillus genus [5, 15]. logical processes: activate RNA and protein Gibberellins are the most common group synthesis in cells with activation of RNA- of phytohormones among plants and micro- polymerase, stimulate plant cell division, pro- organisms, which number is more than 100 mote branching and stimulate seed germina- compounds. Gibberellins belong to the class tion, regulate the formation of chloroplasts, of terpenes and consist of isoprene residues increase stability of photosynthetic apparatus that form four rings as usual. Gibberellic acids during the water stress, contribute to cells HK3, HK7, HK1 and HK4 are the most com- stability residing in adverse environmental mon and biologically active phytohormones conditions [5]. of this group. Microorganisms capable to synthesize The effects of gibberellins aimed at divi- cytokinins are kynetyn, zeatyn, izopentenila- sion and elongation of cells that form a part of denin and some others. Compounds with cy- intercalary meristem, stimulating flowering, tokinin activity are educed in molds of genus activation of membrane synthesis and starch- Paxillus, Rhizopogon, Suillus (forming mycor- splitting enzymes. Unripe seeds are characteri- rhiza with plants) as well as pathogenic fungi zed by the highest content of gibberellins in belonging to the genus Uromyces, Schizophyl- plants. Different stages of plant ontogenesis lum, Taphrina [9, 17]. can differ by contents and set of gibberellins. For a long time plants failed to identify Gibberellins are synthesized in different parts genes of cytokinins biosynthesis. This gave of plants, but generally in leaves [13]. a reason to doubt that plants actually create The ability of gibberellins’ biosynthesis these hormones, but in 2001 Arabidopsis tha- is detected among all groups of microorga- liana was explored the genes that encode func- nisms, but the most active producers, capable tionally active key of cytokinins enzyme — to form more than 1000 mg/l of gibberellic isopentenyltransferase biosynthesis were acid are the molds Phaeosphaeria and Gib- identified [4, 9]. The same genes were also berella fujikuroi. The molds belong to species found in bacteria and pathogenic fungi such Aspergillus flavus, A. niger, Penicillium cory- as Taphrina cerasi [9, 18]. lophilum, P. cyclopium, P. funiculosum, Ver- Exogenous cytokinins stimulate micro- ticillum sp., Rhizopus stolonifer, Shizophillum organisms’ antibiotic, amino acids and some

166 AGROECOLOGICAL JOURNAL • No. 2 • 2017 SOIL FUNGI AS A BIOTIC FACTOR AFFECTING ON THE PLANTS enzymes biosynthesis and also affect on con- competence is determined by the presence of tent of endogenous phytohormones in micro- specific receptors [13]. organisms. It is important that mixed culture 2. Soil fungi-producers of phytotoxic of microorganisms form a larger number of substances. auxins, gibberellins and cytokinins than pure Soil molds are able to synthesize phyto- cultures. As a result, biosynthesis of phytotoxins depressing growth and plants’ develop- hormones has been increasing greatly in pres- ment as well as they produce different kinds ence of microorganisms’ associations interact- of phytohormones. ing with plants [9, 18, 19]. A lot of soil microorganisms are charac- Plants’ metabolites exuding in rhizosphere terized by phytotoxic activity. Thus, among contain a variety of biologically active com- all the selected soils microorganisms in cher- pounds that are the source of microorganisms nozem soils 11–28% occurs, in sod-podzolic nutrition, phytohormones can be signal mole- soils — 32–38% phytotoxic microorganisms cules for harmonizing interactions between [21, 22]. Largely content of phytotoxic mi- plants and rhyzosphere microorganisms. For croorganisms depends on agriculture kind. example, the interaction with plants in root In cultivated soils their content is much less exudates containing tryptophan biosynthesis than in virgin soils. Particularly, strong influ- of auxins by microorganisms also increases, ence on phytotoxic microorganism content because tryptophan is a precursor of auxins has permanent crops growing and their high and rhyzosphere plant microflora has a key rotation. In addition, the content of phyto- role in its transformation into IAA. Syn- toxic microorganisms depends on soil type, thesized by microorganisms phytohormonal degree of cultivation, farming practices and substances, in turn, affect both the plant vegetation characteristics [23, 24]. and the producers. Therefore plants and as- Despite the fact that ability to produce sociated microorganisms that inhabit one phytotoxic substances was found in many ecological niche should be considered as a types of soil microorganisms, phytotoxic sub- solitary system. However, each participant stances are isolated and characterized only for in this system is characterized by its own certain types. This is due to the fact the estab- biochemical activity, and finally synthesizes lishment of the secondary metabolites chemi- the same plant hormones, the difference of cal structure is quite a challenge. Instability which is in concentration only. In struggle and lability of many phytotoxic substances in for existence, those rhizosphere microorgan- soil further complicates the problem. isms receive benefits which can secrete phy- In 1970 T. Mirchynk proposed a division tohormones, that allows them to colonize between toxins, phytotoxins and antibiotics rhizosphere soil, root surface and penetrate undertaken on the basis of concentrations into the internal plant tissues more succes- within their effect on the object. This ap- sfully [9, 20]. proach has been very effective. On this basis The activity of phytohormones produced active phytotoxins can be compounds in con- by molds is provided by their interaction with centrations that do not override 100 mkg/ml specific receptors (allosteric proteins) that negative effect on plants, without showing recognize plant hormones, specifically bind effects on animals and microorganisms. It be- with it, forming a hormone-receptor complex. longs to phytoxins-antibiotics group when This complex transmits signals required to phytotoxic and antibiotic effect is expressed run cell appropriate physiological response. within the compound concentrations up to It is important that the same hormone can 100 mg/ml. Thus, viktorin is the typical phy- connect to different receptors, causing under totoxin because its activity expresses in con- different physiological responses. This fact centration of 0.02 mkg/ml, while it does not explains the reasons of phytohormones mul- influence on animals and microorganisms. As tifunctional action. Phytohormones influence well, fusaric acid is the typical phytotoxin on the so-called «competent» cells, and their because its phytotoxic activity expresses in

2017 • № 2 • АГРОЕКОЛОГІЧНИЙ ЖУРНАЛ 167 E. KOPYLOV, O. NADKERNICHNA concentration of 0.1–5.0 mkg/ml, while an- are in the same concentrations have nega- tibiotic activity occurs only in concentration tive effect on the microorganisms. So they are of 500 mkg/ml. Generally, the majority of soil phytotoxins-antibiotics. molds toxic compounds can be attributed to Patulin is the most studied phytotoxin- phytotoxins-antibiotics [21]. antibiotic (producers — Penicillium and As- Mold phytotoxic substances related to pergillus), citrinin (producers — Penicillium the chemical nature of peptides or amino and Aspergillus), penicilloic acid (producers — acid derivatives were investigated. These Penicillium and Aspergillus), rubratoxin (pro- compounds are formed by phytopathogenic ducer — Penicillium purpurogenum), alternaric molds as usually and characterized by high acid (producers — Alternaria tenuis aandnd Alter- biological activity and specificity for host- naria solani) and others [1, 25, 26, 28]. plant. This group includes viktorin (produ- Saprophytic microorganisms are also able cer — Helminthosporium sp.), HC-toxin (pro- to synthesize typical phytotoxins that don’t ducer — Helminthosporium sp.), alternarin demonstrate antibiotic activity. Thus, the soil (producer — Alternaria sp.), tentoxin (pro- molds of Chaetomium and Gliocladium genus ducer — Alternaria alternaria), AM-toxin produce phytotoxic substances with active (producer — Alternaria mali) and others [1]. concentration of range 5–10 mkg/ml accord- Some saprophytic molds from genus As- ing to a wide range of crops. These are glycoli- pergillus produce malformin, its phytotoxic pids and ketones by their chemical structure. activity is detected in concentrations of 0.1– The action of phytotoxic effects is in violation 0.2 mkg/ml. By its chemical structure mal- of plant cells penetration mechanism, reduc- formins are cyclical pentapeptides, consisting ing cell growth in stretching zone. Besides, of cysteine, valine, leucine at different ratios the profound violation in nuclear cell takes [1, 25, 26]. place: structural changes of chromosomes oc- Phytotoxic activity towards to tomatoes, cur, vacuolation of nuclear and their lizis also potatoes and grapes has some amino acids can happen [29]. derivatives like lycomarasmine (some species Aflatoxins are the group of compounds of Fusarium are producers) and lycomaras- similar to dihydrofuran (coumarin). Some mine acid (some species of genus Fusarium, species of Aspergillus pproduceroduce tthem.hem. Aspergil- Aspergillus, Colletotrichum, Pyrenophora are lus flavus is the most active toxin-maker. At producers) [27, 28]. low concentrations these compounds are tox- Some soil molds (mainly phytopathogenic ic to warm-blooded animals, fish, insects and fungi) form compounds related to glycopep- microorganisms, thus they can be described tides and other carbohydrates derivatives. as toxins-antibiotics [1, 25, 28]. This group of substances (producers — Heterocyclic compounds containing nitro- Helminthosporium sp.) and other phytotoxins gen have a high phytotoxic activity. Among is characterized by high activity and specifici- them there are picolinic acid, fusaric acid ty for certain plants (producers — Helminthos- (which is a derivative of picolinic acid) and porium maydis, Phomatra cheiphila, Phialo- viridikatin. Pseudomonas (P. putida) bacte- phora cinerescens, Verticillium dahliae, some ria can be active producer of picolinic acid. species of Cladosporium). All the above-men- Different species of Fusarium molds produce tioned toxins, occurring high activity against picolinic and fusaric acids. Phytotoxic effect plants do not act on microorganisms, namely of these compounds is in the range of 1– they are typical phytotoxins [1, 28]. 10 mkg/ml, cotton and tomato plants are par- Pathogenic microorganisms toxins are ticularly susceptible to them [1]. intensively studied due to their role in the From Dendrodochium toxicum individual plants pathogenesis. There is a great interest substances called Dendrodochium mold toxin to toxins of soil saprophytic microorganisms. I, II, III, IV were isolated. The substances But unlike pathogenic microorganisms these demonstrate strong toxic properties and cause molds produce phytotoxic compounds which disease, called Dendrodochiotoxicosis. At the

168 AGROECOLOGICAL JOURNAL • No. 2 • 2017 SOIL FUNGI AS A BIOTIC FACTOR AFFECTING ON THE PLANTS same time the substances were characterized crop hybrids resistable to diseases and ad- by phytotoxic properties (active concentra- verse environmental factors of creation an tion of 30 mkg/ml) in relation to seedlings of artificial infectious background. Their usage oats, barley, lupine, beans. The most sensitive is justified by the fact that phytotoxins are to the toxic actions were cabbage and radi- able to decompose quickly and not to be shes. The chemical nature of the toxins were accumulated in soil and other substrates, terpenoids (macrocyclic compounds), rather which is very important for the environment trichothecenes [30]. safety. The complex of highly toxic metabolites 3. The symbiosis between fungi and plants produced by the mold Stachybotrys alter - (mycorrhiza). nansis ccalledalled Stachybotrys-toxin.Stachybotrys-toxin. ConsideringConsidering Many of soil fungi are able to engage into the highly toxic activity toward to animals close symbiotic relationships with plants, and humans Stachybotrys-toxin demonstrates forming mycorrhiza. According to the lite- phytotoxic activity, provokes necrosis and rature sources of last decades mycorrhizal death of plant tissues, and inhibits germina- symbioses between fungi and plants are wide- tion of crops. The chemical nature of Stachy- spread and comprehend up to 85% of vascular botrys-toxin belongs to steroids [28]. plants on the Earth. Carbocyclic terpenes produced by Fusi- According to modern appreciation mycor- coccum amygdali also have a strong phyto- rhiza is a structural formed mutualistic sym- toxic effect on tomato plants, peaches and biotic association between plant roots and almonds.Fusicoccin, allofusicoccin and iso- fungi where the organisms coexist in mutually fusicoccin are known among them. By their beneficial relationship. chemical structure they are similar, but differ The development of symbiosis between by their phytotoxic activity. Thus, the active fungi and plants is a complex multistage proc- fusicoccin concentration is 2, allofusicoccin — ess that involves recognition, signaling and 20, isofusicoccin 50 mkg/ml [1]. interaction between fungi and plants. Mycor- Many species of soil molds (Aspergillus rhiza formation is mutually beneficial for both niger, Penicillium oxalicum, P. citrinum, P. are- fungus and plant. However, plants are able to naria, P. luteus, Sclerotinia sclerotiorum) pro- grow and develop without mycorrhizal fungi duce oxalic and citric acids, which phytotoxic while fungal spores are able for only limited effects appeared in concentrations of 250– germination and hyphae growth without 300 mkg/ml on vetch plant, lupine and peas. plants. This demonstrates that plant signals Dibasic unsaturated fumaric acid was isolated perfom the leading role to the symbiosis ini- from the culture liquid of Rhizopus sp. — al- tiation. Last years a large number of attention mond roots and branches pathogen. Effect was paid to studying signal interaction in of pure fumaric acid causes the same symp- processes of mycorrhiza forming. In spite of toms. The mold Rhizoctonia solani produces this the nature of plant signals of different phenylacetic and hydroxyphenylacetic acids stages is not described yet. demonstrating phytotoxic effects at doses of It was shown that some plant flavonoids 5–50 mkg/ml to rice, cotton, sugar beet and are capable at the low concentrations stimu- lucerne. Penicillium molds are capable to pro- late arbuscular-vesicular mycorrhiza fungi duce salicylic and cinnamic acid, which phy- growth. Estradiol is the most active among totoxic activity occurs at the concentration the flavonoids that make a stimulating effect within 150–200 mkg/ml, [1, 25–27, 31]. on mycorrhizal fungi. There is information Disclosure of the interaction features be- about the role of plant phytohormones, par- tween phytotoxic molds, other units of rhizo- ticularly cytokinins in mycorrhiza forming. sphere microbiota and plants has essential Despite the results, most researchers believe scientific and practical importance. The toxic that no flavonoids or plant hormones are the substances of microbial origin have practi- key signaling molecules in colonization of cal usage in breeding the new varieties and plant roots by mycorrhizal fungi. Perhaps un-

2017 • № 2 • АГРОЕКОЛОГІЧНИЙ ЖУРНАЛ 169 E. KOPYLOV, O. NADKERNICHNA known secondary metabolites of plants are dense mesh (mantle). Hyphae don’t penetrate acting this role [32]. into root cells but there is septate mycelium During last years, much researching was among root cells. The level of chlorophyll is devoted to studying the molecular processes usually accrued in such case. Most of gymno- that occur during mycorrhizae formation. sperms as usual as angiosperms of Pinaceae, Interaction between mycorrhizal fungi and Betulaceae, Dipterocarpaceae, Myrtaceae, plants is a complex process, implemented Fagaceae and Rosaceae families form ecto- through the molecular mechanisms. During mycorrhiza [35]. symbiosis formation and functioning the in- Arbutoides mycorrhiza is formed by ba- teraction between partners combining into sidiomycetes, ascomycetes and zygomycetes supraorganismal genetic system occurs. Close fungi class together with Ericales plants. The integration between metabolic partners, for- most typical examples are strawberry tree mation of specialized symbiotic structures (Arbutus unedo L.) forming mycorrhiza both and reproductive velocity regulation by sym- with Arctostaphylos and Pyrola plants. The biont plant is the result of mentioned system. roots are covered with hyphal mantle like Symbiosis forming is a special development ectomycorrhiza but differ from it penetrating strategy evolutionarily related to the general into root cells [36]. morphological programs. It had been organi- Monotropoides mycorrhiza is like arbu- zed during the evolution process together toides but Monotropaceae plants don’t in- with microorganisms [32–34]. crease chlorophyll maintenance forming as- Today several types of mycorrhizawere are sociation with fumgi. Thus Tricholoma fungi described. Vesicular-arbuscularmycorrhiza is form mycorrhiza with Pityopus and Allotropa the most studied. It is usually formed by ob- plants. Basidiomycete Hydnellum form my- ligate symbiont fungi from class Zygomycetes corrhizal symbiosis in biocenosis containing order Glomales, genera Glomus and Sclero- Hemitomes and Monotropsis plants. Mono- cystis. At various times the exhibitors of these tropoidesmycorrhiza usually formed by Ba- genues were isolated from penitsetum roots sidiomycetes, Ascomycetes and Zygomycetes tissues (Pennisetum pedicellatum Trin.), euca- fungi [36]. lyptus (Eucalyptus camaldulensis Dehnh.), Ericoides mycorrhiza is formed by ba- white acacia (Faidherbia albida (Delile) A. sidiomycetes and ascomycetes together with Chev.), himonobambuku (Chimonobambusa Ericales plants order, for example — Hy- quadrangularis (Fenzi) Markino), erehtytesu menoscyphus ericae. This type of mycorrhiza (Erechthites valerianifolia (Walf.) DC.), hin- is characterized by penetrating hyphae into hobiloba (Gingobiloba L.), taro (Colocasi for- root cells and hyphae curls in root hair cells mosanum Hayata, Colocasia formosa-num TT [36]. Chang & T. Chen) and rice (Oryza sativa L.) Orquidoides mycorrhiza is distinctive for [35, 36]. the orchid plants (genera Gastrodia) which Arbuscular mycorrhiza is characterized by often suffer from chlorophyll deficiency and arbusculs and vesiculs in plants’ roots cortical they are forced to join an association with Ba- cells. Straight hyphae and their swirls mostly sidiomycetes fungi. Fungi hyphae are braided aseptate can be identified in tissues. Coloniza- around the orchid plants’ roots inside and tion is occurred only in rhizoderma and root outside. Hyphae curls are present also in bark parenchyma. Fungi never penetrate into stems of plants [32]. the vascular cylinder and meristem region Ectomycorrhiza and endomycorrhiza [35]. Spores are formed in soil or in roots. In formed by Basidiomycetes, Ascomycetes soil foliar hyphae are also developed forming and Zygomycetes fungi classes with gymno- the «external mycelium» [32]. sperms and flowering plants is specific for Ectomycorrhiza is formed by Basidio my- them. Ectomycorrhiza fungi cover with dense cetes, Ascomycetes and Zygomycetes fungi mesh (mantle) thick lateral roots. Septate classes; they cover thick lateral roots with a mycelium is growing among root cells. Ecten-

170 AGROECOLOGICAL JOURNAL • No. 2 • 2017 SOIL FUNGI AS A BIOTIC FACTOR AFFECTING ON THE PLANTS domycorrhiza has been less studied. It is tablished that Chaetomium globosum had been similar to endomycorrhiza but differ with its present among complex of endophytic fungi hyphae presenting inside root cells. Hyphal infecting leaf tissues, stems and roots of pink mantle also can be absent. Both ecto- and periwinkle (Catharanthus roseus) [45]. endomycorrhiza lead to rising up chlorophyll We revealed that soil saprophytic mold maintenance in plant leaves [32, 36]. Chaetomium cochliodes can form mycorrhiza Mycorrhiza formation is mutually benefi- with plants of spring wheat and soybeans. It cial process both for plants and fungi. There- grows rapidly on plants’ roots forming car- from fungi get an access to products of plants’ posomes on the root surface and hairs and photosynthesis, at the same time fungal hy- penetrates into rhizoderma cells which can phae branch in soil giving the opportunity for be the evidence of endophytic association mycorrhizal plants to rise up the bulk of soil between the mold and plants. It has all the available for them. Plants with mycorrhizal hallmarks of mycorrhiza, namely ectendomy- roots are better adapted to the environment. corrhiza. Chaetomium cochliodes produces They are more protected from adverse en- phytohormonal substance referring to auxins vironmental conditions including drought, and gibberellins by their action and different negative temperature, salinity, soil and air fatty acids. There is arachidonic acid among pollution [37–40]. them. It activates systemic immune response 4. Endophytic associations of sapro- of plants on the effect of pathogens and ad- phytic soil fungi with plants. verse environmental factors [46, 47]. It is well known that some saprophytic Some endophyte fungi are known as pro- soil fungi of genus Trichoderma, Fusarium, ducers of growth regulating substances and Acremonium make endophytic associations can be used as the basic for biological prepara- with plants’ roots. Herewith inherent specific tions creation [48]. Such kinds of biological structures are not formed and no signs of dis- preparations have a number of significant ad- ease are observed [9]. vantages on synthetic growth regulatory sub- During last years some statement appea- stances. They are cheaper and multifunctional red that Chaetomium fungi are able to ex- in comparison with traditional. Also that hibit endofit properties. It has been shown fungi can produce not only phytohormones that Chaetomium globosum infects tissues of but another biological active compound such tropical cereals and legumes Glinus lotoides, as amino acids, fatty acids, vitamins and so Canavalia cathartica and Imperata cylindrica on which have positive influence on plants [42–44]. Using sequences analysis it was es- growth and development.

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