BIOLOGICAL FACTORS OF SOIL FERTILITY
The diversity and abundance of the living population of the soil wasdiscussed in the preceding chapter. The living mass of microbes: bacteria, fungi,actinomycetes, and algae, by itself comprises more than 10 tons in the plow layerof 1 hectare of a well-cultivated, fertile soil. Besides, a great number of protozoa,insects, worms, and other representatives of the living world exist in the soil.
All this soil population performs an immense work, processing considerableamounts of different mineral and organic substances, decomposing plant and animalresidues, participating in the transformation of their decomposition products.
Microbes synthesize and excrete different metabolic products, which,upon entering the soil, confer upon it fertility.
Thanks to the microbial population the dead, loose, geological formationassumes life and becomes a productive body. Conditions necessary for the nutritionand growth of higher plants are thereby created. Microorganisms constitute the mostimportant and indispensable link in the nutrition of plants.
Microorganisms of the soil, not only create the conditions necessaryto the growth of higher plants, but also have a direct effect on them through theirmetabolic products. This chapter deals with the effect of microorganisms as agentsof mineralization of organic compounds of plant and animal residues and as a biologicalfactor necessary for the normal nutrition and growth of plants.
To obtain high yield, fertilizers have been used in agriculture fromancient times. Men used fertilizers long before science established and solved themain problems of soil science, agriculture, agrochemistry, and plant physiology.The rules of fertilization were worked out empirically but, as Pryanishnikov pointedout, many of these rules attained high accuracy.
The Romans, for example, knew of the valuable fertilizer propertiesof animal excrements and of some mineral substances such as ash, gypsum, calciumand marl. Moreover, they knew that the fertilizing value of excrements of differentanimals varied. Of highest esteem was the excrement of birds.
The Romans also knew about green fertilizers. Thus, they plowed ingreen manure on the slopes of Vesuvius in order to increase the fertility of thesoil.
The theory of plant nutrition had not yet been elaborated. Vague assumptionson the presence of some "fat" of the earth (terrae adeps) were made, This"fat" was responsible for the fertility of the soil. In order to -increasethe amount of this "fat", animal excrements were necessary.
Those assumptions contained the nucleus of the humus theory, whichsubsequently became widespread. This theory assumes that the organic compounds areof utmost importance in the nutrition of plants. "Echoes of these ideas canbe heard in the language of different nations. Let us recall that our word 'TUK'(fertilizer) once had two meanings, one of them being 'fat'." (Pryanishnikov,D. N., Plant Nutrition, Coll. Papers, Vol 1, 1952, p 58).
The humus theory of plant nutrition stated that plants feed on organicsubstances present in the excrements of animals and in general in humus. This theory,widespread in the 18th century, was favored by the plant breeders and agrotechniciansof that time, since it was well confirmed by agricultural practice.
The explanations of the favorable effect which organic substanceshad on the growth and fertility of plants differed. The most widespread conceptionwas the assumption that the plant derives (from the organic substances) carbon whichit subsequently incorporates into its body (Davy, 1813).
Other authors thought that the excrements contained certain specialsubstances. Thus, for example, Prof. Vallerius in 1766 assumed that only the organicsubstances or "fat" substances of humus of soil play any role in plantnutrition, other components of the soil serve merely as "fat" solvents.
Some scientists of the 16th--18th centuries and in particular Olivierde Serres, (1600), assumed that the cause of the action of fertilizer is in its heat.
Bernard Palissy in his paper (1563) put forward the idea that thesalt content of the fertilizer plays a role in the growth of plants.
First experimental attempts to elucidate the problem of plant nutritionwere made by Van-Helmont. In his paper (1629) he presented results of five yearsof experiments on growing ivy branches in soil which was given only rain water. In5 years the branch grew and attained a final weight which was 33 times higher thanthe initial weight. The soil thereby did not lose weight. Since the composition ofthe air was not known in those times, Helmont concluded that the plant utilized onlywater and this was sufficient for the plant to build its body.
Analogous conclusions were reached by the French investigator Duhamel.He grew plants in Seine water. He did not have distilled water at his disposal forcontrol experiments, and positive results obtained by him are therefore not trustworthy,since the water from the Seine contained various organic and inorganic substances.
Woodword showed that the point of view of Van-Helmont was erroneous.In his experiments he demonstrated that mint grows better in river water than inrain water and it grows even better and gives greater increase if soil is added tothe water. He presents the following data: the plant-weight gain in grains* during77 days, was as follows: in rain water, 17; in the sewage water of Hyde Park, 139;the same with addition of soil, 284. [*"Grains" is a unit of weight.]
Woodword concluded that not only water but also something else whichis present in the soil is necessary for the growth of plants.
The agricultural practice of those times did not possess any scientificbasis for the elucidation of the observed link between the growth of plants, itsyield and the soil. Foundations of sound scientific knowledge were layed down whenfirst M. V. Lomonosov and then Lavoisier discovered the law of the conservation ofmatter.
Lavoisier discovered the composition of air and the essence of theprocesses of oxidation, burning and respiration. Not long before his death (1794)he wrote, concerning the nutrition and growth of plants, that plants get materialsnecessary for their organization from the surrounding air, from water, and generallyfrom the mineral kingdom (according to Pryanishnikov, 1952).
New methods of chemical investigations elaborated by Lavoisier wereemployed by Priestley, Senebe and Sossur, in order to study metabolism in plants.These scientists showed that plants obtain carbon from air, and that apart from carbonplants require salts.
While noting the importance of atmospheric carbon dioxide as a sourceof carbon, Sossur also thought that the humus of the soil is of great importance.Humus contains a certain substance indispensable for plants; the daily experienceof farmers pointed to a close link between the fertility of the soil and the presenceof organic substances in it.
The English scientist Davy (1813) drew attention to various sugary,glueing, oily, slimy, extractable substances, and to the carbon dioxide of the soil.These elements, according to him, contain all the elements needed for the life ofplants.
The humus theory became very popular after the well-known works ofTeer (1752-1828), the founder of the first agricultural school and the propagatorof crop rotation instead of the three-field system. He wrote that fertility of thesoil depends entirely on humus. since apart from water, humus is the only substanceof the soil which can serve as a nutrient for the plants (according to Pryanishnikov,1952).
These ideas were the basis of a theory of the exhaustion and regenerationof the soil's fertility. It was assumed that the more the plants absorb humic substances,the better they grow, and the greater the crop. Different plants absorb differentamounts of organic substances. For example, wheat requires more humus than rye does.
Teer and his adherents considered humus to be an important productof plants and a substance of the utmost importance for the life of plants. Humusis formed at the expense of plants; some plants excrete more humus than they absorb.In other words, some plants enrich the soil in humus and others exhaust its reserves.To the former category belong clover and other leguminous plants.
The propounders of the humus theory did not take into account mineralsubstances. The latter, according to them, enhance the decomposition of humus andtransform it into a form which can be assimilated by plants.
The humus theory was very popular even in the thirties of the lastcentury in different countries such as Germany, England, France and Russia.
Of the Russian investigators of the late 18th and the beginning of19th centuries, who drew attention to the importance of organic fertilizers, A. Bolotov,I. Komov and A. Poshman should be mentioned. The works of these scientists showedthat fertilizers have an immense influence on the crops, Komov assumed that organicsubstances are necessary for plants to the same extent as they are necessary foranimals, and he recommended to use them in practice. According to him, the organicfertilizers cannot be replaced by salts.
At the beginning of the 19th century the role of nitrogenous compoundsin the nutrition of plants began to be better understood.
Liebig assumed that plants obtain nitrogen at the expense of atmosphericammonia and that its presence in the atmosphere is sufficient for them. However,experiments disproved this. It was found, on the contrary, that this substance ismost insufficient for plants.
The well-known studies of Bussengo revealed the sources of the nitrogenousnutrition of plants, In 1837-38 he developed his theory on nitrogenous fertilizersand recommended the use of fertilizers rich in nitrogen. He connected soil exhaustionwith the depletion of sources of nitrogenous nutrition. In this process, he ascribedvarying importance to different plants. Some plants absorb more nitrogen from thesoil, others less. He ascribed an active role in the enhancement of soil fertilityto certain plants, e. g., clover. "One should think", said he "thatcultures which improve the soil do not limit themselves to its enrichment with C,H, and 02 only, but also enrich it with nitrogen" (according to Pryanishnikov,1945).
Hellriegel (1889), discovered the reason for the peculiar action ofleguminous plants on the fertility of the soil. By his experiments he found thatleguminous plants assimilate nitrogen from the air. Voronin (1886) studied the rootnodules of leguminous plants and found microorganisms in them, which in his wordsare: "The culprits of the formation of the nodules." Later, Hellriegelby thorough experimentation showed that these symbiotic organisms are the cause ofthe nitrogen fixation by leguminous plants.
Thus, the conclusions of the old investigators, for example Teer,have been confirmed by the later experiments of Bussengo, Hellriegel, and others,who found that plants not only exhaust but also enrich the soil with nutrient organicsubstances.
Thus, the humus theory of plant nutrition, of the 18th and first halfof the 19th centuries, was very popular. Fertilization with organic substances wasconsidered to be an essential measure, not only for the increase of yields, but onthe whole for the increase of soil fertility.
The attitude toward the theory of humus or organic nutrition of plants,and in general toward fertilizers changed abruptly after Liebig put forward his theoryof the mineral nutrition of plants. He severely criticized the humus theory of nutritionand considered it basically wrong. He considered all the studies, performed beforehim by physiologists and agronomists, to be inconsistent and meaningless for thesolution of the problem of plant nutrition. He criticized the humus theory of nutrition:"Taking it", in Pryanishnikov's words,"in its extreme expression,and bringing it ad absurdum."
Liebig completely rejected even the possibility of assimilation ofthe organic substances by plants. In his opinion only inorganic compounds can serveas sources of nutrition for plants. He considered humus as a source of CO2which enhances the process of the erosion of silicates and prepares the mineral foodfor the plant.
Liebig did not recognize the role of plants in the enrichment of soil.He severely negated and criticized the notion of "enrichment of soil in sourcesof nutrition." Plants, according to him, deplete soil, carrying off elementsof mineral nutrition with the crops. But the depletion of the soil is carried outby various plants at different rates and in different directions. Some of them takeout from the soil mainly calcium (for instance, peas), others--potassium and silicon(wheat grains). Therefore, the crop rotation, recommended by previous investigators,only slows down the depletion of the soil.
In accordance with his theory, Liebig recommended the introductioninto the soil of mineral fertilizers. The amount of these fertilizers applied shouldtake into account the utilization by plants.
Owing to the authority of its author--Liebig, the theory of mineralnutrition of plants was accepted by his contemporaries with hardly any criticismat all. The authority of Liebig's chemical school supressed all the previous ideasand theories of organic nutrition of plants. Liebig, says Ressel (1933), gave thefinal blow to the theory of humus. Only the most daring would still venture to maintainthat plants take the necessary carbon not from CO2 but from another source.Although. one should admit that we have no proof that plants obtain all the necessaryCO2 in this way.
Liebig's theory was developed and subjected to changes correspondingto the newly acquired factual data. In our country the theory of Liebig was subjectedto a thorough revision by the Academician Pryanishnikov and his followers. Pryanishnikovoriginated his own direction in agrochemistry; he and his students elaborated a seriesof valuable postulates laying a basis for practical measures in agriculture. To himgoes the honour of solving the problem of basic improvements of the nitrogen balancein the agriculture of the USSR. In counterbalance to the theory of Liebig, he ascribeda major importance to the biological processes of the soil and especially of nitrogenaccumulation. Pryanishnikov did not deny the possibility of the assimilation of organicsubstances by plants and he himself showed it experimentally.
Notwithstanding this, the theory of Liebig is still reflected in thestudies of many specialists. In the theory of plant nutrition one observes an obviousunderestimation of the role of the organic substances of the soil, and its importanceof the nutrition of plants is often denied altogether. As a rule, the significanceof the organic substances of the soil is basically formulated in two postulates:
1. Humus substances are reserves of plant-nutrient elements whichbecome available only after they are mineralized.
2. Humus improves the physicochemical properties of the soil, increasesits absorptive capacity, and therefore, promotes also the accumulation of nutrientsubstances--it strengthens the structure of soil particles and with it improves manyother soil properties. Organic fertilizers--manure, compost, etc, prepare the soilfor the acceptance of mineral fertilizers, increase its buffer capacity, etc.
All this is quite true and is confirmed by age-old practice and bymany experiments. However, to reduce the importance of these fertilizers only tothe given postulates will, in our opinion, be inadequate.
The fact of positive action of humus and organic fertilizers on thegrowth of plants cannot be explained by the action of the mineral elements of nutritionpresent in them. Russel (1933), summarizing the experimental data of 60 years workof the Rothamstead Station, said that, although plants can grow satisfactorily andreach full development on inorganic nutritious substances only, under natural conditions,however, their nutrition takes place in the presence of organic substances. The questionwhether these substances play any active role in this process has been very muchdiscussed. The experimental data are not very conclusive. In the Rothamstead fieldexperiments none of the combinations of the artificial fertilizers is as effectiveas manure in maintaining crops from year to year.
The extensive field experiments of the German investigators Gerlach,Hansen, Schultz, Wagner, Schneidewind, and others, lead us to the conclusion thatwhatever the amount of the mineral fertilizer may be, if using mineral fertilizersonly, one cannot reach as high yields as by the simultaneous introduction of manure(Schneidewind, 1933). Summarizing experiments of many years in the Lauchstadt Station,Schneidewind gives us as an example the following data from sugar-beet yields incentners per hectare: with only mineral fertilization--roots, 487.6; sugar content,77.66; tops, 291.7; under mixed fertilization mineral and organic (manure)--roots,533.6; sugar content, 88.11 and tops, 366.6.
Similar data are given by Schneidewind for potato crops. By usingartificial fertilizers only he could not get more than 240 centners of potatoes perhectare, while by the introduction of mineral fertilizers and manure the yield roseto 306-312 centners per hectare. This effect of manure repeated itself year afteryear and was independent of the amount of precipitation whether it was a dry, wet,or average year.
Russel (1933) and his co-workers have shown that the organic substancesof the soil stimulate the growth of plants and increase crops. He concludes thatno mixture of artificial fertilizers can be as effective as manure in maintainingsteady high crops year after year.
Academician V. I. Palladin (1924), concerning the problem of plantnutrition, wrote that green plants can nourish themselves on ready-made organic compounds.Such nutrition may go on parallel to the assimilation of carbon from the atmosphere.According to the author's observations, green isolated leaves of plants grown withartificial, sugar-containing nourishment always accumulate more organic substancesin their tissues and have a higher turgor than plants nourished with mineral elements.The carbohydrate increment on sugar nutrition reaches 5 grams per 1 M2of leaf area.
Lebedyantsev (1936) in an annotation to his translation of Liebig'sbook (Chemistry as applied to Agriculture and Physiology) mentioning the work ofSossur on nutrition of plants, has written: "Sossur considered the CO2of the air to be the main source of carbon nutrition, not denying, however, the possibilityof utilizing carbon of organic compounds of the soil, since he was not in possessionof facts enabling him to deny this. We shall note that today we do not possess suchfacts and the question of the assimilation of organic compounds from the soil stillremains to a large extent an open one, although, undoubtedly, the main source ofcarbon for green plants is after all CO2." (page 396)
As can be seen from the above, the question of plant nutrition, notwithstandingthe numerous studies which have been carried out, remains unresolved in may respects.
It is hard to agree with the concept according to which during allthe history of their evolution, plants, although having been in contact with organicsubstances of the soil, did not acquire the ability to assimilate them in one formor another.
There is no basis for denying the well-known facts and experimentaldata showing that plants utilize mineral compounds for their nutrition. Numerousobservations speak in favor of this method of plant nutrition being the most importantone under natural conditions. However, is such a nutrition sufficient to obtain highyields and fully viable seeds year after year? This question seems to us not to havebeen sufficiently solved.
Not so long ago, the assimilation by roots of CO2 fromthe medium was said not to take place, but now this may be considered an establishedfact. Plants absorb CO2 not only from the atmosphere but also from thesoil (Samokhvalov, 1952; Kursanov, 1953, 1954).
It should be assumed that plants that experience lack of CO2in the atmosphere gladly assimilate it from the soil. Under various unfavorable conditionsthe photosynthetic activity of plants may decrease considerably. Thus, for example,during drought the stomata are closed, and the influx of CO2 stops orweakens. Respiration of plants, however, under these conditions does not cease andmay even increase. Starving ensues, to a larger or a smaller degree. Weakening ofphotosynthesis may also be caused by other factors. In all such cases, evidently,plants can switch to a heterotrophic nutrition, assimilating organic compounds fromthe soil supplementing their nutrition.
Heterotrophism of Plants
The ability to assimilate ready-formed organic compounds and use themas nourishment is observed in many representatives of the plant kingdom; from thelower forms such as blue-green and green algae, to the higher flowering plants.
It is known that many (if not all) algae, may under certain conditions,grow and develop on synthetic media with mineral sources of nutrition, as well ason organic media containing different nitrogenous and carbonaceous complex compounds.It was shown by special experiments that these organisms, and especially the greenunicellular organisms, which usually grow on pure mineral nutrious media, grow muchbetter upon the addition of organic substances to the solution. They can assimilatecarbonaceous and nitrogenous substances (Gollerbach and Polyanskii, 1951).
Blue-green algae of the Cyanophyceae--Oscillaria, Nostoc Anabaena,Lyngbya, and others, also green algae of the groups Chroococcum, Spirogyra,etc, cannot be cultivated indefinitely on artificial organic media without a noticeableweakening of their viability. In our laboratory we have been maintaining a pure cultureof the green alga Chlorella for already more than 25 years. We do not observeany essential lowering of life functions. This alga assimilates nitrogen from peptoneand amino acids and grows quite well on must agar and even on meat-peptone agar (MPA)and gelatin.
According to the observations of many investigators, green algae Chroococcumand Spirogyra, blue-green algae Phormidium, Nostoc, Anabaena, Gloeocapsa,and others, readily assimilated sugars, amino acids, alcohols, organic acids, urea,casein, and other organic substances. Studies with pure cultures of algae performedfirst by Pringsheim (1913) and later by many others (Harder and Humfeld, 1917; Cataldi,1941; Gerloff, 1950) have shown that these organisms grow on organic media in thedark as well as in the light. Chlorella assimilates sodium and potassium oxalatesin the light, and malic, tartaric and some other acids in the dark.
Allen (1952) studied 26 cultures of blue-green and some green algaebelonging to 11 genera--Anabaena, Nostoc, Oscillatoria, Lyngbya. Phormidium. Gloeocapsa.Aphanocapsa, Plectonema Cladothrix, Chroococcum. and Synechococcus. Thesecultures were grown in mineral media with different sources of organic nutrients,Yeast extract, various sugars (glucose, saccharose, lactose, maltose, etc) mannitol,glycerol, ethanol, organic acids, amino acids, casein, urea, casein hydrolysate,etc were added to the media. In the presence of these substances many algae grewbetter than in media with mineral sources of nutrition only. Assimilation of organicsubstances takes place in many species at the same intensity in the dark as in light.Upon prolonged cultivation on organic media some algae lose their pigment and continueto live as typical saprophytes (Fogg and Wolff, 1955).
Authors who studied algae concluded that they can live and grow asheterotrophs, utilizing organic compounds, such as nitrogenous and carbonaceous substances,In the same way as the ordinary saphrophytes. This is understandable because thetwo kinds of organisms live in a milieu rich in organic substances--in soils andwater reservoirs, where animal and plant residues serve as sources of organic nutrientsafter their decomposition.
Green moss of the genera Splachnum and Getrapladon,settle and grow on excrements of animals, utilizing organic substances for theirnutrition.
Among higher flowering plants a group is known as the so-called "humusplants"--various representatives of which can be observed to be in differentstages of degradation of the chlorophyll apparatus. The humus plants are so calledbecause they grow on substrates rich in humus and decomposing organic animal andplant residues.
The character of nutrition and the conditions of the existence ofthese organisms have left a certain imprint on their structure and appearance. Someof them lose the green coloration, the leaves are reduced (but only in the lowerpart of the stem) and lose the capacity to assimilate carbon dioxide from the atmosphere.To such plants belong the species of the following genera: Monotropa Dum., Zymodorum,Neottia Sw., Corallorhiza Rale, Epipogon S. G. Gmel., VoyriaAubl, Fletia, Pogonia Less, Voyriella Miq., and others (see below).
In other representatives of humus plants the green leaves are preservedand they remain autotrophs by assimilating carbon dioxide of the atmosphere but,nevertheless, they can utilize ready organic substances. To such plants species belongthe species: Dentaria L., Pyrola L., Goodyera R. Br., CephalantheraRich., Epipactis Adans,Platanthera Rich., and others. All these plants,to a greater or lesser degree, live and nourish like heterotrophs, assimilating organiccompounds together with mineral sources of nutrition.
The group of insectivorous plants is well known. In our latitudessuch flowering plants are encountered an Drosera rotundifolia L., and Utriculariavulgaris L. To this group belong such southern plants as Cephalotus follicularisLabill, many species of Nepenthe L., Dionaea muscipula Ellis, DrosophillumLink, Aldrovanda Monti, Sarracenia L., and others.
About 500 species of such insectivorous plants are described in theliterature. These plants have a complex apparatus for catching insects and specialglands for their digestion.
Small animals falling into the trap of these plants are decomposedby enzymes to the soluble forms of organic compounds containing nitrogen and nonnitrogenouscompounds which are then absorbed by the plants and utilized by them for nutrition.
It is characteristic that those insectivorous clearly heterotrophicplants do not lose their capacity to assimilate atmospheric CO2. Manyspecies which obtain ready-made organic nourishment from the living body of otherplant species also belong to the heterotrophic plants. These are the parasitic plants.They are divided into facultative and obligatory parasites.
Among the obligatory parasite plants, the climbing plants of the genusCassytha L. (fam. Lauraceae L.) and Cuscuta L. (fam. ConvolvulaceaeL.) are the well-known species.
The biology of Cuscuta L. is known in great detail (up to 50species are recognized). They are parasites of the cereals, bushes and trees. Theypenetrate the tissues of the host with their haustoria and such nutrient substancesout of the host. Leaves of this plant are weakly developed and can hardly be seen,the stems lack chlorophyll.
Orobanche L. are also etiolated plants with weakly developedleaves (in the form of scales) lacking chlorophyll. They are parasitic on the rootsof sunflower, flax, cabbage, and others. About 180 parasitic plants of this genusare known. The shoots of Orobanche are so coalesced with the roots of theplant host that it becomes impossible to distinguish between the cells of the hostand the parasite.
Lathraea squaniaria also belongs to the group of parasiticplants. In contrast to the aforesaid this plant does not climb; it consists of athick, colorless, watery stem. The leaves of this plant are weakly developed andare in the form of colorless scales. The root system of this plant is close to theroot of the host, from which the parasitic plant sucks the sap of the host with theaid of haustoria. The plant at first grows under the earth's surface, then its shootspierce through the surface. The aerial parts are of a violet-red color.
The Balanophoraceae are tropical plants--parasites living on rootsof various trees. Forty species of these parasites are known (14 genera). These plants,like the Orobanche grow in such intimacy with the roots of the host that novisible border between them is discernible.
Parasitic plants related to Balanophoraceae are the RafflesiaceaeDum., which parasitize trees of tropic and subtropic regions. These plants penetratethe bark of the tree host, embrace its stem and roots and suck the, sap of the latter.
Parasitic plants from the family Loranthaceae D. Dow include morethan 300 species. They live exclusively on stems and branches of different trees.A typical representative of this group of plants is our ordinary Viscum albumL., which lives on deciduous and coniferous trees. This plant penetrates the branchesof the host with its roots and haustoria. The stem of Viscum album which hasthe form of a dichotomically branched bush carries elongated leathery leaves of ayellowish-green color.
The group of plants of the mistletoe family is characterized by thefact that its representatives--arboreal plants--did not completely lose the capacityof photosynthesis and preserved the normal appearance in their stems. They are theintermediate group placed between the nonchlorophyll, flowering, obligatory parasites,which nourish on ready-made organic food, and the facultative parasites which preservetheir normal structure in all their parts, as well as the capacity of assimilatingatmospheric CO2.
To the facultative parasites belong about 100 species of the familySantalaceae R. Br., and more than 500 species of the family Scrophulariaceae R. Br.In our flora, species of the genus Thesium L. (family Santalaceae) and speciesof the genus Euphrasia L., Alectorolophus Boehm., MelampyrumL., Pedicularis Boehm., Odontites Pers and others (family Scrophulariaceae)are encountered.
They are all grasses growing in meadows or in forests. They possessgreen leaves and a well-defined photosynthetic capacity. In the initial stage theydevelop as typical autotrophs without the slightest inclination to become parasites.However, when their roots reach a definite size (1- 2 cm) haustoria appear, withthe aid of which they become attached to the root of another plant host, encounteredduring their growth. From this moment on the semiparasite plants begin to supplementtheir nourishment at the expense of the plant host. They can, however, grow withoutthe host in the event of their not having encountered it in the course of growth.They can also parasitize each other.
There are in nature a great many epiphytic plants developing and growingon plants as on substrate. It is assumed that they nourish independently, at theexpense of mineral substances present on the plant barks. However, the possibilityof their using organic substances such as dead tissues, or their decomposition products,is not excluded. This problem is still inadequately studied.
Many plants assimilate organic substances, metabolic products of microbeswhich live on and inside the roots. The best known plants are those in the tissuesof which there are bacterial microbe-symbionts, actinomycetes, and fungi.
The best known symbiosis is that of plants with mycorhiza fungi. Accordingto the data in the literature, there are mycorhiza fungi on the roots of almost allplants which are to a greater or lesser degree symbionts. The symbiosis is such,that some plant species cannot grow without the fungi. Such plants are apparentlyobligatory parasites, heterotrophs whose nutrition depends on the metabolic productsof the fungus. Some orchids serve as an example of such parasitism. They requirefungi for their normal growth and development. They grow badly without them, andcertain species such as Neottia nidusavis Rich., encountered in our oak andpine forests cannot grow at all without the symbiotic fungi. This orchid grows anddevelops under the soil surface and appears above the surface only for floweringand fruit bearing. It has no green color and its pale, thick stems carry weakly developed,slightly yellowish sprouts with scaly leaves. Neottia nidusavis Rich. Hascompletely lost the capacity of independent nourishment on mineral compounds. Itis almost completely devoid of chlorophyll. Its nutrition is at the expense of decompositionproducts of fungi which grow inside its stem and roots.
There is a theory that orchids of this species can assimilate organiccompounds directly from the soil, and that the fungi serve merely for the processingof these compounds into the form in which they are more easily assimilated. The cytologicalpicture of the growth of fungi inside the orchid tissues shows that the myceliumgrows to a certain size followed by coiling and lysis. The products of lysis areassimilated by the plant.
Other species of orchids which have lost their green color and areentirely dependent on fungi can be encountered in our forests. To such orchids belong:Epipogon aphyllus Sw. and Corallorhiza trifida Chat., which grow inforests of the moderate belt. Such orchid parasites are also encountered in tropicalforests (Burgeff, 1932). In the literature, orchids are described in which parasitismbecomes manifest only at a certain growth phase. The species of the genus Myrmechis(Myrm. glabra Bl., Myrm. gracilis Bl. ) when young grow in the form ofa root obtaining their nourishment entirely at the expense of fungi; afterward theyform aerial organs, flowering sprouts with green leaves and start to nourish themselves.When the sprouts fade away they become parasites again.
According to the data of Bernard, the seeds of orchids cannot germinatewithout the mycorhiza fungi. Bernard has shown that the orchids cannot germinatewithout fungi and he elaborated methods for the artificial infection of these plantswith the mycorhiza.
Parasitic plants which have lost their green coloration are encounteredamong the other representatives of green plants. Such for example is Monotropahypopithys L., of the family Pirolaceae Drude. They are devoid of green colorationand their leaves have been transformed into brownish scales. This and other plantsof the genus Monotropa L., receive their nourishment entirely at the expenseof fungi growing inside their tissues. Gordyagin (1922) described a fern Ophioglossumsymplex the nonsexual sporiferous generation of which is nourished at the expenseof fungi, absorbing organic products of their metabolism and decomposition.
According to the observations of that author, ferns and other greenplants are encountered in the forests of the Tatar Autonomous Republic, which assimilatecarbon from the atmospheric CO2 but cannot exist without symbiosis withfungi. Such plants are widespread in nature. Higher plants of such a type preservethe green coloration and the capacity of assimilation of atmospheric CO2,but cannot normally develop and reach the stage of flowering and fruit bearing inthe absence of the fungus.
The majority of plants have fungi on their roots. They are usefulthough not indispensable. Fungi, in such cases, promote their growth and nutrition.The plants, as experience shows, grow better and adapt themselves to new places andgive a higher mass increment (Lobanov, 1953, Reiner and Nelson-Jones, 1949).
Keller (1948) and Lyubimenko (1923). when comparing the degree ofsymbiosis of different plants with fungi, and the degree of parasitism on the fungi,considered these phenomena as subsequent stages of evolution, as stages of transitionfrom autotrophism to saprophitism and parasitism, i.e., to heterotrophy. In his book"The Fundamentals of Plant Evolution" Keller writes: "In the courseof evolution the individual higher green plants of different families pass from thisstage, and, under the pressure of appropriate natural conditions, change to nutritionat the expense of fungi. Thereby, the leaves lose their significance as organs ofassimilation and become undeveloped, remaining only in the form of scales devoidof green coloration."
Lyubimenko (1923) stressed that there is no sharp difference betweenautotrophic and heterotrophic plants. Saprophitism, according to him, is the naturalconsequence of the synthesis of organic compounds: "Organisms capable of synthesizingorganic compounds from mineral ones, preferably use ready organic compounds and arecapable of receiving their nutrition in the same way as saprophites. Saprophitismis not per se, a special specific property of a certain group of organisms; on thecontrary, it is characteristic of all organisms with a possible exception of nitrifyingbacteria, and therefore, it appears in nature in different degrees. On one hand wefind plants which only accidentally assimilate organic compounds from the environment;these are the facultative saprophytes, for them the saprophytic nutrition is notindispensable." "On the other hand we find plants which are true saprophytes,which have completely lost the capacity of synthesizing organic from inorganic compounds.Between these two categories there is a gradual transition of forms lessening thedivision between them and in reality cancelling this division, (Lyublmenko, 1923,page 186).
As can be seen from the above citation, Lyubimenko considers thatall plants are capable of organic nutrition to a greater or lesser extent. The onlyexceptions are, according to him, the nitrifiers. We can add that, recently, materialis being accumulated showing that even these organisms may utilize organic nutrientsand grow on organic nutritious media In the same way as many bacteria-saprophytes.
It to known that plants may be in close symbiosis, not only with fungi,but also with bacteria. The root-nodule bacteria which penetrate the roots of leguminousplants, with the formation of colonies in the form of nodules are well known. Thenodules represent swollen roots filled with bacterial cells. These bacteria growabundantly, multiply in the cells, and produce nitrogenous substances which are utilizedby the plants.
Analogous nodules are formed on roots of some other plants (nonleguminous).For example, nodules have been described on roots of Alnus Gaertn., MyricaL., Podocarpus L'Her., representatives of the family Elaeagnaceae Lindl.;E. multiflora Thunb., E. angustifolius L., on Shepherdia canadensisNutt., on various species of Ceanothus L., on Coraria japonica Gray,and others. The nodules on these plants are formed by different representatives ofthe microbes such as bacteria, mycobacteria, actinomycetes and, according to ourinvestigations, also by proactinomycetes.
These organisms have a definite positive effect on plants much thesame as the root-nodule bacteria have on leguminous plants. Under conditions wherethe bacteria and, consequently, the nodules are absent. the plants grow weakly andoften they do not reach the stage of flowering and fruiting (Fred, Baldwin and McCoy,1932; Jongh, 1938).
There are many microbial symbionts which live on plant leaves, formingunique swellings--knots in the tissues. Such knots are formed by bacteria and mycobacteria.These organisms upon multiplying fill the cells of the knots in the same way as theroot-nodule bacteria fill the nodules in the root tissues. These microorganisms,according to our investigations, exert a positive effect on the growth of plants.Without them the plants grow weakly and some species do not reach the stage of floweringand fruiting, as can be observed in Ardisia Thunb. The plants remain dwarfs,but after they are infected with the corresponding bacteria, knots appear on theirleaves, the plants improve, they assume normal appearance, begin to flower and bearfruit (Jongh, 1938).
About 400 species of plants with the above-described knots are describedin the literature, including 30 species of the genus Ardisia Thunb., 244 speciesof the genus Pavetta L., 42 species of the genus Psychotri L., 5 speciesof the genera Amblyanthopsis and Amblyanthus D. C., 1 species of thegenus Dioscorea L., and others. The bacteria forming the knots pass from plantto plant through the seeds,
According to the data of many investigators, all these microbe-symbiontswhich live in the tissues of roots or in leaves of green plants affect the plantsthrough their metabolic products. Some of them form and excrete biotic compoundswhich activate the growth of the plants, others, in addition, fix atmospheric nitrogenand pass it on to the plant in the fixed state.
Having ascribed such a great importance to the above-listed bacteriaand mycorhiza fungi which provide organic nutrition for the green plants, we mustdraw attention to other species of microorganisms which are closely linked with theroot system of plants, although this link is of a different character. We have inmind the rhizosphere microflora.
An immense number of microorganisms live around the plant roots. Themost numerous among them are the bacteria. Have they any effect on the nutritionof the plants? What effect do their metabolic products have on the plant? Are theyassimilated by plants and what role do they play in the growth of the latter? Ifplants utilize the metabolic products of microbial symbionts with such readinesswhy then can they not use analogous substances formed by the free-living organisms?
Apparently, the difference lies in the fact that in the first case,symbiosis between the plant and the microbe, the metabolic products of the microbesremain inside the tissue, while, in the latter case, these compounds are being formedand accumulated outside the plant in the surrounding milieu, and, in order to becomeavailable to the plant, they must find their way inside the plant via the roots orsome other way.
Many authors think that the permeability of the root system for mineralsubstances differs from that for organic compounds. The suction power of the rootsis different in these two cases. The suction power of the heterotroph plant parasite(Lathraea squamaria) is 22.7 atm, and the suction power of the root of theplant host (Prunus padus L. ) is only 3.7 atm (Kostychev, 1933).
Many typical autotrophs, whose suction power is no more than average,readily assimilate organic compounds, Hutchinson and Miller (1912), studying nitrogenabsorption by the pea seedling, found a phenomenon which, from the point of viewof the prevalent opinion that they absorbed nitrogenous organic compounds more readilythan nitrate nitrogen, was paradoxical. They tested many organic nitrogenous compounds,and in all cases the results were the same.
These data were confirmed by numerous investigators (see later).
As can be seen from the above, the subdivision of plants, accordingto their nutrition, to autotrophs and heterotrophs, should be considered as relative.Each of the so-called autotrophic plants is capable of assimilating organic compoundsto a greater or lesser extent.
Indeed the meaning of "nutrition" should be distinguishedfrom the term "synthesis of organic substances." Nutrition in the realsense of the word, should be called all the processes which are directly involvedin assimilation of substances by the living parts of the organism from the momentwhen the organic compound in prepared. (Lyubimenko, 1923, page 180). This processproceeds similarly in all organisms belonging either to the plant or animal kingdoms.They all feed on organic compounds. To build a living body, all cells, whether theyare microbial, animal or plant, should possess ready-made elementary organic compoundsor their building blocks--nitrogenous and nonnitrogenous compounds, which participatein the general process.
The difference between plant and animal nutrition lies only in thatthe latter obtain ready-made synthesized organic compounds from the outside and theplants synthesize them for themselves.
The process of plant nutrition consists therefore of two elements:a) synthesis of organic substance from inorganic elements; this process Lyubimenkoconsiders as the preparative one, dispensable, from the point of view of nutritionin the narrow sense of the word; and b) nutrition proper, i.e., uptake or assimilationof elementary organic particles for the formation of a living organism; this processproceeds in the same way in plants and animals.
The nutrition of plants and microorganisms may proceed according tothe first or the second process, but each process may be manifested to a variousdegree in relation to the conditions of existence and to generic differences.
Vinogradskii, in his brilliant studies on the chemotrophy of microorganisms,drew a sharp line between these two types of nutrition by dividing all the microorganismsinto autotrophs and heterotrophs. Lebedev (1921). on the contrary, assumed that thesetwo types of microorganisms differ from each other, not by their manner of nutrition,but by the way they obtain their energy. Lebedev thinks that both the autotrophsand heterotrophs assimilate CO2, but while the former obtain their energyat the expense of the oxidation of inorganic substances the latter obtain their energyat the expense of the oxidation of organic compounds. This scientist was the firstwho showed experimentally that the heterotrophs utilize CO2. His datawere confirmed by many other investigators.
At present, it has been confirmed that many microorganisms, even heterotrophscan assimilate CO2, and Werkman even assumes that all the organisms ingeneral assimilate CO2 and that this is an important physiological function,insuring the synthesis of indispensable intermediate metabolic products (Werkmanand Wilson, 1954).