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Part IV

INTERACTION BETWEEN SOIL MICROORGANISMS AND PLANTS

 

  We have already noted the importance of microorganismsin the life of plants as being among the biological factors of soil fertility. Betweenthe two there exist special interrelationships which express themselves to some degreeby the total productivity of the soils.

  Investigations show that the vegetative cover is apowerful factor in the life of microorganisms. The peculiarities of the plant speciesleave their imprint on the quantitative and qualitative composition of the microflorabiocoenoses of soils. Plants create and form microbial societies, which effect themicrobial population of the entire root system and harvest remains. During theirlife, plants excrete through their roots various organic and mineral substances whichattract microorganisms. During the growth cycle of the plant, roots constantly formand shed root hairs, lose necrotic epidermal cells, etc. All these elements are thentaken up by the microbes and become the source of their nourishment.

  The species composition of the microflora, just asthe soil, has a definite and considerable influence on the growth and developmentof plants, and consequently on the crop yield. The study of the nature of the interactionbetween microorganisms and plants is one of the main and most interesting problems,not only of microbiology, but also of the study of soil and plant cultivation.

 

Effect of Plants on the Soil Microflora

  The effect of the vegetative cover on the microfloraof the soil was studied long ago by various investigators. Plants not only have aninfluence on living microorganisms (through their root system) but also influencethem after their death and after the harvesting of the crops (in cultivated fields),In the former case, this effect is caused by root excretion and by the dying particlesof the roots themselves. In the latter case, the active factors are the remnantsof the roots and the aerial parts. In both cases, great changes take place in thecomposition of the soil microflora. In addition, the roots exert a beneficial effecton the physical and chemical properties of the soil, improving the conditions forthe existence of microorganisms. One can judge the importance of plant roots in thebiology of soils by the great bulk of the root mass and its extension.

 

Root mass of plants

  The studies made by Kachinskii (1925), Chizhov (1931),and others showed that the root system is a great mass by weight with a vast surface.This was observed by Tol'skii (1904-1911) when he studied the root system of forestplantations in the Buzuluk forest. The author gives numerical data on the developmentof the root system and its dispersion in woods on different soils and with differingdensities of planting. At a density of 77 trees per 0.2 hectares, the length of theroots of one plant is 0.21 km, and at a density of 260 trees per 0.2 hectares, itis 0.42 km.

  L. P. and L. L. Golodkovskii (1937), on the basis ofobservations made on the development of the root system of lucerne under differingsoil-climatic conditions of its growth, obtained the following data (Table 62).

Table 62
Development of the root system of a 3-year-old lucerne
under various soil and climatic conditions
(Weight of the air-dried mass of roots in 1 cubic meter of soil, in grams)

Horizon, cm

serozem, watered

meadow, watered

weak podsolized

typical podsol

southern chernozem

0-10

343.1

253.7

315.0

348.0

692.0

10-20

149.2

157.0

386.0

386.0

181.3

20-30

95.1

57.0

100.0

95.0

47.3

  According to data obtained by Dittmer (1937, 1938),one plant of winter rye has a total root length (without hairs) of 623.4 km. Thethinner the roots, the greater their length. The main roots have a length of 0.07km; the secondary roots 5.4 km; the roots of the third order, 175 km, and those ofthe fourth order, 442.8 km. The largest mass consists of the active part of the rootsystem.

  The area of all the roots of one plant is 237.4 m2;the area of the roots of the first order, 0.1 m2 ; the root area of thesecond order 4.2 m2; the root area of the third order, 70.5 m2;and the area of the roots of the fourth order, 162.8 m2.

  The root hairs on the roots of one plant number to14.3 billions. They are mainly located on the roots of the third and fourth orders(14.1 billions). The length of all the hairs of one plant is more than 10,000 km.Their total area (one hair is 700-1,000 µ in length) is double the surface areaof the root, i. e., more than 400 m2. Consequently, the roots of one ryeplant in the fourth month of growth have a total length of 11,250 km and an areaof 6,388 m2.

  In the textbooks written by Kursanov, Keller, and Golenkin,smaller figures are given for the length of roots. For instance, according to theirdata, the total length of melon roots without hairs is 25 km; in wheat, about 20km; and in spring rye, 623 km. The surface of the root system of one rye plant is237 m2. The surface of the roots of rye is 130 times greater than thesurface of the aerial organs (Kursanov, 1940).

  According to Pavlichenko (1938), the length of rootsof the wild oat (Avena fatua) is 87.8 km, and of wheat, 71.2 km. In one cubicdecimeter of soil, the total length of roots in as follows: in oats, 6 5 cm; in rye,90 m; and in meadow grass, 553 m. The length of the root hairs is as follows: inoats, 11.6 km; in rye, 24.3.km; in meadow grass, 73 km.

  Detailed studies of the root system of fescue plants,conducted by Savvinov and Pankova (1942) in the Volga steppes, showed the following:in a two-meter 2 layer of soil there are 1.75 kg dry mass of roots per m2,of which one third to one quarter are living. The weight of the aerial part of theseplants comprises 0.48 kg, i. e., about one quarter of the total weight of the roots.

  The nature of the distribution of the roots in thesoil is illustrated in Table 63.

Table 63
Distribution of roots in soil layers, per 1 m2
(according to Savvinov and Pankova, 1942)

Type of plants and soils

Depth, cm

Root length, cm

Root surface, m2

Weight of dry root mass, gm, living roots

Weight of dry root mass, gm, total

Fescue vegetation, chestnut soil

0-25

18.5

12.3

278

1,112

 

0-50

28.0

18.09

344

1,419

 

0-100

32.0

20.77

418.4

1,735

 

0-300

36.0

22.40

436.3

1,757

 

 

 

 

 

 

Cereal-grass vegetation, chestnut soil

 

 

 

 

 

 

0-25

61.6

10.3

186.8

1,547

 

0-50

80.4

13.96

251.1

1,792.5

 

0-100

94.5

16.97

310.9

2,002.3

 

0-200

100.0

18.10

 

 

  Shalyt and Kalmykova (1935) studied the formation ofthe roots of steppe vegetation in chernozem soils ("Askaniya-Nova" NationalReserve). According to their data, the air-dry mass of roots of the Festuca-Stipavegetative association is 3,002.5 g (30 tons/hectare). and in the Basaltic solonetsof the same reserve 1,175.8 g per 1m3 (11.75 tons/hectare). The totalsurface of the Festuca roots is 225 m2, and for the Stipa,126.2 m2. Savvinov and Pankova consider these numbers to be somewhat exaggerated.One can assume that the cited differences have a purely ecological cause and arenot the result of a methodical error. It is obvious that under the conditions ofthe southern Ukraine, which has chernozem soils, the relationship a between rootsand their aerial parts will differ from those of the chestnut soils near the Volga.Moreover, the differences discussed by the authors are not very striking and fundamental.As in the data submitted by Savvinov and Pankova, as wen as that of Shalyt and Kalmykova,the numerical indicators are of about the same order.

  Muntz and Girard (1888) measured the length and diameterof the roots of plants grown on the experimental fields of the Paris AgriculturalInstitute and obtained the following data. In 1 m3 of soil, there wasa 5.18 m2 total area of clover roots; in the case of meadow grasses, 7.58;oats, 10.70; winter wheat, 11.30; and poppies, 2.17m2.

  According to Belyakova (1947), the root mass of thedry roots of lucerne in the soils of the Vakhsh valley is as follows: in the firstyear of growth, 11.12 tons, in the second year of growth, 22-24 tons, and in thethird year, 30 tons and more per hectare.

  Nad"yarnyi (1939) found that mixtures, severalyears old, of leguminous and cereal grasses accumulate more roots than pure cultures.In the upper layer of the soil (0-20 cm), over a two-to three-year period, up to40-75 centners* roots per hectare were found. [*One Russian centner equals 100 kg.]A greater accumulation of root mass was observed by Belyakova and Parishkura (1953)in soils having mixed crops of grasses. In other studies, many tons of dry root massper hectare are given.

  The main mass of roots is concentrated in the surfacelayer (0-25 cm) or somewhat deeper, depending on soil-climatic conditions and onthe type of flora. Sometimes, in the deeper layers of soil, a second maximum (lesspronounced) of root concentration is observed. The nature of the distribution ofthe root mass along the horizons of the soil is given in Figure 69.

 

Figure 69. Distribution of wheat roots in the soil (according to Kachinskii, 1950)

 

  According to their distribution, the importance ofthe roots will be greatest in the upper horizons. The biological significance ofthe root system is determined by its activity, i e., by its ability to absorb elementsof nutrition from its surroundings and excrete products of metabolism into the environment,Studies have shown that the active part of the root system is its largest part. Accordingto some date, it comprises 50 to 75 percent of the total root mass.

  The substances which are excreted by the root systemare utilized by microorganisms as nutrient sources. A great number of microbes concentratearound the roots, growing, multiplying, and excreting their metabolites, many ofwhich are assimilated by the plant roots. The whole root system during the life ofplants, as well as after their death, exert an immense influence on the growth anddevelopment of microorganisms.

  The effect of the root system on the composition ofthe microflora may be direct or indirect, positive or negative.

  The utilization of the nutrient elements by the plantsis connected to some degree with the metabolism of microorganisms. A greater influenceof plants on microorganisms is that the former enrich the soil with organic substances.

 

Root excretions

  Roots are no longer looked upon as mere suctorial organsthrough which plants absorb various nutrient elements from the soil. As early asthe 18th century, the ability of roots to excrete certain substances, which affectthe properties of the soil and determine its fertility, was noted.

  The presence of CO2 in the excretions ofroots was noted by many authors including Sossur (1804), Trevisan and Meis (1839),Pollaci (1858), and others. Sachs in 1860-1865 experimentally demonstrated that theroot systems of various plants excreted CO2 (Pryanishnikov, 1952; Konstantinov,1950).

  Lundergardh (1924) determined the amount of CO2liberated by the roots of wheat grown in sterile sand and in sand containing bacteria.He obtained the following results: one gram of a dry mass of roots excretes 3.05mg of CO2 per hour in sterile sand and 5.57 mg in the presence of bacteria.

  The considerable excretion of CO2 by theroots of plants was observed by Zaikovich. According to his observations, the rootsof well-developed corn excreted 0.24 g per day, and, according to Knopp, 0.25 g.In the experiments carried out by Kossovich, mustard roots excreted, on the average,27.3 mg of CO2 per day. Barakov observed the excretion of CO2by the roots of different plants and concluded that the maximum amount of CO2excretion occurs during the period of the most active metabolism of the plant, duringits flowering (according to Konstantinov, 1950).

  Chesnokov and Bazyrina (1934) grew flax in vesselswith podsol soil or sand and determined that the respiration of the soil with theplants growing in it greatly exceeded the sum of the respiration of the same rootsand soil taken separately.

  The more bacteria present in the rhizosphere, the moreintense the formation of CO2 by the roots of plants (Table 64).

Table 64
The influence of plants on the formation of CO2 in soil at a temperature of 20i C
(according to Waksman, 1952)

Plants

Number of bacteria, millions / g

pH of soil

CO2, mg per kg, per day

Triticum vulgare L.

49

6.75

69.4

Secale cereale L.

42

6.44

68.2

Avena sativa L.

45

6.42

79.0

Beta vulgaris L.

78

6.89

74.3

Medicago sativa L.

120

6.89

86.8

Trifolium pratense L.

--

6.66

82.4

  The intensity of CO2 formation depends onthe species of the plants, their age, the season of the year, and other factors.

  The approximate volume of the root respiration of graincultures under conditions of growth in the field comprised 25-30 percent of the respiratoryvolume of the soil as a whole (Konstantinov, 1950).

  During their life, plants excrete different mineraland organic compounds via their roots. Compounds of phosphorus, potassium, calcium,sodium and other elements have been found in root excretions.

  Sabinin (1940, 1955) and his associates (Minina, 1927)have shown that the excretion by roots of elements of mineral nutrition is accomplishedby exosmosis and is regulated by the concentrations of these substances in the externalsubstrate. Tueva (1926) established that the exosmosis of calcium and potassium fromroots takes place until an equilibrium state of these elements is established inthe surrounding medium. Such a regularity was found by Osipova and Yuferova (1926)in relation to the absorption and excretion of sulfur and phosphorus by the rootsof corn and wheat.

  Avdonin (1932) observed the loss of ash elements incultivated oats under field conditions, These losses differ in quantity dependingon the conditions of the growth of the plant.

  Akhromeiko (1936) decided that some plants excretemineral substances via their roots, while others do not. He observed phosphoric acidin the root excretions of lupine, peas, buckwheat, mustard, and rape. The amountof phosphorus excreted attained 14-34 per cent of all the phosphoric acid taken upby the plant.

  There are some writers who deny that it is possiblefor roots to excrete mineral compounds. The authors of these works assume that thesubstances found are the decomposition products of root residues.

  Of the root excretions, the organic substances areof the greatest importance, The presence of these substances was observed for thefirst time at the end of the last century. Dyer (1894) established the presence ofacidic compounds in the root excretion of plants of barley, wheat, oats, foxtail,and others. Acids were detected in root excretions by Lemmerman (1907), Künze,(1906), Schreiner and Reed (1907), Doyarenko (1909), and others.

  Stoklasa and Ernest (1909) found that plants excreteacetic, formic, and oxalic acids through their roots. Maze (1911) and Shulov (1913)found organic acids and sugar in root excretions. Organic substances were found byKostychev (1926), Truffaut and Bessonoff (1925, 1927), and others.

  Mashkovtsev (1934) found that the roots of germinatingseeds of rice excrete sugars, aldehydes, ethyl alcohol, and other compounds precipitatingwith lead acetate.

  Minina (1927) detected organic substances in root excretionsof lupine, beans, corn, barley, oats, and buckwheat, upon cultivating them in Knop'snutrient solution, The excretion in most of these cultures reached its maximum duringthe fourth week of growth, and in buckwheat, at a somewhat earlier period. Upon theripening and aging of the plants, the amount of root excretions decreases and towardthe end of the growth period stops altogether.

  Lyon and Wilson (1928) found nitrogenous and nonnitrogenousorganic compounds in the root excretions of corn. The amount of nitrogenous substancesin root excretions, according to these authors, decreases with the age of the plant.

  Winter and Rümker (1952) observed phosphatides,amino acids, thiamine, biotin, meso-inositol, paraaminobenzoic acid, carbohydrates,tannins and alkaloids in the root excretions of plants. Harley (1952) found sugars,amino acids, vitamins, and other organic compounds in root excretions.

  Virtanen and his associates (Virtanen and Laine, 1937)observed in the root excretions of young sprouts of leguminous plants; peas, clover,etc, aspartic and glutamic acids, tryptophan and ß-alanine.

  Cereals, oats and barley, grown in the same vesselwith leguminous plants in the complete absence of nitrogen sources in the medium,grew normally and developed at the expense of the nitrogen excreted by the leguminousplants. Similar experiments were conducted by Lipman as early as 1912.

  The possibility of transferring metabolic productsfrom certain plant species to others was confirmed by the experiments of Prestonand his associates (Preston, Mitchell and Reeve, 1954). Plants sprayed with methoxyphenylaceticacid were grown in the same vessel with plants which were not sprayed, After sometime, the given substance was detected in all the tissues of the unsprayed plants,in larger or smaller quantities: the nonsprayed plants absorbed the methoxyphenylaceticacid excreted by the roots of the sprayed plants.

  Many investigators have detected a considerable amountof nitrogenous organic compounds in the roots of cereal plants when they were growntogether with legumes (Scholz, 1939; Wyss and Wilson, 1938; Madhok, 1940; Nicol,1934; Isakova and Andreeva, 1938).

  Sabinin (1940) found that the roots of pumpkins excretefrom nine to eleven different amino acids. These acids were determined and differentiatedby paper chromatography (Kursanov, 1953).

  Other investigators deny the presence of nitrogenoussubstances in the root excretions of leguminous plants (Bond, 1937, and others).

  Wilson, Wyss, and others (1937, 1938) assumed the possibiltyof the excretion of nitrogenous compounds by roots. However, these compounds, accordingto these authors, are metabolic products of the nodular tissues and not of the rootsof the leguminous plants themselves.

  Engel and Roberg (1938) in order to verify Virtanen's data, cultivated alder which was inoculated with cultures of proactinomycetes,forming nodules, and observed in the substrate (sand) a considerable quantity oforganic nitrogenous substances excreted by the roots.

  Virtanen, in reply to Wilson, Bond, and others, notedthat the process of the excretion of organic substances is closely linked with externalconditions--sunshine, aeration, nutrition, and the pH of the medium. Confirming earlierdata by new experiments, the author stated that the detected nitrogenous compoundsare products of the fixation of free nitrogen, which were not utilized in the formationof protein and plant tissues and not products of protein decomposition (Virtanenand Torniainen, 1940).

  The organic compounds excreted by the roots of variousplants are not identical. In leguminous plants, one detects more nitrogenous compounds--aminoacids, amide compounds, and others (Virtanen and others, 1937, 1938, 1940). In cereals.the root excretions are richer in carbon substances--sugars, organic acids, and others.According to our observations, peas, broad beans, beans, lupine, and other leguminousplants excrete substances having a neutral or weakly alkaline reaction, and cereals--cornand wheat--secrete substances having an acid reaction, According to the data of someinvestigators, the roots of peas excrete nucleotides and flavins (Lundegardh andStenlid, 1944).

  West and Wilson (1939) observed biotin and thiaminein the root excretions of flax and sugar in the excretions of certain cereals, Brownand others (1949) proved the presence of pentoses or closely related compounds (alpha-ketoxylose)in the root excretions of grasses.

  Brown and Edwards (1944) found special substances whichstimulate the growth of other plants in root excretions.

  Groh (1926) studied the root excretions of lupine,broad beans, wheat, oats, barley, and rye. In some plants, substances were detectedwhich have an acid reaction, and others which have an alkaline one. On the basisof these findings, the author divides plants into two groups: the acid group, includingpeas, broad beans, lupine and wheat; and the alkaline group, including oats, rye,barley, and mustard. According to Pryanishnikov (1905), lupine excretes substancesof an acid nature. Due to these excretions, this plant dissolves the highly solublephosphates, transforming them into an easily assimilated form. Other plants, likemustard and buckwheat, are not able to excrete substances of an acid nature and cannotdissolve the mineral compounds essential for nourishment.

  The studies made by Fred (1918, 1919), conducted understrictly sterile conditions, clearly showed the presence of substances of an acidnature in root excretions, which dissolve marble plates. The author pointed out inthis connection that, in the presence of bacteria, the process of the dissolutionof marble is considerably faster.

  The roots of Italian rice excrete a substance whichfluoresces with a blue light upon ultraviolet irradiation. This substance is so characteristicthat it may, according to the author, serve as an indicator of the given plant (fromAudus,1953)

  The difference in chemical composition between theroot excretions of different varieties of the same species of plant was also notedby other investigators. Timonin (1941) established the presence of substances ina variety of flax resistant to fusariosis (Bizon var.), which activate the growthof the fungus Trichoderma viridis an antagonist of the organism causing fusariosis.In the strain which was sensitive to fusariosis (Novel var. ) substances were foundin the root excretions which stimulate the development of the fungus Fusarium,the cause of fusariosis of flax.

  Chemical analysis has shown that in the root excretionsof the resistant variety of flax, there is a great amount (25-30 mg per plant) ofhydrocyanic acid, which possesses antimicrobial properties. In the excretions ofthe roots of the sensitive variety of flax, this acid is either absent or presentonly in traces.

  Eaton and Rigler (1946) observed an analogous situationin the root excretions of the cotton plant. In the variety resistant to root decaymore carbon compounds were found than in the sensitive variety. According to theauthors, the given substances attract microbe antagonists, which inhibit the developmentof the organism causing root rot.

  It should be noted that the problem of plant-root excretionsonly comparatively recently became a subject of thorough study. Therefore, we possessonly scant information on the qualitative composition of root excretions. In addition,our knowledge of the quantities of the substances excreted by the roots in even morescant.

  The few studies available show that roots excrete considerableamounts of organic substances. Dyer (1894), in determining the amount of acids excretedby the roots of plants, established that 100 ml of nutrient solution from barleycontained 0.38 mg of acids; from wheat, 0.58; oats 0.65, foxtail, 0,86; timothy grams,0.80; orchard grass. 0.81; white clover, 1.28; red clover, 1.55 and from broad beans,1.11 mg of acids.

  According to Maze (1911), one corn plant in a sterilenutrient solution excretes 57 mg of sugar and 84 mg of acids in twenty days of growth.Shulov (1913) found in the root excretions of this plant, after a two-month periodof growth in a nutrient solution, 94 mg of nonreducing and 34 mg of reducing sugarsand 80 mg of malic acid. The roots of peas excreted, during the same period, 140mg of sugar. According to the observations of the author, when plants were cultivatedon ammonium nitrate, there were more root excretions than when the plant was givencalcium nitrate.

  Pfeifer, (1912, 1917) investigated the root excretionsof wheat and buckwheat. According to this author, 0.27 g of wheat roots excreted0.134 mg of organic acids and 0.110 g of buckwheat roots excreted 0.155 mg of organicacids, which comprises 1.3 per cent of the total weight of the plants. Accordingto Shulov (1913), the root excretions of corn comprise 0.6 per cent of the plant'sweight.

  Demidenko (1928) grew corn and tobacco in solutionswhich were either changed or unchanged. The corn roots of one plant, grown in a solutionwhich was not changed excreted 486 mg of organic substances during the whole vegetationperiod and, when the solution was changed seven times. the roots excreted 1,136 mgof organic substances, Roots of tobacco, for the same period, excreted 158 mg inan unchanged solution, while in a changed one, it excreted 439 mg of organic substances.In summarizing these observations, the author concluded that the total root excretioncomprised 27 per cent of the plant mass.

  Mashkovtsev (1934) found that seeds of rice upon germinationlose 20-30 per cent of dry weight, with about one fourth of the loss consisting ofroot excretions of organic compounds.

  Virtanen and his associates (1933) found that the rootsof peas grown in vessels along with cereals excrete 126.4 mg mineral nitrogenouscompounds in 58 days, of which 77.4 per cent is comprised of the nitrogen of aminoacids, 3.3 per cent amide compounds, 2.05 per cent of melanin*, and 2.73 per centof other nitrogenous compounds. *["Melanin" appears in Russian text butit may erroneously refer to "humin."]

  When barley was grown together with peas, it grew normallyand developed, although no nitrogen was introduced into the vessel with sand; inthe tissues of experimental plants of barley, 32.3 mg of nitrogen were found, andin the tissues of the control plants. which were grown without peas, the nitrogenfound amounted to only 0.7 mg and these plants developed very poorly.

  The barley in these experiments did not utilize allthe nitrogen excreted by the peas. A considerable part of it, up to 89.0 mg, remainedin the substrate in the form of these or other organic nitrogen compounds. (Virtanen,Synnöve Karström, 1933; Virtanen, 1937).

  Virtanen and Laine (1936, 1937) found that in the rootexcretions of clover and other leguminous plants in the period preceding flowering,mainly (75 per cent of the total bound nitrogen) aspartic acid, gluconic acid, tryptophanand ß-alanine were detected. During flowering, the major part of the nitrogenousroot excretions consisted of tryptophan.

  Lyon and Wilson (1921) calculated that for the wholevegetative period, the roots of plants excrete up to 5 per cent of the total weightof the plants' organic substances.

  Engel and Roberg (1938) determined that, during a two-monthperiod of growth, the roots of one alder plant, inoculated with proactinomycetes,excreted 27.7 mg of nitrogenous compounds and uninoculated plants excreted 23.6 mgof nitrogenous compounds (Table 65).

Table 65
Excretions of nitrogenous substances by alder roots, mg
(from data supplied by Engel and Roberg, 1938)

Experiment

Nitrogen in the initial substrate (sand)

Nitrogen in substrate after 2 months growth of alder

Increase in nitrogen

Inoculated (with nodules)

3.3

31.0

27.7

Uninoculated

2.5

26.1

23.6

  Meshkov (1953) investigating the root excretions ofpeas and corn grown in a sterile nutrient solution, obtained the following results:during twenty days of growth, the roots of peas excreted into the solution 2.87 mgof reducing sugars in experiments performed during 1946, and 4.28 mg in the experimentscarried out during 1947. The weight of the dry mass of the vegetable crop comprised1.92 g in 1946 and 1.85 g in 1947. The roots of corn for the same period excretedinto the solution 8.4 mg in 1946, and 8.17 mg in 1947. The weight of the dry masswas 3.69 and 2.35 g respectively. According to the observations of the author, theamount of root excretions depends to a considerable degree on the weight of the roots,rather than on the weight of the green parts, leaves and stems. The total weightof the latter amounts to 2 per cent in the case of peas and 1.3 per cent in the caseof corn, of the total weight of the mass of the plants.

  In our investigations (1934 b) we determined the growthof microorganisms in the media to which these substances were added. For this purpose,of a great number of species tested the following cultures were chosen: two culturesof yeast; Torula rosea and Sporobolomyces philippovi, and two bacterialcultures, Pseudomonas fluorescens and Ps. denitrificans.

  These microorganisms were grown in a solution in whichwheat and corn were grown, and also in a pure nutrient solution with various concentrationsof glucose. After certain time intervals, the cells were counted in a Thoma countingcell and plated on liquid and solid nutrient media. The results are given in Tables66 and 67.

Table 66
Growth of microorganisms in a rhizosphere solution of wheat
(in thousands per 10 ml of medium)

Time of action of solution--->

3 days

8 days

15 days

25 days

40 days

Torula rosea

75

1,500

1,000

1,500

1,100

Sporobol. philippovi

150

2,200

2,000

2,000

1,500

Ps. flourescens

1,200

100,000

150,000

7,000

1,000

Ps. denitrificans

1,800

150,000

160,000

7,500

1,500

Table 67
Growth of bacteria and yeasts in a pure initial solution with various concentrations of glucose (in thousands per 10 ml on the eighth day of growth)

Glucose concentration,
mg per 100 ml

Torula rosea

Sporobolom. philippovi

Pseudomonas flourescens

Pseudomonas denitrificans

5

400

650

20,000

1,500

10

680

900

35,000

2,500

20

1,000

1,500

60,000

50,000

50

2,000

3,000

150,000

100,000

100

3,500

5,000

250,000

200,000

  In comparing the maximum numbers of microbial callswhich had grown on the rhizosphere solution with the corresponding numerical indicatorsof growth in glucose-containing medium, we obtained the following results: the maximumnumber of Torula rosea cells, which attains 1,500,000 in the rhizosphere solution,is equal to the same number in the case of a glucose concentration which slightlyexceeds 20 mg. Approximately the same amount is also necessary for Sporobolomycesphilippovi. In order to accumulate 150 million bacterial cells in the rhizospheresolution, we evidently require approximately 50 g of glucose or some other equivalentsubstance.

  Consequently, according to the data of this analysis,the roots of wheat (the vessel contained three plants) excreted in 15 days of growthabout 50 mg of organic substances, utilizable by bacteria, and about 20 mg of substancesutilizable by yeast.

  In experiments with corn, similar results were obtained.Substances utilizable by bacteria were excreted in a larger amount than substancessuitable for the nourishment of yeast.

  It became known recently that the roots of vegetatingplants excrete various enzymes into the medium. The presence of enzymes in root excretionshad already been suspected when the problem of the saprophytism of higher plantsand the problem of their growth and nutrition on organic media was investigated (Kamenskii,1883; Lyubimenko, 1923, 1935; Keller, 1948).

  Eckerson (1932) has shown that plant roots are ableto reduce nitrate to nitrite with the aid of excreted nitrate reductases. Thus, theroots formed up to 2 mg of nitrite nitrogen during 17 hours at 37° C. Kleinand Kisser (1925), growing plants in a sterile nutrient solution, detected aftersome time in this solution an enzyme which reduces nitrate to, nitrite.

  Kuprevich (1949) investigated the root excretions of23 species of plants, belonging to 16 families: oats, wheat, barley, vetch, clover,flax, heather, camomile, willow herb, dandelion, nettle, knotweed, sorrel, tea, oak,birch, poplar, willow, pine, spruce, the common brake, and others. Various enzymeswere detected: catalase, tyrosinase, phenolase, asparaginase, urease, invertase,amylase, cellulase, protease, and lipase.

  The amount of excreted enzymes and their activity variesamong the different species of plants. For example, the activity of amylase was expressedby indices from one to four, i. e., from barely detectable activity to the full decompositionof the substrate. Lipase was detected in traces in only four species of plants (dandelion,touch-me-not, nettle, and pine).

  We studied amylase (1952 a) in the root excretionsof wheat, corn, and peas, grown under sterile conditions. It was observed that whensmall samples of roots were placed in a vessel with starch, the latter was comparativelyquickly decomposed (Table 68). For example, 0.2 g of wheat roots decomposed 20 mgof starch in 60 minutes.

Table 68
Decomposition of starch by enzymes excreted by plant roots

Plants

Root sample, grams

Reaction for 0.5 hours

Reaction for 1 hour

Reaction for 2 hours

Reaction for 4 hours

Reaction for 8 hours

Reaction for 24 hours

Wheat

 

 

 

 

 

 

 

 

0.5

-

-

-

-

-

-

 

0.2

+

-

-

-

-

-

 

0.1

+

+

-

-

-

-

 

0.05

+

+

+

-

-

-

Corn

 

 

 

 

 

 

 

 

0.5

+

+

+

+

-

-

 

0.1

+

+

+

+

+

+/-

Peas

 

 

 

 

 

 

 

 

0.5

+

+

+

+

+

-

 

0.1

+

+

+

+

+

+

A plus stands for the presence, and a minus designates the absenceof starch, plus-minus designates an undetermined reaction.

  Roots of plants grown in the field decomposed starcheven more intensively. In one hour, 25 mg were decomposed by a suspension of 0.1g of wheat roots and by a suspension of 4.5 g of corn roots.

  Starch was most quickly decomposed by roots which werenot detached from the plant. Young wheat plants, extracted from the soil and washedwith water, when submerged in a starch solution, decomposed 25 mg of starch in 30minutes, while corn plants decomposed 5 mg.

  The enzyme amylase was also detected in the water inwhich wheat plants which were taken from the soil were immersed for some time.

  One wheat plant, two years old and grown in the field,excreted into the solution an amount of amylase which decomposed, on the average,20-25 mg of starch in one hour at room temperature.

  It can be seen from the above that starch is most activelydecomposed by the root excretions of wheat and to a lesser degree by the excretionsof peas and corn.

  Ratner and Samoilova (1955) detected in the root excretionsof corn and sunflower, enzymes which break down glycerophosphate and saccharose.The amount of these enzymes, according to these writers, changes with the growthphase of the plant. The maximum excretion of enzymes by corn is observed at the periodpreceeding flowering and during the period of the formation of the spadix (Table69).

Table 69
Excretion of enzymes by corn roots during various phases of growth, per gram of roots (according to Ratner and Samoilova, 1955)

Phases of growth

Phosphorus liberated from glycerophosphate

Reducing sugars, mg

Initial vegetation period

0.06

4.06

Middle vegetation period

0.106

4.28

Formation of pseudo-ears

0.052

3.66

Beginning of formation of spadices

0.102

6.06

Formation of spadices

0.124

4.32

Ripening of seeds

0.068

0.51

  The roots of these plants form enzymes which, in additionto glycerophosphate and saccharose, also split glucose phosphate and ribonucleicacid. Thus, one gram of sunflower roots splits 0.338 mg of ribonucleic acid in threehours, while one gram of corn roots splits 0.048 mg of ribonucleic acid.

  A similar picture is observed in relation to the splittingof glycerophosphate and glucose phosphate. Sunflower roots split 0.375 mg of glycerophosphateand 0.208 mg of glucose phosphate in three hours, while corn roots split 0.129 mgand 0.095 mg, respectively.

  The authors concluded that, due to the enzymatic activityof the roots, the latter can supply the plants demand for phosphorus at the expenseof the organic phosphorous compounds if they are present in the medium.

  In addition to enzymes, the plants excrete into thesoil a number of other biologically active compounds--various biotic substances (vitamins,auxins), toxins, etc. The amount of these substances in soils may be quite considerable.

  All these substances are sources of direct or supplementarynutrition for soil microorganisms and enhance their growth and accumulation in thesoil.


Root residue

  In addition to root excretion, microorganisms utilize,as sources of nutrition, dead root cells, hairs, epidermis, etc.

  The chemical composition of roots varies in differentplants. The roots of some plants contain more water-soluble substances (proteins,sugars. etc), the roots of other plants contain more hemicellulose, cellulose, andlignin. Belyakova and Parishkura (1953) found the, following chemical compositionof roots (Table 70).

Table 70
Chemical composition of various roots of plants, in per cent of dry weight
(Belyakova and Parishkura, 1953)

Substance

Lucerne

Eragrostis

Dactylis glomerata (orchard grass)

Labium multiflorum (rye grass)

Ash

5.19

11.67

12.89

13.69

Carbon

43.75

42.42

41.19

43.05

Nitrogen

2.38

0.75

1.22

1.89

C:N ratio

18.4

56.56

38.8

22.7

Protein

14.87

--

--

11.81

Water-soluble part in percent of carbon

2.36

3.29

4.62

1.39

Fats

3.01

9.0

1.3

2.0

Hemicellulose

18.21

11.26

15.82

12.58

Cellulose

20.67

20.19

18.21

19.04

Lignin

20.0

30.0

20.0

31.0

  It is, obvious that the roots of different plants mayattract different types of microflora and may be decomposed by the various speciesof this microflora.

  Upon the decomposition of roots of different plantsby microorganisms, different products of intermediate decomposition and differentproducts of the metabolism of the microbes themselves are formed. The latter arealso sources of nutrition for other species of microorganisms and, as such, togetherwith the decomposition of roots, attract another population of microbial biocoenoses.The shift of the microbial population continues until the organic substances of theplant, animal, and microbial residues are decomposed into their final products. Thesefinal products may be quite versatile, depending on the composition of the organicresidues, on the microflora forming them, on soil and climatic conditions, and onthe processes of synthesis taking place in the soil outside the cells.

 

Rhizosphere

  The role of roots in the life of microorganisms isnot only limited to the supply of nutrient substances. Around the roots more favorablephysicochemical and biological conditions for the existence of microbes, as wellas for the plants themselves are created.

  In regions where there is an abundant accumulationand development of roots the physical properties of the soil improve. The soil particleshave more structure in the rhizosphere of plants (see chapter on the structure ofsoils). With the structure of the soil particles, the respiration process of rootsand microorganisms improves, moisture is better conserved, temperature is kept ata more constant level, etc.

  The soil around roots is distinguished by a highermoisture content. According to our observations, during the vegetative period, thesoil in the rhizosphere of wheat under conditions of the Volga steppes had a higher(by one-two per cent) moisture content, and its moisture capacity was three to fiveper cent higher, than that of soils outside the root region (Krasil'nikov, 1940),This is evidently connected with the change in the structure and composition of therhizosphere soil and with the capacity of the root systems of plants to activelychange the moisture content of the surrounding soil.

  Breazeale and McGeorge (1953) have shown that whensoil dries out beyond a certain threshold, the plants moisten it in the vicinityof their roots with water transported from their aerial parts. The latter utilizethe atmospheric moisture.

  The authors grew tomatoes in soil which was graduallydried. When the plants began to wither, the vessels were transferred to a room witha high humidity (80-90 per cent of full humidity). The plants soon recovered, turgorwas reestablished in the leaves, and the soil around the roots became more moist.

  The soil in the vicinity of roots also varies considerablywith respect to acidity. Around the roots of clover, lupine, and certain other plants,the strongly acidic podsol soils became less acidic. If the control soil had a pHof 4.5. then the pH in the region of the lupine roots increased to 5-5.4. In lessacidic soils, the neutralization in the zone of the roots is much more noticeable.(Table 71).

Table 71
Change in the acidity of the soil in the root area of different plants

Soil

Clover; control

Clover; rhizo- sphere

Lupine; control

Lupine; rhizo- sphere

Wheat; control

Wheat; rhizo- sphere

Strongly podsolized deforested, the first year after plowing

4.5

4.9

4.7

5.4

4.5

4.7

Cultivated, 15 years

5.1

5.8

4.9

5.8

4.9

5.1

Intensively cultivated garden soil

5.6

6.4

5.6

6.5

5.3

5.9

  The change which takes place in the environment ofthe root zone of plants was observed by Kaserer (1940) and Eklunde (1923, 1930).According to Thom and Humfield (1932), the neutralization of acidic as well as alkalinesoils takes place in the root zone. For instance, acidic clay soils have a pH of4.5 and, in the vicinity of roots--6.1. Alkaline soils of Colorado with a pH of 7.9have a pH of 7.5 in the vicinity of the roots of cereals.

  Heller (1953) has shown that plants reduce the redoxpotential of the soil around the roots. This lowering of the potential, accordingto his data, is caused by the presence of root excretions and the microorganismsattracted by them. Intense photosynthesis of the green parts of beets lower the rH2value (redox potential) of the soil at a distance of one cm from the root surface.Cessation of photosynthesis is immediately accompanied by an increase of the rH2in the soil of the root zone. The introduction and the growth of bacteria in thezone of the roots lowers the rH2 of the best tissues.

  The soil around the roots is richer in organic substances.As noted above, it possesses greater quantities of various products of microbialmetabolism, products of the decomposition of root hairs, epidermal cells, and rootexcretions. In this zone, one also notices higher concentrations of enzymes, vitamins,auxins, certain amino acids and other biotic compounds,

  Nitrate nitrogen is absent from the root zone or isonly present in small quantities. We analyzed the soil around roots of differentplants during the whole vegetation period in the fields of the Volga area. Nitrateshave only been detected in the rhizosphere during the early stages of the growthof plants and at the end of vegetation (Table 72).

Table 72
Nitrate content in the rhizosphere of plants
(in mg per kg of soil)

Date of analysis

Wheat; rhizo- sphere

Wheat; control

Soy; rhizo- sphere

Soy; control

Sunflower; rhizo- sphere

Sunflower; control

31 May

11.4

29.86

0

12.3

4.65

21.4

5 June

15.9

35.22

0

12.68

4.85

21.1

12 June

22.5

33.9

0

14.2

4.12

22.1

15 June

7.7

37.7

0

11.03

3.1

18.5

19 June

0

24.34

0

9.67

0

15.9

26 June

0

23.96

2.9

14.19

0

6.1

2 July

0

22.54

0

2.3

0

3.5

5 July

0

16.34

0

4.58

0

13.33

10 July

0

9.11

0

12.65

0

12.45

16 July

0

11.27

3.0

13.54

0

11.4

22 July

0

10.8

0

8.65

0

19.4

27 July

0

10.3

0

9.54

0

12.54

31 July

-

-

0

7.24

0

7.86

6 August

-

-

3.4

6.9

0

5.7

10 August

-

-

5.4

6.4

0

4.2

15 August

-

-

3.6

4.2

3.4

5.2

19 August

-

0

5.4

4.7

4.6

7.2

25 August

-

0

4.1

4.2

3.6

5.2

  Katznelson and Richardson (1943) have found that thesoil in the root area is less subject to the sterilizing effects of chemical substances.On processing soil with formalin and chloropicrin, the authors detected a much greaterdecrease in the number of microorganisms outside the zone of the root system. Inthe root region of certain plants (tomatoes and others), the microbes did not reactat all to these chemicals and their number did not decrease. Living organisms, theroot region and the root system of plants seem to be less accessible to chemicalaction.

  In our experiments, plants of corn and beans were grownunder sterile and unsterile conditions, in growth containers (9 kg) filled with gardensoil from the Moscow area. When the plants reached the stage of flowering or budformation, antiseptic substances were introduced into the soil: 0.5 liter of a 30per cent solution of formalin and two g of chloropicrin per vessel. In the sterilesoil the plants perished and, in the unsterile soil, they continued to grow normally,

  It can be assumed that, in the rhizosphere of plants,a protective barrier is formed in the form of metabolic products of microbes, whichare much more numerous here than outside the rhizosphere. Evidently, the chemicalsubstances are directly decomposed in the rhizosphere by microbial organisms.

  The metabolism of microorganisms is more intense inthe root region, as are many chemical and biochemical processes, as well as the transformationsof various organic and mineral substances. In the rhizosphere, various minerals,rocks, limestone, marble, etc are decomposed at a faster rate. This process is notonly caused by root excretions (CO2 and other acids) but also by the microfloraof the rhizosphere. The more intense the growth of microbes, the faster the decompositionprocess of substances. Certain compounds, for instance, tricalcium phosphate, donot dissolve in the sterile rhizosphere of plants, but when soil microbes are addedto the vessel the substance becomes available to the plants (Gerretsen, 1948). Oneof the tasks of agricultural microbiology is the enrichment of the root region withmicrobes, which transform nonsoluble phosphorus compounds into the soluble compoundsavailable to the plant.

  Under the influence of the microflora in the rhizosphere,one notices an increase in the solubility of iron and manganese compounds. Accordingto Starkey (1955), this increase is caused by the change in the redox potential,which in quite different here than outside the rhizosphere. In the rhizosphere, iron,manganese. and other metals occur in combination with organic compounds formed bymicrobes. According to the author, amino acids, organic acids, and other metabolitesof microorganisms form stable complex compounds, which are preserved in the soilfor a long time. They are utilized by the plants and used as a source of iron, manganese,and other elements. The quantities of these organometallic compounds are greaterin the rhizosphere than outside this region.

  Weinstein and others (1954) experimentally confirmedthis data. They grew plants (sunflowers) in solutions both with and without the additionof microbial metabolites and they followed the absorption of the mineral salts ofiron. In the presence of metabolites or ethylenediaminetetraacetic acid, the uptakeof iron was faster, while in the absence of these substances and of microbes, theapplied elements were not taken up by the plants. These observations showed thatplants evidently take up iron, not in the form of mineral compounds, but in the formof organomineral substances formed under the influence of microorganisms.

  All the above data show that in the vicinity of theroots of vegetating plants, a special zone is formed in which more favorable conditionsprevail for the existence, not only of microorganisms, but also of the plants themselves.

 

 


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