phytotoxic substances from soil microorganisms and crop residues

29 Pages·2013·5.06 MB·English

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U.S. Department of Agriculture: Agricultural
Publications from USDA-ARS / UNL Faculty
Research Service, Lincoln, Nebraska
June 1964
PPHHYYTTOOTTOOXXIICC SSUUBBSSTTAANNCCEESS FFRROOMM SSOOIILL MMIICCRROOOORRGGAANNIISSMMSS AANNDD
CCRROOPP RREESSIIDDUUEESS
T.M. McCalla
Soil and Water Conservation Research Division, United States Department of Agriculture, and Nebraska
Agricultural Experiment Station, University of Nebraska, Lincoln, Nebraska
F.A. Haskins
Soil and Water Conservation Research Division, United States Department of Agriculture, and Nebraska
Agricultural Experiment Station, University of Nebraska, Lincoln, Nebraska
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McCalla, T.M. and Haskins, F.A., "PHYTOTOXIC SUBSTANCES FROM SOIL MICROORGANISMS AND CROP
RESIDUES" (1964). Publications from USDA-ARS / UNL Faculty. 21.
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BACTERIOLOGICALREVIEWS
Vol.28, No.2,pp. 181-207 June,1964
Copyright@ 1964bytheAmericanSocietyforMicrobiology
Printedin U.S.A.
PHYTOTOXIC SUBSTANCES FROM SOIL MICROORGANISMS AND
CROP RESIDUES'
T. M. MCCALLA AND F. A. HASKINS
Soil and Water Conservation Research Division, U.S. Department ofAgriculture, andNebraska
Agricultural Experiment Station, University ofNebraska, Lincoln, Nebraska
INTRODUCTION................................................................................. 181
SOIL MICROBIAL PRODUCTS INHIBITORY TO MICROBIAL GROWTH ..................... 183
PHYTOTOXIC SUBSTANCES IN PLANTS..............................................................184
Germination Inhibitors....................................................................... 184
Growth Inhibitors........................................................................... 186
Plants containing growth inhibitors.......................................................... 186 D
Nature ofgrowth inhibitors in plants........................................................ 187 ow
EARLYWORKONPHYTOTOXICSUBSTANCESFOUND INPLANTRESIDUESAND SOIL ............. 187 nlo
Isolation ofSpecific Compounds From Soil.................................................... 188 ad
Effect ofStraw on Plant Growth ................................... 188 ed
RECENT WORK ON THE OCCURRENCE OF PHYTOTOXIC SUBSTANCES IN SOIL AND THE PRODUCTION OF fro
InfTlHuEenScEeSofUBCSeTrAtaNiCnESOrBgYanMiIcCCRoOmOpRoGuAnNdIsSMaSn.d..A.nt.i.b.i.o.t.i.c.s..o.n..P.l.a.n.t..G.r.o.w.t.h............................................... 118888 mmm
IOnrfglauneincceAocfidCsarabnodnDAimoixnidoe,AcBiidcsarbionnSaotiels,..N.i.t.r.it.e.,..H.y.d.r.o.g.e..n.S.u.l.f.id.e.,..a.n.d..A.m.m.o..n.i.a..o.n..P.l.a.n.t..G.r.o.w.t.h.. 119910 br.a
s
ProductionofPhytotoxinsbySoilMicroorganisms andPlantPathogens........................... 192 m
Gibberellafujikuroi........................................................................ 193 .org
Penicillium................................................................................ 193 a
Aspergillus................................................................................ 194 t U
Trichoderma and Fusarium................................................................ 194 NIV
Alternaria................................................................................. 195 O
Other microorganisms....................................................................... 195 F N
PhytotoxicSubstancesinDecomposingPlantResidues,SoilOrganicMatter,andSoil..... .......... 195 E
Phytotoxic Substances in Forest Soils ................................ 196 BR
Phytotoxic Effects Encountered in Stubble Mulching............................................ 197 AS
SOMESPECIFICPLANTEFFECTSPOSSIBLYCAUSEDBYTOXINS FROMMICROORGANISMS ............ 198 KA
LegumeBacteriaFactorinthe Chlorosis ofSoybeans............................................. 198 -L
Frenching Disease of Tobacco................................................................ 198 INC
Replant Problem in Peaches. .......... ..................................................... 199 O
Replant Problem in Citrus.................................................................... 199 LN
Sod-binding ofBromegrass.................................................................... 201 on
Stunting of Corn Associated with Stubble Mulching........................................... 201 A
Seedling Disease ofRice...................................................................... 202 ug
u
COINnCoLcUuSlIaOtNiSo.n..F.ai.l.u.r.e..i.n..S.u.b.t.e.r.r.a.n.e.a.n..C.lo.v.e.r................................................................................. 220022 st 30
OUTLOOK............................................................................. 202 , 20
LITERATURE CITED............................................................................ 203 07

INTRODUCTION marysourceofmineralsforplantgrowth.Inaddi-
The role of organic matter in the growth of tion,beneficialeffectsonsoilstructureandwater-
plants has been a subject of much investigation holding capacity were attributed to the presence
andcontroversysincethesixteenthcentury. Dur- oforganic matter. Withthedevelopment ofagri-
ing the earlyera, decompositionofplantresidues cultural chemistry culminating in the work of
and green and animal manures provided a pri- Liebig in the nineteenth century, it was dis-
covered that plants could make satisfactory
I PublishedwiththeapprovaloftheDirectoras growth in the absence of added organic matter if
Paper no. 1354, Journal Series, Nebraska Agricul- suitablekindsandamountsofinorganicnutrients
turalExperiment Station, Lincoln. were supplied. However, persistent efforts were
181
182 MCCALLA AND HASKINS BACTERIOL. REV.
made by various investigators and lay groups to develop normally with adequate supplies ofinor-
emphasize the important role of organic matter, ganic nutrients, but they mayalso take up many
rather than inorganic fertilizers, in soil fertility organic substances which influence growth. In
and plant growth. Because of the complexity of recent years, a renewed interest has developed in
the problem and lack of suitable techniques, no the roleoftheseorganic substances. Thisinterest
satisfactory solution to the controversy was ob- hasbeengreatlystimulated bytheavailability of
tained during Liebig's time. new techniques such as paper, gas, and column
Since the Liebig era, frequent attempts have chromatography and infrared spectrophotometry
been made to determine in detail the influence of whichaidinthe isolation and identification ofor-
organic matter on plant growth. For example, ganic compounds.
D
o
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n
lo
a
d
e
d
fro
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m
m
b
r.a
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FIG. 1. Influenceofstubblemulchingwith8tonsofstrawperacreongrowthofcornatLincoln,Neb. Note o
irregulargrowthofcornonmulchedplot. n A
u
g
u
Schreiner and Shorey (113) attempted to explain Recent field observations disclosed the occur- st 3
the low productivity ofsome soils onthebasis of rence ofreducedplant growth under the system 0
certain toxic organic substances present. Dihy- of farming known as stubble mulching (Fig. 1). , 20
0
droxystearic acid and vanillin were isolated and McCallaandArmy (80)andotherssuggestedthat 7

shown to be toxic to plants in aqueous solution. this effect was the result of toxic decomposition
However, it was shown that soil and fertilizers products of microorganisms or substances from
tend to neutralize the effect of these toxic sub- plant residues. Similar observations of retarded
stances. Since adequate mineral fertilization plant growth encountered in citrus replant and
largely overcame the toxic effects of such com- peach tree replant, seedling inhibition and
pounds, most investigators doubted that organic frenching of tobacco, sod-bound bromegrass, and
substances in the soil had any important direct reducedgrowthofforesttreeseedlingsinsomein-
influenceonplantgrowth.Withthediscoveryand stances add support to the belief that growth in-
utilization of antibiotics and herbicides, there hibitors may accumulate in the soil (9, 72, 95,
wasare-examination ofthisposition. Plants may 96, 128).
VOL. 28, 1964 PHYTOTOXIC SUBSTANCES FROM SOIL MICROORGANISMS 183
Certainly under field conditions, with heavy (122), and others (17, 19, 38, 48, 142, 143, 144)
fertilization, large quantities ofplant and animal have shown that many actinomycetes and fungi
residues are returned to the soil to decompose. can produce detectable quantities of antibiotics
Numerous organic and inorganic substances re- insterilesoils supplemented with organic matter.
sult from this decomposition. The concentration Grossbard (48) also found that antibiotics were
of any one constituent may vary greatly with produced in autoclaved soils enriched with
time and environmental conditions. Minute readily available sources of carbon and inocu-
quantities of many organic substances have pro- lated with Penicillium patulum or Aspergillus
nounced effects on plant growth, and it is highly clavatus. Hessayon (52, 53) and Schmidt (110),
probable that, under certain conditions, concen- in reviews of the literature, cited several reports
trations of these substances become sufficiently of toxicity of soil extracts to fungi and bacteria.
high to cause significant effects on plant growth. Antibiotic production in sterile soil was also re-
The purpose ofthis paper is toreview research ported.
D
o
TABLE 1. Diameter offungal colonies with and without alcohol extracts ofsurface soils wn
lo
a
Avgdiamofcolonyb d
e
d
Fungus ExptA ExptB ExptC fro
m
m
Cltorn IEIxtgraofctP5f5r-oim Control E3xtgroafctP5f5-rio1m Coonto E3xtgraofctP5f4r-oim mb
mm mmn mm mm mm mm r.as
m
Penicillium humicola 1.921..0 . ** 23.5 19.8** 23.2 19.7** .o
Aspergillus8sydowi.10.7 9.2* 13.7 10.8* 12.8 10.7* rg
Zygorhynchus vuillemini 78.5 | 78.7 56.3c 48.5**c 53.Oc 55.5c a
Sporotrichumpruninosum. 20.2 18.7** 24.3 20.7** 22.0 19.5** t U
N
Moniliahumicola.22.0 19. ** 27.8 18.8** 28.0 22.5** IV
O
a Thistable appearedfirst in Soil Sci. 55:377-391, 1943. See reference90. Publishedwithpermissionof F N
The Williams & Wilkins Co. E
B
bAverage ofthree plates after5days ofincubation. Symbols: * = significant by ttest in comparison R
A
withcontrol, beyond 5% level; ** = highlysignificant by ttest incomparison with control, beyond 1% S
level. KA
cDiameter measured on third day of incubation. -L
IN
C
on microbial decomposition products and organic Newman and Norman (90) showed that dried OL
substances in crop residues and soil which may ethanolextractsofsurfacesoilsamplesfromMar- N o
inhibit plant growth. No attempt was made to shall siltloamand Clarion silt loamin Iowa con- n A
review all the literature available. Only typical tained toxic substances, probably of microbial u
g
references are cited to illustrate salient points. origin, that inhibited the growth of soil micro- us
organisms as showninTable 1. The investigators t 3
0
SOIL MICROBIAL PRODUCTS INHIBITORY found that aqueous soil extracts did not reduce , 2
TO MICROBIAL GROWTH the growth of soil bacteria. However, the alco- 00
7
Numerous investigators (17, 44, 48, 69, 125, holic extract of both surface and subsurface soil
130) have shown that microorganisms produce a samples reduced the activity of soil microor-
wide variety of compounds (antibiotics) inhibi- ganisms.
tory to microbial growth. Some of these com- Hessayon (53) foundthat Trichotheciumroseum
pounds are toxic to plant growth, as will be dis- produced lesstrichothecin innonsterile soils than
cussed later. Many of the compounds are selec- in sterile soils. Clay soils had a higher trichothe-
tive in their action; others, such as penicillin, in- cin-producing capacity than did sandy ones.
hibit the growth of a wide variety of micro- Brian (17, 19) indicated that a number of fungi,
organisms. actinomycetes, andbacteriaareknowntoproduce
Stevenson (127), Gottlieb et al. (45), Stallings antibiotics in both sterile and normal soil if the
184 MCCALLA AND HASKINS BACTERIOL. REV.
soil is suitably supplemented with organic stantial amounts of antibiotics were produced in
matter. inoculated sterile soil supplemented with organic
Pincketal. (101, 102) andSoulidesetal. (121), matter, less in inoculated sterile unsupplemented
inastudyoftheadsorptionofantibiotics byclay soil, and little or none in normal soil unless sup-
minerals, showed that the antibiotics could be plemented with large amounts oforganic matter.
classified into three groups: (i) strongly basic In a normal soil there may be local areas where
(streptomycin, dihydrostreptomycin, neomycin, concentrations of organic matter are sufficiently
and kanamycin); (ii) amphoteric (bacitracin, high to favor the production of antibiotics if the
chlortetracycline, and oxytetracycline); and (iii) proper microorganisms are present.
acidic (penicillin) orneutral (chloramphenicoland
PHYTOTOXIC SUBSTANCES IN PLANTS
cycloheximide). The strongly basic antibiotics
with one exception were not released from mont- Manyplantscontainsubstances thatadversely
morillonite, vermiculite, or illite. Streptomycin affect seedgermination andplantgrowth (39, 79,
and dihydrostreptomycin were released to vary- 140). The return to the soil ofresidues from such D
o
ing degrees from kaolinite. The amphoteric anti- plants provides an obvious source of phytotoxic w
n
biotics were released from all the clay minerals. materials whose formation does not dependupon lo
a
Bioassays indicated that, to be effective in in- the activity of microorganisms. d
e
bhiebirteilnegasmeidcrforboimalthgerocwlatyhs,.the antibiotics had to Germination Inhibitors d from
Brian (17, 19) showed that, while many anti- Cox et al. (29) found germination inhibitors in m
biotics, such as penicillin, viridin, gliotoxin, fre- the seed coatof certain varieties of cabbage. The mb
quentin, and albidin, are labile substances and inhibitor could be removed with water, alcohol, r.a
s
are rapidly decomposed in the soil, others like or sulfuric acid. Smith (120) showed that chaff m
fradicin and cycloheximide are very stable in a of small grains inhibited the germination of ce- .org
number of soils. Jefferys (56) tested the stability reals.Siegel (117) foundthatwaterextractsofred a
of the antibiotics albidin, frequentin, gladiolic kidney beans inhibited germination and growth t U
N
acid, gliotoxin, griseofulvin, mycophenolic acid, of flax and wheat. Various experiments with the IV
patulin, viridin, penicillin, and streptomycin in extracted material indicated that more than one OF
various soils. The antibiotics persisted innatural inhibitorwaspresent. BartonandSolt (7) demon- N
E
soils for varying lengths oftime froma few days strated germination inhibitors of wheat seeds in B
R
to more than 20 days, depending on the kind of extracts of seeds of Sorbus aucuparia, Berberis A
S
soil, pH, and microbial activity. Inactivation of thunbergii, of three varieties of Lactuca, and of K
A
the antibiotics was caused by adsorption by soil, nondormant seeds of Phaseolus sp., Triticum sp., -L
microbial activity, or instability of antibiotic at Hordeumsp.,Glycinesp.,Solanummelongena,and IN
C
certainpHlevelsinthesoil. TheeffectofpHwas Nicotiana tabacum. O
L
important inthe inactivation ofalbidin, frequen- Evenari (39), in areviewarticle, reported that N
o
tin, gliotoxin, penicillin, and viridin. Strepto- germination inhibitors are widely distributed in n
A
mycin was inactivated largely by adsorption. many plant species. Thus, inhibitors were found u
g
Biological inactivation of griseofulvin, myco- in the pulp, juice, and coat of fruit, inseed coat u
s
phenolic acid, and patulin was noted. and embryo, in the leaf sap, and in bulbs and t 3
0
Many factorsappeartobeinvolvedinthepro- roots. Some of the materials responsible for ger- , 2
ductionaswellasthepersistenceofantibioticsin mination inhibition were: (i) hydrogen cyanide 00
7
nonsterile soil. A microorganism that grows well fromamygdalinin manyseeds; (ii) ammonia, re-
and produces abundant yields of antibiotic in leased by hydrolysis of nitrogenous compounds;
sterile culture may not be able to survive, much (iii) ethylene, liberated from many fruits as well
less to produce an antibiotic, incompetition with as from whole plants; (iv) mustard oils contain-
theentrenchedflorainanonsterilesoil (57).How- ing isothiocyanate derivatives; (v) organic acids,
ever, Brian (19) states that in certain circum- such as malic and citric acids formed by the
stances antibiotics are produced in appreciable guayule plant, or caffeic and ferulic acids from
quantities by microorganisms in soil. The chief tomato juice; (vi) unsaturated lactones, such as
nutrient requirement for antibiotic production parasorbic acid, anemonin, and coumarin; (vii)
appearstobeasuitable carbonsource. Thus,sub- aldehydes, suchasbenzaldehyde,salicylaldehyde,
VOL. 28, 1964 PHYTOTOXIC SUBSTANCES FROM SOIL MICROORGANISMS 185
TABLE 2. Effect of aqueous extracts ofplants on germination and growth ofMida wheat*
aeroft congeoftl
Plantfamily Species Cogctermnna- oleopthl eg~
tiont g
cm cm
Control 91 3-5 4-6
............
Asclepidaceae Asclepias syriaca 2 64 2-4 1-2
......
5 51 1-3 <1
2 71 2-4 2-3
Carophyllaceae..... Lychnis alba 5 45 1-2 <1
Chenopodiaceae Chenopodium album 2 69 2-3 1-2
... D
o
w
Compositae........ Ambrosia trifida 2 68 1-3 1-2 nlo
5 40 0.5-1.5 <1 a
d
Cirsium discolor 2 66 2-4 1-2 e
d
5 47 1-2 <1 fro
Iva xanthifolia 2 64 1-2 1-2 m
5 50 0.5-1.5 <1 m
m
Solidago spp. 2 55 1-3 2-3 b
r.a
s
Cucurbitaceae...... Cucurbita maxima 2 75 2-3 0.5-1 m
.o
Euphorbiaceae..... Euphorbia esula arg
Stems 5 72 1-2 1-2 t U
Leaves 1 73 2-4 1-3 NIV
2 69 1-3 1-2 O
3 61 1-3 0.5-1.5 F
4 53 1-2 <1 NE
5 56 <1 <1 B
R
A
S
Gramineae......... Avena sativum var. Clinton 2 81 2-4 1-2 KA
Triticum vulgare var. Mida 2 73 2-3 1-3 -L
Zea Mays var. Minhybrid 504 2 71 2-3 1-2 IN
5 69 1-2 <1 CO
L
N
Labiatae.... Nepeta cataria 2 58 2-3 1-2 on
5 40 1-2 <1 A
u
g
Leguminosae....... Pisum sativum var. Alaska 2 71 2-3 1-2 us
5 55 0.5-1.5 <1 t 30
Soja max var. Ottawa-mandarin 5 60 0.5-1.5 <1 , 2
Phaseolus vulgaris var. Black Wax 00
Leaves 5 60 0.5-1.5 <1 7
Stems 5 87 2-3 1-2
Entire plant 5 71 1-2 0.5-1.5
Liliaceae.... Polygonatum spp. (leaves only) 2 65 2-4 1-3
5 57 1-3 1-2
Malvaceae Hibiscus trionum 2 71 2-4 2-4
Malva spp. 2 69 2-3 1-2
Plantaginaceae. .. Plantago spp. 2 83 2-4 1-2
186 MCCALLA AND HASKINS BACTER'I'L. REV.
TABLE 2-(cont.)
Plantfamily Species CoctgePreemnaigeneoaft-- cRlanegoeg*tohpil |Ranlgeengotfhroot
tiont ent
cm cm
Polygonaceae.Polygonum pennsylvanicum 2 76 2-3 1-2
Portulacaceae...... Portulaca oleracea 2 75 2-3 <1
Solanaceae ......... Lycopersicon esculentvumar. Margobe 2 58 1-3 0.5-1.5
Umbelliferae....... Petroselenium hortense 3 68 2-4 1-3
* Thistable appeared first inWeeds4:363-368, 1956. See reference 68. Do
w
t Concentration listed is equal to number of grams of dry plant material extracted with 100 ml of n
water. loa
d
t Germination period was 4 days. e
d
fro
and cinnamaldehyde; (viii) essential oils contain- nitrogen. However, on the basis of Benedict's m
inga wide variety ofaromatic and alicyclic com- work (9), it is reasonable to expect that some m
m
pounds; and (ix) alkaloids, suchascocain, physo- growth-inhibiting factor present in bromegrass b
stigmin, caffein, chinin, berberin,andcodein. roots may be involved insod-binding. r.as
m
In general, substances considered to be germi- Bennett and Bonner (10) made a survey of .o
nation inhibitors were found to have stimulatory shrubs native to the Mojave Desert for the oc- rg
effects ongermination atsuitable concentrations. currence of plant growth inhibitors. Relatively at U
The inhibitors are presumably operative through toxic extracts were obtained from Sarcobatus N
theireffectsonenzymeactivityandotherphysio- virmiculatus, Prosopis juliflora, and Viguiera IV O
logical activities ofthe plant. reticulate. The extract of Thamnosma montana F
Torr. and Frem. was the most toxic to the ex- NE
Growth Inhibitors tracts tested, with tomato as the assay plant. BR
Borner (14) indicatedthatmanyplantscontain Two highlytoxic crystalline compounds wereiso- AS
plant growth inhibitors. Plants such as brome- latedfromthisextractand wereassigned the em- KA
grass, sweetclover, guayule, andwalnut maycon- pirical formulas C16H1506(OCH3) and C11H403- -L
IN
tain or excrete into the soil materials that are in- (OCH3)2. Ultraviolet-absorption spectra of the C
O
hibitorytothegrowthofotherplantsasshownby compounds indicated that they were similar in L
N
Bonner (12), Bonner and Galston (13), and structure. o
Woods (140). LeTourneau et al. (68) found that aqueous ex- n A
Plants containing growth inhibitors. Breazeale tracts of dried plant material representing 24 ug
(16) in 1924 noted the adverse effects ofsorghum different species contained inhibitors of wheat us
on succeeding crops. In 1941, Benedict (9) ob- germination and growth (Table 2). Autoclaving t 30
served a significant reduction in top growth of the aqueous extracts did not destroy their in- , 2
0
bromegrass grown in sand culture with various hibitory activity. 0
7
amounts ofdead bromegrass roots. He concluded Nielsen et al. (92) determined the effect of
that lack of nitrogen was not the cause for the water extracts offive crop residues (alfalfa, corn,
reduced growth, as was suggested later byMyers oats, potatoes, and timothy) on the germination
and Anderson (88), inasmuch as the treatments andgrowthofsixplantspecies:alfalfa, corn,oats,
containing roots were richer in nitrate nitrogen peas, soybeans, and timothy. In general, alfalfa
than were the untreated controls. Pure stands of extractcausedthegreatestreductioninshootand
bromegrass often become sod-bound, a condition root length as well as percentage germination.
which results in reduced top growth and a thin- Plant species differed greatly in tolerance to the
ningofthestand.Sod-bindinghasbeenattributed extracts, alfalfa being the most tolerant and
to dense root growth and to a lack of available timothy the least.
VOL. 28, 1964 PHYTOTOXIC SUBSTANCES FROM SOIL MIVROORGANISMS 187
LeFevre and Clagett (67) foundthatwater ex- growth-inhibiting substances are widely dis-
tracts ofquackgrassrhizomesinhibitedgrowthof tributed among plant species.
eight crop plants by 50to 84%. Uponconcentra- Nature of growth inhibitors in plants. Borner
tion by paper chromatography and ion-exchange (14),inareviewdealingwithliberationoforganic
column techniques, the growth inhibitor was substances from higher plants in relation to soil
found to be anionic, soluble in polar solvents, sickness, discussed the following compounds:
insoluble in nonpolar solvents, and unstable in (i) liberated from roots-amino acids, sugars,
strong acids and bases. scopoletin and scopoletin glycoside, trans-cinna-
Jameson (55) prepared water extracts and 50 mic acid, and enzymes; (ii) liberated from seeds
and 100% ethyl alcohol extracts of leaves and and fruits-amino acids, sugars, flavones, phe-
herbaceous stems ofplants representing20differ- nolic compounds, and gaseous excretions (ethyl-
entspecies, including ninetrees andshrubs, eight ene, ammonia, hydrocyanic acid); (iii) liberated
forbs andhalfshrubs, andthreegrasses. Extracts from plant residues-phenolic compounds, 3-
ofallspecies testedinhibitedthegrowthofwheat acetyl-6-methoxybenzaldehyde, amino acids,
D
radicles. ExtractsofCordylanthuswrightiihadthe amygdalin, coumarin, and phlorizin; (iv) libe- o
w
greatest inhibitory effect; those ofErodium cicu- rated from leaves-absinthin, amino acids, and n
lo
tariumandAgropyron smithiihadtheleasteffect. juglone. a
d
Although the greatest inhibitory effects were Woods (140), inareview ofbiologicalantagon- ed
notedinextractsofspeciesthatalsodisplayedthe ism due to phytotoxic root exudates, indicated fro
strongest toxic effects in the field, Jameson con- that representatives of many plant families pro- m
m
cluded that theexistence ofagrowthinhibitor in duce phytotoxic root exudates containing oils, m
aplantextractdoesnotnecessarilymeanthatthe antibiotics, coumarin, alkaloids, thiamin, biotin, br.a
inhibitor is of ecological importance in the field. mineral salts, enzymes, aldehydes, nitrogenous s
m
Guenzi and McCalla (49) made water extracts compounds, ammonia, amino acids, nucleotides, .o
of sweetclover stems, wheat straw, soybean hay, and nucleic acid derivatives. rg
a
bromegrass hay, oat straw, sweetclover hay, and Garb (43) listed additional plant constituents t U
corn and sorghum stalks, and observed their with growth-inhibiting properties as follows: N
IV
effects on growth of sorghum, corn, and wheat protoanemonin fromAnemonepulsatilla; byakan- O
seedlings. The toxicity of the extracts increased gelicin from Thamnosma montana; parasorbic F N
in the order oftheirlisting. acidfromSorbusaucuparius;vanillinfromvanilla E
B
Cochrane (25) found that corn residue in- bean;arbutinfromBergeniacrassifoliaandPyrus R
A
creased root rot and decreased yield of lettuce. communis; scopoletin from oats (Avena); and S
K
The residue, added to soil inconcentrations of0, umbelliferone, plant not listed. A
1, 2, and 5%, caused lettuce seedling mortalities In other work on the production of growth in- -LIN
of0, 0, 41, and 44%, respectively. After the soil- hibitors by plants, Bonner (12) found that oxalic C
O
residuemixturewasincubatedunderwarm, moist acid was secreted by the roots of oxalis; Bonner L
N
conditions for a period of 30 days, seedling mor- and Galston (13) observed that trans-cinnamic o
n
talities were reduced to 8, 3, 0, and 5%, respec- acidwassecretedbyguayuleroots;andGrayand A
u
tively. Theeffectwasnotattributable tonutrient Bonner (46, 47) identified 3-acetyl-6-methoxy- g
u
starvationnortosimple pathogenesis by anema- benzaldehyde in extracts of Encelia farinosa st 3
tode or microorganism. Cochrane suggested that leaves. 0
the plant residues exerted a direct toxic effect on , 20
EARLY WORK ON PHYTOTOXIC SUBSTANCES 0
the roots of susceptible plants, which was prob- FOUND IN PLANT RESIDUES AND SOIL 7
ably complicated by action of secondary rot-
As indicated in the introduction, Liebig's work
producing microorganisms.
in the nineteenth century was followed by a
Other growth inhibitors have been reported in
periodduringwhichrelatively littleemphasis was
leaves and stems of sugarcane (35), immature
given to studies dealing with the role of organic
soybean seeds (61), guayule roots (13), oxalis matter in plant nutrition. However, sporadic
roots (12),inmacadamia (Macadamiaintegrifolia, efforts have been made to demonstrate the im-
Al.tetraphylla, andtheirhybrids) (86),andinchou portance oforganic matter for plantgrowth. Sev-
moellier (Brassica oleraceae var.) (23). Obviously, eral examples of such work, done between 1900
188 MCCALLA AND HASKINS BACTERIOL. REV.
and 1925, have been selected for inclusion in this kaolin, or quartz largely neutralized the phyto-
review. toxicity of vanillin or guanidine carbonate.
Isolation ofSpecific Compoundsfrom Soil Effect ofStraw onPlant Growth
About 1910, Schreiner and Shorey (113) and Onthebasisofqualitativechemicaltests,Colli-
others (111, 112, 118), in attempting to explain son and Conn (27) concluded that salicylic acid,
the poor growth of plants on some soils, isolated dihydroxystearic acid, and vanillin were present
specific organic compounds from the soil. One of in straw. They suggested that these compounds
the compounds was dihydroxystearic acid, asub- might account for the detrimental effect ofstraw
stancewhichreducedplantsizeandhadtheaddi- on plant growth, although they were also aware
tional effects ofdarkening the root tips, stunting of the carbon-nitrogen relationships which had
root development, causing enlarged root ends been demonstrated by the classical works of
which were often turned upward like fishhooks, Doryland (34) and Murray (87). Collison (26)
andstronglyinhibitingtheoxidizingpowerofthe observed that water extracts ofstraw and alfalfa
D
roots.Whenthiscompoundwasaddedtonutrient hay were toxic to barley seedlings. The extract o
w
solutions, it was toxic to plant growthin concen- from alfalfa hay was more toxic than that from n
lo
trations of about 20 to 100ppm (Table 3). How- wheat straw. Autoclaving the water extract did a
d
ever, the effect of dihydroxystearic acid was not destroy the toxic factor. Later, Myers and ed
Anderson (88) discounted the toxicity idea and fro
TABLEan3.dEtfrfaencstpoifradtiihoyndroofxwyhsteeaatrisceedalciindgsoningrowth concluded from their experiments that the in- mm
hibitory effect resulted simply from the tie-up of m
solution culture* b
available nitrogen by plant residues such as r.a
Concn of dihydroxystearic Percentageofcontrol straw. sm
acid Transpiration Green wt .o
pp2m0 75 87 RPEHCYETNOTTOWXOIRCKSUOBNSTTAHNECEOSCCIUNRSROEINLCAENODF at Urg
THE PRODUCTION OF THESE SUB- N
50 56 78 IV
100 24 53 STANCES BY MICROORGANISMS O
F
200 20 54 The discovery of antibiotics in 1929 by Flem- N
Bur*.ThSoiislstBaubllle.a5p3p:e1-a5r3e,d19fi0r9s.tSieneUr.eSf.erDeenpcte.11A3g.r. siungbsatnadnctehsebdiyscWoevnertyaonfdploatnhtehrsor(m3o,n1e1s,o1r39g)ropwrtoh- EBRA
vided new stimulation forstudies concerned with SK
largely neutralized in soil. Fraps (41) found that the influence of organic soil constituents on A-L
vanillin and coumarin were oxidized rapidly in plants. IN
C
the soil; about 20 to 50% disappeared within 2 Organic substances in the soilare produced by O
weeks. or derived fromanimals, plants, and microorgan- LN
Schreiner and Skinner (114), Fraps (41), and isms. As Starkey (123) indicated, these organic on
Funchess (42) showed that the harmful effect of materials in the rhizosphere may have a variety A
u
dihydroxystearic acid could be largely overcome of effects on plants. For example, plant growth gu
s
by adequate mineral fertilization of the plant. maybestimulatedorinhibited, orthe food value t 3
However, toxic effects of coumarin and vanillin of the plant may be affected. In this review, 0, 2
were not prevented by the application of inor- primaryemphasis is placed on microorganisms as 0
0
ganic nutrients. the sources ofthese organic substances, although 7
Skinner and Noll (119) found vanillin and plant oranimalsourceswillbediscussed,particu-
salicylic aldehyde in a silty clay loam soil at larly as they serve as substrates for microbial
ArlingtonFarms, Va., several months after these action.
compounds wereappliedand after the end ofthe
Influence ofCertain Organic Compounds and
crop season. On plots fertilized with sodium
nitrate, however, vanillin was quickly destroyed. Antibiotics on Plant Growth
Neither vanillin nor salicylic aldehyde persisted Prill et al. (104) studied the growth of wheat
inlimed soil. Truog and Sykora (135) found that rootsinthepresence ofalargenumberoforganic
finely divided soil materials such as lime, soil, acidsinconcentrationsrangingfrom0.002to6.25
TABLE 4. Lowest concentration ofadded organic compounds showing toxicity to ladino clover
seedlings in a complete nutrient culture, and the concentrations allowing optimal normal
growth in the absence ofinorganic nitrogen*
OOrrgngicacconomomiupncound ttoLoiocwxeosintccgroCoowpntctinmhaflor Organiccompound toxLiocwecosntcn Cogoprntociwnmtahflor
ppm ppm ppm ppm
Amino Acids Vitamins (cont.)
L-Cystine................. NT Si Pyridoxine-HlI . ....... 500 Un
D-Isoleucine............... NT 1,000 p-Aminobenzoic acid....... 200 200
DL-Lysine................. NT 500 Niacinamide............... 200 200
L-Tyrosine................ NT 200 Nicotinic acid............. 200 Un
Cysteine-HCl............. 1,000 Un Pyridoxal-HCl............. 200 Un
Hydroxyproline 1,000 500
L-Isoleucine............... 1,000 1,000 Antibiotics
DL-Isoleucine.............. 1,000 1,000 Penicillin G-K............. 1,000
L-Leucine................. 1,000 500 Penicillin G-Na............ 1,000
DL-Serine................. 1,000 500 Chlortetracycline-HCI. 50 D
Tryptophan............... 1,000 200 Oxytetracycline............ 50 o
w
DL-Alanine................ 500 200-500 Streptomycin.............. 50 n
lo
D-Arginine HC1........... 500 50 Bacitracin................. 5 a
d
L-Asparagine.............. 500 200 Chloramphenicol........... 5 e
d
L-Aspartic acid............ 500 500 fro
D-Glutamic acid........... 500 500 Miscellaneous m
Glycine................... 500 200 Fumaric acid.............. NT m
m
L-Histidine-HCI........... 500 500 Maleic anhydride.......... NT b
L-Proline.................. 500 500 Na Cu chlorophyllin....... NT r.a
s
DL-Threonine............. 500 500 Oxamide................... NT m
DDLL--VMaeltihnieon.i.n..e......................... 250000 5U0n0 RSuuctciinni.c..a.c.i.d............................. NNTT a.org
DL-Norleucine............. 200 Si Tannic acid............... NT t U
L(+)-Glutamic acid....... 200 Arbutin................... 1,000 N
IV
Citric acid................. 1,000 O
Nucleic Acid Group Malic acid................. 1,000 F
Nucleic acid.............. NT 1,000 Malonic acid.............. 1,000 NE
Adenylic acid............. 1,000 1,000 Methylamine-HCI. 1,000 200 B
R
Guanine-HCl.............. 500 50 Pancreatin................ 1,000 A
S
Uracil.................... 500 200 Pepsin..................... 1,000 K
A
Adenine sulfate........... 200 50 Vanillin................... 1,000 -L
Xanthine................. 200 Un Catechol.................. 500 IN
C
Cinnamic acid............. 500 O
Alkaloids Creatinine................. 500 50 LN
L-Hyoscyamine............ NT Un Diethylphosphite .......... 500 o
n
Atropine.................. NT Un Phloroglucinol...... 500 A
Brucine................... 500 Un a-Picoline................. 500 Un ug
Morphine................. 500 Un Pyridine................... 500 Un us
Nicotine.................. 500 Un Dimethylhydroresor- t 3
0
Trigonelline............... 500 200-500 cinol.................... 200 , 2
Arecoline................. 200 Un Na taurocholate........... 200 Un 00
Caffeine................... 50 Un Succinimide............... 200 50 7
Quinidine................. 50 Un Aniline nitrate............. 50 Un
Nicotyrine................ 50 Un Barbital................... 50 Un
Nornicotyrine............. 50 Un Biuret..................... 50 Un
Quinine-HlI .............. 50 Un Coumarin................. 50 Un
Theobromine.............. 50 Un Hydroxyquinone........... 50
m-Nitrobenzoic acid....... 50 Un
Vitamins Quinone................... 50
Ca panthothenate......... NT Un Benzidine................. 5 Un
Pyridoxamine............. Un Quinoline.................. 5 Un
Ascorbic acid............. 1,000 Stovaine................... 5
Thiamine................. 1,000 Un Sulfapyridine.............. 5 Un
*This table appeared first in Agron. J. 52:317-319, 1960. See reference 108. NT = not toxic at 1,090
ppm;Un = nitrogenunavailable; SI = nitrogenslightlyavailable; - = nottestedornon-nitrogenous.
189