the effect of soil microorganisms on plant productivity

.- THE EFFECT OF SOIL RICROORGANISMS ON PLANT- PRODUCTIVITY I

J ( .

Y.R. Domergues, H.D. Diem and F. Crmry*

ABSTRACT

I:oilmicroorganismsaffect plant product ivi ty favourably or unfavourably e i t h e r ind i rec t ly , by ac t ing upon s o i l physical o r chemical proper t ies , o r d i r e c t l y by in te rac t ion with plant roo ts . Beneficial or detr imental e f fec ts on s o i l propert ies concern s t ruc tures , coat ing of p a r t i c l e s with water-repellent compounds, redox poten t ia l , s o i l n i t rogen s t a tus ( e . g . gains by N2 - f ixa t ion and losses through d e n i t r i f i c a t i o n ) , a v a i l a b i l i t y of nu t r ien ts (especial ly N and P ) and accumulation o r elimination of phyiotoxic inorganic and organic compounds. a f f e c t plant growth by improving or reducing nut r ien t or wzter uptake (some a r e well-known, e .g . ecto- or endo-mycorrhizae; o thers a re not even character ized, such as microorganisms iwlucing proteoid roocs). a l so produce growth-regulating substances o r p ro tec t t h e @ant against cer ta in 7athogens. highly desirable , but it is d i f f i c u l t t o accomplish. Some mccess has a l reaey been zchieved with d i r e c t inoculation, especial ly in the case of N2 - f i x e r s a d mycorrhizae. methods invol-:ing c l a s s i c a l means, s t e r i l i z a t i o n o r the q F i i c a t i o n of specif ic ccnp’inds, Ls possible provided some requiremenu e r e f u l f i l l e d . Altering the s o i l microflora by act ing through t h e plant 1s another promising poss ib i l i ty . reference t o :heir importance and occurrence i n t r o p i c a l soils.

. . pihny agronomists today would readily ayree that soil micro-

S o i l microorganisms d i r e c t l y

They may

Manipulation of t h e s o i l microflora a-wears t o be

Indi rec t control of s o i l microflora by

The processes a r e discussed with s;r?cial

organisms affect plant productivity, zspecially in the tropics. ü \ ’ Yet this idea took a long time to penetrate, except in the

case of Rhizobium, because microbiologists-were mainly concerned with the yhysiology of microorganisms that had been isolated and skudied in %est-tubes or Petri dishes and were therefore out Òf their natural environment. the study of the very complex soil-plant-microorganism systems is mich more difficult that the study of pure culture.

Another reason is that i

In this paper, we shall consider some of the mechanisms by which soil microorganisms favorably or unfavorably affect’

*Microbiologists, QRST@4/CNRS, Dakur and CNRA/ISRA, 9 f &Eva 8980 tiambey, Senegal

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GQQ~QFFBG~ ~ ~ ~ ~ ~ ~ n G o 1

'.I 206

plant growth by altering the soil physical or chemical pro- pFrties, or by directly acting upon the plant itself. Since other contributors have covered the interactions between plants and mycorrhizae, or N2 - fixing microorganisms, (Kenya, 1979; Redhead, 1979) we shall only briefly mention the role of those microorganisms, focusing our attention upon other groups whose influence is still not always recognized. Two preliminary remarks relate to the unique conditioqs that prevail in the tropics. First, when soil water content is not limiting tropical temperatures are generally high enough to allow much more vigorous microbial activity than in temperate areas. Second, since the organic materials thar originate from the plant debris are only to a slight extent stored as humic compounds and are readil) decomposed, most microbial life.is located on or around the root system of the plants (rhizosphere).

INFLUENCE OF MICROORGANISMS ON SOIL PROPERTIES

EFFECTS ON SOIL PHYSICAL PROPERTIES

The role of microorganisms in the genesis and maintenance of soil structure has recently been reviewed (Hepper, 1975). Our aim here is to emphasize thc inportance of this process in the rhizosphere. It has been demonstrated that there are more water- stable aggregates in the rhizosphere than in the non-rhizosphere soil (Harris et aZ.,1964). Since the number of polysaccharide- producing microorganisms is characteristically higher in the rhizosphere, it can be assumed that soil stabilization around the root can, at least to some extent, be due to 'the rhizosphere microflora. In tropical soils, where most of the microbial population is Concentrated in the root zone, it would be worth- while to elucidate ehe relative importance of the root itself and that of associated microorganisms in soil structure stabilization. Such investigations should not be restricted to free-living microorganisms, (such as Asotojacter spp., B e i j e r i n e k i a i n d i c a or L i p o m g e e s s t a r k e y i , which are well-

own polysaccharide producers) , b u t should be extended to corrhizae which w e r e reported t o be involved i n sand aggre-

a t i o n and' dune s t a b i l i z â t i o n i n c o l d e r c l imates (Koske et aZ.,

9 7 5 ) . In con t r a s t t o t h i s b e n e f i c i a l a c t i v i t y , microorqanisms can be harmful i n two ways: by decomposing the aggregat ing compounds o r ig ina t ing from p l a n t s o r microorganisms; and by coating' s o i l p a r t i c l e s with water-repel lent f i lms (Bond, 1964;

Bond and Har r i s , 1964). By a l t e r i n g the advancing 'contact angle of water with the p a r t i c l e s such f i l m s d i s t u r b the i n f i l t r a t i o n of. water i n t o the s o i l , inducing a patchy d i s t r i b u t i o n of p l a n t s and a marked loss of product ivi ty . Water repel lency, which was mostl? a t t i b u t e d t o basidiomycete hyphae, i s thought by G r i f f i n (1969) t o be of p o t e n t i a l l y wide importance, e s p e c i a l l y i n s e m i - a r i d condi t ions.

Microorganisms may a l s o a l t e r t he s o i l redox p o t e n t i a l . Thus the growth of aerobic microorganisms, most of which grow a t t he expense of decaying p l an t d e b r i s , may l e a d t o a reduct ion i n t h e p l a n t . Alternat ively, photosynthet ic algae can produce oxygen and r a i s e 'che redox p o t e n t i a l , thus ac t ing d i r e c t l y o r i n d i r e c t l y upon t i e p l a n t .

NITROGEN G A I N S AND LOSSES THROUGH BIOLOGICAL PROCESSES

The process of symbiotic N2 f i x a t i o n has already been reviewee (Keya, 19791 , bu t mention should be made of t he e f f e c t of l i m i t i n g f a c t o r s , an aspect o f t en overlooked. Besides t h e possible inadequacy of na t ive N 2 - f ixing micropopulations and the a t t acks of pathogens, e s p e c i a l l y nematodes (Germani, 1 9 7 9 ) , four major f a c t o r s can l i m i t symbiotic N2 f i x a t i o n i n the t rop ic s : moisture stress (e spec ia l ly i n semi-arid condi t ions) , s o i l a c i d i t y and a s soc ia t ed t o x i c i t y , mineral de f i c i enc ie s and, i n some s i t u a t i o n s , an excess of combined ni t rogen i n the s o i l (Table 1). As long as one l i m i t i n g f a c t o r i s operat ing N2 f i x a t i o n i s low o r n i l and t h e i n p u t of ni t rogen t o the ecosystem neg l ig ib l e o r non-existent. Two examples w i l l i l l u s t r a t e t he unfavourable e f f e c t of l i m i t i n g f a c t o r s . These examples a re r e l a t e d t o peanut and r e s u l t from f i e l d experiments

208

+Table 1. Methods to control the effects of environmental factors limiting symbiotic N2 fixation

Limiting factors

1.

2.

3 .

4 .

5.

Moisture stress

Soil acidity and toxicity

Mineral deficiencies, especially phosphorus deficiency

Soil inorganic nitrogen

Pathogens

Methods of control

- Irrigation - Search for drought- resisting cv. of legumes and drought-resisting E% izo bi wn

infection - Stimulating VA mycorrhizal

- Lizing - Addition of organic matter

- Addition of phosphorus - Stimulating VA mycorrhizal infection

- Split application of nitroger

- Slow-release nitrogen

- Cae of compatible

- Sesrch for legumes with

fertilizers

fertilizers

fertilizers

a lower capacity for nitrate assimilation

- Chemical, biological or

- Crop rotations integrated control

Senegal during the last 3 years. The first is illustrated by Fig. 1, which shows that in the arid conditions prevailing in Central Senegal, N2 fixation (measured by the acetylene assay) is closely related to soil water content. The second example concerns the limiting effect of inorganic nitrogen. Using'the A value method, (Ganry, 19761, found that by increasing the rate of application of nitrogen fertilizer from 15 to 60 kg per ha, N2 fixation by peanut decreased from 52 to 25 kg per ha. In spite of those limitations, some N2 - fixing systems can remain active. For example, Casuarina e q u i - s e t i f o Z . i a , a non-leguminous nodule-bearing tree, largely used for reforesting sandy soils on the coast of West Africa, was reported to fix as much as 60 kg N2ha-1 year-1 on the Cap- Vert peninsula (Dommergues, 1963).

Microorganisms can bring about losses through nitrification and denitrification. The activity of nitrifying bacteria varies considerably according to the soil characteristics and to the nature of the vegetation. These bacteria are typically neu- trophilic but nitrification is not necessarJly restricted to neutral soils, but to the neutral micro-habitats. Since such habitats may occur ( e . g . in the vicinity of organic debris) in soils whose overall pH is acid, nitrification can be very active in such soils. Thus acid tropical soils grown with banana, maize, or rain-fed rice exhibit a high nitrifying activity when ammonium fertilizer is applied. (Dommergues e t aZ., 1978: Chabalier, 1978). In forest soils, nitrification may be hindered by antibacterial substances released by the litter: when the forest is cleared, a flush of nitrification usually occurs (Dommergues, 1954). There is increasing agreement that nitrification is a detrimental process since it ip respon'sible for two types of nitrogen loss: through leaching, since nitrate is of an anionic nature, and through denitrification (Focht and Verstraete, 1977). are seldom lcwer than 20-30 per cent of the nitrogen applied as fertilizer. The increased cost and shortage of fertilizer nitrogen, especially in the tropics, must prompt soil microbiologists to gather more information on factors that could

Such losses are highly variable, but they

100

90

- 5 80 a !c

C m - - 70

* I o N 60

u) m - O 50 E

E .- : 40

v

a 30 K Q

20

10.

O

I n

I

- 10 - 9

- 8

- 7 h

-I - O

- 6 Cn

z - 5 !5

ù

I I I 20 40 60 80 100

DAYS AFTER SOWING

Fig. 1: Variations of acetylene reducing a e t i v l t y ASA pez plant) of field-grown peanut and of s o l water cszcent throughout the peanut growth cycle as observed in 197: at the Bambey Experimental Station, Central Senegal (Durezï, 1978)

211

I '

it nitrification in soils, since this process is presumably

the fie'ld o f methodology (especially direct detection of cteria in the soil by the fluorescent-antibody techniques) omise to be most helpful (Schmidt, 19781.

easily controlled than denitrification. Recent advances I

AVAILABILITY OF NUTRIENTS In tropical soils ammonification is usually very active,

so that the potential for the release of ammonium from soil organic nitrogen is high. Unfortunately, the organic nitrogen inputs (through N2 fixation, root and litter deposition) into the spi1 are often limited, so that ammonium release is not high enough to meet the plant's requirements. It is not clear whether nitrate, which is the end product of nitrification, is more available to plants than the ammonium ion..

Microorganisms, especially those thriving in the rhizosphere, are often thought to be able to increase the phosphate avai-

' lable to plants by dissolving water-insoluble mineral phosphate, or by mineralizing phosphate from soil organic matter. As far as mycorrhizae are concerned, their role as solubilizing agents has not yet been demonstrated. Other soil microorganisms'might be involved. I n v i t r o experiments- have clearly shown that many common microorganisms, including Pseudomonas, Achromoba-zer, PZavobacterium, S t r e p t o m y c e s , and especially A s p e r g i i l k s and A r t h r o b a c t e r can solubilize soil phosphorus (Hayman, 1975; Barber, 1978)'. However some authors argue that the increased uptake of phosphate may not only result from an increase in the availability of phosphate, but could also be explained by the effect on plant growth of stimulating substances synthesized by the micro-organisms. With regard to organic phosphate, it is readily mineralized by plant phosphates of the root surface. The soil microflora do

P

not seem to increase this process significantly.

Miçrob{ally-inducsd changes of available trace elements have recently been discussed; (Bawber, 1978).

.4 of microorganisms, as well as plants, synthesize some hydrooxamic Since a variety

acids known to be powerful chelating agents, it is not surprising that so51 microorganisms play a prominent role in the iron metabolism of plants (Waid, 1975). A classical example of the decreased availability of trace elements is that of manganese. Manganese deficiency of oats was shown to occur when the activity of manganese-oxidizing microorganisìzs was too high. Soil fumigation reduced the population of these microorganisms and eliminated the manganese deficiency symptoms (Timonin, 1946).

SOIL TOXICITY

Phytotoxic compounds that may accumulate in the soils are of microbial or plant origin. A classical example of phytotoxicity induced by microorganisms is that of hydrogen sulphide produced by sulphate-reducing bacteria. The growth and activity of these bacteria is triggered in the rhizosphere when the following environmental conditions exist concurrently: active root exudation, soil sulphate contenz of the rhizospheric soil above a minimum threshold, and stricz anaerobiosis. Accumulation of hydrogen sulphide can be high enough to lead to the death of plants (Dommergues e t aZ., 1976; Jacc and Roger 1978). Manganese toxicity which occurs in acid soils t h a t are relatively rich in manganese may be reinforced by rhizosphere microorganisms capable of reducing manganic sourceç. Partial sterilization of such soils may prevent toxicity (Barber, 1978).

Phytotoxic compounds of plant or:gin are responsible €or diminishing plant growth when thev a r e not decomposed. Many examples of such toxic effects have Seen described bv Rice (1974) . Recently, investigations carried out at the Agronomic Research Center of Bambey in Central Senegal showed that sorghum rbots contained phytotoxic compounds vhich, in some circumstances, could significantly reduce the yield of subsequent crops, especiñily sorghum. When sorghum is grown once in a two-course rotation (peanut-sorghum) instead of once in a four-course rotation (green manure-peanut-sorghum-peanut) yields are severely depressed.

213

ffect (known as “soil sickness“) is induced e accumulation in the soil of a phytotoxic compound after irst crop. itory to sorghum, remains in the soil as long as environmental

The phytotoxic compound, which is specifically

rtions prevent its biodegradation by soil microorganisms. Since such unfavorable conditions may prevail in sandy soils for seven to eight months, the phytotoxic compounds are still present when sorghum is re-sown too soon after its last cropping. It should be pointed out that while “soil sickness” does occur in sandy soils containing kaolinite-type clays and showing a poor microbial activity, no symptoms are noted in Vertisols, which contain montmorillonite-type clays and where microorganisms are significantly more active. In Vertisols, the sorghum microflora comprising strains that can actively decompose the phytotoxic compound (Domergues, 1978b).

Another example of phytotoxicity of importance in forestsy is related to the failurs of GreviZZea robus ta regeneration in Australia. Seedlings of this species were reported to be killed by some water-transferable factor associated with the roots of parent trees. The resjlting regulation of population in G .

r o t u s t a is thought to explain the maintenance of floristic diversity in complex tropical rain forests (Webb e t O Z . , 1967) .)

c I - DIRECT EFFECTS ON THE PLANT

As the root grows through soil, it encounters diverse com- ponents of the soil microflora and it is directly affected by the activity of soil microorganisms. Rhizoplane and rhizosphere populations affect the host plant in many ways, but there is‘now increasing evidence that the most important effects of microorganisms on plant growth ccncern the modification of plant nutrition and water uptake, the production of growth-regulating substances and the protection of roots against pathogens.

!4ClDIFICATION OF PLANT NDTRITION AND WATER UPTAKE BY MYCORRHIZAE

The best example of the role of microorganisms as regulating agents of plant nutrition is illustrated by mycorrhizal asso-

ciations., The plan main response to mycorrhizal infection is an increased uptake nutr2ent$, especially phosphorus, Mineral nutrition of plants as stimulated by ectomycorrhizae has been, well treated by Bowen (1973) and the effects of vesicular- - arbuscular mycorrhizae (VAM) have been reviewed by Tinker (1975) Redh.ead (1979) and others.

..7

Many theories have already been proposed to explain the increased uptake of phosphorus by ectomycorrhizal roots (Bowen, 1973). Some of them could apply to VX4 since Gerdemann (1968) considers that the function of VAM may also be very similar to that of the ectomycorrhizae.

It includes the formation of more efficient nutrient-absorbing structures than non-mycorrhizal'roots, The extensive strands of extramatrical hyphae in VAM may also explore a much greater volume of so i l than non-infected roots, as do hyphae of ectomycorrhizal fungi. The possibility of a longer active absorbing life for mycorrhizal as compared with non-mycorrhizal roots, as stated by

. Bowen and Theodorou (Bowen, 1973) for ectotrophic mycorrhizae, - should also apply to VAM (Gerdemann, 1968), although actual

evidence is still lacking. Another interesting facet of the biology of mycorrhizae is related to the behaviour of infected roots under low water regimes in the soil. Tropical soils are quite different from one another in water content because there is a wide range of soil textures and climates in the tropics.

In sandy soils, especially in semi-arid regions, plants are often subjected to a relatively long period of water stress. A

most interesting question is whether soil water supplies could be improved by mycorrhizae. by mycorrhizae has hardly been studied but some investigations have indicated a greater drought resistance in a number of mycorrhizal seedlings (Bowen, 1973).

The physiology of water absorption

In 1971, Safir et aZ. indicated that 'WU4 could probably decrease the resistance to water transport in soybean. But later (Safir e t aZ., 1972) they concluded thatbincreased plant growth in water-stressed conditions was due to the improvement of phosphorus nutrition. Recently, however, Menge et aZ. (1978) have reported that mycorrhizal infection enabled avocado plants to resist transplant shock, suggesting that mycorrhizae could

rove water uptake by the*hostTplant. I Drought resistance

soil by extensive hyphal growth, but also to large ferences between infected and non-infected roots in their

corrh.iza1 plants may be related to the greatex exploitation

biology. As stated Gy Cromer (in Bowen, 1973), mycorrhizal oots of Pinus r a d i a t a seemed to renew growth more quickly han non-infected roots when they are subjected to severe water stress. ships between soil-water regime and mycorrhizal infection is

Another interesting hypothesis on the relation-

iven by Sieverding (in Moawad, 1978) who found that the amount f water used to produce lg of dry matter was much lower in

mycor,rhizal than in non-mycorrhizal plants growing in dry soil fertilized with Ca5 (PO4) 30H (Table 2) . According to Moawad, Sieverding's findings may simply be due to the better utilization of water by plants growing in phosphorus-deficient soils. If we wish to explain the greater drought resistance of plants, the theory of water consumption economy as stated above seems to be more plausible and more attractive than the -principle of increased uptake or transport of water in plants (Safir e t a l . , 1971).

MYCORRHIZAE UNDER TROPICAL CONDITIONS

r The impact of mycorrhizal symbiosis in the growth of tropical plants has been recently discussed by Bogen (1978) and Black (1978). Black noticed that the number of tropical plants associated with ectomycorrhizae appears to be very limited as compared to the wide range of ectomycorrhizal plants in the temperate region. The only crop recordedwith ectomycorrhizae is Pinus (Redhead, 1978). Inventories and other information concerning ectomycorrhizal forest trees are given in Alwis and Abeynayake (1978).

As for endomycorrhizae, although same families such as Casuarinaceae, Chenopodiaceae, U r t i c a c e a e are devoid of VAM (Khan, 1974), most tropical plant species of economic importance are infected: cocoa, tobacco, cotton, corn, sweet potato, peanut, sugar cane, sorghum, rubber, tea, citrus and many species of timber trees (Redhead, 1971). Spores of VAM

levels of soil water content (80 and 20% available water) and with two forms of p (after PlOawad, 1978).

Ca ( I I2PO4)2 H 2 0 Ca5 (Po41 3 OH Plant BPUCiÇ?l?

My cor r hi z al.

t rc a t m e n t 8 0 % 20% 80% 20% - -

NM 1208 1207 2860 4112 M 1237 1177 1574 1436

E . odo79atum

NM 1073 1.005 2563 3397 '7'. P > ' , , * 1 c 1

M 923 1 0 6 0 118 O 1424

NM: Not inoculated with VA mycorrhiza

'

217 \

widely distributed in Niger from the moiPt low- d forest to the regions (Redhead, 77). ?i few oliv

e significance of mycorrhizal symbiosis in the cultivation olives in Pakistan has been discussed by Khan and Saif (1973).

In different soils olc..the arid and semi-arid regions, it is robable that mycorrhizal associations play an important part n the growth and drought-resistance of a number of plants ecause of their ability to regulate uptake of nutrients and oil water. Unfortunately, little is known about the' mycorrhizal

of mycorrhizal effects in these regions of the world would be of great practical interest, particularly in the case of afforestation with plant species that usually are transplanted. In our laboratory, observations of the roots of Azadirachta indica, a tree whose growth is wide-spread in dry sandy soils in Senegal, indicate that most roots, if not all, are infected with VAM (Fig. 2 ) . It is significant to note that Azadirachta indica is able to grow vigorously in non-fertilized soils and in arid conditions.

EFFECT OF VAM INFECTION ON LEGUME-RHIZOBIUM SYMBIOSIS - According to a number of papers VAM also occur in many tropical legumes of ecanomic importance e.g. peanuts, cow-pea, MacroptiZium atropurpurzum, StyZasanthes spp. (Possingham et al., 1971;. Sanni, 1976: Graw and Rehm, 1977). As legumes. have been shown to require high levels of phosphate for nodulation, it is likely that mycorrhizal infection may affect the

s (Crush, 1974: Islam et aZ.,1976; Mosse et al., 1976; and Daft, 1977). Recently, in an excellent essay on the f mycorrhizae in legume nutrition on marginal soils, Mosse

pply of rock phosphate stimulated growth and nodulation of ny legumes. Although the principal cause of this is undoubtly

Fig. 2: A z a d i r a c h t a i n d i c a roots infected with VA mycorrhizae

INDUCED PROTEOID ROOTS ,

stimulates the phosphorus-nutrition of host plants. Despite

absorb soil phosphate has been attributed to-the formation of clusters of rootletk in localized parts of the lupin root system. These clusters of rootlets resemble the den clusters known as proteoid roots which have been described in the family of Proteaceae by Purnell (in Trinick, 1977). Other proteoid roots have also been recorded by Lamont on V i m i n a r i a

' jzincea and by Malajczuk on Kennedia (Trinick, 1977). It has now been shown that proteoid roots play an important role in thephosphorusnutrition of plants due to their increased absorbing ability as compared with normal roots (Jeffrey, 1967;

- Malajczuk and Bowen, 1974). Aicording to published literature, very few plant species

* form 'proteoid roots. In Senegal, one of the authors (H.G.D.) observed that rootlet clusters similar to proteoid roots can be found in Casuarina eqki3ezifoZia usually growing in sandy and deficient soils. In the cluster, lateral rootlets are so numerous that they resemble fingers (Fig. 3 ) . Proteoid roots could therefore provide C. equisetifoZia with an alternative

, system- to mycorrhizae for increasinq P uptake from deficient ns are now in progress in our laboratory to cts of these root formations on the physiology lthough the mechanisms o f the initiation re not clear, some tion experiments oid roots may be in

e root surface (MaLajczuk

;il I 1 220

r

i

Fig. 3 : C l u s t e r of rootlets (pro teo id roots! of C a s x i 1 *orfa growing i n a sandy soll ( S e n e g a l )

. As microbial d a c t i v i t y are m nse i n t h e

roo t .growth: for example r o o t s of tomato, subterranean c love r

ovisa and McDouqall, 1 9 6 7 ) . However, p a r t i c u l a r a t t e n t i o n has een paid t o the b e n e f i c i a l e f f e c t exer ted by rhizosphere in- a b i t a n t s . Typical rhizosphere b a c t e r i a such as A r t h r o b a e t e r , seudoponas and Azrobacterium w e r e found long ago t o be ab le t o roduce substances promoting p l a n t growth (Krasi lnikov, 1958) .

Ectomycorrhizal fungi also provide t h e h o s t p l a n t with phytohormones and growth-regulating B vitamins (S lank i s , 1973) . Detailed discussion about t h e d i r e c t e f f e c t s of b a c t e r i a on r o o t

rowth through the production of p l a n t growth-regulating f a c t o r s an be found i n many reviews (Xrasi lnikov, 1958; Katnelson, 1965;

~ Brown, 1975). The inf luence of ectonycorrhizal hormones on the development of roo t s of the hos t p l a n t has a l s o been amply demonstrated i n S l a n k i s , ( l 9 7 3 ) . However, i n s t ances of increased. p l a n t growth r e s u l t i n g from i n t e r a c t i o n s between s o i l microorganisms and p l a n t s show t h a t when p l a n t s a r e a r t i f i c i a l l y inoculated with a p a r t i c u l a r microorganism known f o r a determined b i o l o a i c a l a c t i v i t y (e.g. N2 f i x a t i o n ; phosphorus s o l u b i l i z a t i o n ) , s t i k i l l a t ion of p l an t growth o f t en was p u t a t i v e l y a t t r i b u t e d t o the e f f e c t of t h i s s p e c i f i c a c t i v i t y , although i t may simply be due t o t h e production of phytohormones by the same microorganism. Three examples found i n d i f f e r e n t f i e l d s r e i n f o r c e t h i s p o i n t of

view: (1) Thir ty years ago, Gerretsen (1948) thought t h a t t he increased growth of p l a n t s i n s t e r i l i z e d sand containing i n s o l u b l e

. ,. , .

7

y i e l d s have o f t en been recorded after inocul

s m a l l mounts of h ighly ~ a c t i v e growth-promoti

Azospim'Zlum b r a s i Z i e n s e , a f a l s o induce increased plant g Table 3 s h w s t h a t growth of t h e a e r i a l p a r t s of rice were i v e l y s t imula ted by inocu la t ion w i t h a non-N~-fixing bacteri th A. b r a s f l i e n s e , and that roo t growth was even more ac t imul&ed. Moreover, s ince inocula t ion w i t h ~ z ~ s p i r i ZZum genera l ly does n o t s i g n i f i c a n t l y improve Na f i x a t i o n , Gaskins and Hube11 (1978) and Tien e t a l . (1979) suggested t h a t the e f f e c t of A z o s p i r i Z t u m inocula t ion on p l a n t growth could be due t o grmth-s t imula t ing substances produced by t h i s bacterium, as i n t h e case of A z o t o b a c t e r . ( 3 )

I n some experiments of b i o l o g i c a l control , roo t disease of wheat assoc ia ted w i t h R h i z o c t o n i a s o l u n i was reduced and grain y i e l d increased by seed inocu la t ion with b a c t e r i a and actinomycetes. Merriman e t al.. (1974) suggested t h a t t he y i e l d inc reases are pr imar i ly due t o p l a r t growth-stimulating f ac to r s r a t h e r th? t o t h e b io log ica l con t ro l of root disease.

, the b a c t e r i a (Brown, 1975). SimLlarly, inocula t ion with ving NZ-fixing bacterium, can

IMPROVEMENT OF PLANT RESISTANCE TO INFECTION

Discussion w i l l be r e s t r i c t e d t o the con t ro l of pathogens through the improvement of p l a n t r e s i s t ance by symbiotic microorganisms o r microorganisms more o r less loosely assoc ia ted with the r o o t s l which i s only one aspect of t he v a s t problem of b io log ica l control . i n t h e type of con t ro l s tud ied here.

Two types of mcchaqisms may be involved

In h i s review, Marx (1975) ind ica t ed t h a t if pine roo t s w e r e assoc ia ted with Laucopaxi 1 Z m c e r e a l i s var. p i c e i n a t o f c r m ectomycorrhizae, they became r e s i s t a n t to i n fec t ions caused by such pathogenic fungi as P h y t o p k t h o r a cinnamomi. Many mchanisms could be involved t o expla in t h e p ro tec t ive r o l e of ectomycorrhizal pine roots . Apart from the explanation t h a t a n t i b i o t i c production i n h i b i t s fungal pathog-rns (Marx, 1975) , t h e fungal mantle of ectomycorrhizae a l s o creates e f f e c t i v e

224 7 '

m c h a n i c a l b a r r i e r s a g a i n g t pene t r a t ion by P. c<nnamomi. There w a s f u r t h e r evidence t h a t funga l m a n t l e s formed by non-ant ibiot ic- producing ectomycorrhizal fungi a l s o p ro tec t ed roo t s f r a pathogenic r o o t i n f e c t i o n s . mycorrhizae may provide p l a n t p ro tec t ion (Milhelm, 1973) - I n t h i s case, t he re i s no phys ica l b a r r i e r , b u t e a r l y t e r r i t o r i a l occupation of Living r o o t t i s s u e s by the endophyte may promote b i o l o g i c a l control .

It i s a l s o suggested t h a t endophytic

I n the presence of saprophyt ic microf lora many p l a n t s produce a mult i tude of compounds, e spec ia l ly the so-called phytoalexins, which can p l ay a r o l e i n roo t disease re s i s t ance . Most have been i d e n t i f i e d i n a e r i a l p l a n t p a r t s , bu t it is l i k e l y t h a t t he same compounds can also be f o m d in t he roo t system (Paxton, 1 9 7 5 ) . For i n s t ance , p i s a t i n , the well-known phytoalexin of the pea p l a n t , occurs i n the roo t s as w e l l a s i n most o the r p a r t s of t h e p l a n t and has a wide spectrum of a n t i b i o t i c a c t i v i t y . a l ex ins i n response t o P h y t o p h t h o r a f r a g a r i a e i n f e c t i o n s (Mussell and Stap le s , 1 9 7 1 ) .

Strawberry r o o t s a l s o produce phyto-

MANIPULATING THE S O I L MICROFLORA

Since the major p a r t of t h e s o i l popu la t i a i i n t r o p i c a l condi t ions i s made up of the rhizosphere microflora, and s i n c e the rhizosphere microf lora must, be viewed as a component of t he whole soil-plant-atmosphere system [Dmergues , 1978a) , t h e soil microflora could p red ic t ab ly be manipulated,' n o t only d i r e c t l y by ac t ing upon t h e microorganisms, bu t a l s o i n d i r e c t l y by ac t ing upon t h e so i l and the p l an t . Direct manipulation of t h e s o i l mic ro f lo ra can be achieved by inocu- l a t i o n p r a c t i c e s , s t e r i l i z a t i o n and the appl icat ion of s p e c i f i c i n h i b i t o r s or s p e c i f i c substrates. I n d i r e c t manipu- l a t i o n of t h e soil-plant-atmosphere system can be achieved by c l a s s i c a l or non-conventional s o i l management p r a c t i c e s , o r by a c t i n g upon t h e p l a n t component itself.

, . In spite of the fact that root colonization by non-path

icroorganisms is still poorly unaerstood , soil microbiologis d agronomists have been trying for many years to alter the osphere microflora by introducing selected microbial strains, er by coating seeds with an inoculum, or by placing the

inoculum into the soil close to the seed or the seedling.

The value of legume inoculation is well recognized, provided I l that the strain used is highly effective and efficient in its

symbiosis with the selected legume cultivar, that it is a good colonizer of the roots and is able to compete with any ,iative root microorqanism, and that the proper environmental prerequisites are fulfilled. However, legume inoculation by classical methods is not always fully satisfactory.

The value of ectomycorrhizal inoculation is also generally acknowledged as long as the proper environmental conditions are met (e.g. Hacskaylo, 1 9 7 2 ; fiarx and Krupa, 1 9 7 8 ) . Inoculation by endomycorrhizae is currer.cly at the experimental stage excepr. in special situations. Preliminary reports suggest that larger responses are more likely in Lropical regions than in temperate - regions, because of higher temperatures and the naturally low- phosphcrrus level of soils (Iiayman, 1 9 7 8 ) .

- Recent experiments carried out in the northern coastal area of Senegal have shown that inoculating .'asuar-ina s ;viser l '?Zi , with crüshed nodules improved that plant's growth markedly (Dubrekrl and Andeque, personal communication). Further investigation OT. the endophyte of i7u T Y . . ~ ~ : is needed in order to improve the currenr method of inoculation, which is obviously hazardous s x z s crushed nodules used as inoculum may carry pathogens.

Although techniques noculation with typically symbioz;z microorganisms (e.g. Rhicc - 1 are already Ln use in the field, or could be used in the near future (e.g. endomycorrhizaef, - techniques of inoculation with loosely symbiotic or non-symbiotic microorganisms (e.g. rhizosphere N2 fixers oz phosphate-solubilizing bacteria) cannot yet be safely recommended.

I ' ,'

-.. The first attempts at using Npfixing rhizosphere bacteria to inoculate grasses or cereals were made (Rubenchick, 1963). Since tha't' date many performed, at first with Azotobacber or B e i j e r i n c k i a ahd later with AzospiriZZum (e.g. Smith e t al., 1976: Dobereiner, 1977). Yield increases have sometimes been reported but up to now results have generally been inconsistent.

c

Fïeld experiments with phosphate-solubilizing bacteria (especially BaciZZus megather ium) have not shown any consistent effect on plant yield. According to Barber (19?8), * this lack of response is not really surprising for two reasons. since a considerable proportion o f soil phosphorus is present in organic compounds and up to 90%' of the rhizosphere microflora axe capable of producing phosphatases, the introduction of other organisms, which would have to compete for available carbon sources, is unlikely to cause any increase in the supply of phosphate to plants. secondly, the inoculum used, BaciZZus megatherium v a r phosphaticum is a spore-forming bacterium and such organisms grow far less readily in the rhizosphere than do other types of bacteria".

Firstly,

When stimulation of plant growth consecutive to inoculation by N2 fixers or phosphate-solubilizing bacteria has been observed, it could not be explained by N2 fixation, nor by an increase of phosphate solubilization. has resulted, at least in part, from the effecc of growth substances produced by the microorganisms added w i t h inoculum, as

already mentioned above. In spite of some recent improvements in the preparation of the inoculum itself (Doumel'gues e t al., 1979) or in the introduction of mixed cultures (Domergues et aZ . , 1978), there would seem to be no easy solution to the difficulties that arise when attempting to inoculate non-sterile soils.

The stimulation of plant growth probably

Soil sickness can result from the presence of plant residues in the soil, especially root litter contáining phytotoxic substances. actively decompose the root litter appears to be a promising approach to curing these soils. Thus inoculating a Eerrallitic sandy soil that contained phytotoxic root debris with E n t e r o b a c t e r

Inoculating such soils with microorganisms that

I

227

aeae restored soil fertility (l'able 4 ) . Phytotoxic sub- nces, pxe-existing in plant residues or formed during decom-

position, can possess a broad spectrum of effects that are jurious to the roots and stems of plants (Toussoun &-ad Patrick, 6 3 ) . il inoculation with proper microbial strains.

Such a deleterious effect could probably be seduced by

SOIL STERILIZATION AND APPLICATTON OF SPECIFIC COMPOUXDS

In sterilization by heating, irradiation and drying is sed in certain circumstances, sterilization is often achieved y fumigation with such chemicals as chloroform, carbon-sulfide methylbromide or chloro-picrin. Such treatments often improve plant growth even in the absence of pathogens (Wilhelm, 1966; Rovira, 1976). This beneficial effect can be attribured to different causes: chemical modifications, especially increase of NH4 zontent, flush of organic matter decQmposition, including

d microorganisms (Anderson and Domsch, 1978), elimination of nitrifying bacteria, which are particularly vulnerablt to fumigation (Jenkinson and Powlson, 1976), and re-colonizeiron of soil by rion-pathogenic microorganisms, especially pseudomcnads, which are thought to stimulate plant growth (Ridge, 1976).

Soil sterilization prior to inoculation wich rr.y-orrhizae u appears to be most helptul in special sltuations (Lai ib and

Richards, 1978). Among these are fumigated nursery s o l l s where severe stunting of citrus was reported: inoculation with vesicular-arbuscular-mycorrhizae appeared to be the kest method to overcome this stunting (Lamb and Richards, 1978; TFmmer and Leyden, 1978; Hayman, 1978).

Among the different specific inhibitors that have been studied [e.g. Anderson and Domsch, 1975), nitrification inhibitors have received much attention because of their possible use in the field. Besides the agronomic practices mentioned above, inhibitors such as 2-chloro-6- (trichloromethy1)-pyridine have been successfully used to inhibit nitrification, thus increasing the efficiency of nitrogen fertilizers by reducing de-nitrification ana leaching f the nitrate ion. Unfortunately, especially in tropical conditions, he inhibitor is readily decomposed by the soil microflora so

NO inoculatirn W i t h inoculatia (ccntrol)

B o t s

65 60

3.9 2.7

48.7 14.7

8.2 1.3

.

stitutes have been proposed, such as neem cake (made of the eds of A z a d i r a c h t a indica), but this material is not as effective 2-chloro-6 (trichloromethy1)-pyridine (Prasad and de Datta,

The stimulation of a given component of the microflora can e achieved by adding a specific substrate to the soil. A lassical example is that of the selective multiplication of

decomposing microflora (Alexander, 1961).

Another example is that of the solubilization of rock- phosphate by T h i o b a c i Z Z i . These chemoautotrophic bacteria are introduced into the soil together with sulphur which is oxidized to sulphuric acid, thus dissolving the phosphate (Swaby, 1975).

FERTILIZATION AND SOIL MANAGEMENT

. . Inoculation even with specific microorganisms, especially n R h i z o b i u m , is unsuccessful when one of the limiting environmental

factors listed in Table 1 is still operating. Therefore, improvement of environmental conditions is a pre-requisite that can be achieved by different soil management practices, such as irrigation, liming, application of organic amendments or slow-release fertilizers. The beneficial effect of liming is illustrated by Table 5 (Expt. 1) which reports on a study of soybean nodulation in a ferrallitic acid soil from Casamance, Senegal. The increased nodulation was attributed to the elimination of Mn and Al toxicity of liming. Table 5 (Expt. 2), shows that the application of organic matter even at low rates (400 kg of peat per ha) favourably affected the growth and nodulation of soybean. This last result confirms those obtained by Dart e t a l . , 1973 with V i g n a mungo and V . r a d i a t a . Neither species grew well in a nitrogen-free sand- rit mixture. rowth and nodulation. t 45OoC for 4 h to remove soil organic matter, plant growth was

But adding 10% of Kettering loam by volume improved When added loam had been previously ignited

E q t . 1

C a l t r o l 4.0 a 14 a 4 2 a 3.38 a

co3 (2500 kg per ha) 7.0 b 39 b U 2 b 3178 a

E x p t . 2

4.0 a 28 a 44 a ' 2.16 a C c n t r o l

Fe a t

(400 kg p r ha) 4.0 a 41 b 88 b 3.03 b

Qle p l a n t per pot cmtaining 5 kg of soi l fran Sefa &sear& Statim,

Senegal. A l 1 plants we= inoculated w i t h 1 ml of a 3-day old culture of f i i z o b i m . jap"mm asp (10 bacteria per ml) . Observatims were made wfen plants VÆE 6 weeks old.

colunns not hrming the smre letter are statistically difkrent

a

In e¿& experirrent, n u n h r s in

(P = .05).

and the plants eventually died.

A combination of liming, ploughing and the application of farm-yard manure was reportea significantly to increase peanut yields in Cent91 Senegal, probably through increasing N2 fixation (Wey and Obaton, 1978).

Since N2 fixation is not always active enough to meet the

To gume's requirements, it is necessary to use nitrogen fertilizers. t it is known that such applications inhibit N2 fixation.

prevent this inhibition in legumes, Hardy e t al. (1973) suggested the use of other form of nitrogen fertilizers that do not inhibit N2 fixation, while providing the plants with the complementary nitrogen required for their growth. Such new forms of chemical fertilizers, which they designated as compatible fertilizers, could also be recommended for use. The possibility, though promising, has not yet been seriously explored.

Nitrification can be controlled by such classical methods as split application of ammonium fertilizers, localization in mud balls (International Rice Research Institute, 1978), or banding, which inhibits nitrification due to the effect of the high -

' concentration of fertilizer on nitrifying bacteria (Wetselaar e t a l . , 1972; Myers, 1978). The use of slow-release fertilizers is

+ also recommended to avoid the harmful effects of nitrification (Fochts and Verstraete , 1977) .

MANIPULATION OF THE PLANT COMPONENT OF THE SOIL-PLANT-MICRO- ORGANISMS SYSTEM

Introducing a specific crop in the rotation system has been used successfully as a basis for the biological control of some pests. Thus in Florida, soils infested by nematodes pathogenic to tomato, are cured by growing a grass, D i g i t a r i a decumbens, after the tomato crop (Salette, personal communication). Crop rotation is often the best method of controlling soil- borne phytopathogenic fungi in cereals (see Baker and Cook, 1974). he possibility of increasing populations of microorganisms eneficial to plants through proper crop rotation was suggested y Krasilnikov (19.58) but the method has not yet been exploited.

w i l l probably be d i f f i c u l t t o i n i t i a t e and develop because of the l a rge v a r i a b i l i t y of climate and so i l conditions.

Genetic v a r i a b i l i t y i n p l a n t s responding t o lhhizobhium i n f e c t i o n is w e l l known. This v a r i a b i l i t y could be used as a b a s i s f o r t h e breeding programmes of legumes. The f u t u r e of t h i s approach w a s envisi0ne.d as follows by Hol1 and La Rue (1974). "Plant genes c o n t r o l l i n g f i x a t i o n do occur, and experience shows t h a t w e can obtain informative and use fu l v a r i a n t s . There i s no obvious, reason why symbiot ic f i x a t i o n cannot be increased by g e n e t i c means. W e can envisage c u l t i v a r s which nodulate e a r l y i n harsh s o i l condi t ions, f i x dini t rogen, even i n the presence of high s o i l n i t r a t e levels, and continue f i e n g throughout t h e i r l i fe . It appears t h a t f i x a t i o n may be l imited by the supply of photosynthate t o t h e r o o t s . Increased f ixa t ion may then require g r e a t e r photosynthesis , decreased photorespirat ion , delayed lodging, o r less pod-nodule competition f o r carbon".

Two examples may se rve as an i l l u s t r a t i o n f o r such a promising approach, which has no t y e t been se r ious ly exp lo i t ed . The first concerns t h e nodulation of peanut. Comparing the t i m e course of nodule dry weight of three peanut c u l t i v a r s grown i n 1977 a t the same t i m e i n i d e n t i c a l conditions (Dior s o i l , Central Senegal) , Germani (1979) found t h a t the maxiinum nodule weight of two of them was much h ighe r th^ t h a t of the t h i r d (F ig . 4 ) .

However, such r e s u l t s should be in t e rp re t ed with caut ion s ince d i f f e rences i n nodule weight a r e also observed from one y e a r t o another. Thus the m a x i m u m nodule weight of cv. 55-437, which was only 70 mg i n 1977, could reach 100 mg i n the same s o i l during more humid yea r s (1973 and 1975) and even more than 200 mg

during an even more humid yea r ( 1 9 7 4 ) (Wey and Obaton, 1978).

The o t h e r example i s r e l a t e d t o soybeaq. I n West African soils, c e r t a i n soybean c u l t i v a r s , such as Malayan, are read i ly nodulated by n a t i v e BaR2izobium of the cow-pea group, whereas other c u l t i v a r s , such as Bossier, a high y i e l a i n g cv. from the USA, r equ i r e i n o c u l a t i o n with the s p e c i f i c lhR2izobium japonieum '%trains . S e l e c t i o n of high-yielding soybean t h a t couldnodulate with n a t i v e %izobitri.: of the cow-pea group would

. .

n F i

I & 300

5

- 2 0 0

a c3 z

c I c3

w 3 w

I

100

Fig . 4 .

O 20 4 0 60 80 100 1 2 0

AGE OF THE PLANT (DAYS)

T i m e course of nodule dry weight of peanu t expressed

as mg p e r p l a n t . A : cv . 28-206 and GH 1 1 9 - 2 0 ;

B : cv. 55-437. A l l d a t a are mean va lues f o r c o l l e c t i o n s i n 1 9 7 7 a t P a t a r , C e n t r a l Senegal (Germani, 1 9 7 9 ) -

CONCLUS IONS

This paper has summarized the numerous ways in which soil microorganisms can affect the fertility of soil and it has noted, with examples, how in some cases they can be manipulated in order to benefit the growth of plants. Up to now practically all work done has been with agricultural, horticultural or forestry land- use systems. There is clearly a very urgent need now to relate specific areas of soil microbiological research to agroforestry systems in which woody and herbaceous plants will be grown either mixed together or in some sequential manner.

The many possible ways in which the activities of soil microorganisms in the soil-plant association of one of these groups of plants can affect the other is an almost untouched field of research. In particular, the effects on microorganisms of soil management, innoculation and nitrogen fixation and transformation, and the consequent influence on soil fertility in agroforestry systems might be given early attention.

D I SCUSSI ON

Keya: Nitrification inhibitors are produced in the rmts of many grasses. The neem (Azadirachta indica) plant also produces such an inhibitor, which might have some prospects in agroforestq.

Scinchez: In North Queensland, Australia, they have observed a competitive relationship between EucaZ@us and grass pastilre for li, but not in legume pasture.

Pereira: The reason for all crops doing poorly after sorghum in dry conditions is that the stubble continues to utilize water from the 2-m deep subsoil for many weeks.

bmergues: A reduction in soil water content may also reduce the microbiological activity responsible for decomposing phytotoxic compounds added by sorghum roots.

Ahn: Some grasses are known to inhibit nitrification in West African savanna soils. the first season followed by grain crops.

Thus, yams (Dioscorea spp.) which demand less U, are grown in

235

es: e ra l i zed and it is only progressively decomposecl. p res idues a r e e a s i l y mineralized.

Pwbably N immobilized ir! t he grass r o o t system i s n o t In con t r

Does the phytotoxic e f f e c t of sorghum on a succeeding crop apply t o a succeeding crop of sorghum also?

rgues: Y e s . However, the phytotoxic e f f e c t i s only on s o i l s with low biological a c t i v i t y and w a t e r reserve.

Zsen: Does g ras s exude n i t r i f i c a t i o n inh ib i to r s , thereby reducing growth of Eucalyptus?

ergU0s: Y e s . But t he re is no published reference f o r t h e inh ib i t i on of Eußalyptus growth.

t: Citrus and peach produce toxic mater ia ls i n t h e i r roo t s which i n h i b i t the development of new trees. inh ib i to r s t h a t prevent germination u n t i l these water-soluble i n h i b i t o r s sre leached away o r changed chemically.

Some seeds of d e s e r t annuals have growth

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