APOPLASM
A. Physical Factors
V. APPLICATION
Despite the fact that rhizosphere exudation patterns are governed by a large vari- ety of factors (plant, microbial, and soil factors). it is clear that there is ample scope to modify root exudation patterns either by using agricultural practices or through plant breeding programs. Both plant breeding programs and agricultural practices have concentrated on reducing the negative impact of plant pathogens directly. Examples include breeding programs that render plants resistant to pathogen attack, rotation schemes that prevent excessive buildup of pathogens, or application of pesticides that protect susceptible plants against pathogenic or- ganisms. In relation to plant nutrition, plant breeding programs have concentrated on the development of plant varieties that give inherited high yields provided
that sufficient nutrients are available. The latter conditions are satisfied using chemical fertilizers that are directly available to plants. Even though these prac- tices have resulted in a dramatic increase in food production during the past half
century. it is questionable whether these approaches on their own are sustainable in the long term. Resistant plant varieties have limited usefulness, as plant resis- tance will be broken by the pathogen in the absence of measures that reduce pathogen populations. Similarly, excessive use of pesticides will inevitably lead to the development of resistance in the pathogen population. Furthermore, lack of “organic” inputs will lead to a reduction of saprophytic biological activity in soil and, consequently, to a decline in the physical and chemical soil quality.
This, in turn leads to an increasing dependence on chemical inputs i n the form of fertilizers and pesticides.
The realization that increased yield and reduced incidence of plant damage resulting from pathogens can also be achieved indirectly by programs aimed at encouraging beneficial organistns in soil and the rhizosphere opens new possibili- ties for plant breeding and soil management programs. Root exudates released by the plant create a “rhizosphere effect,” resulting in intense microbial activity i n the vicinity of the roots. The influence of this microbial activity on plant health and nutrition depends on the net biological effect of the interactions between the rhizosphere populations, the plant, and the soil environment. With increasing
knowledge of which factors influence this exudation process and their influence on rhizosphere microbial populations, it has become possible to nlanipulate these processes in favor of organisms that benetit the plant directly by providing biolog- ical control activity, growth stimulation. induction of resistance, or by mineraliza- tion of organic residues. Indirectly, the activity of soil (micro)organisms will result in improved soil quality (greater aggregate stability, improved soil struc- ture, and better water-holding capacity), all of which benefit plant growth.
Examples of the successful stimulation of microbial populations antagonis- tic to pathogens such as Take-all, Fusarium wilt, and cereal cyst nematodes- using continuous cropping regimes, green manures, and farmyard tnanures- have been well documented (252-254). However, manipulation of rhizosphere populations using plant-breeding programs is at present not seriously pursued.
The latter approach, when integrated with appropriate soil management strategies, might open new possibilities to release the full potential of microorganisms that benefit plants in a variety of ways.
A further application of the manipulation of microbial activity in the rhizo- sphere is their potential to remediate contaminated land. Bioremediation involves the use of microorganisms that break down contaminants. Radwan et al. (255) found that the soil associated with the roots of plants grown in soil heavily con- taminated with oil in Kuwait was free of oil residues, presumably as a result of the ability of the resident rhizosphere microflora to degrade hydrocarbons. The use of plants as a means to accumulate pollutants such a s heavy metals (256,257) to degrade hydrocarbons and pesticides (255) is already widely implemented and has proven to be successful. In some cases, there is no doubt that it is the plant itself that is responsible for the removal of the contaminants. However, in most
cases, it will be the interactions that take place between plant roots, the soil biota, and the soil environment that result in the desired effect. Again, insight in the interactive processes associated with pollutant degradation will open opportuni- ties to decontaminate land more effectively.
REFERENCES
I . 2.
3.
4.
S.
6.
7.
8.
9.
IO.
1 I . 12.
13.
14.
15.
J. M. Lynch, The rhimsphere-form and function, Applied Soil Ecology /:l93
( 1984).
J. M. Lynch, Soil R i o t ~ c h r ~ o l o g ~ ~ - M i c r ~ ~ l ~ i ~ ~ l o g i c a l Fuctors in Crop Productivity.
Blackwell Scientific Publications, Oxford, 1983, p. 191.
A. D. Rovira, R. C. Foster, and J. K. Martin, Note on terminology, origin, nature and nomenclature of organic materials in the rhizosphere, The Soil-Root Interfuce (J. L. Harley and R. Scott-Russell, eds.), Academic Press, London, 1979, p. 1.
W. Cheng, D. Coleman, C. R. Carroll, and C. A. Hoffman, In situ measurement of root respiration and soluble C concentrations in the rhizosphere, Soil Biology urd Bioclwmistry 25: 1 I89 ( 1993).
N. C. Uren and H. M. Reisenauer, The role of root exudates in nutrient acquisition,
Adwnces in Plant Nutrition (P. B. Tinker and A. Lauchli, eds.), Praeger, New York, 1988, p. 79.
A. D. Rovira, Plant root exudates, Rottrrry Review 35:35 (1969).
A. A. Meharg, A critical review of labelling techniques used to quantify rhizosphere carbon flow, Plant nnd Soil 166355 (1994).
E. 1. Newman, The Rhizosphere: carbon sources and microbial populations, Ecolog- ical Inteructions in Soil (A. H. Fitter, ed.), Blackwell Scientific Publications, OX- ford, 1985. p. 107.
D. A. Barber and J. M. Lynch, Microbial growth in the rhizosphere, Soil Biology and Biochernistry 9:305 (1911).
R. Merckx, J. H. Van Ginkel, J. Sinnaeve, and A. Cremers, Plant induced changes in the rhizosphere of maize and wheat. Plant nrrd Soil 96:85 (1986).
R. C. Foster, Microenvironments of soil microorganisms, Biology and FerriIiQ of
Soils 6: 189 ( 1988).
J. Lussenhop and R. Fogel. Soil invertebrates are concentrated on roots, The Rhizo- splrerc. and Plant Growth (D. L. Keiser and P. B. Cregan, eds.), Kluwer Academic Publishers, Boston, 1991,,p. 1 1 I .
J. M. Whipps, Carbon economy, The Rhicosphrre (J. M. Lynch, ed.) John Wiley, Chichester, 1990, p. 59.
J. Swinnen, Rhizodeposition and turnover of root-derived organic material under conventional and integrated management, Agriculture, EcosystLvns and Environ- J. Swinnen, J. A. Van Vecn, and R. Merckx, Root decay and turnover of rhizodepos- its in field-grown winter wheat and spring barley estimated by IJC pulse labelling, Soil Biology and Biochetnistry 2 7 2 1 1 (1995).
I I l P l l t 5l:l 15 (1994).
16.
17.
18.
19.
20.
21.
22.
23.
24.
2.5.
26.
27.
28.
29.
30.
31.
32.
33.
H. Keith, J. M. Oades, and J. K. Martin. Input of carbon to soil from wheat plants, Soil B i o l o g y c u ~ r l Biodlertlistr:\. l8:4.55 (1986).
B . Jensen, Rhizodeposition by “C pulse labelled spring barley grown in small field plots on sandy loam, Soil Biology t r r d Biochemi.sty 25: 1.553 (1993).
J. M. Lynch and J. M. Whipps, Substrate flow in the rhizosphere, Plur~t t ~Soil d
129: 1 (1990).
D. L. Jones and P. R. Darrah, Re-sorption of organic compounds by roots of ZLW rnrcy.~ L. and its consequences in the rhizosphere: I. Re-sorption of “C labelled glucose, mannose and citric acid, P l m t ctnd Soil 143:259 (1992).
D. L. Jones and P. R. Darrah, Influx and efflux of amino acids from Zen r~1ay.s L.
roots and its implications in the rhizosphere, Plnut t r r l d Soil 163: 1 (1994).
D. L. Jones and P. R. Darrah. Re-sorption of organic compounds by roots of Zea mays L. and its consequences in the rhizosphere: 111. Characteristics of sugar influx and efflux, P larlt nr~d Sei( 178: 1 53 (1 996).
S. J. Grayston, D. Vaughan, and D. Jones, Rhizosphere carbon flow in trees, in comparison with annual plants: the importance of root exudation and its impact on microbial activity and nutrient availability. Applied Soil Ecology 5:29 (1996).
L. S. Brophy and G. H. Heichel, Nitrogen release from root of alfalfa and soybean grown in sand culture, Plrlnt urld Soil 116:77 (1989).
J. P. Wacquant, N. Ouknider, and P. Jacquard, Evidence for a periodic excretlon of nitrogen by roots of grass-legume associations, Plant o r d Soil I16:.57 (1989).
A. D. Rovira. Plant root excretions in relation to the rhizosphere effect: I. The nature of root exudates from wats and peas, Plant m d Soil 7 178 (1956).
A. D. Boulter. J. J. Jeremy, and M. Wilding, Amino acids liberated into the culture medium by pea seedling roots, Plant ancl Soil 24: I2 1 (1966).
M. G. Hale, L. D. Moore, and G. J. Griffin, Root exudates and exudation. I r l -
terwtiorls betn.ecw N o t ~ - P n t l l o g e t ~ i c Soil Microorgtlrlisn~s m t l Pltrr1t.r (Y. R.
Dommergues and S. V. Krupa, eds.), Elsevier, Amsterdam, 1978, p. 163.
H. H. Janzen and Y. Bruinsma, Methodology for the quantification of root and rhizosphere nitrogen dynamics by exposure of shoots to ” N labelled ammonia, Soil Biology cmd Biochertistry 21: I89 ( 1 989).
E. S. Jensen, Rhizodeposition of N by pea and barley and its effect on soil N dynan- ics, Soil Biology urd Biochemistry 28:65 (1996).
A. L. Virtanen. S. Von Hausen, and T. Laine, Investigations on the root nodule bacteria of leguminous plants: XIX. Influence of various factors on the excretion of nitrogenous compounds from nodules, Jourrml
of
Agricultural Scierm> 27332( 1937).
P. W. Wilson and 0. Wyss, Mixed cropping and the excretion of nitrogen by legu- minous plants, Soil Scierlcc. Society of America Proceedjr1,q.s l ]:289 ( 1937).
L. Klemedtsson, P. Berg, M. Clarholm, and J. Schnurer. Microbial transforma- tions in the root environment of barley, Soil Biology (uld Biochemistry 19:55 I ( 1 987).
R. Merckx, A. Dijkstra. A. den Hartog, and J. A. Van Veen, Production of root- derived material and associated microbial growth in soil at different nutrient levels. L
Biology n r d Fertility of Soils 5 : 126 ( 1987).
34.
35.
36.
37.
38.
39.
40.
41.
42.
43.
44.
45.
46.
47.
48.
49.
50.
51.
52.
D. Robinson, B. Griffiths. K. Ritz, and R. Wheatley, Root-induced nitrogen miner- alisation: a theoretical analysis, Plant c m / Soil l I 7 185 ( 1989).
D. B. Nehl. S. J. Allen, and J. F. Brown, Deleterious rhizosphere bacteria: an inte- grating perspective, Applied Soil Ecology 5: 1 ( 1997).
R. W. Hedges and E. Messens. Genetic aspects of rhizosphere interactions, The Rkizospl~ere (J. M. Lynch, ed.), John Wiley, Chichester. 1990, p. 129.
H. J. Bolton. J. K. Fredrickson. and L. F. Elliott, Microbial ecology of the rhizo- sphere, Soil Microhid Ecology (F. B. J. Melting. ed.). Marcel Dekker, New York,
1993. p. 27.
G. D. Bowen and A. D. Rovira. The rhizosphere: The hidden half of the hidden half. Plctr~t Roots, The H i d d e t ~ H d f (Y. Waisel, A. Eshel, and U. Katkafi. eds.), Marcel Dekker, New York, 1991. p. 641.
A. D. Rovira and C. B. Davey. Biology of the rhizosphere, The plcrtlt root c u d its
etIllirotlttrcwt (E. W. Carson, ed.), University Press of West Virginia, Charlottesville, 1974, p. 153.
S. J. Pirt, Pritrciples of Microhc c m ( / Cc4 Cdtiwrtiotl, Blackwell. Oxford ( 1975).
J . R. Postgate, New advances and future potential in biological nitrogen lixation.
J o 1 w t d (f Applied Bnctc~riology 3 7 I85 ( 1974).
J. Dobereiner. J. M. Day, and P. J. Dart. Nitrogenase activity and oxygen sensitivity of the Puspcrlurtl tlottrflotl-~;otohcccler- p u p d i association, Jolrrtltrl of Gcwcwrl Mi- crohiology I 7 l03 ( 1972).
J. J. Patel, Microorganisms in the rhizosphere of plants inoculated with A ; o t o b ~ w r chrooc~occltrll, Pltrtlt c l t l d Soil 31 :209 ( 1969).
D. A. Barber and J. K. Martin, The release of organic substances by cereal roots into the soil, New Phytologist 7669 (1976).
M. J. Brimecombe, F. A. A. M. De Leij, and J. M. Lynch. Effect of genetically modified P.selrtiottlotrct.sprrorc~.scetl.s strains on the uptake of nitrogen by pea from
"N enriched organic residucs, Letters it1 App/iecl Mictnhiology 26: 1 S5 (1998).
M. J. Brimecombe, F. A. A. M. De Leij, and J. M. Lynch. Effect of introduced P.sc.rrrlotrlot,as fhorcscctIs strains on the uptake of nitrogen by wheat from I5N- enriched organic rcsidues, World Jorrnltrl of Mic,rol)iology (rtul B i o t r c h o l o ~ y . v 15:
417 (1999).
W. F. Harris, D. Santantonio. and D. McGinty. The dynanlic below-ground ecosys- tem. Forests: Fresh Per.sIx~ctivc~.s frortr Ii~~osystcwr At~rrly.sis. (R. H. Waring, ed.).
Oregon State University Press, Corvallis, 1980, p. I 19.
V. Vancura and A. Hanzlikova, Root exudates of plants: IV. Differences i n chemi- cal composition of seed and seedlings exudates, Plrrrrt m d Soil 36:27 I (1972).
E. A. Curl and B. Truelove, Tlrc Rhi:o,spherc~, Springer, New York, 1985.
G. Cieslinski. K. C. J. Van Recs. and P. M. H L I ~ I I ~ . Low molecular weight organic acids released from roots of durum whcat and flax into sterile nutrient solutions.
J o l t r r d of' P/mt Nulritiorl 20:753 (1997).
E. C. S. Chan. H. Katznelson. and J. W. Rouatt. The influence of soil and root extracts on the associative growth of selected soil bacteria. Cutmlicul Jourtr(r1 Mi- cwhiology!' 9: 187 ( 1962).
A . D. Rovira, Interactions between plant roots and soil microorganisms. AutIucrl Rc)l*icw< o / M i ~ r ~ b i ~ l o g y l P24 I ( 1965).
53.
54.
55.
56.
57.
58.
59.
60.
61.
62.
63.
64.
65.
66.
67,
68.
69
70
C. Christensen-Weniger, A. F. Groneman, and J. A. Van Veen. Associative N ? fixation and root exudation of organic acids from wheat cultivars of different alu- minium tolerance, Plant m d Soil 1 3 9 167 (1992).
P. Juo and G. Stotzky, Electrophoretic separation of proteins from roots and root exudates, Crrrlcrdicrrl J o u r ~ d of Botctny 4 8 9 13 ( 1 970).
R. A. Hamlen, F. L. Lukezic, and J. R. Bloom, Influence of age and stage of devel- opment on the neutral carbohydrate components in root exudates from alfalfa plants grown in a gnotobiotic environment, C m a d i ~ m Jortrnol of Plant Science S2:633 (1972).
E. Liljeroth and E. Biith, Bacteria and fungi on roots of different barley varieties (Horde~tm wlgarc. L.), Biology crrltl Fertility o f Soils 7 5 3 ( 1988).
J. K. Martin. Influence of plant species and plant age on the rhizosphere microflora,
Alrstrnlian Jolrrt~nl of Biologicrrl Scier~ce 24: 1 143 (197 l ) .
Z. Prikryl and V. Vancura, Root exudates of plants: VI. Wheat root exudation as dependent on growth, concentration gradient of exudates and the presence of bacte- ria. P l m t c m / Soil S769 (1980).
S. Prat and R. Retovsky, Root excretion in nutrient solution, Vestrlik Krtrl. Ces spol.
B. Frcnzel, Zur Atiologie der Anreicherung von Animosarum und Amiden im Wurzelraum von Helianthus annus. Plnrttc/ SS: l69 (1960).
R. Schonwitz and H. Zeigler, Exudation of water-soluble vitamins and of some
carbohydratcs by intact roots of maize seedlings ( Z ~ N m r y s L.) into a mineral nutri- ent solution. Z ~ 4 . s c h r ~ ~ , f i r r P~nrl,7erll~hy.siolo~~ie 1077 (1982).
W. K. Gardner. G. D. Parbery, D. A. Barber, and L. Swinden, The acquisition of phosphorus by L ~ ~ p i r ~ l r s crl1~1t.s L. V. The diffusion of exudates away from roots: a computer simulation, Plrrrrt t r r d Soil 72: 13 (1983).
A. D. Rovirn, G. D. Bowen, and R. C. Foster, The significance of rhimsphere microflora and mycorrhizas on plant nutrition. .h:\.c/o]~~iedin of Plant N l m i t i o ~ r (A. Lauchii and R. L. Bielski. eds.). Springer-Verlag, Berlin, 1983. p. 61.
A. A. Meharg and K. Killhan1. A novel method of determining root exudates in the presence of soil microflora. P l m t r r ~ l Soil 133: 1 1 I ( I99 I ).
A. A. Meharg and K. Killham. Loss of exudates from the roots of perennial ryegrass inoculated with a range of microorganisms, Plrrr~t o r ~ d Soil 170345 (1995).
K. J. Lee and M. H. Gaskins, Increased root exudation of “C-compounds by sorghum seedlings inoculated with nitrogen-fixing bacteria, Plrrr~tmclSoil 69391 (1982).
T. Heulin. A. Gukert. and J. Balandreau, Stimulation of root exudation of rice seed- lings by A:o.spiri/l~rr~~ strains: carbon budget under gnotobiotic conditions, Biology
ctrltl Futility OJ‘ Soils 4:9 ( 1987).
R. C. Snellgrove, W. E. Splitstoesser, D. B. Strubket. and P. B. Tinker. The distribu- tion of carbon and the demand of the fungal symbiont in leek plants with vesicular- arbuscular mycorrhizas, N c w P h y t o l o g i . ~ ~ 69:75 ( 1982).
S. M. Schwab. R. T. Leonard, and J. A. Menge, Quantitative and qualitative compo- sition of root exudates of mycorrhizal and non-mycorrhizal plant species. Cc/rltrtlitr/l
J o w m l of’ Bntcrrzy 62: I227 ( 1984).
T. J. Burr and A. Caesar, Beneficial plant bacteria. Critical R e v i w s i r ~ Pltrtlt Sci- errc~’.s 2: I ( 1984).
N u / I ~ . I - 19 ( 1944).
7 1. M. H. Gaskins, Rhizosphere bacteria and their use to Increase plant productivity:
72. J. Davison, Plant beneficial bacteria, Bio/Technology 6:282 (1988).
73. J. M. Lynch, Beneficial interactions between microorganisms and roots, Biotech A ~ I J N I I ~ C S 8:335 (1990).
74. B. J. J. Lugtenberg, L. A. de Weger, and J. W. Bennett, Microbial stimulation of plant growth and protection from disease, Clrrrerlt Opinion irl Biotechnology 2:457 (1991).
75. G. Lazarovits and J. Nowak, Rhizobacteria for improvement of plant growth and establishment, HortScierzce 32: 188 ( 1 997).
76. R. Axon and J. A. Ocampo. Factors effecting the vesicular-arbuscular infection and mycorrhizal dependency o f thirteen wheat cultivars, New Plryrologi.st X7677 (1981).
77. M. N. Schroth and D. C. Hildebrand, Influence of plant exudates on root-infecting fungi, Atrmnl Review of Pl~ytoprrtlrologg 2: I01 (1964).
78. M. C. Hawes, Living plant cells released from the root cap: a regulator of microbial populations in the rhizosphere, P l m r and Soil 12Y: 19 (1990).
79. E. Hozore and M. Alexander. Bacterial characteristics important to rhizosphere competance, Soil Biology c m / Biochernistg’ 23:7 17 (199 I ) .
80. A. J . Dharmatilake and W. D. Baker, Chemotaxis of Rlli:obiwn meliloti towards nodulation gene inducing compounds from alfalfa roots, Applied nr~d Erwiror~~r~erv tal Mic.robiology 5H:I 153 (1992).
81. A. M. Ashby, M. D. Watson, and C. H. Shaw, A Ti-plasmid determined function is responsible for chemotaxis of A g m b a c t e r i u r ~ t r ~ m @ c i ~ m towards the plant wound product acetosyringone, F E M S Microbiology Leftcr.s 41: 189 ( 1987).
82. G. Lopez-de-Victoria and C. R. Lovell. Chemotaxis of Axspirillwn species to aro- tnatic compounds, Applied urd Erlvironr,~erltctl Microbiology 5Y:295 l (1993).
83. T. Nikata, K. Sumida, J. Kato, and H. Ohtake, Rapid method for determining bacte- rial-behavioural responses to chemical stimulii, Applied u r d Emiror~metrfcrl Micro- biology 58:2250 (1992).
84. Y. Bashan and G. Holguin, Root-to-root travel of the beneficial bacterium A:o.spiril- / u r n bm.siletlscJ, Applied and E~~~,iror~tner~tcr/ Microbiology 60:2 120 ( 1994).
85. Y. Bashan and G. Holguin, A:os/’irillurn-plant relationships: Environmental and physiological advances (1990- 1996). C m u k r r l Jonrrtul qf Microhiokjgv 43: 103 ( 1997).
86. S. J. Vesper, Production of pili (fimbriae) by P.s~rrdort~or~rtms~~uorc~.scrr~s and corre- lation with attachment to corn roots, Applied cud Ewironrnerlta/ Microbiology 53:
1397 ( 1 987).
87. A. J. Anderson. Isolation from root and shoot surfaces of agglutinins that show specificity for saprophytic pseudomonads, Crmcuhn Journal [?f Bota~Iy 6/:3438 (1983).
88. A. J. Anderson, P. Habibzadegah-Tari, and C. S. Tepper, Molecular studies 011 the role of a root surface agglutinin in adherence and colonisation by P . s e u f i ~ ) ~ m m ~ s putidrf, Applied m d Envimrrmrntcrl Microbiology 54:375 ( 1987).
89. W. Achomk, T. Heulin, G. Villemin, and J. Balandreau, Root colonisation by SYm- a review. Agricdtrtre, Ecosvsterns cmd Emirormenr 12:99 (1985).
90.
91.
92.
93.
94.
95.
96.
97.
98.
99.
100.
101.
102.
103.
104.
105.
plasmata-forming Etlterobnc.trragglo,r,ert~t~.s. FEMS Microbiology E d o g y 13:287 ( 1994).
L. Van Overbeek and J. D. Van Elsas, Adaptation of bacteria to soil conditions:
application o f molecular physiology in soil microbiology, Modern Soil Microbiol- ogy (J. D. Van Elsas, J. T. Trevors, and E. M. Wellington, eds.), Marcel Dekker.
New York, 1997, p. 441.
J . W. Redmond, M. Batley, M. A. Djordjevic, R. W. Innes, P. L. Kuempel, and B. G. Rolfe, Flavones induce expression of nodulation genes in Khizobiuttl, Nature 323632 (1986).
N. P. J. Price and R. W. Carlson, Rhizobia1 lipo-oligosaccharide nodulation factors:
multidimensional chromatographic analysis of symbiotic signals involved in the development of legume root nodules, G/.ycobiologv 5:233 (1995).
Y. Okon, Azospirillurn as a potential inoculant for agriculture, Trends i r ~ B i o t e c h ) / - ogy 3:223 (1985).
Y. Bashan, M. Singh, and H. Levanony, H. (1989). Contribution of Azo.s/)irillunl brusilerlse Cd to growth of tomato seedlings is not through nitrogen fixation. Car~u- rlitrn Journul of Botuny 67: 13 17.
C. Elmerich, Molecular biology and ecology of diazotrophs associated with non- leguminous plants, Bio/Techr~ology 2:967 ( I 984).
P. Bonfante and S. Perotto, Strategies of arbuscular mycorrhizal fungi when in- fecting host plants, Nen' Phytologist 130:3 (1995).
A. Varma and B. Hock, Mycorrhiza, Springer-Verlag, Berlin, 1995.
X. L. Li. E. George, and H. Marschner, Extension of the phosphorus depletion zone in VA-mycorrhizal white clover in calcareous soil, Plant u r d Soil 131:41 (1991).
X. L. Li, E. George, and H. Marschner, Acquisition of phosphorus and copper by VA-mycorrhizal hyphac and root-to-shoot transport in white clover, Plant urd Soil 135:49 (1991).
N. S. Bolan, A. D. Robson, and N. J. Barrow, Effects of vesicular-arbuscular my- corrhiza on the availability of iron phosphates to plants, Plant u r d Soil YY:401 ( 1987).
P. B. Tinker, The chemistry of phosphorus and mycorrhizal effects on plant growth, B ~ d o t? ~ p co r r l ~ iz a s (F. S. Saunders, B. Mosse, and P. B. Tinker, eds.), Academic Press, London, 1975, p. 353.
X. L. Li, E. George, and H. Marschner, Phosphorus depletion and pH decreasc at the root-soil and hyphae-soil interfaces of VA-mycorrhizal white clover fertilised with ammonium, New Phytologi.st 119397 (1991).
S. E. Smith, B. L. St John, F. A. Smith, and D. J. D. Nicholas, Activity of glutamine synthetase and glutamate dehydrogenase in Trifoliunt .subterralleunl and Allium cepn L., effects of mycorrhizal infection and phosphorus nutrition, NCw Phytologjst YY:211 (1985).
N. S. Bolan, M. J. Hedley, and R. E. White, Processes of soil acidification during nitrogen cycling with emphasis on legume based pastures, Plant m d Soil 13453 N. S. Bolan, A critical review on the role of mycorrhizal fungi in the uptake of phosphorus by plants, Plurlt u r d Soil 134: 189 ( 1 99 I).
(199 l ) .
106.
107.
108.
109.
I I O .
112.
113.
114.
I IS.
116.
117.
118.
I IO.
170.
P. T. Rygiewicz, C. S. Blodsoe. and R. J. Zasoski, Effects of mycorrhizae and solution pH on (''N) ammonium uptake by coniferous seedlings, C m d i m Jorrrr~ol ForcJst Resecrrch /4:885 (1984).
P. H. Vaast and R. J. Zasoski, Effect of VA-mycorrhizae and nitrogen sources on rhizosphere soil characteristics, growth and nutrient acquisition of coffee seedlings (Cofktr eIrcrhiccr L.), Plar~t u r~ d Soil /47:3 1.
L. Rigou, E. Mignard, C. Plassard. J. C. Arvieu, and J. C. Remy, Influence of ectomycorrhizal infection on the rhizosphere pH around roots of maritime pine ( P i r r ~ t s pirrcrsfer Soland in Ait.), New Ph~~toln,qi.sr /30:141 (1995).
T. S. Gahoonia, N. Claassen, and A. Jungk, Mobilisation of phosphate i n different soils by ryegrass supplied with ammonium or nitrate, Plarrr e r r ~ t l Soil /40:241 ( 1992).
C. Hofflnann. E. Ladewig, N. Claassen, and A. Jungk, Phosphorus uptake of maize as effected by ammonium or nitrate nitrogen measurements and model calculations.
Zeitschr$ ff(crr~:~~.r~errrcrhr- B o d d l t r l t l o 157:22S ( 1 994).
I. Ortas. P. J. Harris, and D. L. Rowell, Enhanced uptake of phosphorus by mycor- rhizal sorghum plants as influenced by forms of nitrogen. P l m t c m / Soil /84:255
( 1996).
Y . Guo, E. George. and H. Marschner. Contribution of an arbuscular mycorrhizal fungus to the uptake of cadmiutn and nickel i n bean and maize plants. Plerrrr c t r d
Soil 184: 19.5 ( 1996).
Biologicer/ Cor7trol: R e / w j f . s t r r d Risks (H. M. T. Hokkanen and J. M. Lynch, eds.), Catnbridge University Press, Cambridge, 1995.
A. Ken, Commercial release of a genetically engineered bacterium for the control of crown gall. Agricmlrrtrd Science Nowrtrlwr IYBY:4 I ( 1989).
L. A. Harrison, L. Letendre. P. Kovacevich. E. Pierson, and D. Weller. Purification of an antibiotic effective against Gcreftrllrrrlrrorrly~,~,,s ,yrmttirtis v u . rrific'i produccd by a biocontrol agent, P s e r c e l o r r ~ o r r c r s crrrrc.c!firc,ic,rrs, Soil Biology mrl H i o c h e r r r i s f r y 25:2 I S ( 1993).
L. S. Thomashow and D. M. Weller, Role o f phenazine antibiotic from Psercclortlo-
I I ( ~ . S j?uore.s(~w.s in biological control of Gtr~'[trrrtrr1r1or71?'(.e~ grtrrtrblis var. tritici,
J o ~ r r r ~ a l oj' Bncteriology 170:3499 ( 1988).
P. Shannhan, D. J. O'Sullivan. P. Simpson. J. D. Glennon, and F. O'Gnra, Isola- tion of 2,4-diacctylphIoroglucinol and investigation of physiological parameters inHuencing its production. Applied c m / ~ r ~ ~ , ; r ( ~ r ~ r t r e r ~ r f r / Microbiology W 3 5 3
( 1992).
C. Keel. U. Schnider, M. Maurhofer, C. Voisard. J. Laville, P. Burger. D. Hass, and G. Defago, Suppression of root diseases by P.serrdorrlorlc/.sprro~c.sc,errs CHAO:
importmce of the bacterial secondary metabolite 2,4-dincetylphlorogl~tci1l~~l, M o - leculrrr Plrrrlt-Microbe hlteractiotls 5:4 (1992).
C. R. Howell and R. D. Stipanovic, Control of Rhi:ocrorlitr solnrri on cotton seed- lings with Psplr~k,rttorlcrsj?rtorc.sc.c.rl.s and with ;mantibiotic produced by the bacte- rium, Phyroparhologp W480 ( 1979).
C. R. Howell and R. D. Stipanovic. Suppression of P y f h i r m rrlri/rlrrrrr-induced d:ump- ing-off of cotton seedlings by Pserctlorrlorlejs j / r ~ o r e . s ~ ~ e r ~ s and its antibiotic pyolu- teorin. Ph?~ro)/,ert/rolo~y 70:7 12 ( 1980).