INTERACTION OF LIGHT INTENSITY AND SOIL TEMPERATURE WITH PHOSPHORUS INHIBITION OF VESICULAR-ARBUSCULAR MYCORRHIZA FORMATION
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1 New Phtol. (982) 9, bs NTERACTON OF LGHT NTENSTY AND SOL TEMPERATURE WTH PHOSPHORUS NHBTON OF VESCULAR-ARBUSCULAR MYCORRHZA FORMATON BY J. H. GRAHAM*, R. T. LEONARD Department of Botan and Plant Sciences AND J.A. MENGE Department of Plant Patholog, Universit of California, Riverside, California 9252 U.S.A. {Accepted 3 Januar 982) SUMMARY The interaction between light intensit and soil temperature with phosphorus inhibition of vesicular-arbuscular mcorrhiza (VAM) formation in sudangrass (Sorghum vulgare, Pers.) was investigated in P-deficient (-5 mg P kg~^) sand soil amended with (OP), 5 (5P) and 3 (3P) mg P kg"' soil as superphosphate. For seedlings inoculated with Glomus fasciculatus and grown at, 75, and 5" of glasshouse light intensit, the reduction in VAM formation b added soil P (5 P and 3P) was greatest at the lower light levels, whereas in the OP treatment, VAM fornaation was unaffected b a decrease in light intensit. ncreases in root P concentration resulted from both soil P amendment and, in the 5P treatment, from a decrease in light intensit, and were associated with decreases in root membrane permeabilit and corresponding decreases in root exudation of amino acids and sugars. The reduction in sugar exudation in the 5P treatment at lower light intensit was paralleled b a decrease in root extract levels of sugars, but decreases in amino acid exudation could not be explained b changes in amino acid levels in root extracts. These results suggest that P inhibition of VAM formation is more severe at lower light intensities because of a decrease in membrane-mediated exudation, although a reduction in sugar levels in root cells ma also contribute to tbe observed decrease in exudation. When inoculated seedlings were grown at 25, 3, and 35 C soil temperatures, the reduction in VAM formation in the 5P and 3P treatments was overcome b increase in soil temperature. The increase in VAM formation b increased temperature in the 5P plants was associated with significant increases in root membrane permeabilit and exudation without a corresponding change in root P concentration. n the OP treatment, an increase in soil temperature increased VAM formation with little effect on root exudation, which suggested an effect of temperature on Glomus fasciculatus. Higher soil temperature ma increase VAM formation through either a direct effect of temperature on tbe fungus or an indirect effect via an increase in leakage of root metabolites necessar for fungal activit, or both. NTRODUCTON Phosphorus inhibition of vesicular-arbuscular mcorrhiza (VAM) formation ma be associated with a membrane-mediated decrease in root exudation (Ratnaake, Leonard and Menge, 978; Graham, Leonard and Menge, 98). That is, when the phosphorus (P) content of the host is low, there is an increase in root membrane permeabiht and a greater loss of root cell metabohtes which are presumabl * Present address: Universit of Florida. AREC, 7 Experimental Station Rd, Lake Alfred, Florida 3385, U.S.A $ The New Phtologist 24-2
2 684 J- H. GRAHAM et al. necessar to sustain the germination and growth of the mcorrhizal fungus. To further elucidate the role of root exudation in mcorrhiza formation, it is essential to increase root leakage of sugars and amino acids from plants grown with sufficient P. n this case, the association should form irrespective of the phosphorus nutrition of the host and more directl demonstrate that root exudation is an important factor regulating fungal activit. Light intensit and root temperature are two environmental factors which have major effects on plant growth. These factors are also known to affect rates of root exudation (Rovira, 959) and to influence VAM formation. n general, a reduction in light intensit inhibits mcorrhizal development (Haman, 974; Daft and El-Giahmi, 978), and an increase in root-soil temperature up to 3 C increases colonization of roots (Furlan and Fortin, 973; Haman, 974; Schenck and Schroeder, 974; Smith and Bowen, 979). n studies on the effect of decreased light intensit on the mcorrhizal smbiosis, a decrease in the suppl of photosnthate to the root has been suggested as the factor affecting VAM development. nvestigations on the influence of soil temperature have emphasized the effect of temperature on spore germination (Schenck, Graham and Green, 975) and growth of the fungus during pre- and post-infection. n this report, we examine the interaction between light intensit or soil temperature and P-inhibition of VAM formation. n doing so, we seek not onl to further demonstrate the importance of root exudation in the mcorrhizal smbiosis, but also to identif how light intensit and root soil temperature influence root exudation and VAM formation. MATERALS AND METHODS Light intensit-p interaction A sand soil containing 5 mg kg~^ phosphorus (P) b Olsen analsis (Chapman and Pratt, 96) was autoclaved twice (2 C, kgcm"^)forl h, with a 24 h interval between treatments. Phosphorus as finel-ground superphosphate [Ca(H2PO4)2. HgO] was incorporated into the soil at, 5, and 3 mg P kg~^ dr soil. For (VAM) inoculation, half of the soil at each P level was mixed with inoculum of Glomus fasciculatus (Thaxter) Gerd. & Trappe isolate * from a pot culture on Citrus aurantium L. at a rate of 3 g inoculum ~^ dr soil. The inoculum consisted of soil which contained a mixture of chlamdospores ( spores g~^ soil), hphae and mcorrhizal roots. noculated and uninoculated soil at each P level was potted into cm^ strofoam cups. The microflora associated with the pot culture inoculum was established in non-mcorrhizal treatments b adding an inoculum water extract (Graham et al., 98). Cups were seeded with sudangrass {Sorghum vulgare Pers.), thinned to one seedling per cup, and placed in the glasshouse under 3223 C da night temperatures. Seedlings were fertilized weekl with a nutrient solution minus phosphorus (Menge, Johnson, and Platt, 978). At the time of seedling emergence, 2 plants from each V AM-P combination were subjected to three light intensit treatments. Plants were grown in full glasshouse light (%), and under shaded enclosures providing either 75 or 5% of full light intensit. Supplemental fluorescent light was provided to maintain a dalength * To be described as Glomus deserticola Trappe, Bloss and Menge.
3 Light and temperature effects on P inhibition of VAM 685 of about 4 h during the course of the experiment. Photosntheticall active radiation (mol m"^ s~^ from 4 to 7 nm), which was measured continuousl for 6 das under each light regime, averaged 48 +, , and for the, 75, and 5% light levels respectivel. After 5 weeks, two groups of three plants from each treatment were carefull washed free of soil, and analzed for levels of soluble amino acids and total soluble sugars in root exudates, plant dr wt and total root P as previousl described (Graham et al., 98). Total soluble amino acids and total soluble sugar contents in root exudates were measured b standard procedures using ninhdrin (Spies, 957) and sulphonated a-napthol (Denvor, 95) reagents, respectivel. The concentrations of amino acids and sugars were expressed as milligram equivalents of leucine or glucose, per gram dr wt of root. Phosphorus concentration in root tissue was measured b magnesium-nitric acid digestion followed b colorimetric assa using the molbdenum blue method (Chapman and Pratt, 96). Mcorrhizal formation was assessed for six plants per treatment b sampling a cross-section of the root sstem, and percentage root colonization was measured as previousl described (Graham et al., 98). After 6 weeks, replicate, freshl harvested root tissue samples were obtained from each of two groups of three plants. To obtain root extracts, replicate g samples were homogenized in ml of 95''o ethanol to give a final ethanol concentration of 85% (Graham et al., 98) and samples of extract were tested for total amino acids and sugars as described above. The concentrations were expressed on a root fresh wt basis. Root membrane permeabilit was evaluated for replicate 2 g samples of root tissue, using ** Rb efflux analsis and expressed as one-half time for K+ (**Rb) efflux over a 6h period (Ratnaake, et al., 978; Graham et al, 98). Soil temperature-p interaction Procedures for the soil-temperature stud were generall as described above with the following modifications. Mcorrhizal inoculum was mixed with soil at a rate of 25 g inoculum ' dr soil. noculated and uninoculated soil at each P level was potted into 8 cm^ strofoam cups to a uniform weight. Cups were seeded with sudangrass and thinned to one seedling per cup. Plants from each VAM-P treatment were subjected to three soil temperature treatments b immersing the closed cups to the soil level in circulating water tanks maintained at constant 25, 3 or 35 C. Soil moisture was adjusted dail to a uniform level (about cbar). The maximum light intensit during a 4 h da length was 475 mol m~'^ s~^ for the duration of the experiment. Plants were harvested after 4 weeks' growth for root exudation, dr wt, root P and VAM analsis, and after 5 weeks for efflux analsis. RESULTS Light intensit-p interaction VAM formation b G. fasciculatus was severel reduced in sudangrass seedlings grown in soils amended with 5 (5P) or 3 (3P) mg P kg'^ soil as compared to those grown without (OP) added phosphorus (Table ). The reduction of VAM formation b added P occurred in seedlings grown at all light levels but was more dramatic as light intensit decreased. B contrast, VAM formation in plants grown in OP soil was unaffected b a decrease in light intensit. Thus, when
4 686 J. H. GRAHAM et al. Table. Effect of light intensit on vesicular-arbuscular mcorrhiza (VAM) in sudangrass grown at three soil phosphorus levels Soil P treatment - (mg kg->) VAM formation ( o root colonization) * 75* 5* Vt 4W 5Y 66 V 32 W loy 68V 23 4Z * Percentage of full ligbt intensit. t Values followed b tbe same letter are not significantl different at tbe 5 level according to Duncan's multiple range test. Table 2. Effect of light intensit ongrowth of non-mcorrhizal (NM) and mcorrhizal (M) sudangrass at three soil phosphorus levels Soil P treatment (mg kg-') Mcorrhizal treatment * Plant dr wt (g) 75* 5* NM M -22Zt O-73Y 2Z O38YZ 2Z O-37YZ 5 inm M 26T 3-llS -9UV 92UV W 3 NM M 3-92R 43R 24U 2-8U 62VW 58VW * Percentage of full ligbt intensit. t Values followed b tbe same letter are not significantl different at tbe 5 level according to Duncan's multiple range test. plant growth was limited b P nutrition, the inhibitor eflfect of low light intensit was not apparent. The growth of non-mcorrhizal and mcorrhizal seedlings of sudangrass under P-limiting conditions (OP) was little affected b a decrease in light intensit (Table 2). At the higher P levels, a decrease in light intensit led to a significant decrease in growth of both mcorrhizal and non-mcorrhizal seedlings. Significant growth responses from VAM for the OP and 5P treatments at the highest light level were eliminated b a reduction in light intensit (Table 2). At all light intensities, the 5P and 3P treatments increased P concentration in roots of non-mcorrhizal plants compared to the OP treatment [Fig. l(a)]. The increase in root P as a result of P addition was associated with an increase in the half-time for K+ (^ 'Rb) efflux through root membranes, which reflects a decrease in cell membrane permeabilit [Fig. l(b)]. With an increase in soil P level, there was a corresponding decrease in exudation of amino acids [Fig. l(c)] and sugars [Fig. l(d)] at all light intensities which could not be accounted for b changes in the levels of these substances in root extracts [Fig. l(e) and (f)]- The decrease in membrane-mediated exudation associated with increased P nutrition corresponds with a decrease in VAM formation (Table ), as shown previousl (Ratnaake et al., 978; Graham et al., 98).
5 .; Light and temperature effects on P inhibition of VAM 687 c a. O i o o c E o w n D "o CO (o) (c (^ * (e ; ' \ \ ; V i: i K\\\\\\\\\\ N^ "T \\\ KN o E ^ 3 7 O LO b) Rh ioo d) (f PT- M - \\W\ \ \\ Soil P (mg kg' - % Fig.. Effect of three light levels [ (), 75 (D), and 5 o ( ) of full light intensit] on root phosphorus concentration (a), root membrane permeabilit (one-half time for K+ ['^''Rb] efrux) (b), exudation of amino acids (c) and sugars (d), and root content of soluble amino acids (e) and sugars (f) in non-mcorrbiza) sudangrass. Error bars represent the L.S.D. at the -5 level. n the 5P and 3P treatments, a decrease in light intensit from to 75 or 5% increased root P concentration, although this effect was less apparent in the 3P treatment [Fig. l(a)]. For the 5P treatment, the increase in root P levels with reduced light intensit was associated with an increase in half-time for K"*" influx [Fig. l(b)], i.e. a decrease in membrane permeabiht. There was a corresponding decrease in exudation of amino acids and sugars [Fig. l(c) and (d)] and the expected decrease in VAM formation (Table ). For this P treatment, the decrease in amino acid exudation at the lower light levels occurred without a significant
6 688 J. H. GRAHAM et al. o CNJ CT, ^ E ^ r~^ ^ 'i o - 2 c O -- "D Q) _ E (b i(d 7 7 \!; rj j (e) (f -2 - : ej : : :: :j % 5 3 Soi P (mg kg' 5 3 Fig. 2. Effect of three soil temperatures [25 (), 3 (D) and 35 C (Q)] on root phosphorus concentration (a), root membrane permeabilit (one-half time for K"*" ['^Rb] efflux (b), root exudation of amino acids (c) sugars (d), plant growth (e) and vesicular arbuscular mcorrhiza (VAM) formation (f) in sudangrass. Data presented in (a) to (e) inclusive are for non-mcorrhizal sudangrass. Error bars represented the L.S.D. at the -5 level. change in extract levels. The decrease in sugar exudation was acompanied b a decrease in extract levels, although the decrease in sugar exudation was less marked than the changes which occurred in extract levels. Soil temperature P interaction At all soil temperatures, growth of sudangrass seedlings in 5P or 3P soil resulted in a marked reduction in VAM formation, as compared to the OP treatment [Fig. 2(f)]. For the 5P treatment, the inhibition of VAM formation b
7 Light and temperature effects on P inhibition of VAM 689 phosphorus was overcome b an increase in soil temperature fronn 25 to 35 C and this effect was associated with increases in root membrane permeabilit [Fig. 2(b)] and greater exudation of amino acids and sugars [Fig. 2(c) and (d)]. The changes in permeabilit and exudation occurred without corresponding changes in plant growth [Fig. 2(e)] and root P concentration [Fig. 2(a)]. These trends were not as apparent for the 3P treatment. n the OP treatment, an increase in soil temperature increased VAM formation [Fig. 2(f)], even though there was no clear trend in the effect of temperature on root exudation [Fig. 2(c) and (d)]. The experiments reported above gave similar results when repeated. DSCUSSON Both light intensit and soil temperature affected the relations between P nutrition, root exudation and VAM formation in sudangrass. When P was added to soil, reduced light intensit increased P-induced inhibition of VAM formation. The greater inhibition was apparentl associated with increased P content of roots which corresponded with decreases in root membrane permeabilit and exudation as previousl suggested (Ratnaake et al., 978; Graham et al., 98). B contrast, an increase in soil temperature appeared to counteract P-inhibition of VAM formation b directl altering root membrane permeabilit (i.e., rate of K+ efflux) which led to an increase in root exudation without affecting P nutrition of sudangrass. An increase in cellular leakage of K+ with an increase in temperature up to 3 C has also been reported for carrot root, potato tuber and onion bulb tissues (Murata and Tatsumi, 979). Other factors affected b light intensit and soil temperature ma also be important in the interaction with VAM. t has been suggested that a decrease in light intensit limits the suppl of photosnthate to the roots and is responsible for the reported decreases in VAM infection (Haman, 974; Daft and El-Giahmi, 978). As previousl reported for sudangrass (Ratnaake et al., 978; Graham et al., 98), the changes in root exudation of amino acids and sugars as a function of P nutrition could not be accounted for b differences in root content of these compounds. For example, even though extract levels of sugars in roots of P-deficient sudangrass were no greater than the lowest levels found in P-treated plants (i.e. at the lowest light intensit), sugar exudation from roots of P-deficient plants was morf^ than twice as great at all light intensities. Under low P, VAM formation was not affected b a decrease in light intensit because P content of tissue did not change, roots were highl permeable and root exudation was not substantiall reduced. Thus, in this case, it appears that the inhibition of VAM b decreased light intensit results more from changes in P-control of membrane-mediated root exudation than from a decrease in suppl of root metabolites. These results do not rule out the possibilit that, at high P levels, a decrease of sugars in root extracts due to low light ma contribute to decreased exudation and VAM formation. Most studies on soil temperature have emphasized the effect on the fungus during the pre-infection phase of VAM formation (Furlan and Fortin, 973; Haman, 974; Schenck and Schroeder, 974; Smith and Bowen, 979). We observed greater VAM formation b our isolate of G. fasciculatus on roots at higher soil temperature, even in P-deficient plants where an increase in exudation was not pronounced. This fungus was isolated from a desert soil and is probabl adapted to high soil temperature as suggested b Schenck et al. (975) for Florida isolates of VAM fungi. An increase in germination and growth of the fungus at higher soil
8 69 J. H. GRAHAM et al. temperature ma increase root penetration and infection irrespective of a root exudate effect. Smith and Bowen (979) found that, in subterranean clover roots, an increase in soil temperature was associated with a greater number of root entr-points b VAM fungi sooner after inoculation. Although this assessment does not separate the effect of soil temperature on the fungus from that on the host root, it supports the view that these fungi could also be stimulated b a greater net leakage of root metabolites during pre-infection, which results in a greater number of entr-points and more root colonization. n summar, it appears that the effect of both light intensit and soil temperature on VAM formation is, at least in part, mediated b the influence of these environmental factors on host root exudation. Moreover, b altering soil temperature, we increased root exudation of the host independentl of P nutrition and attempted to demonstrate that exudation is the primar factor controlling the formation of the smbiosis. Even though it was not possible in this stud to separate the effects of soil temperature on the fungus from that on the host, we did identif specific changes in host root phsiolog which could influence fungal activit. ACKNOWLEDGEMENTS We wish to thank C. W. Hotchkiss for his technical assistance. REFERENCES CHAPMAN, H. D. & PRATT, P. F. (96). Methods of Analsis for Soils. Plants and Waters. Universit of California., Division of Agricultural Science, Berkele. DAFT, M. J. & E.-GAHM, A. A. (978). Effect of arbuscular mcorrhiza on plant growth. V. Effects of defoliation and light on selected hosts. Nezv Phtologist, 8, DENVOR, A. W. (95). Carbohdrate tests using sulphonated oc-napthol. jfournal of the American Chemical Societ, 72, FlRLAN, V. & FoRTiN, J. A. (973). F'ormation of endomcorrhizae h Endogone calospora on Allium cepa under three temperature regimes. Naturaliste Canadien,, GRAHAM, J. H., LEONARD, R. T. & MENGE, J. A. (98). Membrane-mediated decrease in root exudation responsible for phosphorus inhibition of vesicular arbuscular mcorrhiza formation. Plant Phsiolog, 68, HAYMAN, D. S. (974). Plant growth responses to vesicular-arbuscular mcorrhiza. \\. Effect of light and temperature. Neiv Phtologist, 73, 7-8. MLRATA, T. & TATSLM, Y. (979). on leakage in chilled plant tissues. n: Low Temperature Stress in Crop Plants (Ed. b J. M. Lons, D. Graham & J. K. Raison) pp Academic Press, New York. MENGE, J. A., JOHNSON, E. L. V. & PLATT, R. G. (978). Mcorrhizal dependenc of several citrus cultivars under three nutrient regimes. New Phtologist, 8, RANAYAKE, M., LEONARD, R. T. & MENGE, J. A. (978). Root exudation in relation to suppl of phosphorus and its possible relevance to mcorrhizal formation. New Phtologist, 8, RoviRA, A. D. (959). Root excretions in relation to the rhizosphere effect. V. nfluence of plant species, age of plant, light, temperature, and calcium nutrition on exudation. Plant and Soil,, ScHENCK, N. C, GRAHAM, S. O. & GREEN, N. E. (975). Temperature and light effect on contamination and spore germination of vesicular-arbuscular mcorrhizal fungi. Mcologia, 67, ScHENCK, N. C. & SCHRODER, V. N. (974). Temperature response oi Endogone m cor r\\\za on sobean roots. Mcologia, 66, SMTH, S. E., & BOWEN, G. D. (979). Soil temperature, mcorrhizal infection and nodulation oi Me die ago trunculatum and Trifolium subterraneum. Soil Biolog and Biochemistr,, SPES, J. R. (957). Colorimetric procedures for amino acids. Methods in Enzmolog, 3,
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