MYCORRHIZAL DEPENDENCY OF SEVERAL CITRUS CULTIVARS UNDER THREE NUTRIENT REGIMES
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1 NewPhytol. (1978)81, MYCORRHIZAL DEPENDENCY OF SEVERAL CITRUS CULTIVARS UNDER THREE NUTRIENT REGIMES By J. A. MENGE*, E. L. V. JOHNSON* and R. G. PLATTf Departments Plant Pathology * and Plan t Sciencef, University of California, Riverside, California 92521, U.S.A. {Received 1 April 1978) SUMMARY Six citrus cultivars were grown with and without the mycorrhizal fungus Glomus fasciculatus under three fertilizer regimes all without phosphorus. The average mycorrhizal dependency (Gerdemann 1975) of Rough lemon and Brazilian sour were greater than the mycorrhizal dependecies of Alemow, Troyer citrange, Bessie sweet and Trifoliate. The mycorrhizal dependency of each cultivar, except Bessie sweet and Trifoliate, was substantially altered by at least one of the fertilizer regimes, and therefore the order of mycorrhizal dependency was different at all three fertilizer regimes. On the average, citrus rootstocks exhibited the greatest mycorrhizal dependency with the least fertilization. The average percentage phosphorus in non-mycorrhizal leaf tissues was inversely correlated with the mycorrhizal dependency of citrus cultivars at the medium fertilizer regime. An inverse correlation was observed between the dry weights of non-mycorrhizal roots of the citrus cultivars and the mycorrhizal dependency of the citrus cultivars. INTRODUCTION imycorrhizal dependency is defined by Gerdemann (1975) as "the degree to which a plant is dependent on the mycorrhizal condition to produce its maximum growth or yield at a given level of soil fertility". Mycorrhizal dependency can be defined numerically by expressing the dry weight of a mycorrhizal plant as a percentage of the dry weight of a non-mycorrhizal plant at a given level of soil fertility. A wide range of mycorrhizal dependencies in plants have been observed. Some species are never mycorrhizal and therefore have no mycorrhizal dependency (Baylis, 1974), but others, like Leptospermum scoparium, may have mycorrhizal plants which are % as large as non-mycorrhizal plants (Hall, 1975). Mycorrhizal dependency of a given plant species can be altered by soil type (Baylis, 1967;Hayman and Mosse, 1971, 1972; Mosse, 1972; Mosse, Hayman and Amold, 1973; Mosse, Powell and Hayman, 1976), soil phosphorus (Baylis, 1970, 1972, 1974; Crush, 1974; Daft and Nicholson, 1966; Hall, 1975; Mosse, 1973; Murdoch, Jackobs & Gerdemann, 1967; Ross, 1971; Ross and Gilliam, 1973), mycorrhizal species (Mosse, 1972; Schenck, Kinloch & Dickson, 1974) and by many other variables. For many years citrus nurserymen have noted stunting of citrus planted in fumigated soil (Kleinschmidt and Gerdemann, 1972; Martin et al., 1953; Martin, Baines and Page, 1963; Newcomb, 1975; Schenck and Tucker, 1974; Tucker and Anderson, 1972). Some Citrus rootstock cultivars appeared to be more severely stunted after fumigation than others, X/78/ $O2.OO 1978 Blackwell Scientific Publications 553
2 554 J. A. MENGE, E. L. V. JOHNSON and R. G. PLATT but observations were conflicting and confusing. Martin, Baines and Page (1963) reported that Rough lemon was highly tolerant to the stunting condition while Troyer citrange and Cleopatra mandarin were very sensitive. In the same nursery, Newcomb (1975) observed that Rough lemon and Troyer citrange were tolerant to stunting after fumigation while sweet and sour frequently grew to only 40 or 50% of their normal size. Field observations from Florida (Tucker and Anderson, 1972) indicated that Sour, Qeopatra mandarin, Carizo citrange and, to a lesser extent. Rough lemon, were stunted following fumigation. Field data from Illinois (Kleinschmidt and Gerdemann, 1972) indicated that Rougli lemon was most mycorrhizal dependent and Cleopatra mandarin, Troyer citrange and Sour were progressively less dependent on mycorrhizae. Glasshouse data of Schenck and Tucker (1974) suggested that although mycorrhizal dependency was similar for rootstocks they tested. Rough lemon was most mycorrhizal dependent while Sour and Cleopatra mandarin were less mycorrhizal dependent. The purpose of this study was to determine the degree of mycorrliizal dependency of six common citrus rootstocks in low P soil under three nutrient regimes. MATERIALS AND METHODS Six citrus rootstock cultivars. Rough lemon {Citrus Jambhiri Lush.), Brazilian sour (C aurantium L.), Alemow (C. macrophylla Webster), Bessie sweet (C sinensis (L.) Osbeck), Trifoliate {Poncirus trifoliata (L.) Raf.) and Troyer citrange {Poncirus trifoliata X Citrus sinensis) were germinated in autoclaved sand. After 3 weeks the seedlings were transplanted to 15-cm clay pots containing an autoclaved sandy soil. The ph of thesoo was 7.9. It contained 6.3 ppm P (Olsen analysis), 2.1 ppm NO3-nitrogen, 2.9 ppm K, 0.8 ppm Na, 0.86 ppm Cl, 0.85 ppm B, 3.8 ppm Ca+ Mg and 0.12% organic matter. Five grams of inoculum of the mycorrhizal fungus Glomus fasciculatus (Thaxter) Gerd. and Trappe were added to the soil in eighteen pots for each citrus variety. The inoculum consisted of soil, roots and spores from a pot containingsudan grass {Sorghum vulgare Pers.) which had grown for 105 days after being infected with Glomus fasciculatus. Autoclaved inoculum was added to eighteen control pots of each citrus variety. Six mycorrhizal and six non-mycorrhizal seedling of each citrus cultivar were fertilized once per week with a 'complete nutrient solution' minus P (106.8 mg NH3NO3, mg Ca (NO3)2, 68.0 mg KNO3, iron chelate (3.08 mg ferrous sulfate, 3.2 mg EDTA and 1.86 mg KOH), copper chelate (1.02 mg cupric sulfate, 1.02 mg EDTA and 0.58 mg KOH), mg MgSOa, 0.22 mg MnSO4-H2O, mg ZnS04 and mg CUSO4). An identical number of mycorrhizal and non-mycorrhizal seedlings of each citrus cultivar received the '1/2 nutrient solution' minus P, consisting of 1/2 of the complete nutrient solution once per week. An identical number of mycorrhizaj and non-mycorrhizal seedlings of each citrus cultivar received no fertilization. Plants were grown under glasshouse conditions (23-36 C) for 6 months. All plants were harvested and dry wei^ts, of roots, stems and tops were recorded. Leaves froin six replicate plants were bulked and then separated into three subsamples. The leaves were analysed for P, Zn and Cu for all rootstocks except Trifoliate which was omitted because of insufficient sample size. RESULTS The mean plant dry weight of each citrus cultivar inoculated with the mycorrhizal fungus
3 Citrus mycorrhizae 555 Glomus fasciculatus was significantly greater {P = 0.05) than the mean plant dry weights of the corresponding non-mycorrhizal plants, with the exception of Trifoliate at the 0 fertilizer level (Table 1). The mean dry weight of all citrus cultivars was small at the 0 fertilizer regime and the plants exhibited symptoms of acute nitrogen deficiency. In this experiment, most mycorrhizal citrus grown at the 1/2 fertilizer regime were significantly larger in dry weight than mycorrhizal citrus grown at the full fertilizer regime (Table 1). The mean dry weight of most non-mycorrhizal citrus at the 1/2 fertilizer regime was smaller, but not significantly smaller than the mean dry weight of non-mycorrhizal citrus at the full fertilizer regime. Table 1. Dry weights of mycorrhizal and non-mycorrhizal citrus grown under three fertilization regimes all without phosphorus Fertilizer levels refer to a weekly fertilization with 200 ml of 0, 1/2 or full strength nutrient solution without phosphorus which is described in the text. Means were averages from six replications. All individual means for plant weights of mycorrhizal plants were significantly greater {P = 0.05) than means for non-mycorrhizal plants with the exception of trifoliate at the 0 fertilizer level Cultivar Rough lemon Brazilian sour Alemow Troyer citrange Bessie sweet Trifoliate Mean 0 fertilizer Myco. +Myco 'LSD{P= 0.05) = 1.76 g /2 fertilizer -Myco. +Myco Full fertilizer -Myco. +Myco. Mean plant dry weight (g) Mean* -Myco. -rmyco The relative mycorrhizal dependency of citrus cultivars was determined by expressing the dry weights of mycorrhizal citrus as a percentage ofthe dry weights of non-mycorrhizal citrus (Table 2). On the average, the relative mycorrhizal dependencies of Rough lemon (923%) and Brazilian sour (723%) were significantly greater than the relative mycorrliizal dependencies observed with Troyer citrange (430%), Bessie sweet (362%) or Trifoliate (252%). Different levels of fertilizer altered the relative mycorrhizal dependency of individual citrus cultivars. The mycorrhizal dependency of Alemow and Troyer citrange decreased as the level of fertilization was increased. Brazilian sour showed the greatest mycorrhizal dependency at the medium level of fertilization while Rougli lemon was most dependent at the 0 fertilization regime. The relative dependencies of Bessie sweet and Trifoliate were not significantly different at any fertilizer regime. On the average, citrus rootstocks exhibited the greatest mean relative dependency on G. fasciculatus at the 0 nutrient regime and the least at the full fertilizer regime (Table 2). The average concentrations of phosphorus in citrus leaf samples from non-mycorrhizal citrus was lowest (0.08%) in Brazilian sour and highest in Troyer citrange (0.14%) (Table 3). The concentration of P in leaf tissues of Rough lemon, Alemow and Bessie sweet were not significantly different (Table 3). An inverse correlation was observed between
4 556 J. A. MENGE, E. L. V. JOHNSON and R. G. PLATT Table 2. Relative mycorrhizal dependency of six citrus cultivars at three fertilizer regimes all without phosphorus Nutrient levels refer to weekly fertilization with 200 ml of 0, 1/2 or full strength nutrient solution without P which is described in the text. Values in table not followed by identical letters are significantly different /' 05 tultivar Mean Rough lemon Brazilian sour Alemow Troyer citrange Bessie sweet Trifoliate Mean* 0 fertilizer mycorrhizal plant dry weight as a 1475 s 'LSD (P = 0.05) - 153%. 474 uvwxy 982 t 667 uv 489 uvw'xy 74 z 694 1/2 fertilizer FuU fertilizer percentage of non-mycorrhizal plant dry weight 638 uvw 658 uv 971 t 561 uvwx 341 wxyz 395 vwxyz 429 uvwxyz tu 229 yz 281 xyz 203 yz 254 yz 392 Mear the percentage of phosphorus in leaf tissue and the relative mycorrhizal dependency of the citrus cultivars especially at the 1/2 fertilizer regime where the correlation was significant {P 0.05) (Tables 2 and 3). No correlations were obser\'ed between mycorrhizal dependency and Zn and Cu concentrations in leaf tissues. An inverse correlation was also observed between the dry weiglits of non-mycorrhizal roots and the relative mycorrhizal dependency (Table 3). The correlation was significant at the 0 (/-=-0.83; P = 0.01), 1/2 (r =-0.61; F = 0.10) and complete fertilizer regimes (r = 0.66; P = 0.10). These correlation values were achieved despite the fact that Trifoliate grew so poorly in the soil provided that the small root weights of this cultivar probably reflect the small seedling size more than root characteristics. No correlations were observed between mycorrhizal dependency and root to shoot ratios (Table 3). Table 3. Comparison of mean mycorrhizal dependency values, mean concentrations of phosphorus in leaf tissues of non-mycorrhizal citrus, mean dry weights of non-mycorrhizal citrus roots and the mean root/shoot ratios of non-mycorrhizal citrus* Cultivar Rough lemon Brazilian sour Alemow Troyer citrange Bessie sweet Trifoliate Mycorrhizal dependency 923 w 723 X 591 X 430 y 362 yz 252 z Percentage of phosphorus in leaves of non-mycorrhizal citrus 0.09 yz 0.08 z 0.1 Oy 0.15 X 0.1 i y Dry weight of roots of non-mycorrhizal citrus 0.97 z 0.79 z 1.39 zy 1.87 y 2.22 y 0.40 z Root/shoot ratio of non-mycorrhizal citrus 1.08 y 1.97 y 0.56 z 1.15 y 1.63 y 0.81 yz *Means are derived from averaging values from the fuu, 1/2 and 0 fertilizer regimes. Leaf tissue ot Trifoliate was not analysed because of an insufficient sample size. Values in each column not followed by identical letters are significantly different, P = 0.05.
5 Citrus mycorrhizae 557 The numbers of G. fasciculatus spores in bulked soil samples from all citrus rootstock varieties decreased significantly {P = 0.05) with increased fertilization. There was an average of 776 spores/gm soil at the 0 fertilizer regime, 534spores/gm soil at the 1/2 fertilizer regime and 276 spores/gm soil at the full fertilizer regime. DISCUSSION The mycorrhizal dependency of citrus cultivars may be substantially different. The ability of a plant to absorb P from low P soils is often thought to be the major contributing factor to mycorrhizal dependency (Baylis, 1970; Crush, 1974; Daft and Nicholson, 1966; Hall, 1975; Mosse, 1973; Murdoch et al., 1967; Ross, 1971; Ross and Gilliam, 1973). Results obtained in this study tend to support this statement since average P concentrations in leaf tissue of non-mycorrhizal citrus were inversely correlated with mycorrhizal dependency at the medium fertility level. Embleton et al. (1973) carefully collected and analysed information regarding the tissue concentrations of N, P, K, Ca, Mg, S, B, Ee, Mg, Zn, Cu, Cl and Na as affected by various rootstocks. These authors have ordered citrus rootstocks according to their abilities to take up these nutrients. Only in the case of phosphate uptake was the order of rootstocks correlated with mycorrhizal dependency as determined in this study. Mycorrhizal dependency of Rougli lemon, Brazilian sour, Alemow and Troyer citrange was substantially altered by varying nutrient supply even though P levels remained constant. This indicates that certain nutrients other than P may alter mycorrhizal dependency and is in agreement with other authors who have indicated that although mycorrhizal dependency can be altered on different soils, it cannot always be correlated with either soil P or the P concentration in plant tissues (Hayman and Mosse, 1971; Mosse et al., 1976; Hayman and Mosse, 1972). Hall (1975) showed that additions of Ca, N and Ee could alter mycorrhizal dependency, and McDveen and Cole (1974) found that Zn may also affect mycorrhizal dependency. Baylis (1970, 1972, 1974) proposed the theory that the length of the root hairs is indicative of the degree of mycorrhizal dependency. Short root hairs indicate a relatively liigh degree while long root hairs indicate a low degree of mycorrhizal dependency. Long root hairs allow for better uptake of P and other elements, thereby eliminating the need for a strong mycorrhizal relationship. None of the citrus varieties tested, possess measurable root hairs so they were not a factor in this study. However, the size of non-mycorrhizal roots (dry weights) of the individual cultivars was inversely proportional to their mycorrhizal dependency. Since the root weiglits are used to compute the numerical mycorrhizal dependencies, this relationship must be viewed with caution. Nevertheless, figures from Savage, Cooper & Piper (1945) indicated that Sour and Rough lemon, which were the most mycorrhizal dependent in this study, have less fibrous roots than other citrus rootstocks. Ford (1954) found that among young citrus. Sour had 6.8 g of feeder roots in the top 10 in of soil. Rough lemon had 9.6 g and Sweet had 11.7 g. These amounts of Jeeder roots could be inversely correlated with the mycorrhizal dependencies found in the medium and high fertility nutrient regimes in this experiment. It appears that P concentrations in plant tissues do not necessarily govern mycorrhizal dependency, but frequently do. Eactors such as root hairs (Baylis, 1970, 1972, 1974), root geometry (Mosse et al., 1973), plant growth rates (Hall, 1975) and phosphate transport and utilization (Nassery, 1970) can all influence P absorption and thus mycorrhizal dependency. It is also clear that other nutrients besides P can alter mycorrhizal dependency.
6 558 J. A. MENGE, E. L. V. JOHNSON and R. G. PLATT The conflicting reports on the mycorrhizal dependency of different citrus cultivars in fumigated soils (Martin et al., 1953; Martin, Baines and Page, 1963;Newcomb, 1975;Kleinschmidt and Gerdemann, 1972; Tucker and Anderson, 1972; Schenck and Tucker, 1974) can be explained by the effects of different nutrient regimes on mycorrhizal dependency. However, some citrus cultivars such as Rough lemon can vary considerably in their ability to absorb P, depending upon the seed source (Embleton et al., 1973). Thus, variation within a citrus cultivar in some cases is great enough to cause changes in mycorrhizal dependency. ACKNOWLEDGM ENTS This research was supported in part by a grant from the California Citrus Advisory Board. REFERENCES BAYLIS, G. T. S. (1967). Experiments on the ecological significance of phycomycetous mycorrhizas. New Phytol, 66, 231. BAYLIS, G. T. S. (1970). Root hairs and phycomycetous mycorrhizas in phosphorus-deficient sou. Plant Soil, 33, 713. BAYLIS, G. T. S. (1972). Fungi, phosphorus and the evolution of root systems. Search, 3, 257. BAYLIS, G. T. S. (1974). The magnoloid mycorrhiza and mycotrophy in root systems derived from it. In: Endomycorrhizac (Ed. by V. E. Sanders, B. Mosse and P. B. Tinker), pp Academic Press, London. CRUSH, J. R. (1974). Plant growth responses to vesicular-arbuscular mycorrhiza. VIE Growth and nodulation of some herbage legumes. New Phytol, 73, 743. DAFT, M. J. & NICHOLSON, T. H. (1966). Effect ot Endogone mycorrhiza on plant growth. New Phvtol, 65, 343. EMBLETON. T. W., JONES, W. W., JONES, W. W., LABANAUSKAS, C. K. & REUTHER, W. (1973). Eeaf analysis as a diagnostic tool and guide to fertilization. In: The Citrus Industry. Vol. III. Production Technology (Ed. by W. Reuther), pp University of California Press, Berkeley. FORD, H. W. (1954). The influence of rootstock and tree age on root distribution of citrus. Proc. Am. Soc. Hort. Sci., 63, 137. GERDEMANN, J. W. (1975). Vesicular-arbuscular myeorrhizae. In: The development and function of roots (Ed. by J. G. Torrey and D. T. Clarkson), pp Academic Press, London. HALL, I. R. (1975). Endomycorrhizas of Metrosideros umbcllata and Weinmannia raccmosa. N. Z. J. Botany, 13,463. HAYMAN, D. S. & MOSSE, B. (1971). Plant growth responses to vesicular-arbuscular mycorrhiza. I. Growth oiendogone-'mozwvdiiqd plants in phosphate-deficient ^o\[%. New Phytol, 70, 19. HAYMAN, D. S. &. MOSSE, B. (1972). Plant growth responses to vesicular-arbuscular mycorrhiza. III. Increased uptake of labile P from soil. New Phytol., 71,41. KEEINSCHMIDT, G. D. & GERDEMANN, J. W. (1972). Stunting of citrus seedlings in fumigated nursery soils related to the absence of >indomycorx\\'\zsq. Phvtopathology, 62, MARTIN, J. P., AEDRICH, D. G., MURPHY, W. S. & BRADFORD, G. R. (1953). Effect of soil fumigation on growth and chemical composition of citrus plants. Soil Sci., 75, 137. MARTIN, J. P.^ BAINES, R. C. & PAGE, A. L. (1963). Observations on the occasional temporary growth inhibition of citrus seedlings following heat or fumigation treatment of soil. Soil Sci., 95, 175. MCILVEEN, W. D. & COLE, H. Jr. (1974^). Effect of zinc on germination of spores of Glomus mosseae and infection of soybean roots. Proc Am. Phytopathol. Soc, 1, 140. MOSSE, B. (1972). The influence of soil type and Endogone strain on the growth of mycorrhizal plants in phosphate-deficient soils. Rev. Ecol. Biol Sol, 9, 529. MOSSE, B. (1973). Plant growth responses to vesicular-arbuscular mycorrhiza. IV. In soil given additional phosphate. New Phytol, 72, 127. MOSSE, B., HAYMAN, D. S. & ARNOLD, D. J. (1973). Plant growth responses to vesicular-arbuscuiar mycorrhiza. V. Phosphate uptake by three plant species from P-deficient soils labelled with ^^P- New Phytol, 72, 809. MOSSE, B., POWELL, C. L. & HAYMAN, D.S. (1976). Plant growth responses to vesicular-arbuscular mycorrhiza. IX. Interactions between vesicular-arbusculai mycorrhiza, rock phosphate and symbioticnitrogen hxdiiion. New Phytol, 76, 331.
7 Citrus mycorrhizae 559 MURDOCH, C. L., JACKOBS, J. A. & GERDEMANN, J. W. (1967). Utilization of phosphorus sources of different availability by mycorrhizal and non-myhcorrhizal maizt. Plant and Soil, 27, 329. NASSERY, H. (1970). Phosphate absorption by plants from habitats of different phosphate status. II. Absorption and incorporation of phosphate by intact plants. A^(?H'/'/7.vro/., 69, 197. Ni'WCOMB, D. A. (1975). Mycorrhiza effects following soil fumigation. Intemat. Plant Propagat. Soe., 25, 102. ROSS, J. p. (1971). Effect of phosphate fertilization on yield of mycorrhizal and non-mycorrhizal soybeans. Phytopathology', 61, ROSS, J. P. & GIELIAM, J. W. (1973). Effect ofendogone mycorrhiza on phosphorus uptake by.soybeans from inorganic phosphates. Soil Sci. Soe. Am. Proc., 37, 237. SAVAGE, E. M., COOPER, W. C. & PIPER, R. B. (1945). Root systems of various citrus rootstocks. Proc. Fla. State Hort. Soc, 58, 44. SCHENCK, N.C., KINEOCH, R. A. & DICKSON, D. W. (1974). Interaction of endomycorrhizal fungi and root-knot nematode on soybean. In: Endomycorrhizas (Ed. by F. E. Sanders, B. Mosse & P. B. Tinker), pp Academic Press, Eondon. SCHENCK, N. C. & TUCKER, D. P. H. (1974). Endomycorrhizal fungi and the development of citrus seedlings in Florida fumigated Soils. /. Am. Soc. Hort. Sci., 99, 284. TUCKER, D. P. H. & ANDERSON, C. A. (1972). Correction of citrus seedling stunting on fumigated soils by phosphate application, froc. Fla. Hort. Soc, 85, 10.
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