Photosynthate Partitioning in Split-Root Citrus Seedlings with Mycorrhizal and Nonmycorrhizal Root Systems

Abstract

Photosynthate partitioning was examined in seedings of sour orange (Citrus aurantium L.) and Carrizo citrange (Poncirus trifoliata jL.j Raf. x C. sinensis [L.] Osbeck) grown with split root systems inoculated on one side with vesicular-arbuscular mycorrhizal fungus (Glomus intra-radices Schenck and Smith). Source-sink relations were studied without mitipting differences in mineral content or physiological age that can occur in separate plant comparisons, because phosphorus was evenly distributed between leaves on opposite sides of the seedlings. Above-ground portions of each plant were exposed to '4CO2 for 8.5 minutes and ambient air for 2 hours, followed by extraction and identification of labeled assimilates. Mycorrhizal halves of root systems accumulated 66 and 68% of the '4C-labeled photosynthates translocated to roots of sour orange and 'Carrizo' citrange, respectively, as well as an average of 77% greater disintegrations per minute per gram fresh weight. Distribution of '4C-labeled assimilates was independent of phosphorus effects on pho-tosynthate partitioning in leaves and did not reflect fresh or dry weights of roots or degree of mycorrhizal dependency of the species. Differences in radioactivity between mycorrhizal and nonmycorrhizal root halves after 2 hours indicated at least 3 to 5% of the whole plant '4C-labeled pbotosynthates were allocated to mycorrhizae-related events on one side and that twice this amount, or 6 to 10%, might be expected if the entire root system was infected. Vesicular-arbuscular mycorrhizae are believed to benefit both host and fungi in most situations; however, the cost of this association in terms of photosynthate demand is not clear. Many studies have compared dry matter partitioning within mycorrhi-zal and nonmycorrhizal plants measured with different environmental conditions (3, 15), with different species (4, 8, 20), or at various stages of development. VAM2 plants tend to grow taller than uninoculated controls in most experiments, produce greater total dry matter, and often partition more C to below-ground tissues (8, 19). In addition, inoculation can stimulate N assimilation (5), raise levels oftissue P, Zn, and Cu (2, 21), and increase resistance to moisture stresses (28). 2Abbreviations: VAM; vesicular-arbuscular mycorrhizae; PPFD, pho-tosynthetic photon flux density; RuBP, ribulose bisphosphate; IBA, indolebutyric acid. may not always outweigh the cost to the host. In some situations, the proportion of carbon diverted to the fungi is apparently great enough to decrease plant growth (2, 3). Fungal dependence on photosynthate supply can be further seen in the decreased rate of infection and VAM development when alternate sinks are present on host plants (1, 14) or when light intensity is lowered (9, 12). Dry matter distribution and long term allocation of 14C-labeled photosynthates have also been compared in mycorrhizal and nonmycorrhizal plants. Resulting estimates of mycorrhizal demand for carbohydrates range from nearly zero up to 12% of the total plant C (3, 4, 29, 30). These may vary among species (4), and few include CO2 losses due to fungal respiration (24). The basis for sink strength of VAM has not been determined. Several possible factors have been suggested, which include fungal respiration (4, 11, 29), conversion of host photosynthates to glycogen and/or lipids in the fungus (4, 7, 19), root exudation of assimilate (10, 15, 30) growth regulators from fungi, sucrose hydrolysis (18, 23), and others (11, 18). Vesicular-arbuscular mycorrhizal fungi could also indirectly affect partitioning of photosynthates by altering phosphorus levels of source leaves. Phosphate in leafmesophyll cells is known to have striking effects on the partitioning of photosynthate between translocatable assimilates and stored starch (13). Increased phosphate uptake by VAM-infected plants would favor allocation ofcarbon to sucrose and subsequent export to roots. Such effects have not been considered in the past, and previous comparisons of mycorrhizal and nonmycorrhizal plants have been confounded by lower phosphorus content in the uninfected plants. This can be countered to varying degrees by phosphorus fertilization, yet the rate and pattern of host plant development often still differ (29). Split-root citrus seedlings, half mycorrhizal and half unin-fected, provide a valuable method for quantifying sink strength independent of phosphate effects on source leaves. The uniform phosphorus content between sides of the shoot obtained in the present study allows control of this important variable. Furthermore , short term '4C02-labeling experiments are used to minimize the amount of 14C lost through respiration or translocation into those soil hyphae not sampled with roots. The purpose of this research was first, to distinguish sink strength of mycorrhizal fungi from phosphorus effects on photosynthate partitioning in leaves, and second, determine the cost of the symbiosis in terms of host photosynthate utilized. MATERIALS AND METHODS Plant Material. Split-root seedlings were grown in a greenhouse using sour orange (Citrus aurantium L.) and Carrizo citrange (Poncirus trifoliata x Citrus sinensis [L.] Osbeck). Two pots were used for one plant so that separate mycorrhizal and nonmycorrhizal root systems could be grown. Split-root systems were initiated by removing tap roots of seedlings at the three-leaf stage, and dipping remaining segments into 2500 mg L' IBA 26 www.plantphysiol.org on June 6, 2020-Published by Downloaded from