DYNAMICS OF ARBUSCULE DEVELOPMENT AND DEGENERATION IN A ZEA MAYS MYCORRHIZA

A quantitative light and electron microscope study of developing and degenerating mycorrhizal arbuscules of Glomus fasciculatum in Zea mays was carried out in order to estimate three parameters during the colonization cycle. These were: 1) Vv(tc) the fraction of the host cell volume occupied by a volume offungus; 2) Vv(cy,c), the fraction ofthe host cell volume occupied by host cytoplasm; 3) Sv(prc)> the surface-area-to-volume ratio of the host protoplast to the whole host cell. Uninfected cortical cells had an Sv(pr,c) of 0. 13 ,um2/,um3. As the fungus penetrates the cell wall, the protoplast invaginates, causing a decrease in protoplast volume and an increase in protoplast Sv. The Sv(pr,c) of a cell containing a mature arbuscule is 1.275 ,um2/,um3. Because of the shrinkage of the protoplast, the Sv of the protoplast to its own volume rather than the original cell volume is 2.55 ,um2/,um3, or almost a 20-fold increase. Total cell size is unaffected. When the arbuscule is mature, the fungus occupies 42% of the cell, with 24% as 1,um-diam branches, and 18% as trunk. Arbuscular branch formation progresses at a linear rate and is the most important factor in causing the increased host Sv. The correlation coeEcient for Vv(br,c) the volume fraction for arbuscular branches, vs. Sy(pr,c) is r = 0.932 (P < 0.001). Degeneration of the arbuscule is marked by a rapid decrease in branches, host Sv, and host cytoplasm. The trunk develops and degenerates at a slower rate than the branches. INFECTION of land plants by mycorrhizal fungi can lead to a growth increase (Gerdemann, 1968; Mosse, 1973). This increase usually is due to the increased level of mineral nutrients, especially phosphorus, that the fungus absorbs and transports to the host (Hattingh, Gray and Gerdemann, 1973; Pearson and Tinker, 1975; Rhodes and Gerdemann, 1975) primarily by cytoplasmic streaming of phosphate granules (Cox et al., 1980). Carbohydrates produced by the host are absorbed by the fungus (Rhodes and Gerdemann, 1978). The site of exchange t Received for publication 25 September 1982; revision accepted 4 August 1983. This study was supported in part by a Northern Illinois University Graduate School Fund grant and a Faculty Research Participation grant to the senior author while at Argonne National Laboratory; the remainder of the fundingwas providedby the U.S. Department of Energy's Office of Energy Research through its University/National Laboratory Cooperative Program. The authors wish to thank Ms. Paula Rebert and Ms. Andrea S. White for technical assistance. is presumed to be the arbuscule, which is ideally suited for such a function because of the large surface areas of host and fungus that are in contact. Several different vesicular-arbuscular mycorrhizal associations have been observed at the ultrastructural level. Results of these studies have been summarized (see Brown and King, 1982a, b; Carling and Brown, 1982; Nemec, 1982, for bibliographies). Exclusions from these reviews include studies by Bonfante-Fasolo (1978, 1982), Bonfante-Fasolo and Grippiolo (1982), Bonfante-Fasolo et al. (1981), Capaccio and Callow (1982), Gianinazzi-Pearson et al. (1978), Kariya and Toth (1981), Marx etal. (1982), Scannerini, Bonfante and Fontana (1975), and Strullu, Gourret and Garrec (1981). These studies have led to two theories concerning the transfer of nutrients between host and fungus. BurgeS(1938) (cited in Cox and Tinker, 1976) suggested that the main mechanism of nutrient transfer to the host was digestion of fungal structures. Kinden and Brown (1975) supported this concept. However, transport of carbon moieties to the fungus prior to fungal degeneration must occur. Transport during the mature arbuscule stage could also account for the transfer of inorganic nutrients, especially phosphorusS to the host (Cox and Tinker, 1976). In order to assess the contribution, if any, of each of these mechanisms