SAITO Masanori

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SAITO, Masanori

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Significance of Arbuscular Mycorrhizal Fungi in Re-Vegetation Process in Nitrogen-Limited Degraded Ecosystems

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Significance of Arbuscular Mycorrhizal Fungiin Re-Vegetation Process in Nitrogen-LimitedDegraded Ecosystems著者 SAITO  Masanorijournal orpublication titleJournal of Integrated Field Sciencevolume 7page range 37-40year 2010-03URL http://hdl.handle.net/10097/4883337Symposium PaperSignifi cance of Arbuscular Mycorrhizal Fungi in Re-Vegetation Processin Nitrogen-Limited Degraded EcosystemsMasanori SAITO      Field Science Center, Graduate School of Agricultural Science, Tohoku University,Naruko-Onsen, Osaki, Miyagi, 989-6711, Japane-mail: msaito@bios.tohoku.ac.jpKeywords: degraded soil, hyphae, pioneer plant, succession, 15NReceived 11 January 2010; accepted 1 February 2010AbstractIt is well documented that arbuscular mycorrhizal (AM) fungi absorb phosphorus (P) from soil and sup-ply P to host plant in exchange for carbon (C) from plants. Currently it is also recognized that AM fungi absorb nitrogen (N) from soil and supply it to plants. We examined possible roles of AM fungi in terms of N acquisition and establishment of plants under N-limited conditions. First, we used a split compart-ment system composed of root and hyphal compart-ments. By using the system, we successfully showed that growth of Welsh onion inoculated with AM fungi was increased by supplying N through AM fungi, when movement of soil mineral N to plant roots was limited. Secondly, we investigated how AM fungi were functioning through primary development of vegetation occurring in the lahar (mud ﬂ ow of volca-nic deposit) area of Mt. Pinatubo, Philippines. Pio-neer plants in this area were a few gramineous plants, especially Saccharum spontaneum. Secondary plant species were wild leguminous plants, such as Calo-pogonium muconoides, which were characterized by co-existence of the gramineous plants. The growth of the gramineous plants was greatly enhanced due to N2 ﬁ xation of leguminous plants. Laboratory inocula-tion experiments with AM fungi showed that some of the pioneer gramineous species responded to added N only when these were mycorrhizal. These suggest that AM fungi might help their host plants to acquire N efﬁ ciently in N-limited soil environments.IntroductionArbuscular mycorrhiza (AM) is a sophisticated symbiotic system composed of arbuscular mycorrhi-zal (AM) fungi and plant roots. It is well documented that AM fungi absorb phosphorus (P) from soil and supply P to host plant in exchange for carbon (C) from plants (Saito 1997). Since 1980’s, it has been recognized that AM fungi also absorb nitrogen (N) from soil and supply it to plant (Ames et al. 1983). A main form of mineral nitrogen in soil is nitrate-N under aerobic conditions. In contrast to phosphate, nitrate-N in soil is not adsorbed with soil particles and moves easily along with mass flow of water. Therefore, unlike P, N supply through AM fungi to plant roots may not be critical for plant growth. It is now recognized that AM fungi may not increase plant growth under usual arable conditions (Reynolds et al. 2005). Although metabolic process of N transfer from AM fungi to plant has been clariﬁ ed (Govindarajulu et al. 2005, Guether et al. 2009), it is still uncertain if N transfer from AM fungi to plant is important under natural conditions.In this manuscript, first, we examine if AM fungi can enhance plant growth through their N supply to plant using a model system. Secondly, the signifi-cance of AM fungi in nitrogen-limited degraded soils is discussed with emphasis on re-vegetation process.Can AM fungi enhance plant growth by sup-plying N through their hyphae?Various compartment systems have been used to study nutrient transfer from AM fungi to plant. In most systems, the roots compartment is separated with ﬁ ne nylon mesh from extraradical hyphal com-partment. In the case of P, such mesh is effective to prevent P transfer between the compartments because of extreme slow mobility of phosphate in soil. Unlike phosphate, mineral N moves easily across the mesh. So it is difﬁ cult to quantitatively evaluate the effect of JIFS, 7 : 37 ? 40 (2010)38AM fungi on N transfer. We modiﬁ ed a two-compart-ment system having roots and hyphal compartments (Tanaka and Yano 2005). In the system, the compart-ments were separated with fine nylon mesh and air gap so that neither movement of mineral nitrogen nor roots elongation between the compartments occurred. Washed river sand was used as a medium in both plant and hyphal compartments (Fig. 1). A 30 days seedling of Welsh onion, “Naga-Negi” in Japanese, (Allium fi stulos CV. Motokura) was transplanted and inoculated with Glomus sp. R10 (Idemitsu Kosan Co.) in the root compartment (RC). After transplant-ing, 15N labeled ammonium nitrate was added either RC or hyphal compartment (HC). The treatment was combination of N addition to HC or RC; A) No N, B) N to only HC, C) N to only RC, and D) N to both RC and HC. After 3 weeks, the system was dismantled. Plant growth and fungal growth parameters were measured. Polyphosphate which is a main P storage substance in AM fungi was also determined (Takani-shi et al. 2009).ANOVA analyses showed that “N to RC” treatment increased almost all plant and fungal growth param-eters (plant dry weights, N and P concentrations, N uptake, colonization). “N to HC” treatment increased plant dry weight, shoot N and root 15N concentra-tions, and P uptake. These indicate that AM fungi can enhance plant growth by supplying N under nitrogen-limited conditions (Fig. 2). Interestingly, P uptake and polyphosphate concentration in roots were also sig-nificantly increased by “N to HC” treatment. These further suggest that P transfer through AM fungi may be regulated by soil N availability.Roles of AM fungi in re-vegetation process in nitrogen-defi cit volcanic depositSecondly, we investigated how AM fungi were functioning through primary development of vegeta-tion occurring in the lahar (mud flow of volcanic deposit) area of Mt. Pinatubo, Philippines (Saito et al. 2002; Oba et al. 2004). Because the lahar is com-prised of newly erupted volcanic materials, it contains little organic matter and nutrients available for plants. Most of the area was sparsely vegetated with only a few gramineous plants, especially Saccharum sponta-neum. However, some densely vegetated areas could be found in patch. These patches were characterized by co-existence of the gramineous plants and legumi-nous plants such as Calopogonium muconoides and Centrosema pubescens, which were well nodulated. Growth of the gramineous plants in these patches was greatly favored.The δ15N values in wild legumes in densely veg-etated (DV) sites were near to atmospheric δ15N (0‰), suggesting that these legumes actively fixed atmospheric nitrogen. S. spontaneum in sparsely veg-etated (SV) sites showed much lower δ15N values, probably because it absorbed N from a small amount of N in precipitation and/or in the soil extremely poor in organic N. On the other hand, the same plants in DV sites showed the medium values between the two formers, suggesting that S. spontaneum in DV sites used the N ﬁ xed by the legumes and its supported its vigorous growth in DV sites.M. SAITOFig. 1. Split compartment system for nitrogen ad-dition experiment. Nitrogen was added to from the top of root compartment or hyphal compartment. Arrows indicate movement of nitrogen and elongation of roots and hyphae, respectively.Fig. 2. Effect of nitrogen addition to different com-partment on shoot growth of Welsh onion. A) No N, B) N to only HC, C) N to only RC, and D) N to both RC and HC.39The plant roots were colonized with AM fungi. The wild legumes such as C. muconoides were well colonized and the mycorrhiza was typical VA-type. S. spontaneum was less colonized, and the coiled hyphae were characteristics. In the dry season, the colonization, especially occurrence of arbuscule, was much less in both gramineous and leguminous plants than in the rainy season, suggesting the very weak activities of mycorrhiza in dry season.The inoculation experiment indicated that S. spon-taneum was not responsive to inoculation at least un-der nitrogen deﬁ cit conditions such as the lahar soils but increased the spore numbers of AM fungi. Some of other gramineous species responded to added N only when these were mycorrhizal (Fig. 3). This ﬁ nd-ings suggest that some gramineous plants may con-tribute to increase the population of AM fungi in soil although the AM fungi are not beneﬁ cial to the host plants, and further suggest that AM fungi might help their host plants to acquire N efﬁ ciently in N-limited soil environments.The present study indicated that the re-vegetation process in the lahar area of Mt. Pinatubo involved the complex biological interaction among plants, microorganisms and environment. Based upon the results, we propose a picture of re-vegetation in the lahar soil. First, small seeds of the gramineous plants such as S. spontaneum are easily dispersed by wind from the area whose vegetation was not affected by volcanic activity, and they start to grow in the lahar. Secondly, spores of AM fungi are also dispersed by wind or ﬂ ooding to the lahar area. The fungi colonize the gramineous plants, and host plants increase the fungal density. AM fungi might improve N nutrient of some gramineous species under such nitrogen-limited conditions, although we were not able to show direct evidence. Thirdly, seeds of legumes are dispersed into the lahar. The high population density of AM fungi supports the growth of the legumes, because legumi-nous plants are known to be highly mycorrhiza de-pendent (Crush,1974) and require higher P absorption for their nitrogen ﬁ xation. Vigorous growth of the le-gumes promotes the growth of associated gramineous plants through the supply of the ﬁ xed nitrogen. Then, once the vegetation is established, the erosion of the soil may be reduced so that organic matter starts to accumulate in the lahar soil, which will support the further growth of other plant species.In conclusion, AM fungi have a potential to pro-mote plant growth by supplying N to their host. Pro-moting effect of AM fungi on plants in a soil deﬁ cit of N was evident for some plant species when N was added to the soil. In re-vegetaion process in a volca-nic deposit, AM fungi may have a role to facilitate vegetational succession.ReferencesAmes, R. N., C. P. P. Reid, L. K. Porter and C. Cam-bardella (1983) Hyphal uptake and transport of nitrogen from two 15N-labelled sources by Glomus mosseae, a vesicular-arbuscular mymycorrhizal fungus. New Phytologist, 95: 381-396.Arbuscular Mycorrhizal Fungi in Nitrogen-limited ConditionsFig. 3. Effect of AM fungal inoculation on wild gramineous plant species growing in a volcanic deposit deﬁ cit of nitrogen. Plants showing no-response with AM fungal inoculation were also colonized.40Crush, J. R. (1974) Plant growth responses to ve-sicular-arbuscular mycorrhiza. VII. Growhth and nodulation of some herbage legumes. New Phy-tologist, 73: 743-749.Govindarajulu, M., P. E. Pfeffer, H. R. Jin, J. Abu-baker, D. D. Douds, J. W. B. Allen, H. Bücking, P. J. Lammers and Y. Shachar-Hill (2005) Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature, 435: 819-823.Guether, M., B. Neuhäuser, R. Balestrin, M. Dynows-ki, U. Ludewig and P. Bonfante (2009) A mycor-rhizal-spicific ammonium transporter from Lotus japonicus acquires nitrogen released by arbuscular mycorrhizal fungi. Plant Physiology, 150: 73-83.Oba, H., N. Shinozaki, H. Oyaizu, K. Tawaraya, T. Wagatsuma, W. L. Barraquio and M. Saito (2004) Arbuscular mycorrhizal fungal community associ-ated with some pioneer plants in the lahar of Mt. Pinatubo, Philippines. Soil Science and Plant Nu-trition, 50: 1195-1203.Reylonds, H. L., A. E. Hartley, K. M. Vogelsang, J. D. Bever and P. A. Schults (2005) Arbuscular my-corrhizal fungi do not enhance nitrogen acquisition and growth of old-ﬁ eld perennials under low nitro-gen supply in glasshouse culture. New Phytologist, 167: 869-880.Saito, M., K. Minamisawa and W. Barraquio (2002) Significance of symbiotic microorganisms in re-vegetation process in lahar area of Mt. Pinatubo. Proceedings of World Congress of Soil Science (Bangkok), No. 1275.Saito, M. (1997) Regulation of arbuscular mycorrhiza symbiosis: hyphal growth in host roots and nutri-ent exchange. JARQ, 31: 179-183.Takanishi, I., R. Ohtomo, M. Hayatsu and M. Saito (2009) Short-chain polyphosphate in arbuscular mycorrhizal roots colonized by Glomus spp.: A possible phosphate pool for host plants. Soil Biol-ogy and Biochemistry, 41: 1571-1573.Tanaka, Y. and K. Yano (2005) Nitrogen delivery to maize via mycorrhizal hyphae depends on the form of N supplied. Plant and Cell Environment, 10: 1247-1254.M. SAITO

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Significance of Arbuscular Mycorrhizal Fungi in Re-Vegetation Process in Nitrogen-Limited Degraded Ecosystems

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