Plant carbon limitation does not reduce nitrogen transfer from arbuscular mycorrhizal fungi to Plantago lanceolata

Abstract

Aims The stress-gradient-hypothesis predicts that interactions among organisms shift from competition to facilitation as environmental stress increases. Whether the strength of mutualism will increase among symbiotically associated organisms when partners are forced into resource limitation remains unknown. Plants exchange photosynthetic carbohydrates (plant C) for nutrients in mycorrhizal symbiosis but how this exchange varies with plant C limitation is not fully understood. Methods We investigated the influence of plant C availability and of arbuscular mycorrhizal fungi (AMF) on plant nitrogen (N) uptake and resource allocation using 13C and 15N labeling. We grew Plantago lanceolata with and without AMF Rhizophagus irregularis under ambient (400 ppm, AC) and low (100 ppm, LC) atmospheric [CO2] and physically restricted plant root but not mycorrhizal access to soil N. Results We found that plants grown under LC used AMF to obtain the same amount of N as those grown under AC, but the amount of newly fixed C correlated with the acquisition of N only under LC. The LC plants allocated more of their C to aboveground tissues. Conclusions Overall our results suggest a more beneficial role of symbiosis under C limitation. The tight reciprocal control on N transfer and C allocation under C limited conditions supports the stress-gradient hypothesis of mutualistic symbiotic functioning

Understanding the roles of nonstructural carbohydrates in forest trees – from what we can measure to what we want to know

“…Radiocarbon measurements of mycorrhizal fruiting bodies and parasitic plants indicate that C being transferred is mostly fixed within the last year (Gaudinski et al ., ), which would seem to indicate that this is a high priority, although few systematic measurements exist. Questions about the role of NSC supply can be answered with manipulative experiments (Udvardi & Poole, ) and some studies have cleverly manipulated C supply via shading or low CO 2 and used isotope labelling to quantify tradeoffs between plant C availability and nitrogen ( 15 N) and phosphorus ( 33 P) uptake (Fellbaum et al ., ; Zhang et al ., ). Interestingly, nutrient uptake did not decrease even though shaded or low‐CO 2 plants decreased the absolute amount of C transferred to mycorrhiza.…”

“…Interestingly, nutrient uptake did not decrease even though shaded or low‐CO 2 plants decreased the absolute amount of C transferred to mycorrhiza. Instead, plants optimized internal resource distribution by allocating proportionally more C and N to aboveground tissues to maximize the potential for CO 2 assimilation (Zhang et al ., ). A similar resource limitation experiment applied atmospheric N 2 removal to force rhizobia to ‘cheat’ on their hosts, thereby addressing plant sanctions for nonrewarding symbionts (Kiers et al ., ).…”

Unity in diversity: structural and functional insights into the ancient partnerships between plants and fungi

“…Furthering our understanding of the diversity, biology and ecology of symbiotic Mucoromycotina fungi, of the roles in and mechanistic basis of C‐for‐nutrient exchanges in both Mucoromycotina– and Glomeromycotina–plant symbioses, and of the impacts of mycorrhizal networks on ecosystem nutrient cycling also has important implications for determining the influence – past, present and future – of the environment on this key partnership between plants and fungi. Recent advances in mycological research, including the development of high‐throughput molecular tools (van der Heijden et al ., ) and ever more sophisticated isotope tracer techniques to quantify plant‐to‐fungus nutrient exchange dynamics (Field et al ., 2015b, 2016a; Zhang et al ., ), present us with unrivalled opportunities to dissect the ‘diversity within unity’ of this ancient and widespread mutualistic partnership between plants and fungi, its past roles in facilitating plant terrestrialistation > 500 Ma, and present and future roles in ecosystem functioning.…”

“…Alternatively, the amount of CO 2 available for photosynthesis can be altered. In such experiments, fungal-acquired nutrient transfer to the plant is not always linked in a linear manner to plant C transfer Field et al, 2012Field et al, , 2015aField et al, , 2016aZhang et al, 2015). A common limitation is that single growth chambers for each CO 2 condition are often used in these experiments, raising the possibility that observations occur through chamber effects rather than solely CO 2 effects (Werner et al, 2018).…”

Effects of Pb, Cd, Zn, and Cu on Soil Enzyme Activity and Soil Properties Related to Agricultural Land-Use Practices in Karst Area Contaminated by Pb-Zn Tailings

“…Urease belongs to a group of enzymes acting on the carbon-nitrogen bond of urea. The mycorrhizal fungi gain nitrogen and carbohydrate from the degradable soil organic matter which, in turn, increases the supply of available nitrogen [37]. So, the TN and SOC are not easily accumulated in the cornfields and the "elusive" carbon and nitrogen pools appear in the paddy fields due to the different accumulation conditions under Pb, Cd, Zn, and Cu stress (Tables 1 and 2).…”