Interdependency of efficient nodulation and arbuscular mycorrhization inPiptadenia gonoacantha,a Brazilian legume tree

Abstract

Tripartite interactions between legumes and their root symbionts (rhizobia and arbuscular mycorrhizal fungi, AMF) are poorly understood, although it is well established that only specific combinations of symbionts lead to optimal plant growth. A classic example in which to investigate such interactions is the Brazilian legume tree Piptadenia gonoacantha (Caesalpinioideae), for which efficient nodulation has been described as dependent on the presence of AMF symbiosis. In this study, we compared the nodulation behaviour of several rhizobial strains with or without AMF inoculation, and performed analyses on nodulation, nodule cytology, N-fixing efficiency, and plant growth response. Nodulation of P. gonoacantha does not rely on the presence of AMF, but mycorrhization was rhizobial strain-dependent, and nodule effectiveness and plant growth were dependent on the presence of specific combinations of rhizobial strains and AMF. The co-occurrence of both symbionts within efficient nodules and the differentiation of bacteroids within nodule cells were also demonstrated. Novel close interactions and interdependency for the establishment and/or functioning of these symbioses were also revealed in Piptadenia, thanks to immunocytochemical analyses. These data are discussed in terms of the evolutionary position of the newly circumscribed mimosoid clade within the Caesalpinioid subfamily and its relative proximity to non-nodulated (but AMF-associated) basal subfamilies.

Nutrient demand and fungal access to resources control the carbon allocation to the symbiotic partners in tripartite interactions of Medicago truncatula

“…We found that plants in tripartite interactions had a significantly higher root and shoot biomass, N tissue concentrations and contents, and P contents than plants that were only colonized by rhizobia or AM fungi (Figures a,b; c,d; and S3a,c). Synergistic responses in tripartite interactions have also been described by other authors especially under low P and N supply conditions (Bournaud et al, ; Larimer et al, ). The dual inoculation with rhizobia and AM fungi can lead to higher photosynthetic rates and improves the harvest index (proportion of seed yields in relation to the total plant biomass) of legumes (Afkhami & Stinchcombe, ; Kaschuk, Kuyper, Leffelaar, Hungria, & Giller, ).…”

“…It is well established that a synergy of benefits can occur and that the host plant can gain more from tripartite interactions than from single inoculations with either symbiont (Afkhami & Stinchcombe, 2016;Antunes, de Varennes, Zhang, & Goss, 2006;Bournaud et al, 2017;Meng et al, 2015;Yasmeen, Hameed, Tariq, & Ali, 2012). The N-fixing capability of rhizobia is often limited by the P availability, and AM fungi can stimulate root nodulation, nitrogenase activity, and BNF through their positive effect on plant P nutrition (Ding et al, 2012;Owino-Gerroh, Gascho, & Phatak, 2005;Püschel et al, 2017;Vesterager, Nielsen, & Hogh-Jensen, 2006).…”

Beneficial Plant Microbe Interactions and Their Effect on Nutrient Uptake, Yield, and Stress Resistance of Soybeans

“…In natural environments, legume roots form tripartite interactions and are simultaneously colonized by both AM fungi and rhizobia [7,79]. Tripartite interactions have been shown to improve plant productivity, seed yield, P and N acquisition, and photosynthetic rates [10,80,81]. The rhizobial nitrogenase complex requires at least 16 ATP to reduce one N 2 molecule into two NH 3 .…”

“…Consequently, nodules act as strong P sinks in legume root systems to provide sufficient P resources to the bacteroids for optimum BNF [79,82]. Since AM fungi are able to improve the P nutrition of legume plants, AM fungi can increase the BNF by root nodules by at least 50% [10]. Nonmycorrhizal soybean plants have lower nodule numbers and weights and particularly under low P supply lower N fixation rates [7,83].…”

“…However, while the symbiosis of soybeans with rhizobia and AM fungi is well characterized, the functional role of endophytes is only known for a limited number of isolates. Our functional understanding of these interactions is mainly based on experiments with individual symbionts, but there is increasing evidence that individual symbionts can also affect the interactions of the plant with other symbionts [7][8][9][10]. We summarize here the effects of different beneficial microbes on nutrient uptake, yield, and stress resistance of soybeans and identify knowledge gaps that hinder the application of these interactions to their full potential in soybean production systems.…”