Kai Sun
Fang-Dong Zhan
Yu Shi
Jiayu Zhou
Jun Zhou
Long Peng- 1Jiangsu Key Laboratory for Microbes and Functional Genomics, Jiangsu Engineering and Technology Research Center for Industrialization of Microbial Resources, College of Life Sciences, Nanjing Normal University, Nanjing, Jiangsu, China
- 2College of Resources and Environment, Yunnan Agricultural University, Kunming, China
- 3State Key Laboratory of Crop Stress Adaptation and Improvement, School of Life Sciences, Henan University, Kaifeng, China
- 4Henan Dabieshan National Field Observation and Research Station of Forest Ecosystem, Zhengzhou, China
- 5Xinyang Academy of Ecological Research, Xinyang, China
- 6Institute of Botany, Jiangsu Province and Chinese Academy of Sciences, Nanjing, China
- 7Chrono-Environnement UMR 6249, CNRS, Université Bourgogne Franche-Comté, Besançon, France
- 8Research Institute of Subtropical Forestry, Chinese Academy of Forestry, Hangzhou, China
Editorial on the Research Topic
New insights into the influences of soil nutrients on plant-fungal symbiosis in agro- and forest ecosystems
Symbiotic fungi are widely distributed and form associations with over 90% of terrestrial plant species, playing an essential role in global agro- and forest ecosystems (Behie and Bidochka, 2014). These symbionts provide various benefits to host plants, including increased biomass accumulation (Hiruma et al., 2016), enhanced nutrient uptake (Guether et al., 2009; Fochi et al., 2017), and improved environmental adaptation (Sui et al., 2019). In return, host plants offer suitable habitats and accessible photosynthate for fungal survival and reproduction (Siegel et al., 1987; Jiang et al., 2017). However, in natural ecosystems, plant-fungal symbioses often face changing soil conditions, particularly variations in nutrient status (Sun et al., 2020, 2022). Different nutrient availabilities, forms, and compositions can significantly affect plant metabolism, growth, and immunity, which are crucial for maintaining the interplay between plants and fungi (Saikkonen et al., 2004; Sánchez-Bel et al., 2018). Conversely, soil nutrient status can influence the community composition of soil fungi, thereby impacting the establishment of symbionts.
The goal of this Research Topic is to showcase the latest studies focusing on the global effects of soil nutrients on plant-fungi interactions, enhancing our understanding of the mechanisms underlying the colonization and community dynamics of symbiotic fungi during their interaction with host plants across various species/genotypes, soil types, and nutrient levels and forms. The Research Topic covers studies on arbuscular mycorrhizal fungi (AMF), fungal endophytes and the plant-associated fungal community.
Insights into the impact of soil nutrients on AMF symbiosis
Ancient AMF symbioses can be seen as the bridge between plants and soils (Saia and Jansa, 2022; Kuyper and Jansa, 2023). The AMF symbionts are influenced by the forms and levels of nutrients in the soil, including nitrogen (N), phosphorus (P), and potassium (K). Yu et al. pointed out that AMF are sensitive to N addition over short timescales (1 year). Beneficial AMF associations are promoted under N-deficient conditions (Bonfante and Genre, 2010; Sanchez-Bel et al., 2016; Sánchez-Bel et al., 2018). Additionally, ammonium reduced AMF colonization levels in numerous plant species compared to nitrate (Pattinson et al., 2000).
Two noteworthy perspectives highlight the important roles of AMF symbiosis in plant invasion in agro-ecosystems based on greenhouse experiments. Du et al. revealed that the AMF Septoglomus constrictum provides host plants with higher N and P accumulation, conferring invasive plants with greater advantages over native congeners. Chen et al., through the analysis of AMF community associated with the invasive species Solidago canadensis and its native congener S. decurrens, clarified that AMF could confer invasive plants with greater advantages over native congeners, dependent on the forms of P in the soil.
Inorganic orthophosphate (Pi) is the available form of P that plants can acquire and utilize. However, Pi is often insufficient in the field due to its low solubility and relative immobilization (Nagy et al., 2009). Under P starvation, AMF can efficiently promote Pi uptake and homeostasis in host plants (Dierks et al., 2021). In this Research Topic, Zhang et al. identify a HLH domain containing transcription factor, RiPho4, from Rhizophagus irregularis. Through subcellular localization, yeast one-hybrid experiments, and using virus-induced gene silencing approaches, the authors demonstrated that RiPho4 acts as a transcriptional activator in AMF to maintain arbuscule development and regulate Pi uptake in host plants during Pi starvation. This study provides new insights into the mechanisms underlying how AMF regulates Pi uptake in host plants under Pi deficiency.
Apart from N and Pi, the AMF-plant interaction is also sensitive to changes in soil K nutrient (Han et al., 2023). In a greenhouse experiment, Yuan et al. investigated sweet potato (Ipomoea batatas (L.) Lam.]), a versatile crop with high K requirements for enhanced yield. Their study showed that K application and the presence of AMF Claroideoglomus etunicatum exhibited a synergistic effect on the root development and K acquisition of the “Xu28” variety of sweet potato, which has high K use efficiency, resulting in significant yield promotion. These results, combined with previous studies, expand our knowledge of the influences of soil nutrients on plant-AMF symbiosis.
Impact of heavy metal contamination on plant-fungal interactions
Heavy metal contamination in soil is a pressing global issue (Marrugo-Negrete et al., 2017) that affects plant-fungal interactions (Motaharpoor et al., 2019). Dark septate endophytes (DSEs) are ubiquitous colonizers of plant roots in various terrestrial ecosystems, often found in stressful environments, especially heavy metal-polluted soils (Su et al., 2021). Wang et al. highlighted the ability of Exophiala pisciphila H93, a beneficial dark septate endophyte which colonizes maize roots, to withstand cadmium exposure without compromising its growth-promotion effect on maize. They found that H93 colonization enhances plant resistance to heavy metal by influencing the expression of genes involved in signal transduction, hormonal pathway, and glutathione metabolism.
Influence of soil nutrients on plant-associated fungal communities
The response of the plant-associated fungal community to global changes plays a crucial role in understanding carbon and N cycling processes in agro- and forest ecosystems (Falkowski et al., 2008). In this Research Topic, Yu et al. demonstrated that the interaction between N addition and rainfall patterns has significant effects on soil fungal diversity in a grassland ecosystem. Similarly, Zhao et al. showed in a forest ecosystem that climate factors, such as temperature and precipitation, significantly influence dominant fungal genera and functional guilds in soil, particularly ectomycorrhizal fungi. Furthermore, fungal diversity and composition are strongly influenced by seasonal variation in soil nutrients, including total N and available P. The effect of vegetation type on rhizosphere microbes is also of great interest across different ecosystems. Liu et al. compared fungal communities in the rhizosphere of three typical vegetation types (herb, shrubs, and arbors). They discovered that the fungal community structure in the rhizosphere can vary across vegetation types and is primarily governed by deterministic processes. Additionally, plant metabolism has a significant impact on the plant-associated microbiome (Trivedi et al., 2020). Zhu et al. demonstrated that by applying exogenous salicylic acid, beneficial rhizosphere microorganisms were selectively enriched to enhance watermelon resistance to Fusarium wilt. These community analyses provide insights into the potential of plant-associated fungi in sustainable agriculture.
In this Research Topic, the majority of the studies aimed to elucidate the influences of changing environmental conditions, particularly soil nutrients, on plant-fungal symbiosis. However, more efforts are needed to clarify the molecular mechanisms underlying how nutrient factors drive the maintenance and breakdown of plant-fungi symbionts. Additionally, limited studies have been conducted under field conditions, which could provide better guidance for agricultural production. We anticipate further novel discoveries in the future.
Author contributions
KS wrote the manuscript. All authors reviewed and revised the manuscript.
Funding
KS was funded by the Jiangsu Funding Program for Excellent and Postdoctoral Talent (2022ZB357) and China Postdoctoral Science Foundation (2021M701748). FDZ was funded by the National Natural Science Foundation of China (42177381 and 42267002) and the expert workstation of Longhua Wu in Yunnan Province (202305AF150042). YS was funded by the Natural Science Foundation of Henan (222300420035) and Xinyang Academy of Ecological Research Open Foundation (2023DBS09). JYZ was funded by the Open Fund of Jiangsu Key Laboratory for the Research and Utilization of Plant Resources (JSPKLB201926). JZ was funded by the project of Sustainable Innovations for Regenerative Agriculture in the Mediterranean area-SIRAM (ANR-22-PRIM-0001).
Acknowledgments
The guest editors thank Dr. Madeleine Berger and Dr. Fabian Vaistij (University of York, UK) for proofreading the manuscript. The guest editors are heart fully thanks the reviewers in their aid helping this Research Topic.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
References
Behie, S. W., and Bidochka, M. J. (2014). Nutrient transfer in plant-fungal symbioses. Trends Plant. Sci. 19, 734–740. doi: 10.1016/j.tplants.2014.06.007
Bonfante, P., and Genre, A. (2010). Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nat. Commun. 1, 48. doi: 10.1038/ncomms1046
Dierks, J., Blaser-Hart, W. J., Gamper, H. A., Nyoka, I. B., and Six, J. (2021). Trees enhance abundance of arbuscular mycorrhizal fungi, soil structure, and nutrient retention in low-input maize cropping systems. Agric. Ecosyst. Environ. 318, 107487. doi: 10.1016/j.agee.2021.107487
Falkowski, P. G., Fenchel, T., and Delong, E. F. (2008). The microbial engines that drive Earth's biogeochemical cycles. Science. 320, 1034–1039. doi: 10.1126/science.1153213
Fochi, V., Chitarra, W., Kohler, A., Voyron, S., Singan, V. R., Lindquist, E. A., et al. (2017). Fungal and plant gene expression in the Tulasnella calospora-Serapias vomeracea symbiosis provides clues about nitrogen pathways in orchid mycorrhizas. New Phytol. 213, 365–379. doi: 10.1111/nph.14279
Guether, M., Balestrini, R., Hannah, M., He, J., Udvardi, M. K., and Bonfante, P. (2009). Genome-wide reprogramming of regulatory networks, transport, cell wall and membrane biogenesis during arbuscular mycorrhizal symbiosis in Lotus japonicus. New Phytol. 182, 200–212. doi: 10.1111/j.1469-8137.2008.02725.x
Han, S., Wang, X., Cheng, Y., Wu, G., Dong, X., He, X., et al. (2023). Multidimensional analysis reveals environmental factors that affect community dynamics of arbuscular mycorrhizal fungi in poplar roots. Front. Plant Sci. 13, 1068527. doi: 10.3389/fpls.2022.1068527
Hiruma, K., Gerlach, N., Sacristán, S., Nakano, R. T., Hacquard, S., Kracher, B., et al. (2016). Root endophyte Colletotrichum tofieldiae confers plant fitness benefits that are phosphate status dependent. Cell 165, 464–474. doi: 10.1016/j.cell.2016.02.028
Jiang, Y., Wang, W., Xie, Q., Liu, N., Liu, L., Wang, D., et al. (2017). Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi. Science 356, 1172–1175. doi: 10.1126/science.aam9970
Kuyper, T. W., and Jansa, J. (2023). Arbuscular mycorrhiza: advances and retreats in our understanding of the ecological functioning of the mother of all root symbioses. Plant Soil. doi: 10.1007/s11104-023-06045-z
Marrugo-Negrete, J., Pinedo-Hernández, J., and Díez, S. (2017). Assessment of heavy metal pollution, spatial distribution and origin in agricultural soils along the Sinú River Basin, Colombia. Environ. Res. 154, 380–388. doi: 10.1016/j.envres.2017.01.021
Motaharpoor, Z., Taheri, H., and Nadian, H. (2019). Rhizophagus irregularis modulates cadmium uptake, metal transporter, and chelator gene expression in Medicago sativa. Mycorrhiza. 29, 389–395. doi: 10.1007/s00572-019-00900-7
Nagy, R., Drissner, D., Amrhein, N., Jakobsen, I., and Bucher, M. (2009). Mycorrhizal phosphate uptake pathway in tomato is phosphorus-repressible and transcriptionally regulated. New Phytol. 181, 950–959. doi: 10.1111/j.1469-8137.2008.02721.x
Pattinson, G. S., Sutton, B. G., and Mcgee, P. A. (2000). Leachate from a waste disposal centre reduces the initiation of arbuscular mycorrhiza, and spread of hyphae in soil. Plant Soil. 227, 35–45. doi: 10.1023/A:1026519527211
Saia, S., and Jansa, J. (2022). Editorial: Arbuscular mycorrhizal fungi: the bridge between plants, soils, and humans. Front. Plant Sci. 13, 875958. doi: 10.3389/fpls.2022.875958
Saikkonen, K., Wäli, P., Helander, M., and Faeth, S. H. (2004). Evolution of endophyte-plant symbioses. Trends Plant Sci. 9, 275–280. doi: 10.1016/j.tplants.2004.04.005
Sánchez-Bel, P., Sanmartín, N., Pastor, V., Mateu, D., Cerezo, M., Vidal-Albalat, A., et al. (2018). Mycorrhizal tomato plants fine tunes the growth defence balance upon N depleted root environments. Plant Cell. Environ. 41, 406–420. doi: 10.1111/pce.13105
Sanchez-Bel, P., Troncho, P., Gamir, J., Pozo, M. J., Camañes, G., Cerezo, M., et al. (2016). the nitrogen availability interferes with mycorrhiza-induced resistance against Botrytis cinerea in tomato. Front. Microbiol. 7, 1598. doi: 10.3389/fmicb.2016.01598
Siegel, M. R., Latch, G. C. M., and Johnson, M. C. (1987). Fungal endophytes of grasses. Annu. Rev. Ecol. Evol. Syst. 15, 462e468. doi: 10.1146/annurev.py.25.090187.001453
Su, Z. Z., Dai, M. D., Zhu, J. N., Liu, X. H., Li, L., Zhu, X. M., et al. (2021). Dark septate endophyte Falciphora oryzae-assisted alleviation of cadmium in rice. J. Hazard. Mater. 419, 126435. doi: 10.1016/j.jhazmat.2021.126435
Sui, X. L., Zhang, T., Tian, Y. Q., Xue, R. J., and Li, A. R. (2019). A neglected alliance in battles against parasitic plants: arbuscular mycorrhizal and rhizobial symbioses alleviate damage to a legume host by root hemiparaitic Pedicularis species. New Phytol. 221, 470–481. doi: 10.1111/nph.15379
Sun, K., Lu, F., Huang, P. W., Tang, M. J., Xu, F. J., Zhang, W., et al. (2022). Root endophyte differentially regulates plant response to and nutrition by modulating N fluxes at the plant-fungal interface. Plant Cell Environ. 45, 1813–1828. doi: 10.1111/pce.14304
Sun, K., Zhang, W., Yuan, J., Song, S. L., Wu, H., Tang, M. J., et al. (2020). Nitrogen fertilizer-regulated plant-fungi interaction is related to root invertase-induced hexose generation. FEMS Microbiol. Ecol. 96, fiaa139. doi: 10.1093/femsec/fiaa139
Keywords: soil nutrient availability, nutrient forms, symbiotic fungi, arbuscular mycorrhizal fungi, fungal endophyte, fungal community, plant-fungal symbiosis, agroecosystem and forest ecosystem
Citation: Sun K, Zhan F-D, Shi Y, Zhou J, Zhou J and Peng L (2023) Editorial: New insights into the influences of soil nutrients on plant-fungal symbiosis in agro- and forest ecosystems. Front. Microbiol. 14:1237534. doi: 10.3389/fmicb.2023.1237534
Received: 09 June 2023; Accepted: 05 July 2023;
Published: 18 July 2023.
Edited and reviewed by: Trevor Carlos Charles, University of Waterloo, Canada
Copyright © 2023 Sun, Zhan, Shi, Zhou, Zhou and Peng. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Kai Sun, sunkainnu@sina.cn
†ORCID: Kai Sun orcid.org/0000-0003-2746-4131
Jun Zhou orcid.org/0000-0003-3618-1037