The Potential Role of Mucoromycotina 'fine Root Endophytes' in Plant Nitrogen Nutrition

Overview

Journal Physiol Plant

Specialty Biology

Date 2022 May 13

PMID 35560043

Authors

Nathan Howard

Silvia Pressel

Ryan S Kaye

Tim J Daniell

Katie J Field

Affiliations

Soon will be listed here.

Abstract

Mycorrhizal associations between fungi and plant roots have globally significant impacts on nutrient cycling. Mucoromycotina 'fine root endophytes' (MFRE) are a distinct and recently characterised group of mycorrhiza-forming fungi that associate with the roots of a range of host plant species. Given their previous misidentification and assignment as arbuscular mycorrhizal fungi (AMF) of the Glomeromycotina, it is now important to untangle the specific form and function of MFRE symbioses. In particular, relatively little is known about the nature of MFRE colonisation and its role in N uptake and transfer to host plants. Even less is known about the mechanisms by which MFRE access and assimilate N, and how this N is processed and subsequently exchanged with host plants for photosynthates. Here, we summarise and contrast the structures formed by MFRE and arbuscular mycorrhizal fungi in host plants as well as compare the N source preference of each mycorrhizal fungal group with what is currently known for MFRE N uptake. We compare the mechanisms of N assimilation and transfer to host plants utilised by the main groups of mycorrhizal fungi and hypothesise potential mechanisms for MFRE N assimilation and transfer, outlining directions for future research.

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References

Brundrett M, Tedersoo L . Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol. 2018; 220(4):1108-1115. DOI: 10.1111/nph.14976. View

Kuga Y, Sakamoto N, Yurimoto H . Stable isotope cellular imaging reveals that both live and degenerating fungal pelotons transfer carbon and nitrogen to orchid protocorms. New Phytol. 2014; 202(2):594-605. DOI: 10.1111/nph.12700. View

Carafa A, Duckett J, Ligrone R . Subterranean gametophytic axes in the primitive liverwort Haplomitrium harbour a unique type of endophytic association with aseptate fungi. New Phytol. 2021; 160(1):185-197. DOI: 10.1046/j.1469-8137.2003.00849.x. View

Field K, Bidartondo M, Rimington W, Hoysted G, Beerling D, Cameron D . Functional complementarity of ancient plant-fungal mutualisms: contrasting nitrogen, phosphorus and carbon exchanges between Mucoromycotina and Glomeromycotina fungal symbionts of liverworts. New Phytol. 2019; 223(2):908-921. DOI: 10.1111/nph.15819. View

Orchard S, Hilton S, Bending G, Dickie I, Standish R, Gleeson D . Fine endophytes (Glomus tenue) are related to Mucoromycotina, not Glomeromycota. New Phytol. 2016; 213(2):481-486. DOI: 10.1111/nph.14268. View

Albornoz F, Ryan M, Bending G, Hilton S, Dickie I, Gleeson D . Agricultural land-use favours Mucoromycotinian, but not Glomeromycotinian, arbuscular mycorrhizal fungi across ten biomes. New Phytol. 2021; 233(3):1369-1382. DOI: 10.1111/nph.17780. View

Bidartondo M, Read D, Trappe J, Merckx V, Ligrone R, Duckett J . The dawn of symbiosis between plants and fungi. Biol Lett. 2011; 7(4):574-7. PMC: 3130224. DOI: 10.1098/rsbl.2010.1203. View

Field K, Rimington W, Bidartondo M, Allinson K, Beerling D, Cameron D . Functional analysis of liverworts in dual symbiosis with Glomeromycota and Mucoromycotina fungi under a simulated Palaeozoic CO2 decline. ISME J. 2015; 10(6):1514-26. PMC: 5029179. DOI: 10.1038/ismej.2015.204. View

Kobae Y, Tamura Y, Takai S, Banba M, Hata S . Localized expression of arbuscular mycorrhiza-inducible ammonium transporters in soybean. Plant Cell Physiol. 2010; 51(9):1411-5. DOI: 10.1093/pcp/pcq099. View

10.

Hoysted G, Kowal J, Jacob A, Rimington W, Duckett J, Pressel S . A mycorrhizal revolution. Curr Opin Plant Biol. 2018; 44:1-6. DOI: 10.1016/j.pbi.2017.12.004. View

11.

Field K, Pressel S . Unity in diversity: structural and functional insights into the ancient partnerships between plants and fungi. New Phytol. 2018; 220(4):996-1011. DOI: 10.1111/nph.15158. View

12.

Cappellazzo G, Lanfranco L, Fitz M, Wipf D, Bonfante P . Characterization of an amino acid permease from the endomycorrhizal fungus Glomus mosseae. Plant Physiol. 2008; 147(1):429-37. PMC: 2330287. DOI: 10.1104/pp.108.117820. View

13.

Li T, Hu Y, Hao Z, Li H, Wang Y, Chen B . First cloning and characterization of two functional aquaporin genes from an arbuscular mycorrhizal fungus Glomus intraradices. New Phytol. 2012; 197(2):617-630. DOI: 10.1111/nph.12011. View

14.

Govindarajulu M, Pfeffer P, Jin H, Abubaker J, Douds D, Allen J . Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature. 2005; 435(7043):819-23. DOI: 10.1038/nature03610. View

15.

Fellbaum C, Gachomo E, Beesetty Y, Choudhari S, Strahan G, Pfeffer P . Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci U S A. 2012; 109(7):2666-71. PMC: 3289346. DOI: 10.1073/pnas.1118650109. View

16.

Nygren C, Edqvist J, Elfstrand M, Heller G, Taylor A . Detection of extracellular protease activity in different species and genera of ectomycorrhizal fungi. Mycorrhiza. 2007; 17(3):241-248. DOI: 10.1007/s00572-006-0100-7. View

17.

Truu M, Nolvak H, Ostonen I, Oopkaup K, Maddison M, Ligi T . Soil Bacterial and Archaeal Communities and Their Potential to Perform N-Cycling Processes in Soils of Boreal Forests Growing on Well-Drained Peat. Front Microbiol. 2020; 11:591358. PMC: 7744593. DOI: 10.3389/fmicb.2020.591358. View

18.

Lopez-Pedrosa A, Gonzalez-Guerrero M, Valderas A, Azcon-Aguilar C, Ferrol N . GintAMT1 encodes a functional high-affinity ammonium transporter that is expressed in the extraradical mycelium of Glomus intraradices. Fungal Genet Biol. 2006; 43(2):102-10. DOI: 10.1016/j.fgb.2005.10.005. View

19.

Stuart E, Plett K . Digging Deeper: In Search of the Mechanisms of Carbon and Nitrogen Exchange in Ectomycorrhizal Symbioses. Front Plant Sci. 2020; 10:1658. PMC: 6971170. DOI: 10.3389/fpls.2019.01658. View

20.

Fochi V, Chitarra W, Kohler A, Voyron S, Singan V, Lindquist E . Fungal and plant gene expression in the Tulasnella calospora-Serapias vomeracea symbiosis provides clues about nitrogen pathways in orchid mycorrhizas. New Phytol. 2016; 213(1):365-379. DOI: 10.1111/nph.14279. View