The unfaithful companion of plants – mycorrhizae

By Runtian Wu

Mycorrhizae are fungi that share a close relationship with the plant’s roots. Such a relationship often involves a direct exchange of resources such as carbon and phosphorus that can impact the growth of plants. Although hidden on earth and invisible to most non-specialists, mycorrhiza has an important role in the ecosystem. They are present in more than 80% of land plants1 and account for 5-36% biomass of the soil and 9-55% biomass of soil microorganisms.2 Traditionally, the interaction between mycorrhiza and plants is regarded as an example of mutualism, in which mycorrhizae provide plants with nutrients such as nitrogen and phosphorus in exchange for carbon, but the relationship between mycorrhiza and plants is increasingly being regarded as mutual parasitism.3 The recent molecular and genetic analysis allowed us to understand further how such a relationship is maintained despite both sides trying to take advantage of the other side. In many cases, a relatively stable mutualism is maintained, and plants can experience positive effects such as quicker growtH4,  increased reproductive capacity5, greater water tolerance6 and pathogen resistance.7

The two main types of mycorrhizae are endomycorrhiza and ectomycorrhiza. Ectomycorrhiza, often colonises the roots of trees and shrubs, usually forms extracellular hyphae that don’t penetrate into the cell. In contrast, endomycorrhiza such as arbuscular (AM) have hyphae penetrating the root cells. Both types of mycorrhizae rely on a series of signalling events to recognise and colonise roots. Some structures such as hyphopodia in Arbuscular mycorrhiza (AM fungi is the most common type of endomycorrhiza) may be developed that act as a bridge to transport nutrients between mycorrhizae and plants.8 Although molecular mechanisms remain unclear, it has been demonstrated that nutrient transport can be bidirectional between some mycorrhiza and plants. AM fungi have active phosphate transporter in their hyphae that can take up inorganic phosphate from the soil to allow for delivery into the plants9, and plants possess phosphate transporters to absorb phosphate that is mycorrhiza specific8. It has also been demonstrated that carbon can be transferred from plants to mycorrhiza, though the molecular mechanism remains unclear.10 Fungal hyphae are analogous to plant root hairs that can take up nutrients, including areas where the plant roots do not reach. By forming a mutualistic relationship, plants can receive the limiting nutrients, and mycorrhizae can receive carbon rewards from plants. The importance of mycorrhizae is more significant under stressful conditions. For example, nutrients become less available during water stress because the tortuosity of diffusion increases.11 But hyphae of mycorrhiza fungi can help plant roots take up the nutrients to alleviate the water stress. It has been found that AM fungi can help to improve soil condition in sand dunes during the afforestation process in southwest Iran.12 Many AM fungi have also been reported to increase the number and weight of nodules formed by nitrogen-fixing plant species13, suggesting an interaction between mycorrhiza and nitrogen-fixing bacteria.

Although mycorrhiza has traditionally been thought to be an example of mutualism, recent research has found that on some occasions, mycorrhiza can have negative impacts on plant growth. When plants form associations with mycorrhiza, while receiving nutrients from mycorrhiza, plants also provide nutrients such as carbon to mycorrhiza. Such a relationship can be destabilised and become pure parasitism when mycorrhiza stops providing nutrients to plants or vice versa. Research has found that some kinds of mycorrhiza, while facilitating the growth of some types of plants, can negatively impact other types of plants. For example, while a kind of AM fungi called Acaulospora morrowiae can promote the growth of Rudbeckia hirta by 45%, the same fungi can reduce the growth of Plantago lanceolata by 47%.14 Klironomos reported that the number of negative and positive responses of plants to mycorrhizae were almost equal for the 100 plant individuals analysed, with the magnitude of plant growth response from -49% to +46%14. Johnson also reported the negative effects of mycorrhiza on plants in agricultural soils that have been repeatedly fertilised.15 There is no evidence that there is a single AM fungi that can promote the growth of all plant species within a community.14 Whether there will be a mutual relationship between plants and mycorrhiza depends on both the plant’s and mycorrhiza genotype, the environmental conditions, and even the life stage of plants. For example, it has been demonstrated that ectomycorrhiza is most beneficial to plants during the plant’s first year of growth.16 This is because seedlings have yet to develop an extensive root system and thus are susceptible to resource limitations. As the seedling develops a more extensive root system, it will be less reliant on nutrients obtained from mycorrhiza, and providing mycorrhiza with resources may therefore impede its growth. Similarly, under stressful environments, the plants and mycorrhiza would increasingly rely on each other for limiting recourses, and thus the relationship can be more inclined to mutualism than parasitism. Competition between species decreases as the environmental severity increases, but mutualism only increases at a certain degree of environmental severity, characterised by a hamp-shaped distribution.17 The drop in mutualism under high environmental severity may be due to very stress-tolerant species acting as an overly-important benefactors to other less stress-tolerant plants.18 Under such circumstances, other less stress-tolerant plants could be acting in a more parasitic relationship with stress-tolerant plants, producing no net benefits to the stress-tolerant plants but obtaining resources from stress-tolerant plants via connected mycorrhizae.

So far, I have mentioned mostly the exploitation of mycorrhiza on plants. But it’s also important to note that plants can also be “parasitic” on mycorrhiza by obtaining the nutrients without providing enough rewards. The saprophytic plants (e.g., Monotropa hypopitys) are plants that do not have the photosynthetic ability but obtain most of their carbon and nutrients from mycorrhizae. Saprophytic plants can be regarded as parasites on both mycorrhizae and nearby plants since the nutrients they obtain are sometimes transferred from other plants via mycorrhizae.19

Despite the ubiquitous parasitism and exploitation, mycorrhizae often maintain a stable mutualistic relationship with plants. How such a relationship is stabilised is still under research, but existing evidence has supported a number of hypotheses. For example, Hoeksema and Kummel found that plants can control root mortality to sanction exploitative fungi.20 Such evidence supports the hypothesis that mutualism can be stabilised by differentially sanctioning exploiters or rewarding cooperators.21 The mutualistic relationship between plants and mycorrhizae is also proposed as a “market economy”, in which both plants and mycorrhiza are able to detect the difference in the resources supplied by the symbiotic partner and adjust the amount of resources they provide to the partner accordingly.22 Kiers et al. strengthened this hypothesis experimentally by finding that plants would supply more carbon to more cooperative fungal species, and AM fungi that are being rewarded carbon resources by the host plants supplied greater P resources to the host plant.22 Such kind of mutualism, in another word, is maintained in a bidirectional way that both parties reward mutualism and sanction exploiters.

There may not be a clear distinction between “mutualistic” and “parasitic” mycorrhiza in mycorrhizae’s world. The study of mycorrhiza is still in the beginning, and we have just started to realise the complexity of the soil ecosystem, such as the interaction and signalling between mycorrhizae and soil bacteria revealed in a recent study.13 Although there is no conclusive evidence suggesting that using mycorrhiza will promote plant growth in agricultural practices, mycorrhiza can positively influence plants if factors such as the species of plants and mycorrhizae and soil conditions are taken into consideration. The research of mycorrhizae will also be an important step in understanding soil biodiversity and the signalling mechanism between soil organisms.

References:

1.           Bonfante P, Anca IA. Plants, Mycorrhizal Fungi, and Bacteria: A Network of Interactions. Annual Review of Microbiology. 2009;63(1):363–83.

2.           Olsson PA, Thingstrup I, Jakobsen I, Bååth E. Estimation of the biomass of arbuscular mycorrhizal fungi in a linseed field. Soil Biology and Biochemistry. 1999 Nov 1;31(13):1879–87.

3.           Egger KN, Hibbett DS. The evolutionary implications of exploitation in mycorrhizas. Can J Bot. 2004 Aug 1;82(8):1110–21.

4.           Smith SE, Read DJ. Mycorrhizal Symbiosis. Academic Press; 2010. 815 p.

5.           Lu X, Koide RT. The effects of mycorrhizal infection on components of plant growth and reproduction. New Phytologist. 1994;128(2):211–8.

6.           Gupta RK, Kumar P. Mycorrhizal Plants in Response to Adverse Environmental Conditions. In: Mukerji KG, Chamola BP, Singh J, editors. Mycorrhizal Biology [Internet]. Boston, MA: Springer US; 2000 [cited 2022 May 19]. p. 67–84. Available from: https://doi.org/10.1007/978-1-4615-4265-0_5

7.           Ricken B, Höfner W. Bedeutung der arbuskulären Mykorrhiza (AM) für die Schwermetalltoleranz von Luzerne (Medicago Sativa L.) und Hafer (Avena sativa L.) auf einem klärschlammgedüngten Boden. Zeitschrift für Pflanzenernährung und Bodenkunde. 1996;159(2):189–94.

8.           Harrison MJ. Signaling in the Arbuscular Mycorrhizal Symbiosis. Annual Review of Microbiology. 2005;59(1):19–42.

9.           Harrison MJ, Buuren ML van. A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature. 1995 Dec;378(6557):626–9.

10.         Smith SE, Read D, editors. Mycorrhizal Symbiosis (Third Edition). In: Mycorrhizal Symbiosis (Third Edition) [Internet]. London: Academic Press; 2008 [cited 2022 May 20]. p. 637–768. Available from: https://www.sciencedirect.com/science/article/pii/B9780123705266500209

11.         Čatská V. Smith, S.E., Read, D.J.: Mycorrhizal Symbiosis. Biologia Plantarum. 1997 Jul 1;40(1):154–154.

12.         Moradi M, Naji HR, Imani F, Moradi Behbahani S, Ahmadi MT. Arbuscular mycorrhizal fungi changes by afforestation in sand dunes. Journal of Arid Environments. 2017 May 1;140:14–9.

13.         Rose SL, Youngberg CT. Tripartite associations in snowbrush ( Ceanothus velutinus ): effect of vesicular–arbuscular mycorrhizae on growth, nodulation, and nitrogen fixation. Can J Bot. 1981 Jan 1;59(1):34–9.

14.         Klironomos JN. Variation in Plant Response to Native and Exotic Arbuscular Mycorrhizal Fungi. Ecology. 2003;84(9):2292–301.

15.         Johnson NC. Can Fertilization of Soil Select Less Mutualistic Mycorrhizae? Ecological Applications. 1993;3(4):749–57.

16.         Simard SW, Jones MD, Durall DM. Carbon and Nutrient Fluxes Within and Between Mycorrhizal Plants. In: van der Heijden MGA, Sanders IR, editors. Mycorrhizal Ecology [Internet]. Berlin, Heidelberg: Springer; 2003 [cited 2022 May 20]. p. 33–74. (Ecological Studies). Available from: https://doi.org/10.1007/978-3-540-38364-2_2

17.         Simard SW, Beiler KJ, Bingham MA, Deslippe JR, Philip LJ, Teste FP. Mycorrhizal networks: Mechanisms, ecology and modelling. Fungal Biology Reviews. 2012 Apr 1;26(1):39–60.

18.         Butterfield BJ. Effects of facilitation on community stability and dynamics: synthesis and future directions. Journal of Ecology. 2009;97(6):1192–201.

19.         Bidartondo MI, Redecker D, Hijri I, Wiemken A, Bruns TD, Domínguez L, et al. Epiparasitic plants specialized on arbuscular mycorrhizal fungi. Nature. 2002 Sep;419(6905):389–92.

20.         Hoeksema JD, Kummel M. Ecological Persistence of the Plant‐Mycorrhizal Mutualism: A Hypothesis from Species Coexistence Theory. The American Naturalist. 2003 Oct;162(S4):S40–50.

21.         Yu TE, Egger KN, Peterson LR. Ectendomycorrhizal associations – characteristics and functions. Mycorrhiza. 2001 Sep 1;11(4):167–77.

22.         Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, et al. Reciprocal Rewards Stabilize Cooperation in the Mycorrhizal Symbiosis. Science. 2011 Aug 12;333(6044):880–2.

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