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Utopia & Lost Futures: Symbiosis between Crops and Fungi

A glimpse into plant basic research and how it affects modern agriculture.



June 2022. Lecture notes from Barbara Brunschweiger


Introduction

I do not want to bore you. I do not want to talk about why climate change is threatening food security and that research is now funded to improve crop stability and soil health. I want to talk about the fascination, the thrill to uncover tiny bits in the complexity of biological processes in the environment – tiny pieces, that plant scientists try to discover and understand. And with this understanding, maybe aid a shift in agriculture practices so that others can do the hard work and provide us with food.



The tree

Why is researching the fundamental interactions in an environment so difficult? Let’s take a tree. Let’s assume that it successfully germinated in the soil and got carried through tree “adolescence” into tree “adulthood”. It is a normal, healthy tree. Its growth and survival are dependent on abiotic factors like sun light, water, wind, and temperature – to just the right degree. It needs adequate soil composition and nutrient availability which are shaped by worms, bacteria, and fungi. Other biotic factors can threaten tree survival, like insect attacks and infection with pathogenic bacteria and viruses. All these factors do interact with each other, leading to synergetic or diminished effects, weaving an interplay network too complex to grasp – until now?


How do trees handle multiple stressors? Trees are adaptive, and not defenseless by themselves. They have an innate immune system and can change their physiology in response to dangers like water deficiency, light deprivation, and sunburns. Moreover, they do not face threats alone – they form symbiosis with other trees regardless of which species, and they employ more helpers. Like fungi. In the soil.



Terms

Let’s get some terminology done: Symbiosis. Symbiosis just means that two living things interact with each other. This can be either good or bad for the host (aka the plant). If it is a parasitic (bad) symbiosis, only the intruder benefits and the host suffers – like mistle toes growing in tree crowns, draining water and nutrients from the host tree. But often disregarded in science are supportive interactions, mutualistic symbiosis like plant-fungi mycorrhiza, which is beneficial for both parties.


So what is mycorrhiza? Mycorrhiza (myco = fungi, rhiza = root) is a general term for belowground symbiosis between plants and fungi. It manifests when mycelium, the delicate thread-like hyphae of fungi connects with the plant roots. If the mycelium only encloses the plant roots, it is called ectomycorrhiza - formed between 10% of all plant species, predominantly woody species like trees. In endomycorrhiza, the fungi hyphae penetrates the plant root cell. A particularly fascinating form of endomycorrhiza is called arbuscular mycorrhiza; a symbiosis which is formed by 80% of all land plants such as crops and legumes and which is fricking old - It has been established over 500 Mio years of coevolution. And we only obtained knowledge in 50 years of research [1].


But we do know stuff and already figured out quite a bit:


1. The HOW: How does this symbiosis manifests? [2]

In the soil, the plant elongates its roots in search for water and nutrients. But there is only so much ground it can cover, depths to reach and physiological modifications to make, considering the trade-off between cellular growth and resource availability. That’s when the plant calls for help. With plant hormones. These soluble molecules are released into the soil and trigger fungi spores, abundant in the near vicinity, to grow mycelium, scouting for the hormone source. Once reaching the plant root, physical contact triggers a cascade of molecular responses and cellular modifications in the plant root – all to ensure that the fungi hyphae can penetrate the sturdy root epidermis. Once breaching this barrier, the hyphae sprouts between cell layers until finding a suitable root cell to enter and form arbuscules. These tiny, tree-like looking fungi structures are the place where the magic happens – but WHAT? and WHY?


2. The WHAT and WHY[2]

It’s rather simple. The plant captures carbon from the atmosphere by photosynthesis and produces sugar with it. The fungi, capable to produce seemingly endless mycelium highways through the soil, reaches water and soluble nutrients like phosphorus and nitrogen easily, but requires energy. So they arrange a trade-off, where the arbuscules in the root cells are the interface, the table: here the fungi releases nutrients and water in exchange for soluble sugars. The available water and nutrients are needed by the plant for cellular growth. The cool thing is – that’s not the only benefit for the plant: the presence of mycorrhiza and trading molecules increases pathogen resistance to biotic factors like insects and bacteria. It increases tolerance to drought and high concentrations of salt that would otherwise drain water from the cells. For ectomycorrhiza of trees, there is even evidence that they use the fungi like phone wires to communicate with each other– the so-called WOOD WIDE WEB! [3]



Ambiguity in research

I do have a confession to make. I made it sound as if we researchers are know-it-alls and are sure about everything. Which we are not. Which we never truly are. On some occasions, we can say more confidently: that is probably how it works. We are fairly certain that the trade is beneficial for both fungi and plant. We know some (but probably not all) of the necessary molecules that are exchanged[2]: sugars like sucrose and nutrients like nitrogen and phosphorus. We also know some of the molecules needed for the attraction of mycelium to the plant root. Like the plant hormone strigolactone and the Myc factor as fungal response. But we certainly do not have an overview of the whole molecular cascade, which element affects which, triggering which event. Not even mentioning the influence of the environment growing stage and soil composition. We know what we can see (when grown under controlled conditions) – we know the beginning and the result and are just figuring out the path in between.


But that’s the beauty of science – there is always more to see and to discover in the complexity of things. And I am a great advocate to demystify science and to go against the common misconception that research results are final, indefinite, and undisputable. But let’s go back to agriculture and take it as an example of the influence of fundamental research.


So far, we agreed that mycorrhiza is good, that we want more of it to have healthier, better crops – and that we have evidence that it helps with the nutrition of the plant and could therefore reduce the amount of fertilizer needed to apply on fields. On field soil, where we disturb the natural abundance of fungi with our traditional agriculture techniques like frequent tillage, applying fertilizer and using annual crops, applying more mycorrhiza spores would be beneficial for all parties. Right? …. Maybe not? Let’s say, there are divided opinions.


Early meta-analysis papers [4,5] (which is like a summary of all known experiments regarding a research question until the date it is published) of laboratory, greenhouse and field experiments conclude that with mycorrhiza, we have better yield and healthier plants on the fields. Significantly. But in 2018, a contradictory review paper [6] was published – commenting on the so-far conducted meta-analyses, criticizing the methodology and conclusions that were drawn from the results. They claimed with very clear words that the benefits of mycorrhiza promotion in farming are overrepresented and overestimated. This very salty paper provoked an immediate response from authors of the early review papers [7] and researchers hold on to contrasting views to this day.


The argument of the contradictory paper reveals a common problem that we face in science: Comparing apples with oranges. This can be avoided if every researcher would use the same methods, calculates the results in the same way, looks at the same parameters and, in the best-case scenario, looks at all parameters without being selective. That is almost impossible. Another problem is: comparing results from lab and greenhouse experiments with actual conditions on the fields. Research in the laboratory, even in greenhouses is quite different than field experiments, where the influencing environment cannot be controlled. In lab or greenhouse experiments, if you want to investigate the effect of mycorrhiza on crop yield, you can manipulate outside parameters like water availability, sun light and temperature, soil composition and mycorrhiza occurrence, making it the same for all plants. Without having to account for the influence of these parameters, comparing the yield from plants grown with mycorrhiza to the yield of no-mycorrhiza plants is greatly facilitated and normally delivers significant results. Don’t get me wrong – lab and greenhouse trials are more detached from real-life conditions but enable us to pick out single parameters and shed light on certain aspects of biological processes. In comparison, field trials that are closer to common agriculture practices often lack the cleanness of results, as we cannot control said parameters and it is hard to monitor all relevant factors, if we even know them. Significance suffers – making the results more diluted, where we can only be certain about strong changes and clear influences. What I want to say is that laboratory and greenhouse experiments are important to discover detail knowledge about plant biology, whereas field trials deliver the reality check in nature – but extrapolating results from greenhouse experiments onto the field is not always possible.



Bottom-line

To this day, scientists argue about the merits of mycorrhiza in agriculture. Making it hard for policy makers to promote application of mycorrhiza spores in fields, and leaving farmers with the fear of yield losses, powerless in the face of increasingly extreme weather conditions. While research progresses and new results in science are constantly generated, the public and farmers are demanding changes – but changes are slow to implement. Ambiguity in research is, in my opinion, one reason that agriculture is still predominantly conservative (with high-tech upgrades like GPS controlled tractors and drone observation). I do not want to go too deep here – as I don’t know the agriculture, the real-life crop production, as I do know fundamental science (which is honestly also very limited). But I know that science is thriving, technology is advancing, and the will is there to change – to adapt, like plants adapting to the sun and the wind.



Note: Did I make you curious? I didn`t talk about what my research really was about. Or the methods that are used in the molecular or the applied science world. Even though I love talking about myself and what I do, I considered it to be too complex to summarize it on only a few pages. And generalizing it would honestly be too boring. I am happy to tell you more about plant science, in whatever subject you are interested (and I am knowledgeable) in and maybe discuss a thing or two.

Feel free to contact info@assoziation-e.org, they will forward your request to me :))



References

[1] L. A. Harrier, “The arbuscular mycorrhizal symbiosis: A molecular review of the fungal dimension,” J. Exp. Bot., vol. 52, no. SPEC. ISS. MAR., pp. 469–478, 2001, doi: 10.1093/jxb/52.suppl_1.469.

[2] M. Parniske, “Arbuscular mycorrhiza: The mother of plant root endosymbioses,” Nat. Rev. Microbiol., vol. 6, no. 10, pp. 763–775, 2008, doi: 10.1038/nrmicro1987.

[3] S. W. Simard, D. A. Perry, M. D. Jones, D. D. Myrold, D. M. Durall, and R. Molina, “Net transfer of carbon between ectomycorrhizal tree species in the field,” Nature, vol. 388, no. August, pp. 579–582, 1997, https://doi.org/10.1038/41557.

[4] Y. Lekberg and R. T. Koide, “Is plant performance limited by abundance of arbuscular mycorrhizal fungi? A meta-analysis of studies published between 1988 and 2003,” New Phytol., vol. 168, no. 1, pp. 189–204, 2005, doi: 10.1111/j.1469-8137.2005.01490.x.

[5] E. Pellegrino, M. Öpik, E. Bonari, and L. Ercoli, “Responses of wheat to arbuscular mycorrhizal fungi: A meta-analysis of field studies from 1975 to 2013,” Soil Biol. Biochem., vol. 84, pp. 210–217, 2015, doi: 10.1016/j.soilbio.2015.02.020.

[6] M. H. Ryan and J. H. Graham, “Little evidence that farmers should consider abundance or diversity of arbuscular mycorrhizal fungi when managing crops,” New Phytol., vol. 220, no. 4, pp. 1092–1107, 2018, doi: 10.1111/nph.15308.

[7] M. C. Rillig et al., “Why farmers should manage the arbuscular mycorrhizal symbiosis,” New Phytol., vol. 222, no. 3, pp. 1171–1175, 2019, doi: 10.1111/nph.15602.


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