Biology:Plant to plant communication via mycorrhizal networks

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Short description: Connections through mycorrhizal networks that facilitate communication between plants

Plants communicate via mycorrhizal networks with other plants of the same or different species. Mycorrhizal networks allow for the transfers of signals and cues between plants which influence the behavior of the connected plants by inducing morphological or physiological changes. The chemical substances which act as these signals and cues are referred to as infochemicals. These can be allelochemicals, defensive chemicals or nutrients. Allelochemicals are used by plants to interfere with the growth or development of other plants or organisms, defensive chemicals can help plants in mycorrhizal networks defend themselves against attack by pathogens or herbivores, and transferred nutrients can affect growth and nutrition. Results of studies which demonstrate these modes of communication have led the authors to hypothesize mechanisms by which the transfer of these nutrients can affect the fitness of the connected plants.

Mycorrhizal networks

Plants and fungi form mutualistic symbiotic relationships called mycorrhizae, which take several forms, such as arbuscular mycorrhizae (AM) and ectomycorrhizae (ECM), and are widespread in nature.[1][2][3] Host plants provide photosynthetically derived carbohydrates to the mycorrhizal fungi, which use them in metabolism, either for energy or to increase the size of their hyphal networks; and the fungal partner provides benefits to the plant in the form of improved uptake of soil derived nutrients, drought resistance, and increased resistance to soil and foliar pathogens and other organisms.[2][4][5]

The physical unit created by interconnected networks of mycorrhizal fungal hyphae connecting plants of the same or different species is termed a common mycorrhizal network (CMN), or simply a mycorrhizal network, and it provides benefits to both partners.[6][7] Mycorrhizal networks are created by the fungal partner and can range in size from square centimeters to tens of square meters and can be initiated by either AM or ECM fungi.[6] AM networks tend to be less expansive than ECM networks, but AM networks can attach many plants, because AM fungi tend to be less specific in which host they choose and, therefore, can create wider networks.[2][8][9] In the establishment of AM networks, hyphae can either directly attach to different host plants or they can establish connections between different fungi by way of anastomoses.[10]

Communication

Reports discuss the ongoing debate within the scientific community regarding what constitutes communication, but the extent of communication influences how a biologist perceives behaviors.[11] Communication is commonly defined as imparting or exchanging information. Biological communication, however, is often defined by how fitness in an organism is affected by the transfer of information in both the sender and the receiver.[11][12] Signals are the result of evolved behavior in the sender and effect a change in the receiver by imparting information about the sender's environment. Cues are similar in origin but only effect the fitness of the receiver.[12] Both signals and cues are important elements of communication, but workers maintain caution as to when it can be determined that transfer of information benefits both senders and receivers. Thus, the extent of biological communication can be in question without rigorous experimentation.[12] It has, therefore, been suggested that the term infochemical be used for chemical substances which can travel from one organism to another and elicit changes. This is important to understanding biological communication where it is not clearly delineated that communication involves a signal that can be adaptive to both sender and receiver.[3]

Behavior and information transfer

A morphological or physiological change in a plant due to a signal or cue from its environment constitutes behavior in plants, and plants connected by a mycorrhizal network have the ability to alter their behavior based on the signals or cues they receive from other plants.[1] These signals or cues can be biochemical, electrical, or can involve nutrient transfer.[1] Plants release chemicals both above- and below-ground to communicate with their neighbors to reduce damage from their environment.[13] Changes in plant behavior invoked by the transfer of infochemicals vary depending on environmental factors, the types of plants involved and the type of mycorrhizal network.[1][14] In a study of orange seedlings, mycorrhizal networks acted to transfer infochemicals, and the presence of a mycorrhizal network affected the growth of plants and enhanced production of signaling molecules.[4] One argument in support of the claim mycorrhizal can transfer various infochemicals is that they have been show to transfer molecules such as lipids, carbohydrates and amino acids.[8] Thus, transfer of infochemicals via mycorrhizal networks can act to influence plant behavior.

There are three main types of infochemicals shown to act as response inducing signals or cues by plants in mycorrhizal networks, as evidenced by increased effects on plant behavior: allelochemicals, defensive chemicals and nutrients.

Allelopathic communication

Allelopathy

Allelopathy is the process by which plants produce secondary metabolites known as allelochemicals, which can interfere with the development of other plants or organisms.[14] Allelochemicals can affect nutrient uptake, photosynthesis and growth; furthermore, they can down regulate defense genes, affect mitochondrial function, and disrupt membrane permeability leading to issues with respiration.[14]

Allelochemicals

Plants produce many types of allelochemicals, such as thiopenes and juglone, which can be volatilized or exuded by the roots into the rhizosphere.[10] Plants release allelochemicals due to biotic and abiotic stresses in their environment and often release them in conjunction with defensive compounds.[14] In order for allelochemicals to have a detrimental effect on a target plant, they must exist in high enough concentrations to be toxic, but, much like animal pheromones, allelochemicals are released in very small amounts and rely on the reaction of the target plant to amplify their effects.[10][14] Due to their lower concentrations and the ease in which they are degraded in the environment, the toxicity of allelochemicals is limited by soil moisture, soil structure, and organic matter types and microbes present in soils.[10] The effectiveness of allelopathic interactions has been called into question in native habitats due to the effects of them passing through soils, but studies have shown that mycorrhizal networks make their transfer more efficient.[3] These infochemicals are hypothesized be able to travel faster via mycorrhizal networks, because the networks protect them from some hazards of being transmitted through the soil, such as leaching and degradation.[3][7] This increased transfer speed is hypothesized to occur if the allelochemicals move via water on hyphal surfaces or by cytoplasmic streaming.[3][10] Studies have reported concentrations of allelochemicals two to four times higher in plants connected by mycorrhizal networks.[3][7] Thus, mycorrhizal networks can facilitate the transfer of these infochemicals.

Communication

Studies have demonstrated correlations between increased levels of allelochemicals in target plants and the presence of mycorrhizal networks. These studies strongly suggest that mycorrhizal networks increase the transfer of allelopathic chemicals and expand the range, called the bio-active zone, in which they can disperse and maintain their function.[3] Furthermore, studies indicate increased bio-active zones aid in the effectiveness of the allelochemicals because these infochemicals cannot travel very far without a mycorrhizal network.[7] There was greater accumulation of allelochemicals, such as thiopenes and the herbicide imazamox, in target plants connected to a supplier plant via a mycorrhizal network than without that connection, supporting the conclusion that the mycorrhizal network increased the bio-active zone of the allelochemical.[3] Allelopathic chemicals have also been demonstrated to inhibit target plant growth when target and supplier are connected via AM networks.[3] The black walnut is one of the earliest studied examples of allelopathy and produces juglone, which inhibits growth and water uptake in neighboring plants.[10] In studies of juglone in black walnuts and their target species, the presence of mycorrhizal networks caused target plants to exhibit reduced growth by increasing the transfer of the infochemical.[10] Spotted knapweed, an allelopathic invasive species, provides further evidence of the ability of mycorrhizal networks to contribute to the transfer of allelochemicals. Spotted knapweed can alter which plant species a certain AM fungus prefers to connect to, changing the structure of the network so that the invasive plant shares a network with its target.[15] These and other studies provide evidence that mycorrhizal networks can facilitate the effects on plant behavior caused by allelochemicals.

Defensive communication

Overview

Mycorrhizal networks can connect many different plants and provide shared pathways by which plants can transfer infochemicals related to attacks by pathogens or herbivores, allowing receiving plants to react in the same way as the infected or infested plants.[7] A variety of plant derived substances act as these infochemicals.

Defensive reactions

When plants are attacked they can manifest physical changes, such as strengthening their cell walls, depositing callose, or forming cork.[16] They can also manifest biochemical changes, including the production of volatile organic compounds (VOCs) or the up-regulation of genes producing other defensive enzymes, many of which are toxic to pathogens or herbivores.[2][16][17][18] Salicylic acid (SA) and its derivatives, like methyl salicylate, are VOCs which help plants to recognize infection or attack and to organize other plant defenses, and exposure to them in animals can cause pathological processes.[17][19] Terpenoids are produced constituently in many plants or are produced as a response to stress and act much like methyl salicylate.[19] Jasmonates are a class of VOCs produced by the jasmonic acid (JA) pathway. Jasmonates are used in plant defense against insects and pathogens and can cause the expression of proteases, which defend against insect attack.[18] Plants have many ways to react to attack, including the production of VOCs, which studies report can coordinate defenses among plants connected by mycorrhizal networks.

Communication

Many studies report that mycorrhizal networks facilitate the coordination of defenses between connected plants using volatile organic compounds and other plant defensive enzymes acting as infochemicals.

Priming occurs when a plant's defenses are activated before an attack. Studies have shown that priming of plant defenses among plants in mycorrhizal networks may be activated by the networks, as they make it easier for these infochemicals to propagate among the connected plants. The defenses of uninfected plants are primed by their response via the network to the terpenoids produced by the infected plants.[20] AM networks can prime plant defensive reactions by causing them to increase the production of terpinoids.[20]

In a study of tomato plants connected via an AM mycorrhizal network, a plant not infected by a fungal pathogen showed evidence of defensive priming when another plant in the network was infected, causing the uninfected plant to up-regulate genes for the SA and JA pathways.[2] Similarly, aphid-free plants were shown to only be able to express the SA pathways when a mycorrhizal network connected them to infested plants. Furthermore, only then did they display resistance to the herbivore, showing that the plants were able to transfer defensive infochemicals via the mycorrhizal network.[5]

Many insect herbivores are drawn to their food by VOCs. When the plant is consumed, however, the composition of the VOCs change, which can then cause them to repel the herbivores and attract insect predators, such as parasitoid wasps.[19] Methyl salicylate was shown to be the primary VOC produced by beans in a study which demonstrated this effect. It was found to be in high concentrations in infested and uninfested plants, which were only connected via a mycorrhizal network.[5] A plant sharing a mycorrhizal network with another that is attacked will display similar defensive strategies, and its defenses will be primed to increase the production of toxins or chemicals which repel attackers or attract defensive species.[2]

In another study, introduction of budworm to Douglas fir trees led to increased production of defensive enzymes in uninfested ponderosa pines connected to the damaged tree by an ECM network. This effect demonstrates that defensive infochemicals transferred through such a network can cause rapid increases in resistance and defense in uninfested plants of a different species.[13]

The results of these studies support the conclusion that both ECM and AM networks provide pathways for defensive infochemicals from infected or infested hosts to induce defensive changes in uninfected or uninfested conspecific and heterospecific plants, and that some recipient species generally receive less damage from infestation or infection.[1][2][8][13]

Nutrient communication

Overview

Numerous studies have reported that carbon, nitrogen and phosphorus are transferred between conspecific and heterospecific plants via AM and ECM networks.[2][13][21][22] Other nutrients may also be transferred, as strontium and rubidium, which are calcium and potassium analogs respectively, have also been reported to move via an AM network between conspecific plants.[23] Workers believe that transfer of nutrients by way of mycorrhizal networks could act to alter the behavior of receiving plants by inducing physiological or biochemical changes, and there is evidence that these changes have improved nutrition, growth and survival of receiving plants.[13]

Mechanisms

Several mechanisms have been observed and proposed by which nutrients can move between plants connected by a mycorrhizal network, including source-sink relationships, preferential transfer and kin related mechanisms.

Transfer of nutrients can follow a source-sink relationship where nutrients move from areas of higher concentration to areas of lower concentration.[1] An experiment with grasses and forbs from a California oak woodland showed that nutrients were transferred between plant species via an AM mycorrhizal network, with different species acting as sources and sinks for different elements.[23] Nitrogen has also been shown to flow from nitrogen-fixing plants to non-nitrogen fixing plants through a mycorrhizal network following a source-sink relationship.[22]

It has been demonstrated that mechanisms exist by which mycorrhizal fungi can preferentially allocate nutrients to certain plants without a source-sink relationship.[24][25] Studies have also detailed bi-directional transfer of nutrients between plants connected by a network, and evidence indicates that carbon can be shared between plants unequally, sometimes to the benefit of one species over another.[9][22]

Kinship can act as another transfer mechanism. More carbon has been found to be exchanged between the roots of more closely related Douglas firs sharing a network than more distantly related roots.[6] Evidence is also mounting that micronutrients transferred via mycorrhizal networks can communicate relatedness between plants. Carbon transfer between Douglas fir seedlings led workers to hypothesize that micronutrient transfer via the network may have increased carbon transfer between related plants.[6][13]

Communication

These transfer mechanisms can facilitate movement of nutrients via mycorrhizal networks and result in behavioral modifications in connected plants, as indicated by morphological or physiological changes, due to the infochemicals being transmitted. One study reported a three-fold increase in photosynthesis in a paper birch transferring carbon to a Douglas fir, indicating a physiological change in the tree which produced the signal.[26] Photosynthesis was also shown to be increased in Douglas fir seedlings by the transport of carbon, nitrogen and water from an older tree connected by a mycorrhizal network.[27] Furthermore, nutrient transfer from older to younger trees on a network can dramatically increase growth rates of the younger receivers.[28] Physiological changes due to environmental stress have also initiated nutrient transfer by causing the movement of carbon from the roots of the stressed plant to the roots of a conspecific plant over a mycorrhizal network.[13] Thus, nutrients transferred through mychorrhizal networks act as signals and cues to change the behavior of the connected plants.

Evolutionary and adaptational perspectives

Overview

It is hypothesized that fitness is improved by the transfer of infochemicals through common mycorrhizal networks, as these signals and cues can induce responses which can help the receiver survive in its environment.[13] Plants and fungus have evolved heritable genetic traits which influence their interactions with each other, and experiments, such as one which revealed the heritability of mycorrhizal colonization in cowpeas, provide evidence.[1][29][30] Furthermore, changes in behavior of one partner in a mycorrhizal network can affect others in the network; thus, the mycorrhizal network can provide selective pressure to increase the fitness of its members.[1]

Adaptive mechanisms of mycorrhizal fungi and plants

Although they remain to be vigorously demonstrated, workers have suggested mechanisms which might explain how transfer of infochemicals via mycorrhizal networks may influence the fitness of the connected plants and fungi.

A fungus may preferentially allocate carbon and defensive infochemicals to plants that supply it more carbon, as this would help to maximize its carbon uptake.[13] This may happen in ecosystems where environmental stresses, such as climate change, cause fluctuations in the types of plants in the mycorrhizal network.[13] A fungus might also benefit its own survival by taking carbon from one host with a surplus and giving it to another in need, thus it would insure the survival of more potential hosts and leave itself with more carbon sources should a particular host species suffer.[1] Thus, preferential transfer could improve fungal fitness.

Plant fitness may also be increased in several ways. Relatedness may be a factor, as plants in a network are more likely to be related; therefore, kin selection might improve inclusive fitness and explain why a plant might support a fungus that helps other plants to acquire nutrients.[1][31] Receipt of defensive signals or cues from an infested plant would be adaptive, as the receiving plant would be able to prime its own defenses in advance of an attack by herbivores.[19] Allelopathic chemicals transferred via CMNs could also affect which plants are selected for survival by limiting the growth of competitors through a reduction of their access to nutrients and light.[3] Therefore, transfer of the different classes of infochemicals might prove adaptive for plants.

References

  1. ↑ 1.0 1.1 1.2 1.3 1.4 1.5 1.6 1.7 1.8 1.9 Gorzelak, Monika A.; Asay, Amanda K.; Pickles, Brian J.; Simard, Suzanne W. (2015). "Inter-plant communication through mycorrhizal networks mediates complex adaptive behaviour in plant communities". AoB Plants 7: plv050. doi:10.1093/aobpla/plv050. ISSN 2041-2851. PMID 25979966. 
  2. ↑ 2.0 2.1 2.2 2.3 2.4 2.5 2.6 2.7 Song, Yuan Yuan; Zeng, Ren Sen; Xu, Jian Feng; Li, Jun; Shen, Xiang; Yihdego, Woldemariam Gebrehiwot (2010-10-13). "Interplant Communication of Tomato Plants through Underground Common Mycorrhizal Networks". PLOS ONE 5 (10): e13324. doi:10.1371/journal.pone.0013324. ISSN 1932-6203. PMID 20967206. Bibcode: 2010PLoSO...513324S. 
  3. ↑ 3.0 3.1 3.2 3.3 3.4 3.5 3.6 3.7 3.8 3.9 Barto, E. Kathryn; Hilker, Monika; Müller, Frank; Mohney, Brian K.; Weidenhamer, Jeffrey D.; Rillig, Matthias C. (2011-11-14). "The Fungal Fast Lane: Common Mycorrhizal Networks Extend Bioactive Zones of Allelochemicals in Soils". PLOS ONE 6 (11): e27195. doi:10.1371/journal.pone.0027195. ISSN 1932-6203. PMID 22110615. Bibcode: 2011PLoSO...627195B. 
  4. ↑ 4.0 4.1 ZHANG, Yi-Can; LIU, Chun-Yan; WU, Qiang-Sheng (2017-05-12). "Mycorrhiza and Common Mycorrhizal Network Regulate the Production of Signal Substances in Trifoliate Orange (Poncirus trifoliata)". Notulae Botanicae Horti Agrobotanici Cluj-Napoca 45 (1): 43. doi:10.15835/nbha45110731. ISSN 1842-4309. 
  5. ↑ 5.0 5.1 5.2 Babikova, Zdenka; Gilbert, Lucy; Bruce, Toby J. A.; Birkett, Michael; Caulfield, John C.; Woodcock, Christine; Pickett, John A.; Johnson, David (2013-05-09). "Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack". Ecology Letters 16 (7): 835–843. doi:10.1111/ele.12115. ISSN 1461-023X. PMID 23656527. 
  6. ↑ 6.0 6.1 6.2 6.3 Simard, Suzanne W.; Beiler, Kevin J.; Bingham, Marcus A.; Deslippe, Julie R.; Philip, Leanne J.; Teste, François P. (2012-04-01). "Mycorrhizal networks: Mechanisms, ecology and modelling". Fungal Biology Reviews 26 (1): 39–60. doi:10.1016/j.fbr.2012.01.001. ISSN 1749-4613. 
  7. ↑ 7.0 7.1 7.2 7.3 7.4 Barto, E. Kathryn; Weidenhamer, Jeffrey D.; Cipollini, Don; Rillig, Matthias C. (2012-11-01). "Fungal superhighways: do common mycorrhizal networks enhance below ground communication?". Trends in Plant Science 17 (11): 633–637. doi:10.1016/j.tplants.2012.06.007. ISSN 1360-1385. PMID 22818769. 
  8. ↑ 8.0 8.1 8.2 Gilbert, L.; Johnson, D. (2017), "Plant–Plant Communication Through Common Mycorrhizal Networks", Advances in Botanical Research (Elsevier): pp. 83–97, doi:10.1016/bs.abr.2016.09.001, ISBN 9780128014318 
  9. ↑ 9.0 9.1 Simard, Suzanne W.; Perry, David A.; Jones, Melanie D.; Myrold, David D.; Durall, Daniel M.; Molina, Randy (1997-08-07). "Net transfer of carbon between ectomycorrhizal tree species in the field". Nature 388 (6642): 579–582. doi:10.1038/41557. ISSN 0028-0836. Bibcode: 1997Natur.388..579S. 
  10. ↑ 10.0 10.1 10.2 10.3 10.4 10.5 10.6 Achatz, Michaela; Morris, E. Kathryn; Müller, Frank; Hilker, Monika; Rillig, Matthias C. (2014-01-13). "Soil hypha-mediated movement of allelochemicals: arbuscular mycorrhizae extend the bioactive zone of juglone". Functional Ecology 28 (4): 1020–1029. doi:10.1111/1365-2435.12208. ISSN 0269-8463. 
  11. ↑ 11.0 11.1 SCOTT-PHILLIPS, T. C. (2008-01-18). "Defining biological communication". Journal of Evolutionary Biology 21 (2): 387–395. doi:10.1111/j.1420-9101.2007.01497.x. ISSN 1010-061X. PMID 18205776. 
  12. ↑ 12.0 12.1 12.2 Padje, Anouk van’t; Whiteside, Matthew D; Kiers, E Toby (2016-08-01). "Signals and cues in the evolution of plant–microbe communication". Current Opinion in Plant Biology 32: 47–52. doi:10.1016/j.pbi.2016.06.006. ISSN 1369-5266. PMID 27348594. https://research.vu.nl/en/publications/c745b0c0-7789-4fc5-8d93-3edfa94ec108. 
  13. ↑ 13.0 13.1 13.2 13.3 13.4 13.5 13.6 13.7 13.8 13.9 Song, Yuan Yuan; Simard, Suzanne W.; Carroll, Allan; Mohn, William W.; Zeng, Ren Sen (2015-02-16). "Defoliation of interior Douglas-fir elicits carbon transfer and stress signalling to ponderosa pine neighbors through ectomycorrhizal networks". Scientific Reports 5 (1): 8495. doi:10.1038/srep08495. ISSN 2045-2322. PMID 25683155. Bibcode: 2015NatSR...5E8495S. 
  14. ↑ 14.0 14.1 14.2 14.3 14.4 Latif, S.; Chiapusio, G.; Weston, L.A. (2017), "Allelopathy and the Role of Allelochemicals in Plant Defence", Advances in Botanical Research (Elsevier): pp. 19–54, doi:10.1016/bs.abr.2016.12.001, ISBN 9780128014318 
  15. ↑ Mummey, Daniel L.; Rillig, Matthias C. (2006-08-30). "The invasive plant species Centaurea maculosa alters arbuscular mycorrhizal fungal communities in the field". Plant and Soil 288 (1–2): 81–90. doi:10.1007/s11104-006-9091-6. ISSN 0032-079X. 
  16. ↑ 16.0 16.1 Prasannath, K. (2017-11-22). "Plant defense-related enzymes against pathogens: a review". AGRIEAST: Journal of Agricultural Sciences 11 (1): 38. doi:10.4038/agrieast.v11i1.33. ISSN 1391-5886. 
  17. ↑ 17.0 17.1 Lu, Hua (2009-08-01). "Dissection of salicylic acid-mediated defense signaling networks". Plant Signaling & Behavior 4 (8): 713–717. doi:10.4161/psb.4.8.9173. ISSN 1559-2324. PMID 19820324. 
  18. ↑ 18.0 18.1 Turner, John G.; Ellis, Christine; Devoto, Alessandra (2002-05-01). "The Jasmonate Signal Pathway". The Plant Cell 14 (suppl 1): S153–S164. doi:10.1105/tpc.000679. ISSN 1040-4651. PMID 12045275. 
  19. ↑ 19.0 19.1 19.2 19.3 Dempsey, D’Maris Amick; Klessig, Daniel F. (2017-03-23). "How does the multifaceted plant hormone salicylic acid combat disease in plants and are similar mechanisms utilized in humans?". BMC Biology 15 (1): 23. doi:10.1186/s12915-017-0364-8. ISSN 1741-7007. PMID 28335774. 
  20. ↑ 20.0 20.1 Sharma, Esha; Anand, Garima; Kapoor, Rupam (2017-01-12). "Terpenoids in plant and arbuscular mycorrhiza-reinforced defence against herbivorous insects". Annals of Botany 119 (5): 791–801. doi:10.1093/aob/mcw263. ISSN 0305-7364. PMID 28087662. 
  21. ↑ Philip, Leanne; Simard, Suzanne; Jones, Melanie (2010-09-22). "Pathways for below-ground carbon transfer between paper birch and Douglas-fir seedlings". Plant Ecology & Diversity 3 (3): 221–233. doi:10.1080/17550874.2010.502564. ISSN 1755-0874. 
  22. ↑ 22.0 22.1 22.2 Selosse, Marc-André; Richard, Franck; He, Xinhua; Simard, Suzanne W. (2006-11-01). "Mycorrhizal networks: des liaisons dangereuses?". Trends in Ecology & Evolution 21 (11): 621–628. doi:10.1016/j.tree.2006.07.003. ISSN 0169-5347. PMID 16843567. 
  23. ↑ 23.0 23.1 Meding, S.M.; Zasoski, R.J. (2008-01-01). "Hyphal-mediated transfer of nitrate, arsenic, cesium, rubidium, and strontium between arbuscular mycorrhizal forbs and grasses from a California oak woodland". Soil Biology and Biochemistry 40 (1): 126–134. doi:10.1016/j.soilbio.2007.07.019. ISSN 0038-0717. 
  24. ↑ Fellbaum, Carl R.; Mensah, Jerry A.; Cloos, Adam J.; Strahan, Gary E.; Pfeffer, Philip E.; Kiers, E. Toby; Bücking, Heike (2014-05-02). "Fungal nutrient allocation in common mycorrhizal networks is regulated by the carbon source strength of individual host plants". New Phytologist 203 (2): 646–656. doi:10.1111/nph.12827. ISSN 0028-646X. PMID 24787049. 
  25. ↑ Kiers, E. T.; Duhamel, M.; Beesetty, Y.; Mensah, J. A.; Franken, O.; Verbruggen, E.; Fellbaum, C. R.; Kowalchuk, G. A. et al. (2011-08-11). "Reciprocal Rewards Stabilize Cooperation in the Mycorrhizal Symbiosis". Science 333 (6044): 880–882. doi:10.1126/science.1208473. ISSN 0036-8075. PMID 21836016. Bibcode: 2011Sci...333..880K. https://semanticscholar.org/paper/634db4c306fa3a357f08dbe5276ed7ae9a4efe73. 
  26. ↑ SIMARD, SUZANNE W.; JONES, MELANIE D.; DURALL, DANIEL M.; PERRY, DAVID A.; MYROLD, DAVID D.; MOLINA, RANDY (2008-06-28). "Reciprocal transfer of carbon isotopes between ectomycorrhizal Betula papyrifera and Pseudotsuga menziesii". New Phytologist 137 (3): 529–542. doi:10.1046/j.1469-8137.1997.00834.x. ISSN 0028-646X. PMID 33863069. 
  27. ↑ Teste, François P.; Simard, Suzanne W.; Durall, Daniel M.; Guy, Robert D.; Berch, Shannon M. (2010-01-25). "Net carbon transfer betweenPseudotsuga menziesiivar.glaucaseedlings in the field is influenced by soil disturbance". Journal of Ecology 98 (2): 429–439. doi:10.1111/j.1365-2745.2009.01624.x. ISSN 0022-0477. 
  28. ↑ Teste, François P.; Simard, Suzanne W.; Durall, Daniel M.; Guy, Robert D.; Jones, Melanie D.; Schoonmaker, Amanda L. (2009-10-01). "Access to mycorrhizal networks and roots of trees: importance for seedling survival and resource transfer". Ecology 90 (10): 2808–2822. doi:10.1890/08-1884.1. ISSN 0012-9658. PMID 19886489. 
  29. ↑ ROSADO, S. C. S.; KROPP, B. R.; PICHÉ, Y. (1994-01-01). "Genetics of ectomycorrhizal symbiosis". New Phytologist 126 (1): 111–117. doi:10.1111/j.1469-8137.1994.tb07544.x. ISSN 0028-646X. 
  30. ↑ Mercy, M. A.; Shivashankar, G.; Bagyaraj, D. J. (1989-04-25). "Mycorrhizal colonization in cowpea is host dependent and heritable". Plant and Soil 122 (2): 292–294. doi:10.1007/bf02444245. ISSN 0032-079X. 
  31. ↑ File, Amanda L.; Klironomos, John; Maherali, Hafiz; Dudley, Susan A. (2012-09-28). "Plant Kin Recognition Enhances Abundance of Symbiotic Microbial Partner". PLOS ONE 7 (9): e45648. doi:10.1371/journal.pone.0045648. ISSN 1932-6203. PMID 23029158. Bibcode: 2012PLoSO...745648F. 




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