Networking via mycorrhizae
Xiaofan MA, Erik LIMPENS
Networking via mycorrhizae
● Evidence for interplant communication via common mycorrhizal networks is reviewed. | |
● Potential transport routes for semiochemicals via fungal hyphae are identified. | |
● Drivers of signal exchange via CMNs are discussed. |
Interplant communication is of vital importance for plant performance in natural environments. Mycorrhizal fungi have emerged as key contributors to the below ground communication between plants. These mutualistic fungi form connections between the roots of plants via their hyphae, known as common mycorrhizal networks (CMNs). These hyphal networks are thought to be important ways for the exchange of signals between plants. This paper reviews the evidence for CMN-based transfer of semiochemicals between plants upon exposure to pathogen infection, herbivory or mechanical damage. Potential transport routes are explored, asking whether the fungi can actively contribute to the distribution of such signals within the network and discussing potential drivers for signal exchange. It is concluded that identification of the signals that are exchanged remains an important challenge for the future.
Mycorrhizal fungi / common mycorrhizal network / signal transfer / defensive response
[1] |
Smith S E, Read D J. Introduction. In: Smith S E, Read D, eds. Mycorrhizal Symbiosis. 2nd ed. London: Academic press, 2010, 1–10
|
[2] |
Gilbert L, Johnson D . Plant-plant communication through common mycorrhizal networks. Advances in Botanical Research, 2017, 82: 83–97
CrossRef
Google scholar
|
[3] |
Massicotte H B, Peterson R, Ackerley C, Piché Y . Structure and ontogeny of Alnus crispa–Alpova diplophloeus ectomycorrhizae. Canadian Journal of Botany, 1986, 64(1): 177–192
CrossRef
Google scholar
|
[4] |
Gutjahr C, Parniske M . Cell and developmental biology of arbuscular mycorrhiza symbiosis. Annual Review of Cell and Developmental Biology, 2013, 29(1): 593–617
CrossRef
Google scholar
|
[5] |
Maya M A, Matsubara Y I . Influence of arbuscular mycorrhiza on the growth and antioxidative activity in cyclamen under heat stress. Mycorrhiza, 2013, 23(5): 381–390
CrossRef
Google scholar
|
[6] |
Van Wees S C, Van Der Ent S, Pieterse C M . Plant immune responses triggered by beneficial microbes. Current Opinion in Plant Biology, 2008, 11(4): 443–448
CrossRef
Google scholar
|
[7] |
Helgason T, Daniell T, Husband R, Fitter A H, Young J . Ploughing up the wood-wide web. Nature, 1998, 394(6692): 431
CrossRef
Google scholar
|
[8] |
Karst J, Jones M D, Hoeksema J D . Positive citation bias and overinterpreted results lead to misinformation on common mycorrhizal networks in forests. Nature Ecology & Evolution, 2023, 7(4): 501–511
CrossRef
Google scholar
|
[9] |
Henriksson N, Marshall J, Högberg M, Högberg P, Polle A, Franklin O, Näsholm T . Re-examining the evidence for the mother tree hypothesis—Resource sharing among trees via ectomycorrhizal networks. New Phytologist, 2023, 239(1): 19–28
CrossRef
Google scholar
|
[10] |
Klein T, Rog I, Livne-Luzon S, Van Der Heijden M G A, Körner C . Belowground carbon transfer across mycorrhizal networks among trees: facts, not fantasy. Open Research Europe, 2023, 3: 168
CrossRef
Google scholar
|
[11] |
Robinson D, Fitter A . The magnitude and control of carbon transfer between plants linked by a common mycorrhizal network. Journal of Experimental Botany, 1999, 50(330): 9–13
CrossRef
Google scholar
|
[12] |
Vohník M, Sadowsky J J, Kohout P, Lhotáková Z, Nestby R, Kolařík M . Novel root-fungus symbiosis in Ericaceae: sheathed ericoid mycorrhiza formed by a hitherto undescribed basidiomycete with affinities to Trechisporales. PLoS One, 2012, 7(6): e39524
CrossRef
Google scholar
|
[13] |
Leake J, Johnson D, Donnelly D, Muckle G, Boddy L, Read D . Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Canadian Journal of Botany, 2004, 82(8): 1016–1045
CrossRef
Google scholar
|
[14] |
Chagnon P L . Ecological and evolutionary implications of hyphal anastomosis in arbuscular mycorrhizal fungi. FEMS Microbiology Ecology, 2014, 88(3): 437–444
CrossRef
Google scholar
|
[15] |
Taylor A F . Common mycelial networks: life-lines and radical addictions. New Phytologist, 2006, 169(1): 6–8
CrossRef
Google scholar
|
[16] |
Egerton-Warburton L M, Querejeta J I, Allen M F . Common mycorrhizal networks provide a potential pathway for the transfer of hydraulically lifted water between plants. Journal of Experimental Botany, 2007, 58(6): 1473–1483
CrossRef
Google scholar
|
[17] |
Finlay R, Read D . The structure and function of the vegetative mycelium of ectomycorrhizal plants: I. Translocation of 14C-labelled carbon between plants interconnected by a common mycelium. New Phytologist, 1986, 103(1): 143–156
CrossRef
Google scholar
|
[18] |
Van Der Heijden M G, Horton T R . Socialism in soil? The importance of mycorrhizal fungal networks for facilitation in natural ecosystems. Journal of Ecology, 2009, 97(6): 1139–1150
CrossRef
Google scholar
|
[19] |
Cardini A, Pellegrino E, Declerck S, Calonne-Salmon M, Mazzolai B, Ercoli L . Direct transfer of zinc between plants is channelled by common mycorrhizal network of arbuscular mycorrhizal fungi and evidenced by changes in expression of zinc transporter genes in fungus and plant. Environmental Microbiology, 2021, 23(10): 5883–5900
CrossRef
Google scholar
|
[20] |
Bago B, Zipfel W, Williams R M, Jun J, Arreola R, Lammers P J, Pfeffer P E, Shachar-Hill Y . Translocation and utilization of fungal storage lipid in the arbuscular mycorrhizal symbiosis. Plant Physiology, 2002, 128(1): 108–124
CrossRef
Google scholar
|
[21] |
Cabral C, Wollenweber B, António C, Rodrigues A M, Ravnskov S . Aphid infestation in the phyllosphere affects primary metabolic profiles in the arbuscular mycorrhizal hyphosphere. Scientific Reports, 2018, 8(1): 14442
CrossRef
Google scholar
|
[22] |
Kachroo A, Kachroo P . Mobile signals in systemic acquired resistance. Current Opinion in Plant Biology, 2020, 58: 41–47
CrossRef
Google scholar
|
[23] |
Hodge A, Storer K . Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystems. Plant and Soil, 2015, 386(1−2): 1–19
CrossRef
Google scholar
|
[24] |
Walder F, Niemann H, Natarajan M, Lehmann M F, Boller T, Wiemken A . Mycorrhizal networks: common goods of plants shared under unequal terms of trade. Plant Physiology, 2012, 159(2): 789–797
CrossRef
Google scholar
|
[25] |
Fellbaum C R, Mensah J A, Cloos A J, Strahan G E, Pfeffer P E, Kiers E T, Bücking H . Fungal nutrient allocation in common mycorrhizal networks is regulated by the carbon source strength of individual host plants. New Phytologist, 2014, 203(2): 646–656
CrossRef
Google scholar
|
[26] |
Kiers E T, Duhamel M, Beesetty Y, Mensah J A, Franken O, Verbruggen E, Fellbaum C R, Kowalchuk G A, Hart M M, Bago A, Palmer T M, West S A, Vandenkoornhuyse P, Jansa J, Bücking H . Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science, 2011, 333(6044): 880–882
CrossRef
Google scholar
|
[27] |
Noë R, Hammerstein P . Biological markets. Trends in Ecology & Evolution, 1995, 10(8): 336–339
CrossRef
Google scholar
|
[28] |
Schwartz M W, Hoeksema J D . Specialization and resource trade: biological markets as a model of mutualisms. Ecology, 1998, 79(3): 1029–1038
CrossRef
Google scholar
|
[29] |
Weremijewicz J, Janos D P . Common mycorrhizal networks amplify size inequality in Andropogon gerardii monocultures. New Phytologist, 2013, 198(1): 203–213
CrossRef
Google scholar
|
[30] |
Bennett A E, Groten K . The costs and benefits of plant-arbuscular mycorrhizal fungal interactions. Annual Review of Plant Biology, 2022, 73(1): 649–672
CrossRef
Google scholar
|
[31] |
Figueiredo A F, Boy J, Guggenberger G . Common mycorrhizae network: a review of the theories and mechanisms behind underground interactions. Frontiers in Fungal Biology, 2021, 2: 735299
CrossRef
Google scholar
|
[32] |
Luo X, Liu Y N, Li S Y, He X H . Interplant carbon and nitrogen transfers mediated by common arbuscular mycorrhizal networks: beneficial pathways for system functionality. Frontiers in Plant Science, 2023, 14: 1169310
CrossRef
Google scholar
|
[33] |
Chamberlain K, Guerrieri E, Pennacchio F, Pettersson J, Pickett J A, Poppy G M, Powell W, Wadhams L J, Woodcock C M . Can aphid-induced plant signals be transmitted aerially and through the rhizosphere. Biochemical Systematics and Ecology, 2001, 29(10): 1063–1074
CrossRef
Google scholar
|
[34] |
Dicke M, Dijkman H . Within-plant circulation of systemic elicitor of induced defence and release from roots of elicitor that affects neighbouring plants. Biochemical Systematics and Ecology, 2001, 29(10): 1075–1087
CrossRef
Google scholar
|
[35] |
Alaux P L, Naveau F, Declerck S, Cranenbrouck S. Common mycorrhizal network induced JA/ET genes expression in healthy potato plants connected to potato plants infected by Phytophthora infestans. Frontiers in Plant Science, 2020, 11: 602
|
[36] |
Song Y Y, Ye M, Li C Y, He X H, Zhu-Salzman K, Wang R L, Su Y J, Luo S M, Zeng R S . Hijacking common mycorrhizal networks for herbivore-induced defence signal transfer between tomato plants. Scientific Reports, 2014, 4(1): 3915
CrossRef
Google scholar
|
[37] |
Song Y Y, Zeng R S, Xu J F, Li J, Shen X, Yihdego W G . Interplant communication of tomato plants through underground common mycorrhizal networks. PLoS One, 2010, 5(10): e13324
CrossRef
Google scholar
|
[38] |
Babikova Z, Gilbert L, Bruce T J, Birkett M, Caulfield J C, Woodcock C, Pickett J A, Johnson D . Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack. Ecology Letters, 2013, 16(7): 835–843
CrossRef
Google scholar
|
[39] |
Zhang Y C, Zou Y N, Liu L P, Wu Q S . Common mycorrhizal networks activate salicylic acid defense responses of trifoliate orange (Poncirus trifoliata). Journal of Integrative Plant Biology, 2019, 61(10): 1099–1111
CrossRef
Google scholar
|
[40] |
Zhang Y C, Liu L P, Zou Y N, Liu C Y, Wu Q S. Responses of signal substances to canker in trifoliate orange roots through mycorrhizal hyphal bridge. Mycosystema, 2017, 36(7): 1028-1036 (in Chinese)
|
[41] |
Barto E K, Hilker M, Müller F, Mohney B K, Weidenhamer J D, Rillig M C . The fungal fast lane: common mycorrhizal networks extend bioactive zones of allelochemicals in soils. PLoS One, 2011, 6(11): e27195
CrossRef
Google scholar
|
[42] |
Inderjit, Weston L A, Duke S O. Inderjit, Weston L A, Duke S O. Challenges, achievements and opportunities in allelopathy research. Journal of Plant Interactions, 2005, 1(2): 69−81
|
[43] |
Song Y Y, Simard S W, Carroll A, Mohn W W, Zeng R S . Defoliation of interior Douglas-fir elicits carbon transfer and stress signalling to ponderosa pine neighbors through ectomycorrhizal networks. Scientific Reports, 2015, 5(1): 8495
CrossRef
Google scholar
|
[44] |
Li S, Sina Y Z, Xu R, Zi S H, Fan L Y, Liu T. Defense signal transmission between alfalfa plants through underground mycorrhizal network. Journal of Tropical and Subtropical Botany, 2021, 29(4): 382−388 (in Chinese)
|
[45] |
Lian F Z, Lin Y B, Hu L, Wang J, Ceng R S, Song Y Y. Transfer of mechanical wounding signaling between tomato plants through common mycorrhizal networks. Journal of Fujian Agriculture and Forestry University (Natural Science Edition), 2019, 48(1): 9−15 (in Chinese)
|
[46] |
Song Y Y, Wang M, Zeng R S, Groten K, Baldwin I T . Priming and filtering of antiherbivore defences among Nicotiana attenuata plants connected by mycorrhizal networks. Plant, Cell & Environment, 2019, 42(11): 2945–2961
CrossRef
Google scholar
|
[47] |
Schweiger R, Baier M C, Persicke M, Müller C . High specificity in plant leaf metabolic responses to arbuscular mycorrhiza. Nature Communications, 2014, 5(1): 3886
CrossRef
Google scholar
|
[48] |
Jiang F Y, Zhang L, Zhou J C, George T S, Feng G . Arbuscular mycorrhizal fungi enhance mineralisation of organic phosphorus by carrying bacteria along their extraradical hyphae. New Phytologist, 2021, 230(1): 14–16
CrossRef
Google scholar
|
[49] |
de Novais C B, Sbrana C, Da Conceição Jesus E, Rouws L F M, Giovannetti M, Avio L, Siqueira J O, Saggin O J Junior, Da Silva E M R, De Faria S M . Mycorrhizal networks facilitate the colonization of legume roots by a symbiotic nitrogen-fixing bacterium. Mycorrhiza, 2020, 30(2−3): 389–396
CrossRef
Google scholar
|
[50] |
Tedersoo L, Bahram M, Zobel M . How mycorrhizal associations drive plant population and community biology. Science, 2020, 367(6480): eaba1223
CrossRef
Google scholar
|
[51] |
Barto E K, Weidenhamer J D, Cipollini D, Rillig M C . Fungal superhighways: do common mycorrhizal networks enhance below ground communication. Trends in Plant Science, 2012, 17(11): 633–637
CrossRef
Google scholar
|
[52] |
Johnson D, Gilbert L . Interplant signalling through hyphal networks. New Phytologist, 2015, 205(4): 1448–1453
CrossRef
Google scholar
|
[53] |
Allen M F . Mycorrhizal fungi: highways for water and nutrients in arid soils. Vadose Zone Journal, 2007, 6(2): 291–297
CrossRef
Google scholar
|
[54] |
van’t Padje A, Werner G D, Kiers E T . Mycorrhizal fungi control phosphorus value in trade symbiosis with host roots when exposed to abrupt ‘crashes’ and ‘booms’ of resource availability. New Phytologist, 2021, 229(5): 2933–2944
CrossRef
Google scholar
|
[55] |
Mousavi S A, Chauvin A, Pascaud F, Kellenberger S, Farmer E E . GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling. Nature, 2013, 500(7463): 422–426
CrossRef
Google scholar
|
[56] |
Andrew A . Language of fungi derived from their electrical spiking activity. Royal Society Open Science, 2022, 9(4): 211926
CrossRef
Google scholar
|
[57] |
Rillig M C, Lehmann A, Lanfranco L, Caruso T, Johnson D . Clarifying the definition of common mycorrhizal networks. Functional Ecology, 2024, 00: 1–7
CrossRef
Google scholar
|
[58] |
Babikova Z, Johnson D, Bruce T, Pickett J, Gilbert L . Underground allies: how and why do mycelial networks help plants defend themselves? What are the fitness, regulatory, and practical implications of defence-related signaling between plants via common mycelial networks. BioEssays, 2014, 36(1): 21–26
CrossRef
Google scholar
|
[59] |
Babikova Z, Johnson D, Bruce T, Pickett J, Gilbert L . How rapid is aphid-induced signal transfer between plants via common mycelial networks. Communicative & Integrative Biology, 2013, 6(6): 835–843
CrossRef
Google scholar
|
[60] |
Jacoby R P, Koprivova A, Kopriva S . Pinpointing secondary metabolites that shape the composition and function of the plant microbiome. Journal of Experimental Botany, 2021, 72(1): 57–69
CrossRef
Google scholar
|
[61] |
Lebeis S L, Paredes S H, Lundberg D S, Breakfield N, Gehring J, Mcdonald M, Malfatti S, Glavina Del Rio T, Jones C D, Tringe S G, Dangl J L . Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Science, 2015, 349(6250): 860–864
CrossRef
Google scholar
|
[62] |
Lopes L D, Wang P, Futrell S L, Schachtman D P . Sugars and jasmonic acid concentration in root exudates affect maize rhizosphere bacterial communities. Applied and Environmental Microbiology, 2022, 88(18): e00971–22
CrossRef
Google scholar
|
[63] |
Santoyo G . How plants recruit their microbiome? New insights into beneficial interactions. Journal of Advanced Research, 2022, 40: 45–58
CrossRef
Google scholar
|
[64] |
Wen T, Zhao M L, Yuan J, Kowalchuk G A, Shen Q R . Root exudates mediate plant defense against foliar pathogens by recruiting beneficial microbes. Soil Ecology Letters, 2021, 3(1): 42–51
CrossRef
Google scholar
|
[65] |
Huang X F, Chaparro J M, Reardon K F, Zhang R F, Shen Q R, Vivanco J M . Rhizosphere interactions: root exudates, microbes, and microbial communities. Botany, 2014, 92(4): 267–275
CrossRef
Google scholar
|
[66] |
Canarini A, Kaiser C, Merchant A, Richter A, Wanek W . Root exudation of primary metabolites: mechanisms and their roles in plant responses to environmental stimuli. Frontiers in Plant Science, 2019, 10: 422679
CrossRef
Google scholar
|
[67] |
Vives-Peris V, Lopez-Climent M F, Perez-Clemente R M, Gomez-Cadenas A . Root involvement in plant responses to adverse environmental conditions. Agronomy, 2020, 10(7): 942
CrossRef
Google scholar
|
[68] |
Yoneyama K, Xie X N, Kim H I, Kisugi T, Nomura T, Sekimoto H, Yokota T, Yoneyama K . How do nitrogen and phosphorus deficiencies affect strigolactone production and exudation. Planta, 2012, 235(6): 1197–1207
CrossRef
Google scholar
|
[69] |
Yoneyama K, Yoneyama K, Takeuchi Y, Sekimoto H . Phosphorus deficiency in red clover promotes exudation of orobanchol, the signal for mycorrhizal symbionts and germination stimulant for root parasites. Planta, 2007, 225(4): 1031–1038
CrossRef
Google scholar
|
[70] |
Kost T, Stopnisek N, Agnoli K, Eberl L, Weisskopf L. Oxalotrophy, a widespread trait of plant-associated Burkholderia species, is involved in successful root colonization of lupin and maize by Burkholderia phytofirmans. Frontiers in Microbiology, 2014, 4: 70529
|
[71] |
Castrillo G, Teixeira P J P L, Paredes S H, Law T F, de Lorenzo L, Feltcher M E, Finkel O M, Breakfield N W, Mieczkowski P, Jones C D, Paz-Ares J, Dangl J L . Root microbiota drive direct integration of phosphate stress and immunity. Nature, 2017, 543(7646): 513–518
CrossRef
Google scholar
|
[72] |
Ferrell R T, Himmelblau D M . Diffusion coefficients of nitrogen and oxygen in water. Journal of Chemical & Engineering Data, 1967, 12(1): 111–115
CrossRef
Google scholar
|
[73] |
Lead J R, Starchev K, Wilkinson K J . Diffusion coefficients of humic substances in agarose gel and in water. Environmental Science & Technology, 2003, 37(3): 482–487
CrossRef
Google scholar
|
[74] |
van’t Padje A, Oyarte Galvez L, Klein M, Hink M A, Postma M, Shimizu T, Kiers E T . Temporal tracking of quantum-dot apatite across in vitro mycorrhizal networks shows how host demand can influence fungal nutrient transfer strategies. ISME Journal, 2021, 15(2): 435–449
CrossRef
Google scholar
|
[75] |
Zeng T, Holmer R, Hontelez J, Te Lintel-Hekkert B, Marufu L, De Zeeuw T, Wu F Y, Schijlen E, Bisseling T, Limpens E. Host-and stage-dependent secretome of the arbuscular mycorrhizal fungus Rhizophagus irregularis. Plant Journal, 2018, 94(3): 411−425
|
[76] |
Suza W P, Avila C A, Carruthers K, Kulkarni S, Goggin F L, Lorence A . Exploring the impact of wounding and jasmonates on ascorbate metabolism. Plant Physiology and Biochemistry, 2010, 48(5): 337–350
CrossRef
Google scholar
|
[77] |
Babikova Z, Gilbert L, Bruce T, Dewhirst S Y, Pickett J A, Johnson D . Arbuscular mycorrhizal fungi and aphids interact by changing host plant quality and volatile emission. Functional Ecology, 2014, 28(2): 375–385
CrossRef
Google scholar
|
[78] |
Fontana A, Reichelt M, Hempel S, Gershenzon J, Unsicker S B . The effects of arbuscular mycorrhizal fungi on direct and indirect defense metabolites of Plantago lanceolata L. Journal of Chemical Ecology, 2009, 35(7): 833–843
CrossRef
Google scholar
|
[79] |
O’Callaghan J A, Kamat N P, Vargo K B, Chattaraj R, Lee D, Hammer D A . A microfluidic platform for the synthesis of polymer and polymer-protein-based protocells. European Physical Journal E, 2024, 47(6): 37
CrossRef
Google scholar
|
[80] |
Lanekoff I, Sharma V V, Marques C . Single-cell metabolomics: where are we and where are we going. Current Opinion in Biotechnology, 2022, 75: 102693
CrossRef
Google scholar
|
[81] |
Zhang L, Zhou J C, George T S, Limpens E, Feng G . Arbuscular mycorrhizal fungi conducting the hyphosphere bacterial orchestra. Trends in Plant Science, 2022, 27(4): 402–411
CrossRef
Google scholar
|
[82] |
Zhang L, Feng G, Declerck S . Signal beyond nutrient, fructose, exuded by an arbuscular mycorrhizal fungus triggers phytate mineralization by a phosphate solubilizing bacterium. ISME Journal, 2018, 12(10): 2339–2351
CrossRef
Google scholar
|
/
〈 | 〉 |