Abstract
Marchantia polymorpha is a common liverwort whose use as a model plant in physiological and evolutionary processes is increasing in recent years. As far as plant-microorganism interactions are concerned, there are still few studies conducted with M. polymorpha. Specifically, in the interaction of M. polymorpha with arbuscular mycorrhizal fungi (AMF), it has been described how AMF colonize the M. polymorpha tissues, without knowing more about the interaction. In this study, M. polymorpha is inoculated with different AMF formulations, analyzing the direct effect on M. polymorpha’s growth and the nutritional content, along with stress responses. Moreover, expression levels of defense genes in M. polymorpha were analyzed. The results obtained showed how M. polymorpha-AMF interaction is detrimental to plant under in vitro conditions. A reduction in its growth and viability of its tissues was observed, in addition to an increase only in nutritional content of those elements related to plant defenses, together with the reactive oxygen species (ROS) content. Rhizophagus fasciculatus is only present in the formulation that causes major damage to the plant, including symptoms of tissue damage, and that mostly colonizes the plant. It suggests its possible role as a plant pathogen, due to the inability of M. polymorpha to defend it against the AMF by the route of salicylic acid (SA).
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Aguilar E, Almendral D, Allende L, Pacheco R, Chung BN, Canto T, Tenllado F (2015) The P25 protein of potato virus X (PVX) is the main pathogenicity determinant responsible for systemic necrosis in PVX-associated synergisms. J Virol 89:2090–2103. https://doi.org/10.1128/JVI.02896-14
Alonso-Ramírez A, Poveda J, Martín I, Hermosa R, Monte E, Nicolás C (2014) Salicylic acid prevents Trichoderma harzianum from entering the vascular system of roots. Mol Plant Pathol 15:823–831. https://doi.org/10.1111/mpp.12141
Bago B, Pfeffer PE, Shachar-Hill Y (2000) Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiol 124:949–958. https://doi.org/10.1104/pp.124.3.949
Begum N, Qin C, Ahanger MA, Raza S, Khan MI, Ahmed N, Ashraf M, Zhang L (2019) Role of arbuscular mycorrhizal fungi in plant growth regulation: implications in abiotic stress tolerance. Fron Plant Sci 10:1068. https://doi.org/10.3389/fpls.2019.01068
Berruti A, Lumini E, Balestrini R, Bianciotto V (2016) Arbuscular mycorrhizal fungi as natural biofertilizers: let's benefit from past successes. Front Microbiol 6:1559. https://doi.org/10.3389/fmicb.2015.01559
Bowman JL, Kohchi T, Yamato KT, Jenkins J, Shu S, Ishizaki K, Yamaoka S, Nishihama R, Nakamura Y, Berger F, Adam C, Aki SS, Althoff F, Araki T, Arteaga-Vazquez MA, Balasubrmanian S, Barry K, Bauer D, Boehm CR, Briginshaw L, Caballero-Perez J, Catarino B, Chen F, Chiyoda S, Chovatia M, Davies KM, Delmans M, Demura T, Dierschke T, Dolan L, Dorantes-Acosta AE, Eklund DM, Florent SN, Flores-Sandoval E, Fujiyama A, Fukuzawa H, Galik B, Grimanelli D, Grimwood J, Grossniklaus U, Hamada T, Haseloff J, Hetherington AJ, Higo A, Hirakawa Y, Hundley HN, Ikeda Y, Inoue K, Inoue SI, Ishida S, Jia Q, Kakita M, Kanazawa T, Kawai Y, Kawashima T, Kennedy M, Kinose K, Kinoshita T, Kohara Y, Koide E, Komatsu K, Kopischke S, Kubo M, Kyozuka J, Lagercrantz U, Lin SS, Lindquist E, Lipzen AM, Lu CW, de Luna E, Martienssen RA, Minamino N, Mizutani M, Mizutani M, Mochizuki N, Monte I, Mosher R, Nagasaki H, Nakagami H, Naramoto S, Nishitani K, Ohtani M, Okamoto T, Okumura M, Phillips J, Pollak B, Reinders A, Rövekamp M, Sano R, Sawa S, Schmid MW, Shirakawa M, Solano R, Spunde A, Suetsugu N, Sugano S, Sugiyama A, Sun R, Suzuki Y, Takenaka M, Takezawa D, Tomogane H, Tsuzuki M, Ueda T, Umeda M, Ward JM, Watanabe Y, Yazaki K, Yokoyama R, Yoshitake Y, Yotsui I, Zachgo S, Schmutz J (2017) Insights into land plant evolution garnered from the Marchantia polymorpha genome. Cell 171:287–304. https://doi.org/10.1016/j.cell.2017.09.030
Campos P, Borie F, Cornejo P, López-Ráez JA, López-García Á, Seguel A (2018) Phosphorus acquisition efficiency related to root traits: is mycorrhizal symbiosis a key factor to wheat and barley cropping? Front Plant Sci 9:752. https://doi.org/10.3389/fpls.2018.00752
Chen M, Arato M, Borghi L, Nouri E, Reinhardt D (2018) Beneficial services of arbuscular mycorrhizal fungi - from ecology to application. Front Plant Sci 9:1270. https://doi.org/10.3389/fpls.2018.01270
Dellaborta SL, Wood J, Hicks JB (1983) A plant DNA mini preparation. Version II plant. Mol Biol Rep 1:19–21
Feijen FA, Vos RA, Nuytinck J, Merckx VS (2018) Evolutionary dynamics of mycorrhizal symbiosis in land plant diversification. Sci Rep 8:10698. https://doi.org/10.1038/s41598-018-28920-x
Ferlian O, Biere A, Bonfante P, Buscot F, Eisenhauer N, Fernandez I, Hause B, Herrmann S, Krajinski-Barth F, Meier IC, Pozo MJ, Rasmann S, Rillig MC, Tarkka MT, van Dam NM, Wagg C, Martinez-Medina A (2018) Growing research networks on mycorrhizae for mutual benefits. Trends Plant Sci 23:975–984. https://doi.org/10.1016/j.tplants.2018.08.008
Field KJ, Bidartondo MI, Rimington WR, Hoysted GA, Beerling D, Cameron DD, Duckett JG, Leake JR, Pressel S (2019) Functional complementarity of ancient plant–fungal mutualisms: contrasting nitrogen, phosphorus and carbon exchanges between Mucoromycotina and Glomeromycotina fungal symbionts of liverworts. New Phytol 223:908–921. https://doi.org/10.1111/nph.15819
Frater PN, Borer ET, Fay PA, Jin V, Knaeble B, Seabloom E, Sulliven L, Wedin DA et al (2018) Nutrients and environment influence arbuscular mycorrhizal colonization both independently and interactively in Schizachyrium scoparium. Plant Soil 425:493–506. https://doi.org/10.1007/s11104-018-3597-6
Gao X, Zhang S, Zhao X, Wu Q (2018) Potassium-induced plant resistance against soybean cyst nematode via root exudation of phenolic acids and plant pathogen-related genes. PLoS One 13:e0200903. https://doi.org/10.1371/journal.pone.0200903
Gimenez-Ibanez S, Zamarreño AM, García-Mina JM, Solano R (2019) An evolutionarily ancient immune system governs the interactions between Pseudomonas syringae and an early-diverging land plant lineage. Curr Biol 29:2270–2281. https://doi.org/10.1016/j.cub.2019.05.079
Gruhlke MC (2019) Reactive sulfur species: a new player in plant physiology? In: Hasanuzzaman M, Fotopoulos V, Nahar K, Fujita M (eds) Reactive oxygen, nitrogen and sulfur species in plants: production, metabolism, signaling and defense mechanisms. New Jersey, USA, Wiley-Blackwell, pp 715–728
Hocking B, Conn SJ, Manohar M, Xu B, Athman A, Stancombe MA, Webb AR, Hirschi KD, Gilliham M (2017) Heterodimerization of Arabidopsis calcium/proton exchangers contributes to regulation of guard cell dynamics and plant defense responses. J Exp Bot 68:4171–4183. https://doi.org/10.1093/jxb/erx209
Jacobs S, Zechmann B, Molitor A, Trujillo M, Petutschnig E, Lipka V et al (2011) Broad-spectrum suppression of innate immunity is required for colonization of Arabidopsis roots by the fungus Piriformospora indica. Plant Physiol 156:726–740. https://doi.org/10.1104/pp.111.176446
Kamel L, Keller-Pearson M, Roux C, Ané JM (2017) Biology and evolution of arbuscular mycorrhizal symbiosis in the light of genomics. New Phytol 213:531–536. https://doi.org/10.1111/nph.14263
Kanamoto H, Takemura M, Ohyama K (2012) Cloning and expression of three lipoxygenase genes from liverwort, Marchantia polymorpha L., in Escherichia coli. Phytochemistry 77:70–78. https://doi.org/10.1016/j.phytochem.2012.02.009
Krohling CA, Eutrópio FJ, Bertolazi AA, Dobbss LB, Campostrini E, Dias T, Ramos AC (2016) Ecophysiology of iron homeostasis in plants. Soil Sci Plant Nutr 62:39–47. https://doi.org/10.1080/00380768.2015.1123116
Kumar MR, Ashwin R, Bagyaraj DJ (2018) Screening arbuscular mycorrhizal fungi in order to select the best for alleviating wilt disease complex of capsicum. P Nat A Sci B 88:679–684. https://doi.org/10.1007/s40011-016-0804-1
Lee J, Lee S, Young JPW (2008) Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiol Ecol 65:339–349. https://doi.org/10.1111/j.1574-6941.2008.00531.x
Liao D, Wang S, Cui M, Liu J, Chen A, Xu G (2018) Phytohormones regulate the development of arbuscular mycorrhizal symbiosis. Int J Mol Sci 19:3146. https://doi.org/10.3390/ijms19103146
Ligrone R, Carafa A, Lumini E, Bianciotto V, Bonfante P, Duckett JG (2007) Glomeromycotean associations in liverworts: a molecular, cellular, and taxonomic analysis. Am J Bot 94:1756–1777. https://doi.org/10.3732/ajb.94.11.1756
López-Ráez JA, Verhage A, Fernández I, García JM, Azcón-Aguilar C, Flors V, Pozo MJ (2010) Hormonal and transcriptional profiles highlight common and differential host responses to arbuscular mycorrhizal fungi and the regulation of the oxylipin pathway. J Exp Bot 61:2589–2601. https://doi.org/10.1093/jxb/erq089
Matsui H, Iwakawa H, Hyon GS, Yotsui I, Katou S, Monte I, Nishihama R, Franzen R, Solano R, Nakagami H (2020) Isolation of natural fungal pathogens from Marchantia polymorpha reveals antagonism between salicylic acid and jasmonate during liverwort–fungus interactions. Plant Cell Physiol 61:265–275. https://doi.org/10.1093/pcp/pcz187
Monte I, Ishida S, Zamarreño AM, Hamberg M, Franco-Zorrilla JM, García-Casado G, Gouhier-Darimont C, Reymond P, Takahashi K, García-Mina JM, Nishihama R, Kohchi T, Solano R (2018) Ligand-receptor co-evolution shaped the jasmonate pathway in land plants. Nat Chem Biol 14:480–488. https://doi.org/10.1038/s41589-018-0033-4
Mur LA, Simpson C, Kumari A, Gupta AK, Gupta KJ (2017) Moving nitrogen to the Centre of plant defence against pathogens. Ann Bot 119:703–709. https://doi.org/10.1093/aob/mcw179
Nelson JM, Hauser DA, Hinson R, Shaw AJ (2018) A novel experimental system using the liverwort Marchantia polymorpha and its fungal endophytes reveals diverse and context-dependent effects. New Phytol 218:1217–1232. https://doi.org/10.1111/nph.15012
Nelson J, Shaw AJ (2019) Exploring the natural microbiome of the model liverwort: fungal endophyte diversity in Marchantia polymorpha L. Symbiosis 78:1–15. https://doi.org/10.1007/s13199-019-00597-4
Ogura-Tsujita Y, Hirayama Y, Sakoda A, Suzuki A, Ebihara A, Morita N, Imaichi R (2016) Arbuscular mycorrhizal colonization in field-collected terrestrial cordate gametophytes of pre-polypod leptosporangiate ferns (Osmundaceae, Gleicheniaceae, Plagiogyriaceae, Cyatheaceae). Mycorrhiza 26:87–97. https://doi.org/10.1007/s00572-015-0648-1
Poveda J, Hermosa R, Monte E, Nicolás C (2019) Trichoderma harzianum favours the access of arbuscular mycorrhizal fungi to non-host Brassicaceae roots and increases plant productivity. Sci Rep 9:1–11. https://doi.org/10.1038/s41598-019-48269-z
Poveda J (2020a) Marchantia polymorpha as a model plant in the evolutionary study of plant-microorganism interactions. Curr Plant Biol 100152:100152. https://doi.org/10.1016/j.cpb.2020.100152
Poveda J, Abril-Urías P, Escobar C (2020) Biological control of plant-parasitic nematodes by filamentous fungi inducers of resistance: Trichoderma, mycorrhizal and endophytic fungi. Front Microbiol 11:992. https://doi.org/10.3389/fmicb.2020.00992
Poveda J (2020b) Trichoderma parareesei favors the tolerance of rapeseed (Brassica napus L.) to salinity and drought due to a chorismate mutase. Agronomy 10:118. https://doi.org/10.3390/agronomy10010118
Poveda J (2020c) Use of plant-defense hormones against pathogen-diseases of postharvest fresh produce. Physiol Mol Plant Pathol 111:101521. https://doi.org/10.1016/j.pmpp.2020.101521
Powell JR, Rillig MC (2018) Biodiversity of arbuscular mycorrhizal fungi and ecosystem function. New Phytol 220:1059–1075. https://doi.org/10.1111/nph.15119
Pozo MJ, Azcón-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398. https://doi.org/10.1016/j.pbi.2007.05.004
Rimington WR, Pressel S, Duckett JG, Field KJ, Read DJ, Bidartondo MI (2018) Ancient plants with ancient fungi: liverworts associate with early-diverging arbuscular mycorrhizal fungi. P Roy Soc B 285:20181600. https://doi.org/10.1098/rspb.2018.1600
Ruf M, Brunner I (2003) Vitality of tree fine roots: reevaluation of the tetrazolium test. Tree Physiol 23:257–263. https://doi.org/10.1093/treephys/23.4.257
Russell J, Bulman S (2005) The liverwort Marchantia foliacea forms a specialized symbiosis with arbuscular mycorrhizal fungi in the genus Glomus. New Phytol:165567–165579. https://doi.org/10.1111/j.1469-8137.2004.01251.x
Schultz JC, Appel HM, Ferrieri A, Arnold TM (2013) Flexible resource allocation during plant defense responses. Front Plant Sci 4:324. https://doi.org/10.3389/fpls.2013.00324
Shimamura M (2015) Marchantia polymorpha: taxonomy, phylogeny and morphology of a model system. Plant Cell Physiol 57:230–256. https://doi.org/10.1093/pcp/pcv192
Strullu-Derrien C, Selosse MA, Kenrick P, Martin FM (2018) The origin and evolution of mycorrhizal symbioses: from palaeomycology to phylogenomics. New Phytol 220:1012–1030. https://doi.org/10.1111/nph.15076
Verma M, Langer A (2014) Studies on AM associations in Marchantia nepalensis L. et L. J Pharm Biol Sci 9:26–29
Yoshikawa M, Luo W, Tanaka G, Konishi Y, Matsuura H, Takahashi K (2018) Wounding stress induces phenylalanine ammonia lyases, leading to the accumulation of phenylpropanoids in the model liverwort Marchantia polymorpha. Phytochemistry 155:30–36. https://doi.org/10.1016/j.phytochem.2018.07.014
Zare-Maivan H, Khanpour-Ardestani N, Ghanati F (2017) Influence of mycorrhizal fungi on growth, chlorophyll content, and potassium and magnesium uptake in maize. J Plant Nutr 40:2026–2032. https://doi.org/10.1080/01904167.2017.1346119
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Poveda, J. Marchantia polymorpha subsp. ruderalis (Bischl. & Boissel.-Dub.)-arbuscular mycorrhizal fungi interaction: beneficial or harmful?. Symbiosis 82, 165–174 (2020). https://doi.org/10.1007/s13199-020-00708-6
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DOI: https://doi.org/10.1007/s13199-020-00708-6