Arbuscular mycorrhiza can be disadvantageous for weedy annuals in competition with paired perennial plants
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
36456609
PubMed Central
PMC9715701
DOI
10.1038/s41598-022-24669-6
PII: 10.1038/s41598-022-24669-6
Knihovny.cz E-zdroje
- MeSH
- abúzus marihuany * MeSH
- mykorhiza * MeSH
- nádory kůže MeSH
- pigmentový névus MeSH
- plevel MeSH
- půda MeSH
- Senecio * MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- půda MeSH
Arbuscular mycorrhizal (AM) fungi can support the establishment of mycotrophic plants in new environments. However, the role of mycorrhizal symbiosis in interactions between perennial and weedy annual plants is not well understood. In our current study, we examine how widespread generalist AM fungi and soil disturbance, including disturbance of AM fungal networks (CMNs), affect the performance of two late-successional perennial plants of Central Europe, Senecio jacobaea and Crepis biennis, co-occurring with weedy annual forbs, Conyza canadensis and Erigeron annuus. Although presence of weedy annual E. annuus or C. canadensis did not affect the performance of the paired perennials, AM fungi supported perennial C. biennis in competition with weedy annual E. annuus. However, this AM-aided underpinning was independent of disturbance of CMNs. Conversely, although AM fungi benefited perennial S. jacobaea, this did not affect its competitive abilities when grown with weedy annual C. canadensis. Similarly, soil disturbance, independent of AM fungal presence, improved plant tissue P and biomass production of S. jacobaea, but not its competitive abilities. Our results show AM fungi may be advantageous for perennial plants growing in competition with weedy annual plants. Therefore, maintaining healthy soils containing an abundance of AM fungi, may encourage late successional perennial plants, potentially limiting establishment of weedy annual plant species.
Crop Research Institute Drnovská 507 Prague 6 Czech Republic
Department of Natural Resource Ecology and Management Oklahoma State University Stillwater OK USA
Institute of Microbiology Czech Academy of Sciences Vídeňská 1083 Prague 4 Czech Republic
Zobrazit více v PubMed
Smith SE, Read DJ. Mycorrhizal Symbiosis. 3. Academic Press; 2008.
van der Heijden MGA, Martin FM, Selosse MA, Sanders IR. Mycorrhizal ecology and evolution: The past, the present, and the future. New Phytol. 2015;205:1406–1423. doi: 10.1111/nph.13288. PubMed DOI
Štajerová K, Šmilauerová M, Šmilauer P. Arbuscular mycorrhizal symbiosis of herbaceous invasive neophytes in the Czech Republic. Preslia. 2009;81:341–355.
Hempel S, Götzenberger L, Kühn I, Michalski SG, Rillig MC, Zobel M, Moora M. Mycorrhizas in the Central European flora: Relationships with plant life history traits and ecology. Ecology. 2013;94:1389–1399. doi: 10.1890/12-1700.1. PubMed DOI
Soudzilovskaia NA, Vaessen S, Barcelo M, He J, Rahimlou S, Abarenkov K, Brundrett MC, Gomes SIF, Merckx V, Tedersoo L. FungalRoot: Global online database of plant mycorrhizal associations. New Phytol. 2020;227:955–966. doi: 10.1111/nph.16569. PubMed DOI
Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith ME, Berbee ML, Bonito G, Corradi N, Grigoriev I, Gryganskyi A, James TY, O’Donnell K, Roberson RW, Taylor TN, Uehling J, Vilgalys R, White MM, Stajich JE. A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia. 2016;108:1028–1046. doi: 10.3852/16-042. PubMed DOI PMC
Lekberg Y, Hammer EC, Olsson PA. Plants as resource islands and storage units—Adopting the mycocentric view of arbuscular mycorrhizal networks. FEMS Microbiol. Ecol. 2010;74:336–345. doi: 10.1111/j.1574-6941.2010.00956.x. PubMed DOI
Newsham KK, Fitter AH, Watkinson AR. Arbuscular mycorrhiza protect an annual grass from root pathogenic fungi in the field. J. Ecol. 1995;83:991–1000. doi: 10.2307/2261180. DOI
Vigo C, Norman JR, Hooker JE. Biocontrol of the pathogen Phytophthora parasitica by arbuscular mycorrhizal fungi is a consequence of effects on infection loci. Plant Pathol. 2000;49:509–514. doi: 10.1046/j.1365-3059.2000.00473.x. DOI
Pfeffer PE, Douds DD, Becard G, Shachar-Hill Y. Carbon uptake and the metabolism and transport of lipids in an arbuscular mycorrhiza. Plant Physiol. 1999;120:587–598. doi: 10.1104/pp.120.2.587. PubMed DOI PMC
Bago B, Pfeffer PE, Shachar-Hill Y. Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiol. 2000;124:949–958. doi: 10.1104/pp.124.3.949. PubMed DOI PMC
Ramirez R, Mendoza B, Lizaso JI. Mycorrhiza effect on maize P uptake from phosphate rock and superphosphate. Commun. Soil Sci. Plant Anal. 2009;40:13–14. doi: 10.1080/00103620902960583. DOI
Pearson JN, Jakobsen I. The relative contribution of hyphae and roots to phosphorus uptake by arbuscular mycorrhizal plants, measured by dual labeling with 32P and 33P. New Phytol. 1993;124:489–494. doi: 10.1111/j.1469-8137.1993.tb03840.x. DOI
Smith SE, Smith FA, Jakobsen I. Functional diversity in arbuscular mycorrhizal (AM) symbioses: The contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. New Phytol. 2004;162:511–524. doi: 10.1111/j.1469-8137.2004.01039.x. DOI
Smith MD, Hartnett DC, Wilson GWT. Interacting influence of mycorrhizal symbiosis and competition on plant diversity in tallgrass prairie. Oecologia. 1999;121:574–582. doi: 10.1007/s004420050964. PubMed DOI
Bennett JA, Maherali H, Reinhart KO, Lekberg Y, Hart MM, Klironomos J. Plant-soil feedbacks and mycorrhizal type influence temperate forest population dynamics. Science. 2017;355:181–184. doi: 10.1126/science.aai8212. PubMed DOI
Liao H, Huang F, Li D, Kang L, Chen B, Zhou T, Peng S. Soil microbes regulate forest succession in a subtropical ecosystem in China: Evidence from a mesocosm experiment. Plant Soil. 2018;430:277–289. doi: 10.1007/s11104-018-3733-3. DOI
Awaydul A, Zhu WY, Yuan YG, Xiao J, Hu H, Chen X, Koide RT, Cheng L. Common mycorrhizal networks influence the distribution of mineral nutrients between an invasive plant, Solidago canadensis, and a native plant, Kummerowa striata. Mycorrhiza. 2019;29:29–38. doi: 10.1007/s00572-018-0873-5. PubMed DOI
Callaway RM, Newingham B, Zabinski CA, Mahall BE. Compensatory growth and competitive ability of an invasive weed are enhanced by soil fungi and native neighbours. Ecol. Lett. 2001;4:429–433. doi: 10.1046/j.1461-0248.2001.00251.x. DOI
Workman RE, Cruzan MB. Common mycelial networks impact competition in an invasive grass. Am. J. Bot. 2016;103:1041–1049. doi: 10.3732/ajb.1600142. PubMed DOI
Richardson DM, Allsopp N, D'Antonio CM, Milton SJ, Rejmanek M. Plant invasions—The role of mutualisms. Biol. Rev. Camb. Philos. Soc. 2000;75:65–93. doi: 10.1017/S0006323199005435. PubMed DOI
Vogelsang KM, Bever JD. Mycorrhizal densities decline in association with nonnative plants and contribute to plant invasion. Ecology. 2009;90:399–407. doi: 10.1890/07-2144.1. PubMed DOI
Horton TR. Mycorrhizal Networks, Ecological Studies 224. Springer; 2015.
Lin G, McCormack ML, Guo D. Arbuscular mycorrhizal fungal effects on plant competition and community structure. J. Ecol. 2015;103:1224–1232. doi: 10.1111/1365-2745.12429. DOI
Jasper DA, Abbott JK, Robson AD. The effect of soil disturbance on vesicular-arbuscular mycorrhizal fungi in soils from different vegetation types. New Phytol. 1991;118:471–476. doi: 10.1111/j.1469-8137.1991.tb00029.x. DOI
Jansa J, Mozafar A, Anken T, Ruh R, Sanders IR, Frossard E. Diversity and structure of AMF communities as affected by tillage in a temperate soil. Mycorrhiza. 2002;12:225–234. doi: 10.1007/s00572-002-0163-z. PubMed DOI
van der Heyde M, Ohsowski B, Abbott LK, Hart M. Arbuscular mycorrhizal fungus responses to disturbance are context-dependent. Mycorrhiza. 2017;27:431–440. doi: 10.1007/s00572-016-0759-3. PubMed DOI
Verbruggen E, Kiers ET. Evolutionary ecology of mycorrhizal functional diversity in agricultural systems. Evol. Appl. 2010;3:547–560. doi: 10.1111/j.1752-4571.2010.00145.x. PubMed DOI PMC
Řezáčová V, Řezáč M, Gryndlerová H, Wilson GWT, Michalová T. Arbuscular mycorrhizal fungi favor invasive Echinops sphaerocephalus when grown in competition with native Inula conyzae. Sci. Rep. 2020;10:20287. doi: 10.1038/s41598-020-77030-0. PubMed DOI PMC
Callaway RM, Thelen GC, Barth S, Ramsey PW, Gannon JE. Soil fungi alter interactions between the invader Centaurea maculosa and North American natives. Ecology. 2004;85:1062–1071. doi: 10.1890/02-0775. DOI
Abhilasha D, Joshi J. Enhanced fitness due to higher fecundity, increased defence against a specialist and tolerance towards a generalist herbivore in an invasive annual plant. J. Plant Ecol. 2009;2:77–86. doi: 10.1093/jpe/rtp008. DOI
Shah MA, Reshi ZA, Khasa D. Arbuscular mycorrhizal status of some Kashmir Himalayan alien invasive plants. Mycorrhiza. 2009;20:67–72. doi: 10.1007/s00572-009-0258-x. PubMed DOI
Shah MA, Reshi ZA, Rasool N. Plant invasions induce a shift in Glomalean spore diversity. Trop. Ecol. 2010;51:317–323.
Shah MA, Beaulieu M-E, Reshi ZA, Qureshi S, Khasa DP. A cross-city molecular biogeographic investigation of arbuscular mycorrhizas in Conyza canadensis rhizosphere across native and non-native regions. Ecol. Process. 2015;4:7. doi: 10.1186/s13717-015-0034-0. DOI
Řezáčová V, Konvalinková T, Řezáč M. Decreased mycorrhizal colonization of Conyza canadensis (L.) Cronquist in invaded range does not affect fungal abundance in native plants. Biologia. 2020;75:693–699. doi: 10.2478/s11756-020-00446-6. DOI
Shah MA, Reshi Z, Rashid I. Mycorrhizal source and neighbour identity differently influence Anthemis cotula L. invasion in the Kashmir Himalaya, India. Appl. Soil Ecol. 2008;40:330–337. doi: 10.1016/j.apsoil.2008.06.002. DOI
Řezáčová V, Řezáč M, Gryndler M, Hršelová H, Gryndlerová H, Michalová T. Plant invasion alters community structure and decreases diversity of arbuscular mycorrhizal fungal communities. Appl. Soil Ecol. 2021;167:104039. doi: 10.1016/j.apsoil.2021.104039. DOI
Řezáčová V, Michalová T, Řezáč M, Gryndler M, Duell EB, Wilson GWT, Heneberg P. The root-associated arbuscular mycorrhizal fungal assemblages of exotic alien plants are simplified in invaded distribution ranges, but dominant species are retained: A trans-continental perspective. Environ. Microbiol. Rep. 2022 doi: 10.1111/1758-2229.13108. PubMed DOI
Song U, Son D, Kang C, Lee EJ, Lee K, Park JS. Mowing: A cause of invasion, but also a potential solution for management of the invasive, alien plant species Erigeron annuus (L.) Pers. J. Environ. Manag. 2018;223:530–536. doi: 10.1016/j.jenvman.2018.06.057. PubMed DOI
Hempel S, Gotzenberger L, Kuhn I, Michalski SG, Rillig MC, Zobel M, Moora M. Mycorrhizas in the Central European flora: Relationships with plant life history traits and ecology. Ecology. 2013;94:1389–1399. doi: 10.1890/12-1700.1. PubMed DOI
Řezáčová V, Řezáč M, Líblová Z, Michalová T, Heneberg P. Stable colonization of native plants and early invaders by arbuscular mycorrhizal fungi after exposure to recent invaders from the Asteraceae family. IPSM. 2021;14:147–155. doi: 10.1017/inp.2021.17. DOI
Wilson GWT, Hartnett DC. Interspecific variation in plant responses to mycorrhizal colonization in tallgrass prairie. Am. J. Bot. 1998;85:1732–1738. doi: 10.2307/2446507. PubMed DOI
Rinaudo V, Barberi P, Giovanneti M, van der Heijden MGA. Mycorrhizal fungi suppress aggressive agricultural weeds. Plant Soil. 2010;333:7–20. doi: 10.1007/s11104-009-0202-z. DOI
Veiga RSL, Jansa J, Frossard E, van der Heijden MGA. Can arbuscular mycorrhizal fungi reduce the growth of agricultural weeds? PLoS ONE. 2011;6:e27825. doi: 10.1371/journal.pone.0027825. PubMed DOI PMC
Boerner REJ. Plant life span and response to inoculation with vesicular-arbuscular mycorrhizal fungi. Mycorrhiza. 1992;1:153–161. doi: 10.1007/BF00203289. DOI
Wilson SD. Tilman plant competition and resource availability in response to disturbance and fertilization. Ecology. 1993;74:599–611. doi: 10.2307/1939319. DOI
Xiao-Bin W, Dian-Xiong CAI, Hoogmoed WB, Oenema O, Perdok UD. Potential effect of conservation tillage on sustainable land use: A review of global long-term studies. Pedosphere. 2006;16:587–595. doi: 10.1016/S1002-0160(06)60092-1. DOI
Miransari M. Contribution of arbuscular mycorrhizal symbiosis to plant growth under different types of soil stress. Plant Biol. 2010;12:563–569. PubMed
Latef AAHA, Hashem A, Rasool S, Abd Allah EF, Alqarawi AA, Egamberdieva D, Jan S, Anjum NA, Ahmad P. Arbuscular mycorrhizal symbiosis and abiotic stress in plants: A review. J. Plant Biol. 2016;59:407–426. doi: 10.1007/s12374-016-0237-7. DOI
Richardson DM, Allsopp N, D'Antonio CM, Milton SJ, Rejmanek M. Plant invasions—The role of mutualisms. Biol. Rev. 2000;75:65–93. doi: 10.1017/S0006323199005435. PubMed DOI
Řezáčová V, Slavíková R, Zemková L, Konvalinková T, Prochazková V, Šťovíček V, Hršelová H, Beskid O, Hujslová M, Gryndlerová H, Gryndler M, Püschel D, Jansa J. Mycorrhizal symbiosis induces plant carbon reallocation differently in C3 and C4 Panicum grasses. Plant Soil. 2018;425:441–456. doi: 10.1007/s11104-018-3606-9. DOI
Newman EI. A method of estimating total length of root in a sample. J. Appl. Ecol. 1966;3:139–145. doi: 10.2307/2401670. DOI
Bukovská P, Gryndler M, Gryndlerová H, Püschel D, Jansa J. Organic nitrogen-driven stimulation of arbuscular mycorrhizal fungal hyphae correlates with abundance of ammonia oxidizers. Front. Microbiol. 2016;7:711. doi: 10.3389/fmicb.2016.00711. PubMed DOI PMC
Hewitt EJ. Sand and water culture methods used in the study of plant nutrition. CAB Tech. Commun. 1966;22:431–432.
Řezáčová V, Slavíková R, Konvalinková T, Hujslová M, Gryndlerová H, Gryndler M, Püschel D, Jansa J. Imbalanced carbon-for-phosphorus exchange between European arbuscular mycorrhizal fungi and non-native Panicum grasses—A case of dysfunctional symbiosis. Pedobiologia. 2017;62:48–55. doi: 10.1016/j.pedobi.2017.05.004. DOI
Řezáčová V, Zemková L, Beskid O, Püschel D, Konvalinková T, Hujslová M, Slavíková R, Jansa J. Little cross-feeding of the mycorrhizal networks shared between C3-Panicum bisulcatum and C4-Panicum maximum under different temperature regimes. Front. Microbiol. 2018;9:449. PubMed PMC
Ohno T, Zibilske LM. Determination of low concentrations of phosphorus in soil extracts using malachite green. Soil Sci. Soc. Am. J. 1991;55:892–895. doi: 10.2136/sssaj1991.03615995005500030046x. DOI
Thonar C, Erb A, Jansa J. Real-time PCR to quantify composition of arbuscular mycorrhizal fungal communities-marker design, verification, calibration and field validation. Mol. Ecol. Res. 2012;12:219–232. doi: 10.1111/j.1755-0998.2011.03086.x. PubMed DOI
McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA. A new method which gives an objective-measure of colonization of roots by vesicular arbuscular mycorrhizal fungi. New Phytol. 1990;115:495–501. doi: 10.1111/j.1469-8137.1990.tb00476.x. PubMed DOI
Koske RE, Gemma JN. A modified procedure for staining roots to detect VA-mycorrhizas. Mycol. Res. 1989;92:486–505. doi: 10.1016/S0953-7562(89)80195-9. DOI
R Core Team. R: A Language and Environment for Statistical Computing. https://www.R-project.org/ (R Foundation for Statistical Computing, 2022)