Divergent colonization traits, convergent benefits: different species of arbuscular mycorrhizal fungi alleviate Meloidogyne incognita damage in tomato
Jazyk angličtina Země Německo Médium print-electronic
Typ dokumentu časopisecké články
Grantová podpora
CZ.02.2.69/0.0/0.0/18_054/0014676
Ministry of Education, Youth and Sports of the Czech Republic, co-financed by the European Union
No. 23-05453S
Czech Science Foundation
PubMed
38441668
PubMed Central
PMC10998783
DOI
10.1007/s00572-024-01139-7
PII: 10.1007/s00572-024-01139-7
Knihovny.cz E-zdroje
- Klíčová slova
- Arbuscular mycorrhizal fungi, Biological control, Plant nutrition, Root knot nematodes,
- MeSH
- Glomeromycota * fyziologie MeSH
- kořeny rostlin mikrobiologie MeSH
- mykorhiza * fyziologie MeSH
- rostliny MeSH
- Solanum lycopersicum * MeSH
- Tylenchoidea * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
Arbuscular mycorrhizal fungi (AMF) can increase plant tolerance and/or resistance to pests such as the root-knot nematode Meloidogyne incognita. However, the ameliorative effects may depend on AMF species. The aim of this work was therefore to evaluate whether four AMF species differentially affect plant performance in response to M. incognita infection. Tomato plants grown in greenhouse conditions were inoculated with four different AMF isolates (Claroideoglomus claroideum, Funneliformis mosseae, Gigaspora margarita, and Rhizophagus intraradices) and infected with 100 second stage juveniles of M. incognita at two different times: simultaneously or 2 weeks after the inoculation with AMF. After 60 days, the number of galls, egg masses, and reproduction factor of the nematodes were assessed along with plant biomass, phosphorus (P), and nitrogen concentrations in roots and shoots and root colonization by AMF. Only the simultaneous nematode inoculation without AMF caused a large reduction in plant shoot biomass, while all AMF species were able to ameliorate this effect and improve plant P uptake. The AMF isolates responded differently to the interaction with nematodes, either increasing the frequency of vesicles (C. claroideum) or reducing the number of arbuscules (F. mosseae and Gi. margarita). AMF inoculation did not decrease galls; however, it reduced the number of egg masses per gall in nematode simultaneous inoculation, except for C. claroideum. This work shows the importance of biotic stress alleviation associated with an improvement in P uptake and mediated by four different AMF species, irrespective of their fungal root colonization levels and specific interactions with the parasite.
Zobrazit více v PubMed
Abd-Elgawad MMM. Optimizing safe approaches to manage plant-parasitic nematodes. Plants. 2021;10:1911. doi: 10.3390/plants10091911. PubMed DOI PMC
Ahamad L, Bhat AH, Kumar H, Rana A, Hasan MN, Ahmed I, Ahmed S, Machado RAR, Ameen F. From soil to plant: strengthening carrot defenses against Meloidogyne incognita with vermicompost and arbuscular mycorrhizal fungi biofertilizers. Front Microbiol. 2023;14:1206217. doi: 10.3389/fmicb.2023.1206217. PubMed DOI PMC
Ammiraju JS, Veremis JC, Huang X, Roberts PA, Kaloshian I. The heat-stable root-knot nematode resistance gene Mi-9 from Lycopersicon peruvianum is localized on the short arm of chromosome 6. Theor Appl Genet. 2003;106:478e484. doi: 10.1007/s00122-002-1106-y. PubMed DOI
Anjos ÉCTD, Cavalcante UMT, Gonçalves DMC, Pedrosa EMR, Santos VFD, Maia LC. Interactions between an arbuscular mycorrhizal fungus (Scutellospora heterogama) and the root-knot nematode (Meloidogyne incognita) on sweet passion fruit (Passiflora alata) Braz Arch Biol Technol. 2010;53:801–809. doi: 10.1590/S1516-89132010000400008. DOI
Azcon-Aguilar C, Barea JM. Arbuscular mycorrhizas and biological control of soilborne plant pathogens, an overview of the mechanisms involved. Mycorrhiza. 1996;6:457–464. doi: 10.1007/s005720050147. DOI
Banuelos J, Alarcón A, Larsen J, Cruz-Sánchez S, Trejo D. Interactions between arbuscular mycorrhizal fungi and Meloidogyne incognita in the ornamental plant Impatiens balsamina. J Soil Sci Plant Nutr. 2014;14:63–74.
Bergeson GB. Mobilization of minerals to the infection site of root knot nematodes. Phytopathology. 1966;56:1287–1289.
Berruti A, Lumini E, Balestrini R, Bianciotto V. Arbuscular mycorrhizal fungi as natural biofertilizers: let’s benefit from past successes. Front Microbiol. 2016;6:1559. doi: 10.3389/fmicb.2015.01559. PubMed DOI PMC
Blažková A, Jansa J, Püschel D, Vosatka M, Janoušková M. Is mycorrhiza functioning influenced by the quantitative composition of the mycorrhizal fungal community? Soil Biol Biochem. 2021;157:108249. doi: 10.1016/j.soilbio.2021.108249. DOI
Boussageon R, Marro N, Janoušková M, Brulé D, Wipf D, Courty PE. The fine-tuning of mycorrhizal pathway in Sorghum depends on both nitrogen-phosphorus availability and the identity of the fungal partner. Plant Cell Environ. 2022;45:3354–3366. doi: 10.1111/pce.14426. PubMed DOI
Buil PA, Jansa J, Blažková A, Holubík O, Duffková R, Rozmoš M, Püschel D, Kotianová M, Janoušková M. Infectivity and symbiotic efficiency of native arbuscular mycorrhizal fungi from high-input arable soils. Plant Soil. 2023;482:627–645. doi: 10.1007/s11104-022-05715-8. DOI
Cabello MN. Hydrocarbon pollution: its effect on native arbuscular mycorrhizal fungi (AMF) FEMS Microbiol Ecol. 1997;22:233–236. doi: 10.1111/j.1574-6941.1997.tb00375.x. DOI
Carneiro RG, Mazzafera P, Ferraz ICCB, Muraoka T, Trevelin PCO. Uptake and translocation of nitrogen, phosphorus and calcium in soybean infected with Meloidogyne incognita and M. javanica. Fitopatol Bras. 2002;27:141–150. doi: 10.1590/S0100-41582002000200004. DOI
Carrara JE, Heller WP. Arbuscular mycorrhizal species vary in their impact on nutrient uptake in sweet corn (Zea mays) and butternut squash (Cucurbita moschata) Front Agron. 2022;4:1040054. doi: 10.3389/fagro.2022.1040054. DOI
Castagnone-Sereno P, Danchin EGJ, Perfus-Barbeoch L, Abad P. Diversity and evolution of Root-Knot nematodes, Genus Meloidogyne: New insights from the genomic era. Annu Rev Phytopathol. 2013;51:203–220. doi: 10.1146/annurev-phyto-082712-102300. PubMed DOI
Castillo P, Nico AI, Azcón-Aguilar C, Del Río Rincón C, Calvet C, Jiménez-Díaz RM. Protection of olive planting stocks against parasitism of root-knot nematodes by arbuscular mycorrhizal fungi. Plant Pathol. 2006;55:705–713. doi: 10.1111/j.1365-3059.2006.01400.x. DOI
Chan C, Liao YY, Chiou TJ. The impact of phosphorus on plant immunity. Plant Cell Physiol. 2021;62(4):582–589. doi: 10.1093/pcp/pcaa168. PubMed DOI
Chen S, Jin W, Liu A, Zhang S, Liu D, Wang F, Lin X, He C. Arbuscular mycorrhizal fungi (AMF) increase growth and secondary metabolism in cucumber subjected to low temperature stress. Sci Hortic. 2013;160:222–229. doi: 10.1016/j.scienta.2013.05.039. DOI
da Silva Campos MA. Bioprotection by arbuscular mycorrhizal fungi in plants infected with Meloidogyne nematodes: a sustainable alternative. Crop Prot. 2020;135:105203. doi: 10.1016/j.cropro.2020.105203. DOI
de Almeida GQ, de Oliveira Silva J, Copati MGF, de Oliveira Dias F, dos Santos MC. Tomato breeding for disease resistance. Multi-Sci J. 2020;3(3):8–16. doi: 10.33837/msj.v3i3.1287. DOI
De Sá CSB, Campos MAS (2020) Arbuscular mycorrhizal fungi decrease Meloidogyne Enterolobii infection of Guava seedlings. J Helminthol 94:e183 PubMed
Decraemer W, Hunt DJ. Plant nematology. Wallingford UK: CABI; 2006. Structure and classification; pp. 3–32.
Di Rienzo JA, Guzmán AW, Casanoves F. A multiple-comparisons method based on the distribution of the root node distance of a binary tree. J Agric Biol Environ Stat. 2002;7:129–142. doi: 10.1198/10857110260141193. DOI
Diagne N, Ngom M, Djighaly PI, Fall D, Hocher V, Svistoonoff S. Roles of arbuscular mycorrhizal fungi on plant growth and performance: importance in biotic and abiotic stressed regulation. Diversity. 2020;12:370. doi: 10.3390/d12100370. DOI
Dowarah B, Gill SS, Agarwala N. Arbuscular mycorrhizal fungi in conferring tolerance to biotic stresses in plants. J Plant Growth Regul. 2022;41:1429–1444. doi: 10.1007/s00344-021-10392-50. DOI
Escobar C, Barcala M, Cabrera J, Fenoll C. Advances in botanical research. Academic; 2015. Overview of root-knot nematodes and giant cells; pp. 1–32.
Gao X, Starr J, Göbel C, Engelberth J, Feussner I, Tumlinson J, Kolomiets M. Maize 9-lipoxygenase ZmLOX3 controls development, root-specific expression of defense genes, and resistance to root-knot nematodes. Mol Plant Microbe Interact. 2008;21:98–109. doi: 10.1094/MPMI-21-1-0098. PubMed DOI
Grandison GS, Cooper KM. Interaction of vesicular-arbuscular mycorrhizae and cultivars of alfalfa susceptible and resistant to Meloidogyne hapla. J Nematol. 1986;18:141. PubMed PMC
Gutiérrez-Gutiérrez C, Palomares-Rius JE, Jiménez-Díaz RM, Castillo P. Host suitability of Vitis rootstocks to root-knot nematodes (Meloidogyne spp.) and the dagger nematode Xiphinema index, and plant damage caused by infections. Plant Pathol. 2011;60:575–585. doi: 10.1111/j.1365-3059.2010.02404.x. DOI
Hart MM, Reader RJ. Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytol. 2002;153:335–344. doi: 10.1046/j.0028-646X.2001.00312.x. DOI
Hartig F, Lohse L (2020) Residual diagnostics for hierarchical (multi-level/mixed) regression models. Package ‘DHARMa’ Version 0.3.3.0. https://CRAN.R-project.org/package=DHARMa
Herrera-Parra E, Ramos-Zapata J, Basto-Pool C, Cristóbal-Alejo J (2021) Sweet pepper (Capsicum annuum) response to the inoculation of native arbuscular mycorrhizal fungi and the parasitism of root-knot Meloidogyne incognita. Revista Bio Ciencias 8:e982. 10.15741/revbio.08.e982
Hewitt EJ. Sand and water culture methods used in the study of plant nutrition. Technical communication no. 22. Commonwealth Agriculture Bureau; 1966.
Hodge A, Fitter AH. Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. Proc Natl Acad Sci USA. 2010;107:13754–13759. doi: 10.1073/pnas.1005874107. PubMed DOI PMC
Hussey RS, Barker KR. A comparison of methods of collecting inocula of Meloidogyne spp., including a new technique. Plant Dis Rep. 1973;57:1025–1028.
InfoStat versión 2011 (2011) Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina. http://www.infostat.com.ar
Ingraffia R, Amato G, Sosa-Hernández MA, Frenda AS, Rillig MC, Giambalvo D. Nitrogen type and availability drive mycorrhizal effects on wheat performance, nitrogen uptake and recovery, and production sustainability. Front Plant Sci. 2020;11:760. doi: 10.3389/fpls.2020.00760. PubMed DOI PMC
Jansa J, Smith FA, Smith SE. Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? New Phytol. 2008;177:779–789. doi: 10.1111/j.1469-8137.2007.02294.x. PubMed DOI
Johnson NC, Graham JH, Smith FA. Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol. 1997;135:575–585. doi: 10.1046/j.1469-8137.1997.00729.x. DOI
Jones JT, Haegeman A, Danchin EG, Gaur HS, Helder J, Jones MG, Kikuchi T, Manzanilla-López R, Palomares-Rius JE, Wesemael WM, Perry RN. Top 10 plant-parasitic nematodes in molecular plant pathology. Mol Plant Pathol. 2013;14:946–961. doi: 10.1111/mpp.12057. PubMed DOI PMC
Klironomos JN, Hart MM. Colonization of roots by arbuscular mycorrhizal fungi using different sources of inoculum. Mycorrhiza. 2002;12:181–184. doi: 10.1007/s00572-002-0169-6. PubMed DOI
Koerselman W, Meuleman AFM. The vegetation N: P ratio: a new tool to detect the nature of nutrient limitation. J Appl Ecol. 1996;33:1441–1450. doi: 10.2307/2404783. 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
López-Ráez JA, Verhage A, Fernandez I, García JM, Azcon-Aguilar C, Flors V, Pozo M. Hormonal and transcriptional profiles highlight common and differential host responses to arbuscular mycorrhizal fungi and the regulation of the oxylipin pathway. J Exp Bot. 2010;61:2589–2601. doi: 10.1093/jxb/erq089. PubMed DOI PMC
Marro N, Caccia M, Doucet ME, Cabello M, Becerra A, Lax P. Mycorrhizas reduce tomato root penetration by false root–knot nematode Nacobbus aberrans. Appl Soil Ecol. 2018;124:262–265. doi: 10.1016/j.apsoil.2017.11.011. DOI
Marro N, Grilli G, Soteras F, Caccia M, Longo S, Cofré N, Borda V, Burni M, Janoušková M, Urcelay C. The effects of arbuscular mycorrhizal fungal species and taxonomic groups on stressed and unstressed plants: a global meta-analysis. New Phytol. 2022;235:320–332. doi: 10.1111/nph.18102. PubMed DOI
Marro N, Lax P, Doucet ME, Cabello M, Becerra A. Use of the arbuscular mycorrhizal fungus Glomus intraradices as biological control agent of the nematode Nacobbus aberrans parasitizing tomato. Braz Arch Biol Technol. 2014;57:668–674. doi: 10.1590/S1516-8913201402200. DOI
Marulanda A, Azcon R, Ruiz-Lozano JM. Contribution of six arbuscular mycorrhizal fungal isolates to water uptake by Lactuca sativa plants under drought stress. Physiol Plant. 2003;119:526–533. doi: 10.1046/j.1399-3054.2003.00196.x. DOI
Mc Gonigle TP, Miller MH, Evans DG, et al. A new method which gives and 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
Mensah JA, Koch AM, Antunes PM, et al. High functional diversity within species of arbuscular mycorrhizal fungi is associated with differences in phosphate and nitrogen uptake and fungal phosphate metabolism. Mycorrhiza. 2015;25:533–546. doi: 10.1007/S00572-015-0631-X. PubMed DOI
Mitchum MG, Hussey RS, Baum TJ, Wang X, Elling AA, Wubben M, Davis EL. Nematode effector proteins: an emerging paradigm of parasitism. New Phytol. 2013;199:879–894. doi: 10.1111/nph.12323. PubMed DOI
Molinari S, Leonetti P. Bio-control agents activate plant immune response and prime susceptible tomato against root-knot nematodes. PLoS ONE. 2019;14(12):e0213230. doi: 10.1371/journal.pone.021323. PubMed DOI PMC
Montero H, Choi J, Paszkowski U. Arbuscular mycorrhizal phenotyping: the dos and don’ts. New Phytol. 2019;221:1182–1186. doi: 10.1111/nph.15489. PubMed DOI PMC
Munkvold L, Kjøller R, Vestberg M, Rosendahl S, Jakobsen I. High functional diversity within species of arbuscular mycorrhizal fungi. New Phytol. 2004;164:357–364. doi: 10.1111/j.1469-8137.2004.01169.x. PubMed DOI
Murphy J, Riley JP. A modified single solution method the determination of phosphate. Anal Chim Acta. 1962;27:31–36. doi: 10.1016/S0003-2670(00)88444-5. DOI
Oteifa BA, Elgindi DM. Influence of parasitic duration of Meloidogyne javanica (Treub) on host nutrient uptake. Nematologica. 1962;8:216–220. doi: 10.1163/187529262X00459. DOI
Perry R, Moens M. Genomics and molecular genetics of plant-nematode interactions. Springer Netherlands; 2011. Introduction to plant-parasitic nematodes; modes of parasitism; pp. 3–20.
Phani V, Khan MR, Dutta TK. Plant-parasitic nematodes as a potential threat to protected agriculture: current status and management options. Crop Prot. 2021;144:105573. doi: 10.1016/j.cropro.2021.105573. DOI
Powell JR, Parrent JL, Hart MM, Klironomos JN, Rillig MC, Maherali H. Phylogenetic trait conservatism and the evolution of functional trade-offs in arbuscular mycorrhizal fungi. Proc Royal Soc B Biol Sci. 2009;276:4237–4245. doi: 10.1098/rspb.2009.1015. PubMed DOI PMC
Pozo MJ, Azcon-Aguilar C. Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol. 2007;10:393–398. doi: 10.1016/j.pbi.2007.05.004. PubMed DOI
Püschel D, Bitterlich M, Rydlová J, Jansa J. Drought accentuates the role of mycorrhiza in phosphorus uptake. Soil Biol Biochem. 2021;157:1–11. doi: 10.1016/j.soilbio.2021.108243. DOI
Püschel D, Janoušková M, Hujslová M, Slavíková R, Gryndlerová H, Jansa J. Plant–fungus competition for nitrogen erases mycorrhizal growth benefits of Andropogon gerardii under limited nitrogen supply. Ecol Evol. 2016;6:4332–4346. doi: 10.1002/ece3.2207. PubMed DOI PMC
Qin WJ, Yan HY, Zou BY, Guo RZ, Ci DW, Tang ZH, Zou XX, Zhang XJ, Yu XN, Wang YF, Si T. Arbuscular mycorrhizal fungi alleviate salinity stress in peanut: evidence from pot-grown and field experiments. Food Energy Secur. 2021;10:e314. doi: 10.1002/fes3.314. DOI
R Development Core Team (2011) R: A language and environment for statistical computing
Rodriguez-Heredia M, Djian-Caporalino C, Ponchet M, Lapeyre L, Canaguier R, Fazari A, Marteu N, Industri B, Offroy-Chave M. Protective effects of mycorrhizal association in tomato and pepper against Meloidogyne incognita infection, and mycorrhizal networks for early mycorrhization of low mycotrophic plants. Phytopathol Mediterr. 2020;59:377–384. doi: 10.14601/Phyto-11637. DOI
Rolfe SA, Griffiths J, Ton J. Crying out for help with root exudates: adaptive mechanisms by which stressed plants assemble health-promoting soil microbiomes. Curr Opin Microbiol. 2019;49:73–82. doi: 10.1016/j.mib.2019.10.003. PubMed DOI
Säle V, Palenzuela J, Azcón-Aguilar C, Sánchez-Castro I, da Silva GA, Seitz B, Seitz B, Sieverding E, Heijden MG, vander, Oehl F. Ancient lineages of arbuscular mycorrhizal fungi provide little plant benefit. Mycorrhiza. 2021;31:559–576. doi: 10.1007/s00572-021-01042-5. PubMed DOI PMC
Schouteden N, De Waele D, Panis B, Vos CM. Arbuscular mycorrhizal fungi for the biocontrol of plant-parasitic nematodes: a review of the mechanisms involved. Front Microbiol. 2015;6:1280. doi: 10.3389/fmicb.2015.01280. PubMed DOI PMC
Shafiee MF, Jenkins WR. Host-parasite relationships of Capsicum frutescens and Pratylenchus penetrans, Meloidogyne incognita acrita, and M. hapla. Phytopathol. 1963;53:325–328.
Sikes BA, Cottenie K, Klironomos JN. Plant and fungal identity determines pathogen protection of plant roots by arbuscular mycorrhizas. J Ecol. 2009;97:1274–1280. doi: 10.1111/j.13652745.2009.01557.x. DOI
Smith FA, Grace EJ, Smith SE. More than a carbon economy: nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbioses. New Phytol. 2009;182:347–358. doi: 10.1111/j.1469-8137.2008.02753.x. PubMed DOI
Smith SE, Smith FA. Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol. 2011;62:227–250. doi: 10.1146/annurev-arplant-042110-103846. PubMed DOI
Smith SE, Smith FA. Fresh perspectives on the roles of arbuscular mycorrhizal fungi in plant nutrition and growth. Mycologia. 2012;104:1–13. doi: 10.3852/11-229. PubMed 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
Subedi S, Thapa B, Shrestha J. Root-knot nematode (Meloidogyne incognita) and its management: a review. J Agric Nat Resour. 2020;3(2):21–31. doi: 10.3126/janr.v3i2.32298. DOI
Talavera M, Itou K, Mizukubo T. Reduction of nematode damage by root colonization with arbuscular mycorrhiza (Glomus spp.) in tomato-Meloidogyne incognita (Tylenchida: Meloidogynidae) and carrot-Pratylenchus penetrans (Tylenchida: Pratylenchidae) pathosystems. Appl Entomol Zool. 2001;36:387–392. doi: 10.1303/aez.2001.387. DOI
Terry V, Kokkoris V, Villeneuve-Laroche M, Turcu B, Chapman K, Cornell C, Zheng Z, Stefani F, Corradi N. Mycorrhizal response of Solanum tuberosum to homokaryotic versus dikaryotic arbuscular mycorrhizal fungi. Mycorrhiza. 2023;33:333–344. doi: 10.1007/s00572-023-01123-7. PubMed DOI
Tian M, Chen YL, Li M, Liu RJ. Structure and function of arbuscular mycorrhiza: a review. J Appl Ecol. 2013;24:2369–2376. PubMed
Treseder KK, Allen MF. Direct nitrogen and phosphorus limitation of arbuscular mycorrhizal fungi: a model and field test. New Phytol. 2002;155:507–515. doi: 10.1046/j.1469-8137.2002.00470.x. PubMed DOI
Turrini A, Avio L, Giovannetti M, Agnolucci M. Functional complementarity of arbuscular mycorrhizal fungi and associated microbiota: the challenge of Translational Research. Front Plant Sci. 2018;9:1407. doi: 10.3389/fpls.2018.01407. PubMed DOI PMC
Vierheilig H, Steinkellner S, Khaosaad T. Mycorrhiza. Berlin: Springer; 2008. The biocontrol effect of mycorrhization on soilborne fungal pathogens and the autoregulation of the AM symbiosis: one mechanism, two effects? pp. 307–320.
Vilela RMIF, Kuster VC, Magalhães TA, Moraes CA, Paula Filho AC, Oliveira DC, Moench Impact of Meloidogyne incognita (nematode) infection on root tissues and cell wall composition of okra (Abelmoschus esculentus L. Moench, Malvaceae) Protoplasma. 2021;258:979–990. doi: 10.1007/s00709-021-01618-0. PubMed DOI
Voříšková A, Jansa J, Püschel D, Krüger M, Cajthaml T, Vosátka M, Janoušková M. Real-time PCR quantification of arbuscular mycorrhizal fungi: does the use of nuclear or mitochondrial markers make a difference? Mycorrhiza. 2017;27:577–585. doi: 10.1007/s00572-017-0777-9. PubMed DOI
Voříšková A, Jansa J, Püschel D, Vosátka M, Šmilauer P, Janoušková M. Abiotic contexts consistently influence mycorrhiza functioning independently of the composition of synthetic arbuscular mycorrhizal fungal communities. Mycorrhiza. 2019;29:127–139. doi: 10.1007/s00572-018-00878-8. PubMed DOI
Vos C, Claerhout S, Mkandawire R, Panis B, De Waele D, Elsen A. Arbuscular mycorrhizal fungi reduce root-knot nematode penetration through altered root exudation of their host. Plant Soil. 2012;354:335–345. doi: 10.1007/s11104-011-1070-x. DOI
Vos C, Tesfahun AN, Panis B, De Waele D, Elsen A. Arbuscular mycorrhizal fungi induce systemic resistance in tomato against the sedentary nematode Meloidogyne incognita and the migratory nematode Pratylenchus penetrans. Appl Soil Ecol. 2012;61:1–6. doi: 10.1016/j.apsoil.2012.04.007. DOI
Vos C, Schouteden N, Van Tuinen D, Chatagnier O, Elsen A, De Waele D, Panis B, Gianinazzi-Pearson V. Mycorrhiza-induced resistance against the root–knot nematode Meloidogyne incognita involves priming of defense gene responses in tomato. Soil Biol Bioch. 2013;60:45–54. doi: 10.1016/j.soilbio.2013.01.013. DOI
Waghmare C, Singh P, Paul S, Sharma HK. Influence of root-knot nematode, Meloidogyne incognita (Kofoid & White) Chitwood infection on different plant growth parameters in Mungbean, Vigna radiata (L.) Wilczek. Indian J Exp Biol. 2022;60:351–359.
Wang L, Chen X, Tang Z. Arbuscular mycorrhizal symbioses improved biomass allocation and reproductive investment of cherry tomato after root-knot nematodes infection. Plant Soil. 2023;482:513–527. doi: 10.1007/s11104-022-05708. DOI
Zbíral J. Analýza rostlinného materiálu. Jednotné pracovní postupy [Analysis of plant material. Unified techniques] Brno: Státní kontrolní a zkušební ústav zemědělský; 1994.