Advertisement

Mycorrhiza

, Volume 29, Issue 1, pp 29–38 | Cite as

Common mycorrhizal networks influence the distribution of mineral nutrients between an invasive plant, Solidago canadensis, and a native plant, Kummerowa striata

  • Awagul Awaydul
  • Wanying Zhu
  • Yongge Yuan
  • Jing Xiao
  • Hao Hu
  • Xin Chen
  • Roger T. Koide
  • Lei ChengEmail author
Original Article
  • 165 Downloads

Abstract

Invasive species often reduce ecosystem services and lead to a serious threat to native biodiversity. Roots of invasive plants are often linked to roots of native plants by common mycorrhizal networks (CMNs) of arbuscular mycorrhizal (AM) fungi, but whether and how CMNs mediate interactions between invasive and native plant species remains largely uninvestigated. We conducted two microcosm experiments, one in which we amended the soil with mineral N and another in which we amended the soil with mineral P. In each experiment, we grew a pair of test plants consisting of Kummerowia striata (native to our research site) and Solidago canadensis (an invasive species). CMNs were established between the plants, and these were either left intact or severed. Intact CMNs increased growth and nutrient acquisition by S. canadensis while they decreased nutrient acquisition by K. striata in comparison with severed CMNs. 15N and P analyses indicated that compared to severed CMNs, intact CMNs preferentially transferred mineral nutrients to S. canadensis. CMNs produced by different species of AM fungi had slightly different effects on the interaction between these two plant species. These results highlight the role of CMNs in the understanding of interactions between the invasive species S. canadensis and its native neighbor.

Keywords

Arbuscular mycorrhizal fungi Common mycorrhizal networks Kummerowia striata Nutrient uptake Plant invasion Solidago canadensis 

Notes

Acknowledgements

We highly appreciate Dr. Dave Janos’ and two anonymous reviewers’ insightful comments and suggestions on an earlier version of this manuscript.

Funding information

This study was supported by the National Natural Science Foundation of China (NSFC# 31500416, 31422010, and 31670501), the National Key Research and Development Program of China (2016YFC0502704), the Fundamental Research Funds for the Central Universities, and the Zhejiang University K. P. Chao’s High Technology Development Foundation.

Supplementary material

572_2018_873_MOESM1_ESM.docx (43 kb)
ESM 1 (DOCX 43 kb)

References

  1. Ames RN, Reid CPP, Porter LK, Cambardella C (1983) Hyphal uptake and transport of nitrogen from two 15N labeled sources by Glomus mosseae. New Phytol 95:381–396.  https://doi.org/10.1111/j.1469-8137.1983.tb03506.x CrossRefGoogle Scholar
  2. Babikova Z, Gilbert L, Bruce TJA, Birkett M, Caulfield JC, Woodcock C, Pickett JA, Johnson D (2013) Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack. Ecol Lett 16:835–843.  https://doi.org/10.1111/ele.12115 CrossRefPubMedGoogle Scholar
  3. Barto EK, Hilker M, Müller F, Mohney BK, Weidenhamer JD, Rillig MC (2011) The fungal fast lane: common mycorrhizal networks extend bioactive zones of allelochemicals in soils. PLoS One 6:e27195.  https://doi.org/10.1371/journal.pone.0027195 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bunn RA, Ramsey PW, Lekberg Y (2015) Do native and invasive plants differ in their interactions with arbuscular mycorrhizal fungi? A meta-analysis. J Ecol 103:1547–1556.  https://doi.org/10.1111/1365-2745.12456 CrossRefGoogle Scholar
  5. Callaway RM, Thelen GC, Rodriguez A, Holben WE (2004) Soil biota and exotic plant invasion. Nature 427:731–733.  https://doi.org/10.1038/nature02322 CrossRefPubMedGoogle Scholar
  6. Chen X, Tang JJ, Fang ZG, Shimizu K (2004) Effects of weed communities with various species numbers on soil features in a subtropical orchard ecosystem. Agric Ecosyst Environ 102:377–388.  https://doi.org/10.1016/j.agee.2003.08.006 CrossRefGoogle Scholar
  7. Cheng L, Booker FL, Tu C, Burkey KO, Zhou L, Shew HD, Rufty TW, Hu S (2012) Arbuscular mycorrhizal fungi increase organic carbon decomposition under elevated CO2. Science 337:1084–1087.  https://doi.org/10.1126/science.1224304 CrossRefPubMedGoogle Scholar
  8. Cheng L, Chen W, Adams TS, Wei X, Li L, McCormack ML, DeForest JL, Koide RT, Eissenstat DM (2016) Mycorrhizal fungi and roots are complementary in foraging within nutrient patches. Ecology 97:2815–2823.  https://doi.org/10.1002/ecy.1514 CrossRefPubMedGoogle Scholar
  9. Cronk QCB, Fuller JL (1995) Plant invaders: the threat to natural ecosystems. People and Plants Conservation Manuals. Chapman & Hall, LondonGoogle Scholar
  10. Dickie IA, Bufford JL, Cobb RC, Desprez-Loustau ML, Grelet G, Hulme PE, Klironomos J, Makiola A, Nuñez MA, Pringle A, Thrall PH, Tourtellot SG, Waller L, Williams NM (2017) The emerging science of linked plant-fungal invasions. New Phytol 215:1314–1332.  https://doi.org/10.1111/nph.14657 CrossRefPubMedGoogle Scholar
  11. Dong M, Lu JZ, Zhang WJ, Chen JK, Li B (2006) Canada goldenrod (Solidago canadensis): an invasive alien weed rapidly spreading in China. Acta Phytotaxon Sin 44:72–85.  https://doi.org/10.1360/aps050068 CrossRefGoogle Scholar
  12. Dong L-J, Sun Z-K, Gao Y, He W-M (2015) Two-year interactions between invasive Solidago canadensis and soil decrease its subsequent growth and competitive ability. J Plant Ecol 8:617–622.  https://doi.org/10.1093/jpe/rtv003 CrossRefGoogle Scholar
  13. Fellbaum CR, Mensah JA, Cloos AJ, Strahan GE, Pfeffer PE, Kiers ET, Bücking H (2014) Fungal nutrient allocation in common mycorrhizal networks is regulated by the carbon source strength of individual host plants. New Phytol 203:646–656.  https://doi.org/10.1111/nph.12827 CrossRefPubMedGoogle Scholar
  14. Giovannetti M, Mosse B (1980) Evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500.  https://doi.org/10.1111/j.1469-8137.1980.tb04556.x CrossRefGoogle Scholar
  15. Hart MM, Reader RJ (2002) Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytol 153:335–344.  https://doi.org/10.1046/j.0028-646X.2001.00312.x CrossRefGoogle Scholar
  16. Hart MM, Reader RJ, Klironomos JN (2003) Plant coexistence mediated by arbuscular mycorrhizal fungi. Trends Ecol Evol 18:418–423.  https://doi.org/10.1016/s0169-5347(03)00127-7 CrossRefGoogle Scholar
  17. Hoeksema JD (2015) Experimentally testing effects of mycorrhizal networks on plant-plant interactions and distinguishing among mechanisms. In: Horton T (ed) Mycorrhizal networks. Springer, Dordrecht, pp 255–277.  https://doi.org/10.1007/978-94-017-7395-9_9 CrossRefGoogle Scholar
  18. Horton TR (2015) Mycorrhizal networks. Springer, DordrechtCrossRefGoogle Scholar
  19. Jakobsen I, Hammer EC (2015) Nutrient dynamics in arbuscular mycorrhizal networks. In: Horton T (ed) Mycorrhizal Networks. Springer, Dordrecht, pp 91–131.  https://doi.org/10.1007/978-94-017-7395-9_4 CrossRefGoogle Scholar
  20. Janos DP (2007) Plant responsiveness to mycorrhizas differs from dependence upon mycorrhizas. Mycorrhiza 17:75–91.  https://doi.org/10.1007/s00572-006-0094-1 CrossRefPubMedGoogle Scholar
  21. Johnson D, Gilbert L (2015) Interplant signalling through hyphal networks. New Phytol 205:1448–1453.  https://doi.org/10.1111/nph.13115 CrossRefPubMedGoogle Scholar
  22. Johnson D, Leake J, Read D (2001) Novel in-growth core system enables functional studies of grassland mycorrhizal mycelial networks. New Phytol 152:555–562 https://doi.org/http://www.jstor.org/stable/1353726 CrossRefGoogle Scholar
  23. Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A, Palmer TM, West SA, Vandenkoornhuyse P, Jansa J, Bucking H (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–882.  https://doi.org/10.1126/science.1208473 CrossRefPubMedGoogle Scholar
  24. Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301.  https://doi.org/10.1890/02-0413 CrossRefGoogle Scholar
  25. Koide RT, Li M (1989) Appropriate controls for vesicular–arbuscular mycorrhiza research. New Phytol 111:35–44.  https://doi.org/10.1111/j.1469-8137.1989.tb04215.x CrossRefGoogle Scholar
  26. Kormanik PP, Bryan WC, Schultz RC (1980) Procedures and equipment for staining large numbers of plant root samples for endomycorrhizal assay. Can J Microbiol 26:536–538.  https://doi.org/10.1139/m80-090 CrossRefPubMedGoogle Scholar
  27. Lekberg Y, Hammer EC, Olsson PA (2010) Plants as resource islands and storage units—adopting the mycocentric view of arbuscular mycorrhizal networks. FEMS Microbiol Ecol 74:336–345.  https://doi.org/10.1111/j.1574-6941.2010.00956.x CrossRefPubMedGoogle Scholar
  28. Lu JZ, Weng ES, Wu XW, Weber E, Zhao B, Li B (2007) Potential distribution of Solidago canadensis in China. Acta Phytotaxon Sin 45:670–674.  https://doi.org/10.1360/aps06200 CrossRefGoogle Scholar
  29. Menzel A, Hempel S, Klotz S, Moora M, Pyšek P, Rillig MC, Zobel M, Kühn I (2017) Mycorrhizal status helps explain invasion success of alien plant species. Ecology 98:92–102.  https://doi.org/10.1002/ecy.1621 CrossRefPubMedGoogle Scholar
  30. Merrild MP, Ambus P, Rosendahl S, Jakobsen I (2013) Common arbuscular mycorrhizal networks amplify competition for phosphorus between seedlings and established plants. New Phytol 200:229–240.  https://doi.org/10.1111/nph.12351 CrossRefPubMedGoogle Scholar
  31. Mitchell CE, Agrawal AA, Bever JD, Gilbert GS, Hufbauer RA, Klironomos JN, Maron JL, Morris WF, Parker IM, Power AG, Seabloom EW, Torchin ME, Vazquez DP (2006) Biotic interactions and plant invasions. Ecol Lett 9:726–740.  https://doi.org/10.1111/j.1461-0248.2006.00908.x CrossRefPubMedGoogle Scholar
  32. Nuccio EE, Hodge A, Pett-Ridge J, Herman DJ, Weber PK, Firestone MK (2013) An arbuscular mycorrhizal fungus significantly modifies the soil bacterial community and nitrogen cycling during litter decomposition. Environ Microbiol 15:1870–1881.  https://doi.org/10.1111/1462-2920.12081 CrossRefPubMedGoogle Scholar
  33. Nunez MA, Dickie IA (2014) Invasive belowground mutualists of woody plants. Biol Invasions 16:645–661.  https://doi.org/10.1007/s10530-013-0612-y CrossRefGoogle Scholar
  34. Pringle A, Bever JD, Gardes M, Parrent JL, Rillig MC, Klironomos JN (2009) Mycorrhizal symbioses and plant invasions. Ann Rev Ecol Evol Syst 40:699–715.  https://doi.org/10.1146/annurev.ecolsys.39.110707.173454 CrossRefGoogle Scholar
  35. Reinhart KO, Callaway RM (2006) Soil biota and invasive plants. New Phytol 170:445–457.  https://doi.org/10.1111/j.1469-8137.2006.01715.x CrossRefPubMedGoogle Scholar
  36. Richardson DM, Allsopp N, D’Antonio CM, Milton SJ, Rejmanek M (2000) Plant invasions—the role of mutualisms. Biol Rev 75:65–93.  https://doi.org/10.1017/S0006323199005435 CrossRefPubMedGoogle Scholar
  37. Rudgers JA, Orr S (2009) Non-native grass alters growth of native tree species via leaf and soil microbes. J Ecol 97:247–255.  https://doi.org/10.1111/j.1365-2745.2008.01478.x CrossRefGoogle Scholar
  38. Schüßler A, Walker C (2010) The Glomeromycota: a species list with new families and new genera. http://www.amf-phylogenycom. Accessed 8 June 2018
  39. Selosse M-A, Richard F, He X, Simard SW (2006) Mycorrhizal networks: des liaisons dangereuses? Trends Ecol Evol 21:621–628.  https://doi.org/10.1016/j.tree.2006.07.003 CrossRefPubMedGoogle Scholar
  40. Shah MA, Reshi ZA, Khasa DP (2009) Arbuscular mycorrhizas: drivers or dassengers of alien plant invasion. Bot Rev 75:397–417.  https://doi.org/10.1007/s12229-009-9039-7 CrossRefGoogle Scholar
  41. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Elsevier Academic Press Inc, San DiegoGoogle Scholar
  42. Song YY, Ye M, Li C, He X, Zhu-Salzman K, Wang RL, Su YJ, Luo SM, Zeng RS (2014) Hijacking common mycorrhizal networks for herbivore-induced defence signal transfer between tomato plants. Sci Rep 4(3915).  https://doi.org/10.1038/srep03915
  43. Tanaka Y, Yano K (2005) Nitrogen delivery to maize via mycorrhizal hyphae depends on the form of N supplied. Plant Cell Environ 28:1247–1254.  https://doi.org/10.1111/j.1365-3040.2005.01360.x CrossRefGoogle Scholar
  44. van der Heijden MGA, Horton TR (2009) Socialism in soil? The importance of mycorrhizal fungal networks for facilitation in natural ecosystems. J Ecol 97:1139–1150.  https://doi.org/10.1111/j.1365-2745.2009.01570.x CrossRefGoogle Scholar
  45. van der Heijden MGA, Boller T, Wiemken A, Sanders IR (1998) Different arbuscular mycorrhizal fungal species are potential determinants of plant community structure. Ecology 79:2082–2091.  https://doi.org/10.2307/176711 CrossRefGoogle Scholar
  46. van der Heijden MGA, Wiemken A, Sanders IR (2003) Different arbuscular mycorrhizal fungi alter coexistence and resource distribution between co-occurring plant. New Phytol 157:569–578.  https://doi.org/10.1046/j.1469-8137.2003.00688.x CrossRefGoogle Scholar
  47. Vogelsang KM, Bever JD (2009) Mycorrhizal densities decline in association with nonnative plants and contribute to plant invasion. Ecology 90:399–407.  https://doi.org/10.1890/07-2144.1 CrossRefPubMedGoogle Scholar
  48. Walder F, van der Heijden MGA (2015) Regulation of resource exchange in the arbuscular mycorrhizal symbiosis. Nat Plants 1(15159).  https://doi.org/10.1038/nplants.2015.159
  49. Walder F, Niemann H, Natarajan M, Lehmann MF, Boller T, Wiemken A (2012) Mycorrhizal networks: common goods of plants shared under unequal terms of trade. Plant Physiol 159:789–797  https://doi.org/10.1104/pp.112.195727 CrossRefGoogle Scholar
  50. Wan L-Y, Qi S-S, Zou CB, Dai Z-C, Zhu B, Song Y-G, Du D-L (2018) Phosphorus addition reduces the competitive ability of the invasive weed Solidago canadensis under high nitrogen conditions. Flora 240:68–75.  https://doi.org/10.1016/j.flora.2017.12.012 CrossRefGoogle Scholar
  51. Weber E (1997) Morphological variation of the introduced perennial Solidago canadensis L. sensu lato (Asteraceae) in Europe. Bot Jo Linn Soc 123:197–210.  https://doi.org/10.1006/bojl.1996.0086 CrossRefGoogle Scholar
  52. Weremijewicz J, Janos DP (2013) Common mycorrhizal networks amplify size inequality in Andropogon gerardii monocultures. New Phytol 198:203–213.  https://doi.org/10.1111/nph.12125 CrossRefPubMedGoogle Scholar
  53. Weremijewicz J, Sternberg LSLOR, Janos DP (2016) Common mycorrhizal networks amplify competition by preferential mineral nutrient allocation to large host plants. New Phytol 212:461–471.  https://doi.org/10.1111/nph.14041 CrossRefPubMedGoogle Scholar
  54. Weremijewicz J, Sternberg LSLOR, Janos DP (2017) Arbuscular common mycorrhizal networks mediate intra- and interspecific interactions of two prairie grasses. Mycorrhiza 28:71–83.  https://doi.org/10.1007/s00572-017-0801-0 CrossRefPubMedGoogle Scholar
  55. Wolfe BE, Klironomos JN (2005) Breaking new ground: soil communities and exotic plant invasion. Bioscience 55:477–487. https://doi.org/10.1641/0006-3568(2005)055[0477:BNGSCA]2.0.CO;2Google Scholar
  56. Workman RE, Cruzan MB (2016) Common mycelial networks impact competition in an invasive grass. Am J Bot 103:1041–1049.  https://doi.org/10.3732/ajb.1600142 CrossRefPubMedGoogle Scholar
  57. Wu BY, Nara K, Hogetsu T (2001) Can 14C labeled photosynthetic products move between Pinus densiflora seedlings linked by ectomycorrhizal mycelia? New Phytol 149:137–146.  https://doi.org/10.1046/j.1469-8137.2001.00010.x CrossRefGoogle Scholar
  58. Yang R, Zan S, Tang J, Chen X (2011) Invasion mechanisms of Solidago canadensis L.:a review. Acta Ecol Sin 31:1185–1194Google Scholar
  59. Yu H-W, Yang J-X, Gao Y, He W-M (2016) Soil organic nitrogen endows invasive Solidago canadensis with greater advantages in low-phosphorus conditions. Ecosphere 7.  https://doi.org/10.1002/ecs2.1254
  60. Yuan Y, Wang B, Zhang S, Tang J, Tu C, Hu S, Yong JWH, Chen X (2013) Enhanced allelopathy and competitive ability of invasive plant Solidago canadensis in its introduced range. J Plant Ecol 6:253–263.  https://doi.org/10.1093/jpe/rts033 CrossRefGoogle Scholar
  61. Zhang Q, Yang RY, Tang JJ, Yang HS, Hu SJ, Chen X (2010) Positive feedback between mycorrhizal fungi and plants influences plant invasion success and resistance to invasion. PLoS One 5:e12380.  https://doi.org/10.1371/journal.pone.0012380 CrossRefPubMedPubMedCentralGoogle Scholar
  62. Zhang S, Zhu W, Wang B, Tang J, Chen X (2011) Secondary metabolites from the invasive Solidago canadensis L. accumulation in soil and contribution to inhibition of soil pathogen Pythium ultimum. Appl Soil Ecol 48:280–286.  https://doi.org/10.1016/j.apsoil.2011.04.011 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.MOE Key Laboratory of Biosystems Homeostasis & Protection, College of Life SciencesZhejiang UniversityHangzhouChina
  2. 2.School of Life ScienceTaizhou UniversityTaizhouChina
  3. 3.Department of BiologyBrigham Young UniversityProvoUSA

Personalised recommendations