Mycorrhiza

, Volume 25, Issue 8, pp 587–597 | Cite as

Using mycorrhiza-defective mutant genotypes of non-legume plant species to study the formation and functioning of arbuscular mycorrhiza: a review

  • Stephanie J. Watts-Williams
  • Timothy R. Cavagnaro
Review

Abstract

A significant challenge facing the study of arbuscular mycorrhiza is the establishment of suitable non-mycorrhizal treatments that can be compared with mycorrhizal treatments. A number of options are available, including soil disinfection or sterilisation, comparison of constitutively mycorrhizal and non-mycorrhizal plant species, comparison of plants grown in soils with different inoculum potential and the comparison of mycorrhiza-defective mutant genotypes with their mycorrhizal wild-type progenitors. Each option has its inherent advantages and limitations. Here, the potential to use mycorrhiza-defective mutant and wild-type genotype plant pairs as tools to study the functioning of mycorrhiza is reviewed. The emphasis of this review is placed on non-legume plant species, as mycorrhiza-defective plant genotypes in legumes have recently been extensively reviewed. It is concluded that non-legume mycorrhiza-defective mutant and wild-type pairs are useful tools in the study of mycorrhiza. However, the mutant genotypes should be well characterised and, ideally, meet a number of key criteria. The generation of more mycorrhiza-defective mutant genotypes in agronomically important plant species would be of benefit, as would be more research using these genotype pairs, especially under field conditions.

Keywords

Arbuscular mycorrhiza Mycorrhiza-defective mutant genotype Reduced mycorrhizal colonisation (rmcSolanum lycopersicum (tomato) Micro-Tom 

Notes

Acknowledgments

We wish to thank Prof. Sally Smith for comments on a very early draft of the manuscript. We also gratefully acknowledge Prof. Sally Smith and A/Prof. Susan Barker for continued access to the rmc and 76R genotypes of tomato. TRC also thanks Prof. Louise Jackson and members of her group for many valuable discussions over the years. TRC also wishes to acknowledge the Australian Research Council for financial support (FT120100463). SJWW wishes to acknowledge support received from the Monash University Postgraduate Publications Award.

References

  1. Ané J-M, Kiss GB, Riely BK, Penmetsa RV, Oldroyd GED, Ayax C, Lévy J, Debellé F, Baek J-M, Kalo P, Rosenberg C, Roe BA, Long SR, Dénarié J, Cook DR (2004) Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303:1364–1367. doi: 10.1126/science.1092986 PubMedCrossRefGoogle Scholar
  2. Asghari HR, Cavagnaro TR (2011) Arbuscular mycorrhizas enhance plant interception of leached nutrients. Funct Plant Biol 38:219–226. doi: 10.1071/fp10180 CrossRefGoogle Scholar
  3. Asghari HR, Cavagnaro TR (2012) Arbuscular mycorrhizas reduce nitrogen loss via leaching. PLoS One 7:151–155. doi: 10.1371/journal.pone.0029825 CrossRefGoogle Scholar
  4. Asghari HR, Chittleborough DJ, Smith FA, Smith SE (2005) Influence of arbuscular mycorrhizal (AM) symbiosis on phosphorus leaching through soil cores. Plant Soil 275:181–193. doi: 10.1007/s11104-005-1328-2 CrossRefGoogle Scholar
  5. Barker SJ, Larkan NJ (2002) Molecular approaches to understanding mycorrhizal symbioses. Plant Soil 244:107–116. doi: 10.1023/a:1020211624849 CrossRefGoogle Scholar
  6. Barker SJ, Stummer B, Gao L, Dispain I, O’Connor PJ, Smith SE (1998) A mutant in Lycopersicon esculentum Mill. with highly reduced VA mycorrhizal colonization: isolation and preliminary characterisation. Plant J 15:791–797. doi: 10.1046/j.1365-313X.1998.00252.x CrossRefGoogle Scholar
  7. Barker S, Duplessis S, Tagu D (2002) The application of genetic approaches for investigations of mycorrhizal symbioses. In: Smith S, Smith FA (eds) Diversity and integration in mycorrhizas, vol 94. Developments in Plant and Soil Sciences. Springer Netherlands, Dordrecht, pp 85–95. doi: 10.1007/978-94-017-1284-2_9 Google Scholar
  8. Barker SJ, Edmonds-Tibbett TL, Forsyth LM, Klingler JP, Toussaint JP, Smith FA, Smith SE (2005) Root infection of the reduced mycorrhizal colonization (rmc) mutant of tomato reveals genetic interaction between symbiosis and parasitism. Physiol Mol Plant Pathol 67:277–283. doi: 10.1016/j.pmpp.2006.03.003 CrossRefGoogle Scholar
  9. Bender SF, van der Heijden MGA (2015) Soil biota enhance agricultural sustainability by improving crop yield, nutrient uptake and reducing nitrogen leaching losses. J Appl Ecol 52:228–239. doi: 10.1111/1365-2664.12351 CrossRefGoogle Scholar
  10. Bender SF, Conen F, Van der Heijden MGA (2015) Mycorrhizal effects on nutrient cycling, nutrient leaching and N2O production in experimental grassland. Soil Biol Biochem 80:283–292. doi: 10.1016/j.soilbio.2014.10.016 CrossRefGoogle Scholar
  11. Bradbury SM, Peterson RL, Bowley SR (1991) Interactions between 3 alfalfa nodulation genotypes and 2 Glomus species. New Phytol 119:115–120. doi: 10.1111/j.1469-8137.1991.tb01014.x CrossRefGoogle Scholar
  12. Campos-Soriano L, García-Martínez J, Segundo BS (2012) The arbuscular mycorrhizal symbiosis promotes the systemic induction of regulatory defence-related genes in rice leaves and confers resistance to pathogen infection. Mol Plant Pathol 13:579–592. doi: 10.1111/j.1364-3703.2011.00773.x PubMedCrossRefGoogle Scholar
  13. Carey P, Fitter A, Watkinson A (1992) A field study using the fungicide benomyl to investigate the effect of mycorrhizal fungi on plant fitness. Oecologia 90:550–555. doi: 10.1007/BF01875449 CrossRefGoogle Scholar
  14. Carvalho RF, Campos ML, Pino LE, Crestana SL, Zsogon A, Lima JE, Benedito VA, Peres LEP (2011) Convergence of developmental mutants into a single tomato model system: ‘Micro-Tom’ as an effective toolkit for plant development research. Plant Methods 7:18. doi: 10.1186/1746-4811-7-18 PubMedCentralPubMedCrossRefGoogle Scholar
  15. Cavagnaro TR (2008) The role of arbuscular mycorrhizas in improving plant zinc nutrition under low soil zinc concentrations: a review. Plant Soil 304:315–325. doi: 10.1007/s11104-008-9559-7 CrossRefGoogle Scholar
  16. Cavagnaro TR (2014) Impacts of compost application on the formation and functioning of arbuscular mycorrhizas. Soil Biol Biochem 78:34–38. doi: 10.1016/j.soilbio.2014.07.007 CrossRefGoogle Scholar
  17. Cavagnaro TR (2015) Biologically regulated nutrient supply systems: compost and arbuscular mycorrhizas—a review. Adv Agron 129:291–321. doi: 10.1016/bs.agron.2014.09.005
  18. Cavagnaro TR, Smith FA, Hay G, Carne-Cavagnaro VL, Smith SE (2004a) Inoculum type does not affect overall resistance of an arbuscular mycorrhiza-defective tomato mutant to colonisation but inoculation does change competitive interactions with wild-type tomato. New Phytol 161:485–494. doi: 10.1046/j.1469-8137.2004.00967.x CrossRefGoogle Scholar
  19. Cavagnaro TR, Smith FA, Smith SE (2004b) Interactions between arbuscular mycorrhizal fungi and a mycorrhiza-defective mutant tomato: does a noninfective fungus alter the ability of an infective fungus to colonise the roots—and vice versa? New Phytol 164:485–491. doi: 10.1111/j.1469-8137.2004.01210.x CrossRefGoogle Scholar
  20. Cavagnaro TR, Jackson LE, Six J, Ferris H, Goyal S, Asami D, Scow KM (2006) Arbuscular mycorrhizas, microbial communities, nutrient availability, and soil aggregates in organic tomato production. Plant Soil 282:209–225. doi: 10.1007/s11104-005-5847-7 CrossRefGoogle Scholar
  21. Cavagnaro TR, Jackson LE, Scow KM, Hristova KR (2007a) Effects of arbuscular mycorrhizas on ammonia oxidizing bacteria in an organic farm soil. Microb Ecol 54:618–626. doi: 10.1007/s00248-007-9212-7 PubMedCrossRefGoogle Scholar
  22. Cavagnaro TR, Sokolow SK, Jackson LE (2007b) Mycorrhizal effects on growth and nutrition of tomato under elevated atmospheric carbon dioxide. Funct Plant Biol 34:730–736. doi: 10.1071/fp06340 CrossRefGoogle Scholar
  23. Cavagnaro TR, Langley AJ, Jackson LE, Smukler SM, Koch GW (2008) Growth, nutrition, and soil respiration of a mycorrhiza-defective tomato mutant and its mycorrhizal wild-type progenitor. Funct Plant Biol 35:228–235. doi: 10.1071/fp07281 CrossRefGoogle Scholar
  24. Cavagnaro TR, Dickson S, Smith FA (2010) Arbuscular mycorrhizas modify plant responses to soil zinc addition. Plant Soil 329:307–313. doi: 10.1007/s11104-009-0158-z CrossRefGoogle Scholar
  25. Cavagnaro TR, Barrios-Masias FH, Jackson LE (2012) Arbuscular mycorrhizas and their role in plant growth, nitrogen interception and soil gas efflux in an organic production system. Plant Soil 353:181–194. doi: 10.1007/s11104-011-1021-6 CrossRefGoogle Scholar
  26. Chen C, Gao M, Liu J, Zhu H (2007) Fungal symbiosis in rice requires an ortholog of a legume common symbiosis gene encoding a Ca2+/calmodulin-dependent protein kinase. Plant Physiol 145:1619–1628. doi: 10.1104/pp. 107.109876 PubMedCentralPubMedCrossRefGoogle Scholar
  27. Chen CY, Ané JM, Zhu HY (2008) OsIPD3, an ortholog of the Medicago truncatula DMI3 interacting protein IPD3, is required for mycorrhizal symbiosis in rice. New Phytol 180:311–315. doi: 10.1111/j.1469-8137.2008.02612.x PubMedCrossRefGoogle Scholar
  28. Clark RB, Zeto SK (2000) Mineral acquisition by arbuscular mycorrhizal plants. J Plant Nutr 23:867–902. doi: 10.1080/01904160009382068 CrossRefGoogle Scholar
  29. David-Schwartz R, Badani H, Smadar W, Levy AA, Galili G, Kapulnik Y (2001) Identification of a novel genetically controlled step in mycorrhizal colonization: plant resistance to infection by fungal spores but not extra-radical hyphae. Plant J 27:561–569. doi: 10.1046/j.1365-313X.2001.01113.x PubMedCrossRefGoogle Scholar
  30. David-Schwartz R, Gadkar V, Wininger S, Bendov R, Galili G, Levy AA, Kapulnik Y (2003) Isolation of a premycorrhizal infection (pmi2) mutant of tomato, resistant to arbuscular mycorrhizal fungal colonization. Mol Plant-Microbe Interact 16:382–388. doi: 10.1094/mpmi.2003.16.5.382 PubMedCrossRefGoogle Scholar
  31. Delaux P-M, Séjalon-Delmas N, Bécard G, Ané J-M (2013) Evolution of the plant–microbe symbiotic ‘toolkit’. Trends Plant Sci 18:298–304. doi: 10.1016/j.tplants.2013.01.008 PubMedCrossRefGoogle Scholar
  32. Doyle JJ (1998) Phylogenetic perspectives on nodulation: evolving views of plants and symbiotic bacteria. Trends Plant Sci 3:473–478. doi: 10.1016/S1360-1385(98)01340-5 CrossRefGoogle Scholar
  33. Duc G, Trouvelot A, Gianinazzi-Pearson V, Gianinazzi S (1989) 1st report of non-mycorrhizal plant mutants (myc-) obtained in pea (Pisum sativum L) and fababean (Vicia faba L). Plant Sci 60:215–222. doi: 10.1016/0168-9452(89)90169-6 CrossRefGoogle Scholar
  34. Endlweber K, Scheu S (2006) Establishing arbuscular mycorrhiza-free soil: a comparison of six methods and their effects on nutrient mobilization. Appl Soil Ecol 34:276–279. doi: 10.1016/j.apsoil.2006.04.001 CrossRefGoogle Scholar
  35. Endre G, Kereszt A, Kevei Z, Mihacea S, Kalo P, Kiss GB (2002) A receptor kinase gene regulating symbiotic nodule development. Nature 417:962–966. doi: 10.1038/nature00842 PubMedCrossRefGoogle Scholar
  36. Engvild KC (1987) Nodulation and nitrogen fixation mutants of pea, Pisum sativum. Theor Appl Genet 74:711–713. doi: 10.1007/BF00247546 PubMedCrossRefGoogle Scholar
  37. Facelli E, Smith SE, Facelli JM, Christophersen HM, Smith FA (2010) Underground friends or enemies: model plants help to unravel direct and indirect effects of arbuscular mycorrhizal fungi on plant competition. New Phytol 185:1050–1061. doi: 10.1111/j.1469-8137.2009.03162.x PubMedCrossRefGoogle Scholar
  38. Froese-Gertzen EE, Konzak C, Foster R, Nilan R (1963) Correlation between some chemical and biological reactions of ethyl methanesulphonate. Nature 198:447–448CrossRefGoogle Scholar
  39. Gadkar V, David-Schwartz R, Nagahashi G, Douds DD, Wininger S, Kapulnik Y (2003) Root exudate of pmi tomato mutant M161 reduces AM fungal proliferation in vitro. FEMS Microbiol Lett 223:193–198. doi: 10.1016/s0378-1097(03)00357-4 PubMedCrossRefGoogle Scholar
  40. Gange AC, West HM (1994) Interactions between arbuscular mycorrhizal fungi and foliar-feeding insects in Plantago lanceolata L. New Phytol 128:79–87. doi: 10.1111/j.1469-8137.1994.tb03989.x CrossRefGoogle Scholar
  41. Gao LL, Delp G, Smith SE (2001) Colonization patterns in a mycorrhiza-defective mutant tomato vary with different arbuscular-mycorrhizal fungi. New Phytol 151:477–491. doi: 10.1046/j.0028-646x.2001.00193.x CrossRefGoogle Scholar
  42. Gao LL, Smith FA, Smith SE (2006) The rmc locus does not affect plant interactions or defence-related gene expression when tomato (Solanum lycopersicum) is infected with the root fungal parasite, Rhizoctonia. Funct Plant Biol 33:289–296. doi: 10.1071/fp05153 CrossRefGoogle Scholar
  43. Gehring CA, Whitham TG (1994) Interactions between aboveground herbivores and the mycorrhizal mutualists of plants. Trends Ecol Evol 9:251–255. doi: 10.1016/0169-5347(94)90290-9 PubMedCrossRefGoogle Scholar
  44. Gerats AG, Huits H, Vrijlandt E, Maraña C, Souer E, Beld M (1990) Molecular characterization of a nonautonomous transposable element (dTph1) of petunia. Plant Cell 2:1121–1128. doi: 10.1105/tpc.2.11.1121 PubMedCentralPubMedCrossRefGoogle Scholar
  45. Grønlund M, Albrechtsen M, Johansen IE, Hammer EC, Nielsen TH, Jakobsen I (2013) The interplay between P uptake pathways in mycorrhizal peas: a combined physiological and gene-silencing approach. Physiol Plant 149:234–248. doi: 10.1111/ppl.12030 PubMedCrossRefGoogle Scholar
  46. Gutjahr C, Banba M, Croset V, An K, Miyao A, An G, Hirochika H, Imaizumi-Anraku H, Paszkowski U (2008) Arbuscular mycorrhiza-specific signaling in rice transcends the common symbiosis signaling pathway. Plant Cell 20:2989–3005. doi: 10.1105/tpc.108.062414 PubMedCentralPubMedCrossRefGoogle Scholar
  47. Gyaneshwar P, Kumar GN, Parekh LJ, Poole PS (2002) Role of soil microorganisms in improving P nutrition of plants. Plant Soil 245:83–93. doi: 10.1023/a:1020663916259 CrossRefGoogle Scholar
  48. Hallett PD, Feeney DS, Bengough AG, Rillig MC, Scrimgeour CM, Young IM (2009) Disentangling the impact of AM fungi versus roots on soil structure and water transport. Plant Soil 314:183–196. doi: 10.1007/s11104-008-9717-y CrossRefGoogle Scholar
  49. Hartnett DC, Wilson GWT (1999) Mycorrhizae influence plant community structure and diversity in tallgrass prairie. Ecology 80:1187–1195. doi: 10.1890/0012-9658(1999)080[1187:mipcsa]2.0.co;2 CrossRefGoogle Scholar
  50. Hirsch AM, Kapulnik Y (1998) Signal transduction pathways in mycorrhizal associations: comparisons with the Rhizobium–legume symbiosis. Fungal Genet Biol 23:205–212. doi: 10.1006/fgbi.1998.1046 PubMedCrossRefGoogle Scholar
  51. Horváth B, Yeun LH, Domonkos Á, Halász G, Gobbato E, Ayaydin F, Miró K, Hirsch S, Sun J, Tadege M, Ratet P, Mysore KS, Ané J-M, Oldroyd GED, Kaló P (2011) Medicago truncatula IPD3 is a member of the common symbiotic signaling pathway required for rhizobial and mycorrhizal symbioses. Mol Plant-Microbe Interact 24:1345–1358. doi: 10.1094/MPMI-01-11-0015 PubMedCrossRefGoogle Scholar
  52. Imaizumi-Anraku H, Takeda N, Charpentier M, Perry J, Miwa H, Umehara Y, Kouchi H, Murakami Y, Mulder L, Vickers K, Pike J, Allan Downie J, Wang T, Sato S, Asamizu E, Tabata S, Yoshikawa M, Murooka Y, Wu G-J, Kawaguchi M, Kawasaki S, Parniske M, Hayashi M (2005) Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots. Nature 433:527–531. doi: 10.1038/nature03237 PubMedCrossRefGoogle Scholar
  53. Javot H, Penmetsa RV, Terzaghi N, Cook DR, Harrison MJ (2007) A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci U S A 104:1720–1725. doi: 10.1073/pnas.0608136104 PubMedCentralPubMedCrossRefGoogle Scholar
  54. Javot H, Penmetsa RV, Breuillin F, Bhattarai KK, Noar RD, Gomez SK, Zhang Q, Cook DR, Harrison MJ (2011) Medicago truncatula mtpt4 mutants reveal a role for nitrogen in the regulation of arbuscule degeneration in arbuscular mycorrhizal symbiosis. Plant J 68:954–965. doi: 10.1111/j.1365-313X.2011.04746.x PubMedCrossRefGoogle Scholar
  55. Jeffries P, Barea JM (1994) Biogeochemical cycling and arbuscular mycorrhizas in the sustainability of plant-soil systems. In: Gianinazzi S, Schüepp H (eds) Impact of arbuscular mycorrhizas on sustainable agriculture and natural ecosystems. Birkhäuser, Basel, pp 101–115. doi: 10.1007/978-3-0348-8504-1_9 CrossRefGoogle Scholar
  56. Klingner A, Bothe H, Wray V, Marner FJ (1995) Identification of a yellow pigment formed in maize roots upon mycorrhizal colonization. Phytochemistry 38:53–55. doi: 10.1016/0031-9422(94)00538-5 CrossRefGoogle Scholar
  57. Koide RT, Li MG (1989) Appropriate controls for vesicular arbuscular mycorrhiza research. New Phytol 111:35–44. doi: 10.1111/j.1469-8137.1989.tb04215.x CrossRefGoogle Scholar
  58. Koornneeff M, Dellaert LWM, van der Veen JH (1982) EMS- and relation-induced mutation frequencies at individual loci in Arabidopsis thaliana (L.). Heynh Mutat Res 93:109–123CrossRefGoogle Scholar
  59. Krüger M, Krüger C, Walker C, Stockinger H, Schüßler A (2012) Phylogenetic reference data for systematics and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level. New Phytol 193:970–984. doi: 10.1111/j.1469-8137.2011.03962.x PubMedCrossRefGoogle Scholar
  60. Larkan NJ, Smith SE, Barker SJ (2007) Position of the reduced mycorrhizal colonisation (Rmc) locus on the tomato genome map. Mycorrhiza 17:311–318. doi: 10.1007/s00572-007-0106-9 PubMedCrossRefGoogle Scholar
  61. Larkan N, Ruzicka D, Edmonds-Tibbett T, Durkin JH, Jackson L, Smith FA, Schachtman D, Smith S, Barker S (2013) The reduced mycorrhizal colonisation (rmc) mutation of tomato disrupts five gene sequences including the CYCLOPS/IPD3 homologue. Mycorrhiza 23(7):573-584. doi: 10.1007/s00572-013-0498-7
  62. Lazcano C, Barrios-Masias FH, Jackson LE (2014) Arbuscular mycorrhizal effects on plant water relations and soil greenhouse gas emissions under changing moisture regimes. Soil Biol Biochem 74:184–192. doi: 10.1016/j.soilbio.2014.03.010 CrossRefGoogle Scholar
  63. Lévy J, Bres C, Geurts R, Chalhoub B, Kulikova O, Duc G, Journet E-P, Ané J-M, Lauber E, Bisseling T, Dénarié J, Rosenberg C, Debellé F (2004) A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303:1361–1364. doi: 10.1126/science.1093038 PubMedCrossRefGoogle Scholar
  64. Li X, Song YJ, Century K, Straight S, Ronald P, Dong XN, Lassner M, Zhang YL (2001) A fast neutron deletion mutagenesis-based reverse genetics system for plants. Plant J 27:235–242. doi: 10.1046/j.1365-313x.2001.01084.x PubMedCrossRefGoogle Scholar
  65. Manjarrez M, Smith FA, Marschner P, Smith SE (2008) Is cortical root colonization required for carbon transfer to arbuscular mycorrhizal fungi? Evidence from colonization phenotypes and spore production in the reduced mycorrhizal colonization (rmc) mutant of tomato. Botany 86:1009–1019. doi: 10.1139/b08-043 CrossRefGoogle Scholar
  66. Manjarrez M, Wallwork M, Smith SE, Smith FA, Dickson S (2009) Different arbuscular mycorrhizal fungi induce differences in cellular responses and fungal activity in a mycorrhiza-defective mutant of tomato (rmc). Funct Plant Biol 36:86–96. doi: 10.1071/fp08032 CrossRefGoogle Scholar
  67. Manjarrez M, Christophersen HM, Smith SE, Smith FA (2010) Cortical colonisation is not an absolute requirement for phosphorus transfer to plants in arbuscular mycorrhizas formed by Scutellospora calospora in a tomato mutant: evidence from physiology and gene expression. Funct Plant Biol 37:1132–1142. doi: 10.1071/FP09248 CrossRefGoogle Scholar
  68. Marschner H, Dell B (1994) Nutrient uptake in mycorrhizal symbiosis. Plant Soil 159:89–102. doi: 10.1007/BF00000098 Google Scholar
  69. Marschner P, Timonen S (2005) Interactions between plant species and mycorrhizal colonization on the bacterial community composition in the rhizosphere. Appl Soil Ecol 28:23–36. doi: 10.1016/j.apsoil.2004.06.007 CrossRefGoogle Scholar
  70. Marsh JF, Schultze M (2001) Analysis of arbuscular mycorrhizas using symbiosis-defective plant mutants. New Phytol 150:525–532. doi: 10.1046/j.1469-8137.2001.00140.x CrossRefGoogle Scholar
  71. Meissner R, Jacobson Y, Melamed S, Levyatuv S, Shalev G, Ashri A, Elkind Y, Levy A (1997) A new model system for tomato genetics. Plant J 12:1465–1472. doi: 10.1046/j.1365-313x.1997.12061465.x CrossRefGoogle Scholar
  72. 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. doi: 10.1111/nph.12351 PubMedCrossRefGoogle Scholar
  73. Miller RM, Jastrow JD (1990) Hierarchy of root and mycorrhizal fungal interactions with soil aggregation. Soil Biol Biochem 22:579–584. doi: 10.1016/0038-0717(90)90001-g CrossRefGoogle Scholar
  74. Nair A, Kolet SP, Thulasiram HV, Bhargava S (2015) Systemic jasmonic acid modulation in mycorrhizal tomato plants and its role in induced resistance against Alternaria alternata. Plant Biol. doi: 10.1111/plb.12277 PubMedGoogle Scholar
  75. Neumann E, George E (2005) Does the presence of arbuscular mycorrhizal fungi influence growth and nutrient uptake of a wild-type tomato cultivar and a mycorrhiza-defective mutant, cultivated with roots sharing the same soil volume? New Phytol 166:601–609. doi: 10.1111/j.1469-8137.2005.01351.x PubMedCrossRefGoogle Scholar
  76. O’Connor PJ, Smith SE, Smith FA (2002) Arbuscular mycorrhizas influence plant diversity and community structure in a semiarid herbland. New Phytol 154:209–218. doi: 10.1046/j.1469-8137.2002.00364.x CrossRefGoogle Scholar
  77. Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775. doi: 10.1038/nrmicro1987 PubMedCrossRefGoogle Scholar
  78. Paszkowski U (2006) A journey through signaling in arbuscular mycorrhizal symbioses 2006. New Phytol 172:35–46. doi: 10.1111/j.1469-8137.2006.01840.x PubMedCrossRefGoogle Scholar
  79. Paszkowski U, Jakovleva L, Boller T (2006) Maize mutants affected at distinct stages of the arbuscular mycorrhizal symbiosis. Plant J 47:165–173. doi: 10.1111/j.1365-313X.2006.02785.x PubMedCrossRefGoogle Scholar
  80. Poulsen KH, Nagy R, Gao LL, Smith SE, Bucher M, Smith FA, Jakobsen I (2005) Physiological and molecular evidence for Pi uptake via the symbiotic pathway in a reduced mycorrhizal colonization mutant in tomato associated with a compatible fungus. New Phytol 168:445–453. doi: 10.1111/j.1469-8137.2005.01523.x PubMedCrossRefGoogle Scholar
  81. Read DJ, Perez-Moreno J (2003) Mycorrhizas and nutrient cycling in ecosystems—a journey towards relevance? New Phytol 157:475–492. doi: 10.1046/j.1469-8137.2003.00704.x CrossRefGoogle Scholar
  82. Reddy SDMR, Schorderet M, Feller U, Reinhardt D (2007) A petunia mutant affected in intracellular accommodation and morphogenesis of arbuscular mycorrhizal fungi. Plant J 51:739–750. doi: 10.1111/j.1365-313X.2007.03175.x CrossRefGoogle Scholar
  83. Redecker D, Schüßler A, Stockinger H, Stürmer SL, Morton JB, Walker C (2013) An evidence-based consensus for the classification of arbuscular mycorrhizal fungi (Glomeromycota). Mycorrhiza 23(7): 515-531. doi: 10.1007/s00572-013-0486-y
  84. Rillig MC (2004a) Arbuscular mycorrhizae and terrestrial ecosystem processes. Ecol Lett 7:740–754. doi: 10.1111/j.1461-0248.2004.00620.x CrossRefGoogle Scholar
  85. Rillig MC (2004b) Arbuscular mycorrhizae, glomalin, and soil aggregation. Can J Soil Sci 84:355–363. doi: 10.4141/S04-003 CrossRefGoogle Scholar
  86. Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. New Phytol 171:41–53. doi: 10.1111/j.1469-8137.2006.01750.x PubMedCrossRefGoogle Scholar
  87. Rillig MC, Ramsey PW, Gannon JE, Mummey DL, Gadkar V, Kapulnik Y (2008) Suitability of mycorrhiza-defective mutant/wildtype plant pairs (Solanum lycopersicum L. cv Micro-Tom) to address questions in mycorrhizal soil ecology. Plant Soil 308:267–275. doi: 10.1007/s11104-008-9629-x CrossRefGoogle Scholar
  88. Rinaudo V, Barberi P, Giovannetti M, van der Heijden MGA (2010) Mycorrhizal fungi suppress aggressive agricultural weeds. Plant Soil 333:7–20. doi: 10.1007/s11104-009-0202-z CrossRefGoogle Scholar
  89. Ruzicka DR, Hausmann NT, Barrios-Masias FH, Jackson LE, Schachtman DP (2012) Transcriptomic and metabolic responses of mycorrhizal roots to nitrogen patches under field conditions. Plant Soil 350:145–162. doi: 10.1007/s11104-011-0890-z CrossRefGoogle Scholar
  90. Ruzicka D, Chamala S, Barrios-Masias FH, Martin F, Smith S, Jackson LE, Barbazuk WB, Schachtman DP (2013) Inside arbuscular mycorrhizal roots—molecular probes to understand the symbiosis. Plant Gen 6. doi: 10.3835/plantgenome2012.06.0007
  91. Sagan M, Morandi D, Tarenghi E, Duc G (1995) Selection of nodulation and mycorrhizal mutants in the model-plant Medicago-truncatula (Gaertn) after gamma-ray mutagenesis. Plant Sci 111:63–71. doi: 10.1016/0168-9452(95)04229-n CrossRefGoogle Scholar
  92. Senoo K, Solaiman MZ, Kawaguchi M, Imaizumi-Anraku H, Akao S, Tanaka A, Obata H (2000) Isolation of two different phenotypes of mycorrhizal mutants in the model legume plant Lotus japonicus after EMS-treatment. Plant Cell Physiol 41:726–732. doi: 10.1093/pcp/41.6.726 PubMedCrossRefGoogle Scholar
  93. Shirtliffe SJ, Vessey JK (1996) A nodulation (Nod(+)/Fix-) mutant of Phaseolus vulgaris L has nodule-like structures lacking peripheral vascular bundles (Pvb(-)) and is resistant to mycorrhizal infection (Myc(-)). Plant Sci 118:209–220. doi: 10.1016/0168-9452(96)04427-5 CrossRefGoogle Scholar
  94. Shtark OY, Borisov AY, Zhukov VA, Provorov NA, Tikhonovich IA (2010) Intimate associations of beneficial soil microbes with host plants. Soil Microbiol Sustain Crop Prod. doi: 10.1007/978-90-481-9479-7_5 Google Scholar
  95. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, New YorkGoogle Scholar
  96. Smith FA, Smith SE (1981a) Mycorrhizal infection and growth of Trifolium subterraneum: comparison of natural and artificial inocula. New Phytol 88:311–325. doi: 10.2307/2431807 CrossRefGoogle Scholar
  97. Smith FA, Smith SE (1981b) Mycorrhizal infection and growth of Trifolium subterraneum: use of sterilized soil as a control treatment. New Phytol 88:299–309. doi: 10.1111/j.1469-8137.1981.tb01726.x CrossRefGoogle Scholar
  98. Smith SE, Facelli E, Pope S, Smith FA (2010) Plant performance in stressful environments: interpreting new and established knowledge of the roles of arbuscular mycorrhizas. Plant Soil 326:3–20. doi: 10.1007/s11104-009-9981-5 CrossRefGoogle Scholar
  99. Stacey G, Libault M, Brechenmacher L, Wan J, May G (2006) Genetics and functional genomics of legume nodulation. Curr Opin Plant Biol 9:110–121. doi: 10.1016/j.pbi.2006.01.005 PubMedCrossRefGoogle Scholar
  100. Stracke S, Kistner C, Yoshida S, Mulder L, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J, Szczyglowski K, Parniske M (2002) A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417:959–962. doi: 10.1038/nature00841 PubMedCrossRefGoogle Scholar
  101. Sun SB, Wang JJ, Zhu LL, Liao DH, Gu MA, Ren LX, Kapulnik Y, Xu GH (2012) An active factor from tomato root exudates plays an important role in efficient establishment of mycorrhizal symbiosis. PLoS One 7:e43385. doi: 10.1371/journal.pone.0043385 PubMedCentralPubMedCrossRefGoogle Scholar
  102. Tisdall JM (1991) Fungal hyphae and structural stability of soil. Soil Res 29:729–743. doi: 10.1071/SR9910729 CrossRefGoogle Scholar
  103. Tisdall JM, Oades JM (1980) The management of ryegrass to stabilise aggregates of a red brown earth. Soil Res 18:415–422. doi: 10.1071/SR9800415 CrossRefGoogle Scholar
  104. van der Heijden MGA (2010) Mycorrhizal fungi reduce nutrient loss from model grassland ecosystems. Ecology 91:1163–1171. doi: 10.1890/09-0336.1 PubMedCrossRefGoogle Scholar
  105. van der Heijden MGA, Boller T, Wiemken A, Sanders IR (1998a) Different arbuscular mycorrhizal fungal species are potential determinants of plant community structure. Ecology 79:2082–2091. doi: 10.1890/0012-9658(1998)079[2082:damfsa]2.0.co;2 CrossRefGoogle Scholar
  106. van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998b) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72. doi: 10.1038/23932 CrossRefGoogle Scholar
  107. Veiga RSL, Jansa J, Frossard E, van der Heijden MGA (2011) Can arbuscular mycorrhizal fungi reduce the growth of agricultural weeds? PLoS One 6:e27825. doi: 10.1371/journal.pone.0027825 PubMedCentralPubMedCrossRefGoogle Scholar
  108. Wagg C, Jansa J, Schmid B, van der Heijden MGA (2011) Belowground biodiversity effects of plant symbionts support aboveground productivity. Ecol Lett 14:1001–1009. doi: 10.1111/j.1461-0248.2011.01666.x PubMedCrossRefGoogle Scholar
  109. Wamberg C, Christensen S, Jakobsen I (2003) Interaction between foliar-feeding insects, mycorrhizal fungi, and rhizosphere protozoa on pea plants. Pedobiologia 47:281–287. doi: 10.1078/0031-4056-00191 CrossRefGoogle Scholar
  110. Wang B, Yeun LH, Xue JY, Liu Y, Ané JM, Qiu YL (2010) Presence of three mycorrhizal genes in the common ancestor of land plants suggests a key role of mycorrhizas in the colonization of land by plants. New Phytol 186:514–525. doi: 10.1111/j.1469-8137.2009.03137.x PubMedCrossRefGoogle Scholar
  111. Watts-Williams SJ, Cavagnaro TR (2012) Arbuscular mycorrhizas modify tomato responses to soil zinc and phosphorus addition. Biol Fertil Soils 48:285–294. doi: 10.1007/s00374-011-0621-x CrossRefGoogle Scholar
  112. Watts-Williams SJ, Cavagnaro TR (2014) Nutrient interactions and arbuscular mycorrhizas: a meta-analysis of a mycorrhiza-defective mutant and wild-type tomato genotype pair. Plant Soil 384:79–92. doi: 10.1007/s11104-014-2140-7 CrossRefGoogle Scholar
  113. Watts-Williams SJ, Jakobsen I, Cavagnaro TR, Grønlund M (2015a) Local and distal effects of arbuscular mycorrhizal colonisation on direct pathway Pi uptake and root growth in Medicago truncatula. J Exp Bot (in press)Google Scholar
  114. Watts-Williams SJ, Patti AF, Cavagnaro TR (2013) Arbuscular mycorrhizas are beneficial under both deficient and toxic soil zinc conditions. Plant Soil 371:299–312. doi: 10.1007/s11104-013-1670-8 CrossRefGoogle Scholar
  115. Watts-Williams SJ, Turney TW, Patti AF, Cavagnaro TR (2014) Uptake of zinc and phosphorus by plants is affected by zinc fertiliser material and arbuscular mycorrhizas. Plant Soil 376:165–175. doi: 10.1007/s11104-013-1967-7 CrossRefGoogle Scholar
  116. Watts-Williams SJ, Smith FA, McLaughlin MJ, Patti AF, Cavagnaro TR (2015b) How important is the mycorrhizal pathway for plant Zn uptake? Plant Soil. doi: 10.1007/s11104-014-2374-4 Google Scholar
  117. West H (1997) Interactions between arbuscular mycorrhizal fungi and foliar pathogens: consequences for host and pathogen. In: Gange A, Brown V (eds) Multitrophic interactions in terrestrial systems, vol 36. Blackwell Science, Oxford, p 79Google Scholar
  118. West HM, Fitter AH, Watkinson AR (1993) The influence of three biocides on the fungal associates of the roots of Vulpia ciliata ssp. Ambigua under natural conditions. J Ecol 81:345–350. doi: 10.2307/2261504 CrossRefGoogle Scholar
  119. Xie X, Huang W, Liu F, Tang N, Liu Y, Lin H, Zhao B (2013) Functional analysis of the novel mycorrhiza-specific phosphate transporter AsPT1 and PHT1 family from Astragalus sinicus during the arbuscular mycorrhizal symbiosis. New Phytol 198:836–852. doi: 10.1111/nph.12188 PubMedCrossRefGoogle Scholar
  120. Yang S-Y, Grønlund M, Jakobsen I, Grotemeyer MS, Rentsch D, Miyao A, Hirochika H, Kumar CS, Sundaresan V, Salamin N, Catausan S, Mattes N, Heuer S, Paszkowski U (2012) Nonredundant regulation of rice arbuscular mycorrhizal symbiosis by two members of the PHOSPHATE TRANSPORTER1 gene family. Plant Cell 24:4236–4251. doi: 10.1105/tpc.112.104901 PubMedCentralPubMedCrossRefGoogle Scholar
  121. Zhu HY, Riely BK, Burns NJ, Ané JM (2006) Tracing nonlegume orthologs of legume genes required for nodulation and arbuscular mycorrhizal symbioses. Genetics 172:2491–2499. doi: 10.1534/genetics.105.051185 PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.School of Biological SciencesMonash UniversityClaytonAustralia
  2. 2.School of Agriculture, Food and WineThe University of AdelaideGlen OsmondAustralia
  3. 3.Boyce Thompson Institute for Plant ResearchIthacaUSA

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