Friend or foe - Light availability determines the relationship between mycorrhizal fungi, rhizobia and lima bean (Phaseolus lunatus L.)

PLoS ONE

Volumn 11, Issue 5, 2016, Pages

  Ballhorn, Daniel J ^a   Schädler, Martin ^b,c   Elias, Jacob D ^a   Millar, Jess A ^a   Kautz, Stefanie ^a  

^a PORTLAND STATE UNIVERSITY   (United States)

^b HELMHOLTZ CENTRE FOR ENVIRONMENTAL RESEARCH UFZ   (Germany)

^c GERMAN CENTRE FOR INTEGRATIVE BIODIVERSITY RESEARCH IDIV HALLE JENA LEIPZIG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BIOMASS; CONTROLLED STUDY; INOCULATION; LIGHT; MYCORRHIZA; NONHUMAN; PHASEOLUS LUNATUS; PLANT GROWTH; PLANT REPRODUCTION; PLANT ROOT; PLANT SEED; RHIZOBIACEAE; SEED PRODUCTION; SYMBIONT; SYMBIOSIS; METABOLISM; MICROBIOLOGY; NODULATION; PHASEOLUS; PHYSIOLOGY; RADIATION RESPONSE; RHIZOBIUM;

LIGHT; MYCORRHIZAE; PHASEOLUS; PLANT ROOTS; RHIZOBIUM; ROOT NODULES, PLANT; SYMBIOSIS;

EID: 84967145918     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0154116     Document Type: Article

References (46)

1. Smith SE, Read DJ, Harley JL (1997) Mycorrhizal symbiosis, 2nd edn. Academic Press, San Diego.
2. Sprent JI (2001) Nodulation in legumes. Kew Royal Botanical Gardens, Kew.
3. Carney KM, Matson PA (2005) Plant communities, soil microorganisms, and soil carbon cycling: does altering the world belowground matter to ecosystem functioning? Ecosystems 8:928-940.
4. van der Heijden MGA, Bardgett RD, van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296-310. PMID: 18047587
5. Gianinazzi-Pearson V (1996) Plant cell responses to arbuscular mycorrhizal fungi: getting to the roots of the symbiosis. Plant Cell 8:1871-1883. doi: 10.1105/tpc.8.10.1871 PMID: 12239368
6. Goverde M, van der Heijden MGA, Wiemken A, Sanders IR, Erhardt A (2000) Arbuscular mycorrhizal fungi influence life history traits of a lepidopteran herbivore. Oecologia 125:362-369. doi: 10.1007/s004420000465
7. Wardle DA (2002) Communities and ecosystems: linking the aboveground and belowground components. Princeton University Press, Princeton.
8. van der Heijden MGA, Bakker R, Verwaal J, Scheublin TR, Rutten M, van Logtestijn R, et al. (2006) Symbiotic bacteria as a determinant of plant community structure and plant productivity in dune grassland. FEMS Microbiol Ecol 56:178-187. doi: 10.1111/j.1574-6941.2006.00086.x PMID: 16629748
9. Vejsadova H, Siblikova D, Gryndler M, Simon T, Miksik I (1993) Influence of inoculation with Bradyrhizobium japonicum and Glomus claroideum on seed yield of soybean under greenhouse and field conditions. J Plant Nutr 16:619-629. doi: 10.1080/01904169309364561
10. Sefapour M, Ardakani M, Khaghani S, Rejali F, Zargari K, Changizi M, et al. (2011) Response of yield and yield Components of three red bean (Phaseolus vulgaris L.) genotypes to co-inoculation with Glomus intraradices and Rhizobium phaseoli. Am J Agric Environ Sci 11:398-405.
11. Barea JM, Azcón R, Azcón-Aguilar C (1992) Vesicular-arbuscular mycorrhizal fungi in nitrogen-fixing systems. Method Microbiol 24:391-416.
12. Franzini VI, Azcón R, Mendes FL, Aroca R (2010) Interactions between Glomus species and Rhizobium strains affect the nutritional physiology of drought-stressed legume hosts. J Plant Physiol 167:614-619. doi: 10.1016/j.jplph.2009.11.010 PMID: 20044167
13. Kaschuk G, Kuyper TW, Leffelaar PA, Hungriac M, Gillera KE (2009) Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses? Soil Biol Biochem 41:1233-1244. doi: 10.1016/j.soilbio.2009.03.005
14. Ballhorn DJ, Kay J, Kautz S (2014) Quantitative effects of leaf area removal on indirect defense of lima bean (Phaseolus lunatus) in nature. J Chem Ecol 40:294-296. doi: 10.1007/s10886-014-0392-6 PMID: 24573494
15. Lau JA, Bowling EJ, Gentry LE, Glasser PA, Monarch EA, Olesen WM, et al. (2012) Direct and interactive effects of light and nutrients on the legume-rhizobia mutualism. Acta Oecologica 39:80-86. doi: 10.1016/j.actao.2012.01.004
16. Stonor RN, Smith SE, Manjarrez M, Facelli E, Smith FA (2014) Mycorrhizal responses in wheat: shading decreases growth but does not lower the contribution of the fungal phosphate uptake pathway. Mycorrhiza 24:465-472. doi: 10.1007/s00572-014-0556-9. Epub 2014 Jan 24. PMID: 24458842
17. Chirko CP, Gold MA, Nguyen PV, Jiang JP (1996) Influence of direction and distance from trees on wheat yield and photosynthetic photon flux density (Qp) in a Paulownia and wheat intercropping system. Forest Ecol Manag 1127:171-180. doi: 10.1016/0378-1127(96)03721-8
18. Saito M, Kato T (1994) Effects of low temperature and shading on relationships between nodulation, vesicular - arbuscular mycorrhizal infection and shoot growth of soybean. Biol Fert Soils 17:206-211. doi: 10.1007/BF00336324
19. Koo CD, Molina RJ, Miller SL, Li CY (1996) Effects of nitrogen and phosphorus fertilization on ectomycorrhiza development, N-fixation, and growth of red alder seedlings. J Korean Soc 85:96-106.
20. Graham PH, Vance CP (2003) Legumes: importance and constraints to greater use. Plant Physiol 131:872-877. PMID: 12644639
21. Ballhorn DJ, Kautz S, Lion U, Heil M (2008) Trade-offs between direct and indirect defences of lima bean (Phaseolus lunatus). J Ecol 96:971-980. doi: 10.1111/j.1365-2745.2008.01404.x
22. Ballhorn DJ, Younginger BS, Kautz S (2014) Aboveground pathogens inhibit belowground rhizobia and mycorrhizal fungi in Phaseolus vulgaris. BMC Plant Biol 14:321. doi: 10.1186/s12870-014-0321-4 PMID: 25429887
23. Godschalx AL, Schädler M, Trisel JA, Balkan MA, Ballhorn DJ (2015) Ants are less attracted to the extrafloral nectar of plants with symbiotic, nitrogen-fixing rhizobia. Ecology 96:348-354. PMID: 26240856
24. Kautz S, Trisel JA, Ballhorn DJ (2014) Jasmonic acid enhances plant cyanogenesis and resistance to herbivory in lima bean. J Chem Ecol 40:1186-1196. doi: 10.1007/s10886-014-0524-z PMID: 25399357
25. Daft M, El-Giahmi A (1978) Effect of arbuscular mycorrhiza on plant growth. VIII. Effects of defoliation and light on selected hosts. New Phytol 80:365-372. doi: 10.1111/j.1469-8137.1978.tb01570.x
26. Millar JA, Ballhorn DJ (2013) Effect of mycorrhizal colonization and light limitation on growth and reproduction of lima bean (Phaseolus lunatus L.). J Appl Bot Food Qual 86:172-179. doi: 10.5073/JABFQ.2013.086.023
27. Fellbaum CR, Mensah JA, Cloos AJ, Strahan GE, Pfeffer PE, Kiers ET, et al. (2014) Fungal nutrient allocation in common mycorrhizal networks is regulated by the carbon source strength of individual host plants. New Phytol 203:646-656. doi: 10.1111/nph.12827 PMID: 24787049
28. Thornley JHM, Parsons AJ (2014) Allocation of new growth between shoot, root and mycorrhiza in relation to carbon, nitrogen and phosphate supply: teleonomy with maximum growth rate. J Theor Biol 342:1-14. doi: 10.1016/j.jtbi.2013.10.003 PMID: 24140786
29. Jamshidi S, Behm JE, Eveillard D, Kiers ET, Vandenkoornhuys P (2015) Using hybrid automata modelling to study phenotypic plasticity and allocation strategies in the plant mycorrhizal mutualism. Ecol Modell 311:11-19. doi: 10.1016/j.ecolmodel.2015.04.021
30. Konvalinková T, Püschel D, Janoušková M, Gryndler M, Jansa J (2015) Duration and intensity of shade differentially affects mycorrhizal growth- and phosphorus uptake responses of Medicago truncatula. Front Plant Sci 6:65. doi: 10.3389/fpls.2015.00065 PMID: 25763002
31. Biró B, Köves-Péchy K, Vörös I, Takács T, Eggenberger P, Strasser RJ (2000) Interrelations between Azospirillum and Rhizobium nitrogen-fixers and arbuscular mycorrhizal fungi in the rhizosphere of alfalfa in sterile, AMF-free or normal soil conditions. Appl Soil Ecol 15:159-168. doi: 10.1016/S0929-1393(00)00092-5
32. Denison RF, Kiers ET (2011) Life histories of symbiotic rhizobia and mycorrhizal fungi. Curr Biol 21:775-785, doi: 10.1016/j.cub.2011.06.018
33. Blue E, Kay J, Younginger BS, Ballhorn DJ (2015) Differential effects of type and quantity of leaf damage on growth, reproduction and defence of lima bean (Phaseolus lunatus L.) Plant Biol 17:712-719. doi: 10.1111/plb.12285 PMID: 25377879
34. 2-mediated changes of plant traits and their effects on herbivores are determined by leaf age. Ecol Entomol 36:1-13. doi: 10.1111/j.1365-2311.2010.01240.x
35. Ballhorn DJ, Kautz S, Heil M (2013) Distance and sex determine host plant choice by herbivorous beetles PLoS ONE 8:e55602. doi: 10.1371/journal.pone.0055602 PMID: 23405176
36. Thamer S, Schädler M, Bonte D, Ballhorn DJ (2011) Dual benefit from a belowground symbiosis: nitrogen fixing rhizobia promote growth and defense against a specialist herbivore in a cyanogenic plant. Plant Soil 341:209-219. doi: 10.1007/s11104-010-0635-4
37. Ballhorn DJ, Kautz S, Schädler M (2013). Induced plant defense via volatile production is dependent on rhizobial symbiosis. Oecologia 172:833-846. doi: 10.1007/s00442-012-2539-x PMID: 23242424
38. McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115:495-501. doi: 10.1111/j.1469-8137.1990.tb00476.x
39. Larimer AL, Bever JD, Clay K (2010) The interactive effects of plant microbial symbionts: a review and meta-analysis. Symbiosis 51: 139-148
40. Ames RN, Bethlenfalvay GJ (1987) Localized increase in nodulue activity but no competitive interaction of cowpea rhizobia due to pre-establishment of vesicular arbuscular mycorrhiza. New Phytol 106:207-215.
41. Bethlenfalvay GJ, Pacovsky RS (1983) Light effects in mycorrhizal soybeans. Plant Physiol 73:969-972. PMID: 16663353
42. Reinhard S, Martin P, Marschner H (1993) Interactions in the tripartite symbiosis of pea (Pisum sativum L.), Glomus and Rhizobium under non-limiting phosphorus supply. J Plant Physiol 141:7-11. doi: 10.1016/S0176-1617(11)80844-8
43. Kiers ET, Denison RF (2008) Sanctions, cooperation, and the stability of plant-rhizosphere mutualisms. Annu Rev Ecol Evol Syst 39:215-236. doi: 10.1146/annurev.ecolsys.39.110707.173423
44. Reinhard S, Weber E, Martin P, Marschner H (1994) Influence of phosphorus supply and light intensity on mycorrhizal response in Pisum-Rhizobium-Glomus symbiosis. Experientia 50:890-896.
45. Ronsheim ML (2012) The effect of mycorrhizae on plant growth and reproduction varies with soil phosphorus and developmental stage. Am Midl Nat 167:28-39. doi: 10.1674/0003-0031-167.1.28
46. Mortimer PE, Pérez-Fernández MA, Valentine AJ (2008) The role of arbuscular mycorrhizal colonization in the carbon and nutrient economy of the tripartite symbiosis with nodulated Phaseolus vulgaris. Soil Biol Biochem 40:1019-1027. doi: 10.1016/j.soilbio.2007.11.014