Abstract
Aims
Although arbuscular mycorrhizal symbiosis is common in many plants with either C3 or C4 photosynthesis, it remains poorly understood whether photosynthesis type has any significant impact on carbon (C) fluxes in mycorrhizal plants. Thus, we compared mycorrhizal and non-mycorrhizal (NM) plants belonging to Panicum bisulcatum (C3) to its congeneric P. maximum (C4).
Methods
Plants were or were not exposed to arbuscular mycorrhiza (AM) fungal inoculation and/or phosphorus (P) fertilization. Plants’ C budgets were assembled based on 13CO2 pulse-chase labelling and sequential harvesting.
Results
Mycorrhizal plants allocated on average 3.9% more recently fixed C belowground than did their NM counterparts. At low P, mycorrhizal C3-Panicum plants allocated less C to aboveground respiration as compared to their respective NM controls. In contrast, mycorrhizal C4-Panicum increased the rates of photosynthesis and allocated more C to aboveground respiration than the respective NM controls. At high P, the differences were less prominent.
Conclusions
We demonstrated consistent differences in aboveground C allocation due to AM symbiosis formation in congeneric C3 and C4 grasses. Both grasses benefited from AM symbiosis in terms of improved P uptake (at least at low P). These results advocate a holistic (whole-plant) perspective in studying C fluxes in mycorrhizal plants.
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Abbreviations
- AM:
-
Arbuscular mycorrhiza
- C:
-
Carbon
- P:
-
Phosphorus
- M + :
-
Mycorrhizal treatment
- NM:
-
Non-mycorrhizal control
- low P:
-
Unamended with P
- high P:
-
Fertilized with P
References
Aliscioni S, Bell HL, Besnard G, Christin PA, Columbus JT, Duvall MR, Edwards EJ, Giussani L, Hasenstab-Lehman K, Hilu KW, Hodkinson TR, Ingram AL, Kellogg EA, Mashayekhi S, Morrone O, Osborne CP, Salamin N, Schaefer H, Spriggs E, Smith SA, Zuloaga F, II GPWG (2012) New grass phylogeny resolves deep evolutionary relationships and discovers C4 origins. New Phytol 193:304–312. https://doi.org/10.1111/j.1469-8137.2011.03972.x
Augé RM, Toler HD, Saxton AM (2015) Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: a meta-analysis. Mycorrhiza 25:13–24. https://doi.org/10.1007/s00572-014-0585-4
Birhane E, Sterck FJ, Fetene M, Bongers F, Kuyper TW (2012) Arbuscular mycorrhizal fungi enhance photosynthesis, water use efficiency, and growth of frankincense seedlings under pulsed water availability conditions. Oecologia 169:895–904. https://doi.org/10.1007/s00442-012-2258-3
Black KG, Mitchell DT, Osborne BA (2000) Effect of mycorrhizal-enhanced leaf phosphate status on carbon partitioning, translocation and photosynthesis in cucumber. Plant Cell Environ 23:797–809. https://doi.org/10.1046/j.1365-3040.2000.00598.x
Bolan NS (1991) A critical review on the role of mycorrhizal fungi in the uptake of phosphorus by plants. Plant Soil 134:189–207. https://doi.org/10.1007/Bf00012037
Bryla DR, Eissenstat DM (2005) Respiratory costs of mycorrhiza associations. In: Lambers H, Ribas-Carbó M (eds) Plant respiration – advances in photosynthesis and respiration. Springer, Dordrecht, pp 207–224
Calderón FJ, Schultz DJ, Paul EA (2012) Carbon allocation, belowground transfers, and lipid turnover in a plant-microbial association. Soil Sci Soc Am J 76:1614–1623. https://doi.org/10.2136/sssaj2011.0440
Chandrasekaran M, Kim K, Krishnamoorthy R, Walitang D, Sundaram S, Joe MM, Selvakumar G, Hu SJ, Oh SH, Sa T (2016) Mycorrhizal symbiotic efficiency on C3 and C4 plants under salinity stress - a meta-analysis. Front Microbiol 7:1246. https://doi.org/10.3389/fmicb.2016.01246
Couillerot O, Ramirez-Trujillo A, Walker V, von Felten A, Jansa J, Maurhofer M, Defago G, Prigent-Combaret C, Comte G, Caballero-Mellado J, Moenne-Loccoz Y (2013) Comparison of prominent Azospirillum strains in Azospirillum-Pseudomonas-Glomus consortia for promotion of maize growth. Appl Microbiol Biotechnol 97:4639–4649. https://doi.org/10.1007/s00253-012-4249-z
Courty PE, Doubková P, Calabrese S, Niemann H, Lehmann MF, Vosátka M, Selosse MA (2015) Species-dependent partitioning of C and N stable isotopes between arbuscular mycorrhizal fungi and their C3 and C4 hosts. Soil Biol Biochem 82:52–61. https://doi.org/10.1016/j.soilbio.2014.12.005
de Ribou SD, Douam F, Hamant O, Frohlich MW, Negrutiu J (2013) Plant science and agricultural productivity: why are we hitting the yield ceiling? Plant Sci 210:159–176. https://doi.org/10.1016/j.plantsci.2013.05.010
Del-Saz NF, Romero-Munar A, Cawthray GR, Aroca R, Baraza E, Flexas J, Lambers H, Ribas-Carbó M (2017) Arbuscular mycorrhizal fungus colonization in Nicotiana tabacum decreases the rate of both carboxylate exudation and root respiration and increases plant growth under phosphorus limitation. Plant Soil 416:97–106. https://doi.org/10.1007/s11104-017-3188-y
Douds DD, Johnson CR, Koch KE (1988) Carbon cost of the fungal symbiont relative to net leaf-P accumulation in a split-root VA mycorrhizal symbiosis. Plant Physiol 86:491–496. https://doi.org/10.1104/pp.86.2.491
Drigo B, Pijl AS, Duyts H, Kielak A, Gamper HA, Houtekamer MJ, Boschker HTS, Bodelier PLE, Whiteley AS, van Veen JA, Kowalchuk GA (2010) Shifting carbon flow from roots into associated microbial communities in response to elevated atmospheric CO2. P Natl Acad Sci USA 107:10938–10942. https://doi.org/10.1073/pnas.0912421107
Ehleringer JR, Sage RF, Flanagan LB, Pearcy RW (1991) Climate change and the evolution of C4 photosynthesis. Trends Ecol Evol 6:95–99. https://doi.org/10.1016/0169-5347(91)90183-X
Fitter AH (1991) Costs and benefits of mycorrhizas – implications for functioning under natural conditions. Experientia 47:350–355. https://doi.org/10.1007/Bf01972076
Fitter AH, Graves JD, Watkins NK, Robinson D, Scrimgeour C (1998) Carbon transfer between plants and its control in networks of arbuscular mycorrhizas. Funct Ecol 12:406–412
Furbank RT (2016) Walking the C4 pathway: past, present, and future. J Exp Bot 67:4057–4066. https://doi.org/10.1093/jxb/erw161
Garcia K, Doidy J, Zimmermann SD, Wipf D, Courty PE (2016) Take a trip through the plant and fungal transportome in mycorrhiza. Trends Plant Sci 21:937–950. https://doi.org/10.1016/j.tplants.2016.07.010
Ghannoum O, Paul MJ, Ward JL, Beale MH, Corol DI, Conroy JP (2008) The sensitivity of photosynthesis to phosphorus deficiency differs between C3 and C4 tropical grasses. Funct Plant Biol 35:213–221. https://doi.org/10.1071/Fp07256
Grimoldi AA, Kavanová M, Lattanzi FA, Schaufele R, Schnyder H (2006) Arbuscular mycorrhizal colonization on carbon economy in perennial ryegrass: quantification by 13CO2/12CO2 steady-state labelling and gas exchange. New Phytol 172:544–553. https://doi.org/10.1111/j.1469-8137.2006.01853.x
Hetrick BAD, Wilson GWT, Todd TC (1990) Differential responses of C3 and C4 grasses to mycorrhizal symbiosis, phosphorus fertilization, and soil-microorganisms. Can J Bot 68:461–467
Hewitt EJ (1966) Sand and water culture methods used in the study of plant nutrition. Commonwealth Agricultural Bureaux, Farnham Royal
Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT, Pringle A, Zabinski C, Bever JD, Moore JC, Wilson GWT, Klironomos JN, Umbanhowar J (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett 13:394–407. https://doi.org/10.1111/j.1461-0248.2009.01430.x
Jakobsen I (1998) Transport of phosphorus and carbon in arbuscular mycorrhizas. In: Varma A, Hock B (eds) Mycorrhiza: structure, function, molecular biology and biotechnology. Springer, Berlin, pp 305–332
Jakobsen I, Rosendahl L (1990) Carbon flow into soil and external hyphae from roots of mycorrhizal cucumber plants. New Phytol 115:77–83. https://doi.org/10.1111/j.1469-8137.1990.tb00924.x
Jansa J, Mozafar A, Frossard E (2005) Phosphorus acquisition strategies within arbuscular mycorrhizal fungal community of a single field site. Plant Soil 276:163–176. https://doi.org/10.1007/s11104-005-4274-0
Johnson NC, Wilson GWT, Wilson JA, Miller RM, Bowker MA (2015) Mycorrhizal phenotypes and the law of the minimum. New Phytol 205:1473–1484
Joos O, Saurer M, Heim A, Hagedorn F, Schmidt MWI, Siegwolf RTW (2008) Can we use the CO2 concentrations determined by continuous-flow isotope ratio mass spectrometry from small samples for the keeling plot approach? Rapid Commun Mass Spectrom 22:4029–4034. https://doi.org/10.1002/rcm.3827
Kaschuk G, Kuyper TW, Leffelaar PA, Hungria M, Giller 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. https://doi.org/10.1016/j.soilbio.2009.03.005
Keymer A, Pimprikar P, Wewer V, Huber C, Brands M, Bucerius SL, Delaux PM, Klingl V, von Ropenack-Lahaye E, Wang TL, Eisenreich W, Dormann P, Parniske M, Gutjahr C (2017) Lipid transfer from plants to arbuscular mycorrhiza fungi. Elife 6. https://doi.org/10.7554/eLife.29107.001
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, Bücking H (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–882. https://doi.org/10.1126/science.1208473
Koch KE, Johnson CR (1984) Photosynthate partitioning in split-root citrus seedlings with mycorrhizal and nonmycorrhizal root systems. Plant Physiol 75:26–30. https://doi.org/10.1104/pp.75.1.26
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 6:782. https://doi.org/10.3389/fpls.2015.00065
Konvalinková T, Püschel D, Řezáčová V, Gryndlerová H, Jansa J (2017) Carbon flow from plant to arbuscular mycorrhizal fungi is reduced under phosphorus fertilization. Plant Soil 419:319–333. https://doi.org/10.1007/s11104-017-3350-6
Koske RE, Gemma JN (1989) A modified procedure for staining roots to detect VA-mycorrhizas. Mycol Res 92:486–505
Krak K, Janoušková M, Caklová P, Vosátka M, Štorchová H (2012) Intraradical dynamics of two coexisting isolates of the arbuscular mycorrhizal fungus Glomus intraradices sensu lato as estimated by real-time PCR of mitochondrial DNA. Appl Environ Microbiol 78:3630–3637. https://doi.org/10.1128/Aem.00035-12
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
Lendenmann M, Thonar C, Barnard RL, Salmon Y, Werner RA, Frossard E, Jansa J (2011) Symbiont identity matters: carbon and phosphorus fluxes between Medicago truncatula and different arbuscular mycorrhizal fungi. Mycorrhiza 21:689–702. https://doi.org/10.1007/s00572-011-0371-5
Marschner H (1995) Mineral nutrition of higher plants. Academic Press, London
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. https://doi.org/10.1111/j.1469-8137.1990.tb00476.x
Monson RK, Edwards GE, Ku MSB (1984) C3-C4 intermediate photosynthesis in plants. Bioscience 34:563–574. https://doi.org/10.2307/1309599
Mortimer PE, Perez-Fernandez 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. https://doi.org/10.1016/j.soilbio.2007.11.014
Newsham KK, Fitter AH, Watkinson AR (1995) Multi-functionality and biodiversity in arbuscular mycorrhizas. Trends Ecol Evol 10:407–411. https://doi.org/10.1016/S0169-5347(00)89157-0
Nielsen KL, Bouma TJ, Lynch JP, Eissenstat DM (1998) Effects of phosphorus availability and vesicular-arbuscular mycorrhizas on the carbon budget of common bean (Phaseolus vulgaris). New Phytol 139:647–656. https://doi.org/10.1046/j.1469-8137.1998.00242.x
Ohno T, Zibilske LM (1991) Determination of low concentrations of phosphorus in soil extracts using malachite green. Soil Sci Soc Am J 55:892–895
Pang PC, Paul EA (1980) Effects of vesicular-arbuscular mycorrhiza on 14C and 15N distribution in nodulated fababeans. Can J Soil Sci 60:241–250
Paul EA, Kucey RMN (1981) Carbon flow in plant microbial associations. Science 213:473–474. https://doi.org/10.1126/science.213.4506.473
Pearson JN, Jakobsen I (1993a) The relative contribution of hyphae and roots to phosphorus uptake by arbuscular mycorrhizal plants, measured by dual labeling with 32P and 33P. New Phytol 124:489–494. https://doi.org/10.1111/j.1469-8137.1993.tb03840.x
Pearson JN, Jakobsen I (1993b) Symbiotic exchange of carbon and phosphorus between Cucumber and three arbuscular mycorrhizal fungi. New Phytol 124:481–488. https://doi.org/10.1111/j.1469-8137.1993.tb03839.x
Pinto H, Sharwood RE, Tissue DT, Ghannoum O (2014) Photosynthesis of C3, C3-C4, and C4 grasses at glacial CO2. J Exp Bot 65:3669–3681. https://doi.org/10.1093/jxb/eru155
Püschel D, Janoušková M, Hujslová M, Slavíková R, Gryndlerová H, Jansa J (2016) Plant-fungus competition for nitrogen erases mycorrhizal growth benefits of Andropogon gerardii under limited nitrogen supply. Ecol Evol 6:4332–4346. https://doi.org/10.1002/ece3.2207
R Core Team (2013) R: a language and environment for statistical computing (http://www.R-project.org). R Foundation for Statistical Computing, Vienna
Rausch C, Daram P, Brunner S, Jansa J, Laloi M, Leggewie G, Amrhein N, Bucher M (2001) A phosphate transporter expressed in arbuscule-containing cells in potato. Nature 414:462–466. https://doi.org/10.1038/35106601
Řezáčová V, Konvalinková T, Jansa J (2017a) Carbon fluxes in mycorrhizal plants. In: Varma A, Prasad R, Tuteja N (eds) Mycorrhiza – eco-physiology, secondary metabolites, nanomaterials, 4th edn. Springer, Cham, pp 1–21
Řezáčová V, Slavíková R, Konvalinková T, Hujslová M, Gryndlerová H, Gryndler M, Püschel D, Jansa J (2017b) Imbalanced carbon-for-phosphorus exchange between European arbuscular mycorrhizal fungi and non-native Panicum grasses—a case of dysfunctional symbiosis. Pedobiologia 62:48–55
Ripley BS, Cunniff J, Osborne CP (2013) Photosynthetic acclimation and resource use by the C3 and C4 subspecies of Alloteropsis semialata in low CO2 atmospheres. Glob Chang Biol 19:900–910. https://doi.org/10.1111/gcb.12091
Rizzo AL, Jost HJ, Caracausi A, Paonita A, Liotta M, Martelli M (2014) Real-time measurements of the concentration and isotope composition of atmospheric and volcanic CO2 at Mount Etna (Italy). Geophys Res Lett 41:2382–2389. https://doi.org/10.1002/2014gl059722
Ryan MH, Tibbett M, Edmonds-Tibbett T, Suriyagoda LDB, Lambers H, Cawthray GR, Pang J (2012) Carbon trading for phosphorus gain: the balance between rhizosphere carboxylates and arbuscular mycorrhizal symbiosis in plant phosphorus acquisition. Plant Cell Environ 35:2170–2180. https://doi.org/10.1111/j.1365-3040.2012.02547.x
Sage RF, Kubien DS (2003) Quo vadis C4? An ecophysiological perspective on global change and the future of C4 plants. Photosynth Res 77:209–225. https://doi.org/10.1023/A:1025882003661
Sage RF, Christin PA, Edwards EJ (2011) The C4 plant lineages of planet earth. J Exp Bot 62:3155–3169. https://doi.org/10.1093/jxb/err048
Schüßler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421. https://doi.org/10.1017/S0953756201005196
Slavíková R, Püschel D, Janoušková M, Hujslová M, Konvalinková T, Gryndlerová H, Gryndler M, Weiser M, Jansa J (2017) Monitoring CO2 emissions to gain a dynamic view of carbon allocation to arbuscular mycorrhizal fungi. Mycorrhiza 27(1):35–51. https://doi.org/10.1007/s00572-016-0737-2
Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic Press, London
Smith SE, Smith FA, Jakobsen I (2004) 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 162:511–524. https://doi.org/10.1111/j.1469-8137.2004.01039.x
Smith SE, Jakobsen I, Gronlund M, Smith FA (2011) Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol 156:1050–1057. https://doi.org/10.1104/pp.111.174581
Snellgrove RC, Splittstoesser WE, Stribley DP, Tinker PB (1982) The distribution of carbon and the demand of the fungal symbiont in leek plants with vesicular arbuscular mycorrhizas. New Phytol 92:75–87. https://doi.org/10.1111/j.1469-8137.1982.tb03364.x
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 (2016) A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108:1028–1046. https://doi.org/10.3852/16-042
Staddon PL, Ramsey CB, Ostle N, Ineson P, Fitter AH (2003) Rapid turnover of hyphae of mycorrhizal fungi determined by AMS microanalysis of 14C. Science 300:1138–1140. https://doi.org/10.1126/science.1084269
Taylor AFS, Gebauer G, Read DJ (2004) Uptake of nitrogen and carbon from double-labelled (15N and 13C) glycine by mycorrhizal pine seedlings. New Phytol 164:383–388. https://doi.org/10.1111/j.1469-8137.2004.01164.x
Thonar C, Erb A, Jansa J (2012) Real-time PCR to quantify composition of arbuscular mycorrhizal fungal communitiesumarker design, verification, calibration and field validation. Mol Ecol Resour 12:219–232. https://doi.org/10.1111/j.1755-0998.2011.03086.x
Tinker PB, Durall DM, Jones MD (1994) Carbon use efficiency in mycorrhizas - theory and sample calculations. New Phytol 128:115–122. https://doi.org/10.1111/j.1469-8137.1994.tb03994.x
Valentine AJ, Mortimer PE, Kleinert A, Kang Y, Benedito VA (2013) Carbon metabolism and costs of arbuscular mycorrhizal associations to host roots. In: Aroca R (ed) Symbiotic endophytes. Springer-Verlag, Berlin, pp 233–252
Wang GM, Coleman DC, Freckman DW, Dyer MI, Mcnaughton SJ, Acra MA, Goeschl JD (1989) Carbon partitioning patterns of mycorrhizal versus non-mycorrhizal plants: real-time dynamic measurements using 11CO2. New Phytol 112:489–493. https://doi.org/10.1111/j.1469-8137.1989.tb00342.x
Wright DP, Read DJ, Scholes JD (1998a) Mycorrhizal sink strength influences whole plant carbon balance of Trifolium repens L. Plant Cell Environ 21:881–891. https://doi.org/10.1046/j.1365-3040.1998.00351.x
Wright DP, Scholes JD, Read DJ (1998b) Effects of VA mycorrhizal colonization on photosynthesis and biomass production of Trifolium repens L. Plant Cell Environ 21:209–216. https://doi.org/10.1046/j.1365-3040.1998.00280.x
Acknowledgements
Seeds of the plants were kindly donated by Dr. Oula Ghannoum from the Hawkesbury Institute for the Environment, Western Sydney University. She also provided useful hints for germinating and growing the plants. This research was supported by the Ministry of Education, Youth and Sports of the Czech Republic (project LK11224), the Czech Science Foundation (project 14-19191S), Fellowship J. E. Purkyně to JJ, and by the long-term development program of the Academy of Sciences of the Czech Republic (RVO 61388971). We are very grateful for rapid and constructive feedback by two anonymous reviewers, which substantially helped improving the quality of the presentation.
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Responsible Editor: Xinhua He.
Veronika Řezáčová and Renata Slavíková are both first authors.
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Řezáčová, V., Slavíková, R., Zemková, L. et al. Mycorrhizal symbiosis induces plant carbon reallocation differently in C3 and C4 Panicum grasses. Plant Soil 425, 441–456 (2018). https://doi.org/10.1007/s11104-018-3606-9
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DOI: https://doi.org/10.1007/s11104-018-3606-9