Mycorrhizal effects on growth and nutrition of tomato under elevated atmospheric carbon dioxide
Timothy R. Cavagnaro A C , Shannon K. Sokolow B and Louise E. Jackson BA School of Biological Sciences, Monash University, Clayton, Vic. 3800, Australia.
B Department of Land, Air and Water Resources, University of California Davis, One Shields Avenue, Davis, CA 95616-8627, USA.
C Corresponding author. Email: tim.cavagnaro@sci.monash.edu.au
Functional Plant Biology 34(8) 730-736 https://doi.org/10.1071/FP06340
Submitted: 22 December 2006 Accepted: 19 April 2007 Published: 23 July 2007
Abstract
Arbuscular mycorrhizas are predicted to be important in defining plant responses to elevated atmospheric CO2 concentrations. A mycorrhiza-defective tomato (Solanum lycopersicum L.) mutant with reduced mycorrhizal colonisation (rmc) and its mycorrhizal wild-type progenitor (76R MYC+) were grown under ambient and elevated atmospheric CO2 concentrations (eCO2) in a controlled environment chamber-based pot study. Plant growth, nutrient contents and mycorrhizal colonisation were measured four times over a 72-day period. The 76R MYC+ plants generally had higher concentrations of P, N and Zn than their rmc counterparts. Consistent with earlier studies, mycorrhizal colonisation was not affected by eCO2. Growth of the two genotypes was very similar under ambient CO2 conditions. Under eCO2 the mycorrhizal plants initially had higher biomass, but after 72 days, biomass was lower than for rmc plants, suggesting that in this pot study the costs of maintaining carbon inputs to the fungal symbiont outweighed the benefits with time.
Additional keywords: climate change, elevated CO2, mycorrhiza mutant, mycorrhizas, Solanum lycopersicum.
Acknowledgements
The authors wish to thank Professor Sally Smith (University of Adelaide) and Dr Susan Barker (University of Western Australia), for allowing continued access to the rmc tomato mutant/wild-type system. This work would not have possible without the ongoing support of our farmer cooperators Jim and Deborah Durst. Thanks also to Mr Ryan O’Dell for performing C and N analyses on plant tissue, and to various members of the Jackson laboratory for valuable discussions and technical assistance. Finally, thank you to Professor F. Andrew Smith, Professor Sally Smith and Dr Vanessa Carne-Cavagnaro for valuable comments on an earlier version of this manuscript, and to the two anonymous reviewers of this manuscript for their comments. This research was funded by the United States Department of Agriculture National Research Initiative Soils and Soil Biology Program (2004–03329).
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. The Plant Journal 15, 791–797.
| Crossref | GoogleScholarGoogle Scholar |
Burleigh SH,
Cavagnaro TR, Jakobsen I
(2002) Functional diversity of arbuscular mycorrhizas extends to expression of plant genes involved in P nutrition. Journal of Experimental Botany 53, 1593–1601.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Cavagnaro TR,
Gao L-L,
Smith SE, Smith FA
(2001a) Morphology of arbuscular mycorrhizas is influenced by fungal identity. New Phytologist 151, 469–476.
| Crossref | GoogleScholarGoogle Scholar |
Cavagnaro TR,
Smith FA,
Lorimer MF,
Haskard KA,
Ayling SM, Smith SE
(2001b) Quantitative development of Paris-type arbuscular mycorrhizas formed between Asphodelus fistulosus and Glomus coronatum. New Phytologist 149, 105–113.
| Crossref | GoogleScholarGoogle Scholar |
Cavagnaro TR,
Smith FA,
Ayling SM, Smith SE
(2003) Growth and phosphorus nutrition of a Paris-type arbuscular mycorrhizal symbiosis. New Phytologist 157, 127–134.
| Crossref | GoogleScholarGoogle Scholar |
Cavagnaro TR,
Smith FA,
Hay G,
Carne-Cavagnaro VL, Smith SE
(2004) 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 Phytologist 161, 485–494.
| Crossref | GoogleScholarGoogle Scholar |
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.
| Crossref | GoogleScholarGoogle Scholar |
Cavagnaro TR,
Jackson LE,
Scow KM, Hristova KR
(
) Effects of arbuscular mycorrhizas on ammonia oxidizing bacteria in an organic farm soil. Microbial Ecology ,
Eissenstat DM,
Graham JH,
Syvertsen JP, Drouillard DL
(1993) Carbon economy of sour orange in relation to mycorrhizal colonization and phosphorus status. Annals of Botany 71, 1–10.
| Crossref | GoogleScholarGoogle Scholar |
Fitter AH
(1991) Costs and benefits of mycorrhizas: implications for functioning under natural conditions. Experientia 47, 350–355.
| Crossref | GoogleScholarGoogle Scholar |
Fitter AH,
Heinemeyer A, Staddon PL
(2000) The impact of elevated CO2 and global climate change on arbuscular mycorrhizas: a mycocentric approach. New Phytologist 147, 179–187.
| Crossref | GoogleScholarGoogle Scholar |
Gamper H,
Hartwig UA, Leuchtmann A
(2005) Mycorrhizas improve nitrogen nutrition of Trifolium repens after 8 yr of selection under elevated atmospheric CO2 partial pressure. New Phytologist 167, 531–542.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gao L,
Smith FA, Smith SE
(2006) The rmc locus does not affect plant interactions of defence-related gene expression when tomato (Solanum lycopersicum) is infected with the root fungal parasite, Rhizoctonia. Functional Plant Biology 33, 289–296.
| Crossref | GoogleScholarGoogle Scholar |
Gavito ME,
Bruhn D, Jakobsen I
(2002) P uptake by arbuscular mycorrhizal hyphae does not increase when the host plant grows under atmospheric CO2 enrichment. New Phytologist 154, 751–760.
| Crossref | GoogleScholarGoogle Scholar |
Gavito ME,
Schweiger P, Jakobsen I
(2003) P uptake by arbuscular mycorrhizal hyphae: effect of soil temperature and atmospheric CO2 enrichment. Global Change Biology 9, 106–116.
| Crossref | GoogleScholarGoogle Scholar |
Giovannetti M, Mosse B
(1980) An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytologist 84, 489–500.
| Crossref | GoogleScholarGoogle Scholar |
Hoeksema JD, Bruna EM
(2000) Pursuing the big questions about interspecific mutualism: a review of theoretical approaches. Oecologia 125, 321–330.
| Crossref | GoogleScholarGoogle Scholar |
Jakobsen I, Rosendahl IL
(1990) Carbon flow into soil and external hyphae from roots of mycorrhizal cucumber roots. New Phytologist 115, 77–83.
| Crossref | GoogleScholarGoogle Scholar |
Jifon JL,
Graham JH,
Drouillard DL, Syvertsen JP
(2002) Growth depression of mycorrhizal Citrus seedlings grown at high phosphorus supply is mitigated by elevated CO2. New Phytologist 153, 133–142.
| Crossref | GoogleScholarGoogle Scholar |
Johnson NC,
Graham JH, Smith FA
(1997) Functioning of mycorrhizal associations along the mutualism–parasitism continuum. New Phytologist 135, 575–586.
| Crossref | GoogleScholarGoogle Scholar |
Johnson NC,
Wolf J,
Reyes M,
Panter A,
Koch GW, Redman A
(2005) Species of plants and associated arbuscular mycorrhizal fungi mediate mycorrhizal responses to CO2 enrichment. Global Change Biology 11, 1156–1166.
| Crossref | GoogleScholarGoogle Scholar |
Jongen M,
Fay P, Jones MB
(1996) Effects of elevated carbon dioxide and arbuscular mycorrhizal infection on Trifolium repens. New Phytologist 132, 413–423.
| Crossref | GoogleScholarGoogle Scholar |
Klironomos JN,
Ursic M,
Rillig M, Allen MF
(1998) Interspecific differences in the response of arbuscular mycorrhizal fungi to Artemisia tridentata grown under elevated atmospheric CO2. New Phytologist 138, 599–605.
| Crossref | GoogleScholarGoogle Scholar |
Langley JA,
Johnson NC, Koch GW
(2005) Mycorrhizal status influences the rate but not the temperature sensitivity of soil respiration. Plant and Soil 277, 335–344.
| Crossref | GoogleScholarGoogle Scholar |
Lovelock C,
Kyllo D,
Popp M,
Isopp H,
Virgo A, Winter K
(1997) Symbiotic vesicular arbuscular mycorrhizae influence maximum rates of photosynthesis in tropical tree seedlings grown under elevated CO2. Australian Journal of Plant Physiology 24, 185–194.
Marschner H, Dell B
(1994) Nutrient uptake in mycorrhizal symbiosis. Plant and Soil 159, 89–102.
Marschner P, Timonen S
(2005) Interactions between plant species and mycorrhizal colonization on the bacterial community composition in the rhizosphere. Applied Soil Ecology 28, 23–36.
| Crossref | GoogleScholarGoogle Scholar |
McGonigle TP
(1988) A numerical analysis of published field trials with vesicular-arbuscular mycorrhizal fungi. Functional Ecology 2, 473–478.
| Crossref | GoogleScholarGoogle Scholar |
Phillips JM, Hayman DS
(1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society 55, 158–161.
Poulsen KH,
Nagy R,
Gao L-L,
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 Phytologist 168, 445–453.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Rillig MC, Allen MF
(1998) Arbuscular mycorrhizae of Gutierrezia sarothrae and elevated carbon dioxide: evidence for shifts in C allocation to and within the mycobiont. Soil Biology & Biochemistry 30, 2001–2008.
| Crossref | GoogleScholarGoogle Scholar |
Rogers HH,
Prior SA,
Runion GB, Mitchell RJ
(1995) Root to shoot ratio of crops as influenced by CO2. Plant and Soil 187, 229–248.
| Crossref | GoogleScholarGoogle Scholar |
Sah RN, Miller RO
(1992) Spontaneous reaction for acid dissolution of biological tissues in closed vessels. Analytical Chemistry 64, 230–233.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sanders IR,
Streitwolf-Engel R,
van der Heijden MGA,
Boller
, Wiemken A
(1998) Increased allocation to external hyphae of arbuscular mycorrhizal fungi under CO2 enrichment. Oecologia 117, 496–503.
| Crossref | GoogleScholarGoogle Scholar |
Smith SE,
Smith FA, Jakobsen I
(2004) Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlation with mycorrhizal reponses in growth or total P uptake. New Phytologist 162, 511–524.
| Crossref | GoogleScholarGoogle Scholar |
Staddon PL, Fitter AH
(1998) Does elevated atmospheric carbon dioxide affect arbuscular mycorrhizas? Trends in Ecology & Evolution 13, 455–458.
| Crossref | GoogleScholarGoogle Scholar |
Staddon PL,
Fitter AH, Graves JD
(1999) Effect of elevated atmospheric CO2 on mycorrhizal colonization, external mycorrhizal hyphal production and phosphorus inflow in Plantago lanceolata and Trifolium repens in association with the arbuscular mycorrhizal fungus Glomus mosseae. Global Change Biology 5, 347–358.
| Crossref | GoogleScholarGoogle Scholar |
Staddon PL,
Gregersen R, Jakobsen I
(2004) The response of two Glomus mycorrhizal fungi and a fine endophyte to elevated atmospheric CO2, soil warming and drought. Global Change Biology 10, 1909–1921.
| Crossref | GoogleScholarGoogle Scholar |
Syvertsen JP, Graham JH
(1999) Phosphorus supply and arbuscular mycorrhizas increase growth and net gas exchange responses of two Citrus spp. grown at elevated CO2. Plant and Soil 208, 209–219.
| Crossref | GoogleScholarGoogle Scholar |
Treseder KK, Allen MF
(2000) Mycorrhizal fungi have a potential role in soil carbon storage under elevated CO2 and nitrogen deposition. New Phytologist 147, 189–200.
| Crossref | GoogleScholarGoogle Scholar |
Treseder KK
(2004) A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytologist 164, 347–355.
| Crossref | GoogleScholarGoogle Scholar |
Wardle DA,
Bardgett RD,
Klironomos JN,
Setälä H,
van der Putten WH, Wall DH
(2004) Ecological linkages between Aboveground and belowground Biota. Science 304, 1629–1633.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
