Growth, nutrition, and soil respiration of a mycorrhiza-defective tomato mutant and its mycorrhizal wild-type progenitor
Timothy R. Cavagnaro A E , Adam J. Langley B , Louise E. Jackson C , Sean M. Smukler C and George W. Koch DA School of Biological Sciences and Australian Centre for Biodiversity, Monash University, Clayton, Vic. 3800, Australia.
B Smithsonian Environmental Research Centre, Edgewater, MD 21037, USA.
C Department of Land, Air and Water Resources, University of California Davis, One Shields Avenue, Davis, CA 95616-8627, USA.
D National Institute for Climatic Change Research, Box 5640, Northern Arizona University, Flagstaff, AZ 86011, USA.
E Corresponding author. Email: tim.cavagnaro@sci.monash.edu.au
Functional Plant Biology 35(3) 228-235 https://doi.org/10.1071/FP07281
Submitted: 26 November 2007 Accepted: 13 March 2008 Published: 23 April 2008
Abstract
The effects of colonisation of roots by arbuscular mycorrhizal fungi (AMF) on soil respiration, plant growth, nutrition, and soil microbial communities were assessed using a mycorrhiza-defective tomato (Solanum lycopersicum L.) mutant and its mycorrhizal wild-type progenitor. Plants were grown in rhizocosms in an automated respiration monitoring system over the course of the experiment (79 days). Soil respiration was similar in the two tomato genotypes, and between P treatments with plants. Mycorrhizal colonisation increased P and Zn content and decreased root biomass, but did not affect aboveground plant biomass. Soil microbial biomass C and soil microbial communities based on phospholipid fatty acid (PLFA) analysis were similar across all treatments, suggesting that the two genotypes differed little in their effect on soil activity. Although approximately similar amounts of C may have been expended belowground in both genotypes, they may have differed in the relative C allocation to root construction v. respiration. Further, net soil respiration did not differ between the two tomato genotypes, but root dry weight was lower in mycorrhizal roots, and respiration of mycorrhizal roots per unit dry weight was higher than nonmycorrhizal roots. This indicates that the AM contribution to soil respiration may indeed be significant, and nutrient uptake per unit C expenditure belowground in this experiment appeared to be higher in mycorrhizal plants.
Additional keywords: mycorrhiza mutant, mycorrhizas, PLFA, respiration, roots, root respiration, Solanum lycopersicum.
Acknowledgements
We are especially grateful to Sally Smith (University of Adelaide) and Susan Barker (University of Western Australia), for allowing our continued use of the rmc tomato mutant/wild-type system. We also thank Katherine Sides (NAU) for her excellent technical assistance and that from various members of the Jackson Laboratory (UC Davis). Thanks also to Kate Scow for PLFA extraction and identification at UC Davis. The efforts of two anonymous reviewers are also appreciated. The research was funded by the California Department of Food and Agriculture Speciality Crops Program (SA6674), the United States Department of Agriculture National Research Initiative Soils and Soil Biology Program (2004–03329) and a National Science Foundation grant to Nancy Johnson and George Koch (DEB:9806529).
Bakhtiar Y,
Miller D,
Cavagnaro TR, Smith SE
(2001) Interactions between two arbuscular mycorrhizal fungi and fungivorous nematodes and control of the nematode with fenamifos. Applied Soil Ecology 17, 107–117.
| Crossref | GoogleScholarGoogle Scholar |
Baon JB,
Smith SE,
Alston AM, Wheeler RD
(1992) Phosphorus efficiency of three cereals as related to indigenous mycorrhizal infection. Australian Journal of Agricultural Research 43, 479–491.
| Crossref | GoogleScholarGoogle Scholar |
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 |
Blanke V,
Renker C,
Wagner M,
Füllner K,
Held M,
Kuhn AJ, Buscot F
(2005) Nitrogen supply affects arbuscular mycorrhizal colonization of Artemisia vulgaris in a phosphate-polluted field site. New Phytologist 166, 981–992.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bligh EG, Dyer WM
(1959) A rapid method of lipid extraction and purification. Canadian Journal of Biochemistry and Physiology 35, 911–917.
Bossio DA, Scow KM
(1998) Impacts of carbon and flooding on soil microbial communities, phospholipid fatty acid profiles and substrate utilization patterns. Microbial Ecology 35, 265–278.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Bruce A,
Smith SE, Tester M
(1994) The development of mycorrhizal infection in cucumber: effects of P supply on root growth, formation of entry points and growth of infection units. New Phytologist 127, 507–514.
| Crossref | GoogleScholarGoogle Scholar |
Butler JL,
Williams MA,
Bottomley PJ, Myrold DD
(2003) Microbial community dynamics associated with rhizosphere carbon flow. Applied and Environmental Microbiology 69, 6793–6800.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Cavagnaro TR,
Smith FA,
Lorimer MF,
Haskard KA,
Ayling SM, Smith SE
(2001) 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,
Smith FA,
Smith SE, Jakobsen I
(2005) Functional diversity in arbuscular mycorrhizas: exploitation of soil patches with different phosphate enrichment differs among fungal species. Plant, Cell & Environment 164, 485–491.
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 and Soil 282, 209–225.
| Crossref | GoogleScholarGoogle Scholar |
Cavagnaro TR,
Jackson LE,
Scow KM, Hristova KR
(2007a) Effects of arbuscular mycorrhizas on ammonia oxidizing bacteria in an organic farm soil. Microbial Ecology 54, 618–626.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Cavagnaro TR,
Sokolow SK, Jackson LE
(2007b) Mycorrhizal effects on growth and nutrition of tomato under elevated atmospheric carbon dioxide. Functional Plant Biology 34, 730–736.
| Crossref | GoogleScholarGoogle Scholar |
Cheng W
(1996) Measurement of rhizosphere respiration and organic matter decomposition using natural 13C. Plant and Soil 183, 263–268.
| Crossref | GoogleScholarGoogle Scholar |
Coleman DC,
Andrews R,
Ellis JE, Singh JS
(1976) Energy flow and partition in selected managed and natural ecosystems. Agro-Ecosystems 3, 45–54.
| Crossref | GoogleScholarGoogle Scholar |
Cramer MD,
Lewis OAM, Lips SH
(1993) Inorganic carbon fixation and metabolism in maize roots as affected by nitrate and ammonium nutrition. Physiologia Plantarum 89, 632–639.
| Crossref | GoogleScholarGoogle Scholar |
Ezawa T,
Cavagnaro TR,
Smith SE,
Smith FA, Ohtomo R
(2004) Rapid accumulation of polyphosphate in extraradical hyphae of an arbuscular mycorrhizal fungus as revealed by histochemistry and a polyphosphate kinase/luciferase system. New Phytologist 161, 387–392.
| 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 |
Gange AC
(2000) Arbuscular mycorrhizal fungi, collembola and plant growth. Trends in Ecology & Evolution 15, 369–372.
| Crossref | GoogleScholarGoogle Scholar |
Guckert JB,
Hood MA, White DC
(1986) Phospholipid ester-linked fatty acid profile changes during nutrient deprivation of Vibrio chlerae, increase in the trans/cis ratio and proportions of cyclopropyl fatty acids. Applied and Environmental Microbiology 52, 794–801.
| PubMed |
Ingham RE,
Trofymow JA,
Ingham ER, Coleman DC
(1985) Interactions of bacteria, fungi, and their nematode grazers: effects on nutrient cycling and plant growth. Ecological Monographs 55, 119–140.
| Crossref | GoogleScholarGoogle Scholar |
Jackson LE,
Miller D, Smith SE
(2002) Arbuscular mycorrhizal colonization and growth of wild and cultivated lettuce in response to nitrogen and phosphorus. Scientia Horticulturae 94, 205–218.
| 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 |
Johnson NC,
Graham JH, Smith FA
(1997) Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytologist 135, 575–586.
| Crossref | GoogleScholarGoogle Scholar |
Keith H,
Jacobsen KL, Raison RJ
(1997) Effects of soil phosphorus availability, temperature and moisture on soil respiration in Eucalyptus pauciflora forest. Plant and Soil 190, 127–141.
| Crossref | GoogleScholarGoogle Scholar |
Krämer S, Green GM
(1999) Phosphorus pools in tree and intercanopy microsites of a Juniper–Grass ecosystem. Soil Science Society of America Journal 63, 1901–1905.
Kuzyakov Y, Domanski G
(2002) Model for rhizodeposition and CO2 efflux from planted soil and its validation by 14C pulse labeling of ryegrass. Plant and Soil 239, 87–102.
| 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 |
Luo Y,
Jackson RB,
Field CB, Mooney HA
(1996) Elevated CO2 increases belowground respiration in California grasslands. Oecologia 108, 130–137.
| Crossref | GoogleScholarGoogle Scholar |
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 |
Miranda KM,
Espey MG, Wink DA
(2001) A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide 5, 62–71.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Mortimer PE,
Archer E, Valentine AJ
(2005) Mycorrhizal C costs and nutritional benefits in developing grapevines. Mycorrhiza 15, 159–165.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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 Phytologist 139, 647–656.
| Crossref | GoogleScholarGoogle Scholar |
Oliver AJ,
Smith SE,
Nicholas DJD,
Wallace W, Smith FA
(1983) Activity of nitrate reductase in Trifolium subterraneum: effects of mycorrhizal infection and phosphate nutrition. New Phytologist 94, 63–79.
| Crossref | GoogleScholarGoogle Scholar |
Olsson PA,
van Aarle IM,
Allaway WG,
Ashford AE, Rouhier H
(2002) Phosphorus effects on metabolic processes in monoxenic arbuscular mycorrhiza cultures. Plant Physiology 130, 1162–1171.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pang PC, Paul EA
(1980) Effects of vesicular arbuscular mycorrhiza on 14C and 15N distribution in nodulated faba beans. Canadian Journal of Soil Science 60, 241–250.
Peng S,
Eissenstat DM,
Graham JH,
Williams K, Hodge NC
(1993) Growth depression in mycorrhizal citrus at high-phosphorus supply. Plant Physiology 101, 1063–1071.
| PubMed |
Potthoff M,
Steenwerth KL,
Jackson LE,
Drenovsky RE,
Scow KM, Joergensen RG
(2006) Soil microbial community composition as affected by restoration practices in California grassland. Soil Biology & Biochemistry 38, 1851–1860.
| Crossref | GoogleScholarGoogle Scholar |
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, 445–454.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Rillig MC
(2004) Arbuscular mycorrhizae and terrestrial ecosystem processes. Ecology Letters 7, 740–754.
| Crossref | GoogleScholarGoogle Scholar |
Robertson BK, Alexander M
(1992) Influence of calcium, iron, and pH on phosphate availability for microbial mineralization of organic chemicals. Applied and Environmental Microbiology 58, 38–41.
| PubMed |
Rochette P, Angers DA
(1999) Soil surface carbon dioxide fluxes induced by spring, summer, and fall moldboard plowing in a sandy loam. Soil Science Society of America Journal 63, 621–628.
Ryan MH, Ash A
(1999) Effects of phosphorus and nitrogen on growth of pasture plants and VAM fungi in SE Australian soils with contrasting fertiliser histories (conventional and biodynamic). Agriculture Ecosystems and Environments 73, 51–62.
| 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 |
Silsbury JH,
Smith SE, Oliver AJ
(1983) A comparison of growth efficiency and specific rate of dark respiration of uninfected and vesicular-arbuscular mycorrhizal plants of Trifolium subterraneum L. New Phytologist 93, 555–566.
| Crossref | GoogleScholarGoogle Scholar |
Smith SE
(1982) Inflow of phosphate into mycorrhizal and non-mycorrhizal plants of Trifolium subterraneum at different levels of soil phosphate. New Phytologist 90, 293–303.
| 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 |
Tennant D
(1975) A test of the modified line intersect method of estimating root length. Journal of Ecology 63, 995–1001.
| Crossref |
Thomson BD,
Robson AD, Abbott LK
(1991) Soil mediated effects of phosphorus supply on the formation of mycorrhizas by Scutellospora calospora (Nicol. & Gerd.) Walker and Sanders on subterranean clover New Phytologist 118, 463–469.
| Crossref | GoogleScholarGoogle Scholar |
Valentine AJ, Kleinert A
(2007) Phosphate deficiency affects respiratory metabolism of dark CO2 fixation in mycorrhizal roots. Mycorrhiza 17, 137–143.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
van Aarle IM,
Cavagnaro TR,
Smith SE,
Smith FA, Dickson S
(2005) Metabolic activity of Glomus intraradices in Arum- and Paris-type arbuscular mycorrhizal colonization. New Phytologist 166, 611–618.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Vance ED,
Brookes PD, Jenkinson DS
(1987) An extraction method to estimate soil microbial biomass C. Soil Biology & Biochemistry 19, 703–707.
| Crossref | GoogleScholarGoogle Scholar |
Wright DP,
Scholes JD, Read DJ
(1998) Mycorrhizal sink strength influences whole-plant carbon balance of Trifolium repens L. Plant, Cell & Environment 21, 881–891.
| Crossref | GoogleScholarGoogle Scholar |