Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
REVIEW

The mixotrophic nature of photosynthetic plants

Susanne Schmidt A , John A. Raven B and Chanyarat Paungfoo-Lonhienne A C
+ Author Affiliations
- Author Affiliations

A School of Agriculture and Food Sciences, The University of Queensland, St Lucia, Qld 4072, Australia.

B Division of Plant Sciences, University of Dundee at the James Hutton Institute, Invergowrie, Dundee DD2 5DA, UK.

C Corresponding author. Email: chanyarat@uq.edu.au

This review originates from the Peter Goldacre Award 2011 of the Australian Society of Plant Scientists that was received by the last author.

Functional Plant Biology 40(5) 425-438 https://doi.org/10.1071/FP13061
Submitted: 15 February 2013  Accepted: 22 March 2013   Published: 18 April 2013

Abstract

Plants typically have photosynthetically competent green shoots. To complement resources derived from the atmospheric environment, plants also acquire essential elements from soil. Inorganic ions and molecules are generally considered to be the sources of soil-derived nutrients, and plants tested in this respect can grow with only inorganic nutrients and so can live as autotrophs. However, mycorrhizal symbionts are known to access nutrients from organic matter. Furthermore, specialist lineages of terrestrial photosynthetically competent plants are mixotrophic, including species that obtain organic nutrition from animal prey (carnivores), fungal partners (mycoheterotrophs) or plant hosts (hemi-parasites). Although mixotrophy is deemed the exception in terrestrial plants, it is a common mode of nutrition in aquatic algae. There is mounting evidence that non-specialist plants acquire organic compounds as sources of nutrients, taking up and metabolising a range of organic monomers, oligomers, polymers and even microbes as sources of nitrogen and phosphorus. Plasma-membrane located transporter proteins facilitate the uptake of low-molecular mass organic compounds, endo- and phagocytosis may enable the acquisition of larger compounds, although this has not been confirmed. Identifying the mechanisms involved in the acquisition of organic nutrients will provide understanding of the ecological significance of mixotrophy. Here, we discuss mixotrophy in the context of nitrogen and phosphorus nutrition drawing parallels between algae and plants.

Additional keywords: endocytosis, mixotrophy, organic nutrients, plant nutrition, root hairs.


References

Adlassnig W, Koller-Peroutka M, Bauer S, Koshkin E, Lendl T, Lichtscheidl IK (2012) Endocytotic uptake of nutrients in carnivorous plants. The Plant Journal 71, 303–313.
Endocytotic uptake of nutrients in carnivorous plants.Crossref | GoogleScholarGoogle Scholar | 22417315PubMed |

Alberts B, Bray D, Lewis JMR, Roberts K, Watson JD (1989) The plasma membrane. In ‘The cell’. pp. 275–340. (Garland Publishing Inc.: New York)

Arnon DI, Stout PR (1939) The essentiality of certain elements in minute quantity for plants with special reference to copper. Plant Physiology 14, 371–375.
The essentiality of certain elements in minute quantity for plants with special reference to copper.Crossref | GoogleScholarGoogle Scholar | 16653564PubMed |

Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annual Review of Plant Biology 57, 233–266.
The role of root exudates in rhizosphere interactions with plants and other organisms.Crossref | GoogleScholarGoogle Scholar | 16669762PubMed |

Baluska F, Samaj J, Hlavacka A, Kendrick-Jones J, Volkmann D (2004) Actin-dependent fluid-phase endocytosis in inner cortex cells of maize root apices. Journal of Experimental Botany 55, 463–473.
Actin-dependent fluid-phase endocytosis in inner cortex cells of maize root apices.Crossref | GoogleScholarGoogle Scholar | 14739268PubMed |

Bates TR, Lynch JP (1996) Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant, Cell & Environment 19, 529–538.
Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability.Crossref | GoogleScholarGoogle Scholar |

Bolte S, Talbot C, Boutte Y, Catrice O, Read ND, Satiat-Jeunemaitre B (2004) FM-dyes as experimental probes for dissecting vesicle trafficking in living plant cells. Journal of Microscopy 214, 159–173.
FM-dyes as experimental probes for dissecting vesicle trafficking in living plant cells.Crossref | GoogleScholarGoogle Scholar | 15102063PubMed |

Bradfute OE, McLaren AD (1964) Entry of protein molecules into plant roots. Physiologia Plantarum 17, 667–675.
Entry of protein molecules into plant roots.Crossref | GoogleScholarGoogle Scholar |

Bradfute OE, Chapman-Andresen C, Jensen WA (1964) Concerning morphological evidence for pinocytosis in higher plants. Experimental Cell Research 36, 207–210.
Concerning morphological evidence for pinocytosis in higher plants.Crossref | GoogleScholarGoogle Scholar |

Bréda N, Maillard P, Montpied P, Bréchet C, Garbaye J, Courty P-E (2013) Isotopic evidence in adult oak trees of a mixotrophic lifestyle during spring reactivation. Soil Biology & Biochemistry 58, 136–139.
Isotopic evidence in adult oak trees of a mixotrophic lifestyle during spring reactivation.Crossref | GoogleScholarGoogle Scholar |

Brewin NJ (2004) Plant cell wall remodelling in the rhizobium-legume symbiosis. Critical Reviews in Plant Sciences 23, 293–316.
Plant cell wall remodelling in the rhizobium-legume symbiosis.Crossref | GoogleScholarGoogle Scholar |

Bronk DA, See JH, Bradley P, Killberg L (2007) DON as a source of bioavailable nitrogen for phytoplankton. Biogeosciences 4, 283–296.
DON as a source of bioavailable nitrogen for phytoplankton.Crossref | GoogleScholarGoogle Scholar |

Bulgarelli D, Rott M, Schlaeppi K, Ver Loren van Themaat E, Ahmadinejad N, Assenza F, Rauf P, Huettel B, Reinhardt R, Schmelzer E, Peplies J, Gloeckner FO, Amann R, Eickhorst T, Schulze-Lefert P (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488, 91–95.
Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota.Crossref | GoogleScholarGoogle Scholar | 22859207PubMed |

Caldwell BA, Jumpponen A, Trappe JM (2000) Utilization of major detrital substrates by dark-septate, root endophytes. Mycologia 92, 230–232.
Utilization of major detrital substrates by dark-septate, root endophytes.Crossref | GoogleScholarGoogle Scholar |

Cambui CA, Svennerstam H, Gruffman L, Nordin A, Ganeteg U, Näsholm T (2011) Patterns of plant biomass partitioning depend on nitrogen source. PLoS ONE 6, e19211
Patterns of plant biomass partitioning depend on nitrogen source.Crossref | GoogleScholarGoogle Scholar | 21544211PubMed |

Chapin FS (1995) Ecology – new cog in the nitrogen-cycle. Nature 377, 199–200.
Ecology – new cog in the nitrogen-cycle.Crossref | GoogleScholarGoogle Scholar |

Chapin FS, Moilanen L, Kielland K (1993) Preferential use of organic nitrogen for growth by a non-mycorrhizal arctic sedge. Nature 361, 150–153.
Preferential use of organic nitrogen for growth by a non-mycorrhizal arctic sedge.Crossref | GoogleScholarGoogle Scholar |

Chen DL, Delatorre CA, Bakker A, Abel S (2000) Conditional identification of phosphate-starvation-response mutants in Arabidopsis thaliana. Planta 211, 13–22.
Conditional identification of phosphate-starvation-response mutants in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 10923699PubMed |

Clode PL, Kilburn MR, Jones DL, Stockdale EA, Cliff JB, Herrmann AM, Murphy DV (2009) In situ mapping of nutrient uptake in the rhizosphere using nanoscale secondary ion mass spectrometry. Plant Physiology 151, 1751–1757.
In situ mapping of nutrient uptake in the rhizosphere using nanoscale secondary ion mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 19812187PubMed |

Cram WJ (1980) Pinocytosis in plants. New Phytologist 84, 1–17.
Pinocytosis in plants.Crossref | GoogleScholarGoogle Scholar |

Crane KW, Grover JP (2010) Coexistence of mixotrophs, autotrophs, and heterotrophs in planktonic microbial communities. Journal of Theoretical Biology 262, 517–527.
Coexistence of mixotrophs, autotrophs, and heterotrophs in planktonic microbial communities.Crossref | GoogleScholarGoogle Scholar | 19878684PubMed |

Croft MT, Warren MJ, Smith AG (2006) Algae need their vitamins. Eukaryotic Cell 5, 1175–1183.
Algae need their vitamins.Crossref | GoogleScholarGoogle Scholar | 16896203PubMed |

Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant and Soil 245, 35–47.
Root exudates as mediators of mineral acquisition in low-nutrient environments.Crossref | GoogleScholarGoogle Scholar |

Datta S, Kim C, Pernas M, Pires N, Proust H, Tam T, Vijayakumar P, Dolan L (2011) Root hairs: development, growth and evolution at the plant–soil interface. Plant and Soil 346, 1–14.
Root hairs: development, growth and evolution at the plant–soil interface.Crossref | GoogleScholarGoogle Scholar |

Davidson EA, David MB, Galloway JN, Goodale CL, Haeuber R, Harrison JA, Howarth RW, Jaynes DB, Lowrance RR, Nolan BT, et al (2012) Excess nitrogen in the US environment: trends, risks and solution. Issues in Ecology 15, 1–16.

Dinkelaker B, Hengeler C, Marschner H (1995) Distribution and function of proteoid roots and other root clusters. Botanica Acta 108, 183–200.

Dyer B, Wrenshall CL (1941) Organic P in soils: I. The extraction and separation of organic phosphorus compounds from soils. Soil Science 51, 159–170.
Organic P in soils: I. The extraction and separation of organic phosphorus compounds from soils.Crossref | GoogleScholarGoogle Scholar |

Dyhrman ST, Chappell PD, Haley ST, Moffett JW, Orchard ED, Waterbury JB, Webb EA (2006) Phosphonate utilization by the globally important marine diazotroph Trichodesmium. Nature 439, 68–71.
Phosphonate utilization by the globally important marine diazotroph Trichodesmium.Crossref | GoogleScholarGoogle Scholar | 16397497PubMed |

Echeverria E (2000) Vesicle-mediated solute transport between the vacuole and the plasma membrane. Plant Physiology 123, 1217–1226.
Vesicle-mediated solute transport between the vacuole and the plasma membrane.Crossref | GoogleScholarGoogle Scholar | 10938341PubMed |

Eggenberger K, Mink C, Wadhwani P, Ulrich AS, Nick P (2011) Using the peptide Bp100 as a cell-penetrating tool for the chemical engineering of actin filaments within living plant cells. ChemBioChem 12, 132–137.
Using the peptide Bp100 as a cell-penetrating tool for the chemical engineering of actin filaments within living plant cells.Crossref | GoogleScholarGoogle Scholar | 21154994PubMed |

Ellison AM, Adamec L (2011) Ecophysiological traits of terrestrial and aquatic carnivorous plants: are the costs and benefits the same? Oikos 120, 1721–1731.
Ecophysiological traits of terrestrial and aquatic carnivorous plants: are the costs and benefits the same?Crossref | GoogleScholarGoogle Scholar |

Emans N, Zimmermann S, Fischer R (2002) Uptake of a fluorescent marker in plant cells is sensitive to Brefeldin A and Wortmannin. The Plant Cell 14, 71–86.
Uptake of a fluorescent marker in plant cells is sensitive to Brefeldin A and Wortmannin.Crossref | GoogleScholarGoogle Scholar | 11826300PubMed |

Epstein E, Bloom AJ (2005) ‘Mineral nutrition of plants: principles and perspectives. 2nd edn. (SinauerAssociates Inc.: Sunderland, MA, USA)

Esteban GF, Fenchel T, Finlay BJ (2010) Mixotrophy in ciliates. Protist 161, 621–641.
Mixotrophy in ciliates.Crossref | GoogleScholarGoogle Scholar | 20970377PubMed |

Etxeberria E, Baroja-Fernandez E, Munoz FJ, Pozueta-Romero J (2005a) Sucrose-inducible endocytosis as a mechanism for nutrient uptake in heterotrophic plant cells. Plant & Cell Physiology 46, 474–481.
Sucrose-inducible endocytosis as a mechanism for nutrient uptake in heterotrophic plant cells.Crossref | GoogleScholarGoogle Scholar |

Etxeberria E, Gonzalez P, Tomlinson P, Pozueta-Romero J (2005b) Existence of two parallel mechanisms for glucose uptake in heterotrophic plant cells. Journal of Experimental Botany 56, 1905–1912.
Existence of two parallel mechanisms for glucose uptake in heterotrophic plant cells.Crossref | GoogleScholarGoogle Scholar | 15911561PubMed |

Flynn KJ, Stoecker DK, Mitra A, Raven JA, Glibert PM, Hansen PJ, Granéli E, Burkholder JM (2013) Misuse of the phytoplankton–zooplankton dichotomy: the need to assign organisms as mixotrophs within plankton functional types. Journal of Plankton Research 35, 3–11.
Misuse of the phytoplankton–zooplankton dichotomy: the need to assign organisms as mixotrophs within plankton functional types.Crossref | GoogleScholarGoogle Scholar |

Forde BG, Walch-Liu P (2009) Nitrate and glutamate as environmental cues for behavioural responses in plant roots. Plant, Cell & Environment 32, 682–693.
Nitrate and glutamate as environmental cues for behavioural responses in plant roots.Crossref | GoogleScholarGoogle Scholar |

Franche C, Lindstrom K, Elmerich C (2009) Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants. Plant and Soil 321, 35–59.
Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants.Crossref | GoogleScholarGoogle Scholar |

Fuerst JA, Hawkins JA, Holmes A, Sly LI, Moore CJ, Stackebrandt E (1993) Porphyrobacter neustonensis gen. nov., sp. nov., an aerobic bacteriochlorophyll-synthesizing budding bacterium from fresh water. International Journal of Systematic Bacteriology 43, 125–134.
Porphyrobacter neustonensis gen. nov., sp. nov., an aerobic bacteriochlorophyll-synthesizing budding bacterium from fresh water.Crossref | GoogleScholarGoogle Scholar | 8427804PubMed |

Gahoonia TS, Nielsen NE (1996) Variation in acquisition of soil phosphorus among wheat and barley genotypes. Plant and Soil 178, 223–230.
Variation in acquisition of soil phosphorus among wheat and barley genotypes.Crossref | GoogleScholarGoogle Scholar |

Gahoonia TS, Nielsen NE (1998) Direct evidence on participation of root hairs in phosphorus (^32P) uptake from soil. Plant Soil 198, 147–152.

Gahoonia TS, Nielsen NE (2004) Barley genotypes with long root hairs sustain high grain yields in low-P field. Plant and Soil 262, 55–62.
Barley genotypes with long root hairs sustain high grain yields in low-P field.Crossref | GoogleScholarGoogle Scholar |

Gahoonia TS, Care D, Nielsen NE (1997) Root hairs and phosphorus acquisition of wheat and barley cultivars. Plant and Soil 191, 181–188.
Root hairs and phosphorus acquisition of wheat and barley cultivars.Crossref | GoogleScholarGoogle Scholar |

Geldner N (2004) The plant endosomal system – its structure and role in signal transduction and plant development. Planta 219, 547–560.
The plant endosomal system – its structure and role in signal transduction and plant development.Crossref | GoogleScholarGoogle Scholar | 15221385PubMed |

Geldner N, Jurgens G (2006) Endocytosis in signalling and development. Current Opinion in Plant Biology 9, 589–594.
Endocytosis in signalling and development.Crossref | GoogleScholarGoogle Scholar | 17011816PubMed |

George TS, Gregory PJ, Hocking P, Richardson AE (2008) Variation in root-associated phosphatase activities in wheat contributes to the utilization of organic P substrates in vitro, but does not explain differences in the P-nutrition of plants when grown in soils. Environmental and Experimental Botany 64, 239–249.
Variation in root-associated phosphatase activities in wheat contributes to the utilization of organic P substrates in vitro, but does not explain differences in the P-nutrition of plants when grown in soils.Crossref | GoogleScholarGoogle Scholar |

Gómez-Baena G, López-Lozano A, Gil-Martínez J, Lucena JM, Diez J, Candau P, Garcia-Fernández JM (2008) Glucose uptake and its effect on gene expression in Prochlorococcus. PLoS ONE 3, e3416
Glucose uptake and its effect on gene expression in Prochlorococcus.Crossref | GoogleScholarGoogle Scholar | 18941506PubMed |

Gruber N, Galloway JN (2008) An Earth-system perspective of the global nitrogen cycle. Nature 451, 293–296.
An Earth-system perspective of the global nitrogen cycle.Crossref | GoogleScholarGoogle Scholar | 18202647PubMed |

Hamilton JMU, Simpson DJ, Hyman SC, Ndimba BK, Slabas AR (2003) Ara12 subtilisin-like protease from Arabidopsis thaliana: purification, substrate specificity and tissue localization. Biochemical Journal 370, 57–67.
Ara12 subtilisin-like protease from Arabidopsis thaliana: purification, substrate specificity and tissue localization.Crossref | GoogleScholarGoogle Scholar |

Hartmann M, Grob C, Tarran GA, Martin AP, Burkill PH, Scanlan DJ, Zubkov MV (2012) Mixotrophic basis of Atlantic oligotrophic ecosystems. Proceedings of the National Academy of Sciences of the United States of America 109, 5756–5760.
Mixotrophic basis of Atlantic oligotrophic ecosystems.Crossref | GoogleScholarGoogle Scholar | 22451938PubMed |

Helliwell K, Wheeler G, Goldstein R, Smith A (2011) Insights into the evolution of vitamin B12 auxotrophy from sequences algal genomes. Molecular Biology and Evolution 28, 2921–2933.
Insights into the evolution of vitamin B12 auxotrophy from sequences algal genomes.Crossref | GoogleScholarGoogle Scholar | 21551270PubMed |

Hermans C, Hammond JP, White PJ, Verbruggen N (2006) How do plants respond to nutrient shortage by biomass allocation? Trends in Plant Science 11, 610–617.
How do plants respond to nutrient shortage by biomass allocation?Crossref | GoogleScholarGoogle Scholar | 17092760PubMed |

Hill PW, Farrar J, Roberts P, Farrell M, Grant H, Newsham KK, Hopkins DW, Bardgett RD, Jones DL (2011) Vascular plant success in a warming Antarctic may be due to efficient nitrogen acquisition. Nature Climate Change 1, 50–53.
Vascular plant success in a warming Antarctic may be due to efficient nitrogen acquisition.Crossref | GoogleScholarGoogle Scholar |

Hirner A, Ladwig F, Stransky H, Okumoto S (2006) Arabidopsis LHT1 Is a high-affinity transporter for cellular amino acid uptake in both root epidermis and leaf mesophyll. The Plant Cell 18, 1931–1946.
Arabidopsis LHT1 Is a high-affinity transporter for cellular amino acid uptake in both root epidermis and leaf mesophyll.Crossref | GoogleScholarGoogle Scholar | 16816136PubMed |

Holstein SEH (2002) Clathrin and plant endocytosis. Traffic 3, 614–620.
Clathrin and plant endocytosis.Crossref | GoogleScholarGoogle Scholar |

Houlton BZ, Wang YP, Vitousek PM, Field CB (2008) A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature 454, 327–330.
A unifying framework for dinitrogen fixation in the terrestrial biosphere.Crossref | GoogleScholarGoogle Scholar | 18563086PubMed |

Inselsbacher E, Näsholm T (2012) A novel method to measure the effect of temperature on diffusion of plant-available nitrogen in soil. Plant and Soil 354, 251–257.
A novel method to measure the effect of temperature on diffusion of plant-available nitrogen in soil.Crossref | GoogleScholarGoogle Scholar |

Inselsbacher E, Ohlund J, Jamtgard S, Huss-Danell K, Näsholm T (2011) The potential of microdialysis to monitor organic and inorganic nitrogen compounds in soil. Soil Biology & Biochemistry 43, 1321–1332.
The potential of microdialysis to monitor organic and inorganic nitrogen compounds in soil.Crossref | GoogleScholarGoogle Scholar |

Jensen WA, McLaren AD (1960) Uptake of proteins by plant cells: the possible occurrence of pinocytosis in plants. Experimental Cell Research 19, 414–417.
Uptake of proteins by plant cells: the possible occurrence of pinocytosis in plants.Crossref | GoogleScholarGoogle Scholar | 14407138PubMed |

Johnson MD, Oldach D, Delwiche CF, Stoecker DK (2007) Retention of transcriptionally active cryptophyte nuclei by the ciliate Myrionecta rubra. Nature 445, 426–428.
Retention of transcriptionally active cryptophyte nuclei by the ciliate Myrionecta rubra.Crossref | GoogleScholarGoogle Scholar | 17251979PubMed |

Jones DL, Nguyen C, Finlay RD (2009) Carbon flow in the rhizosphere: carbon trading at the soil–root interface. Plant and Soil 321, 5–33.
Carbon flow in the rhizosphere: carbon trading at the soil–root interface.Crossref | GoogleScholarGoogle Scholar |

Julou T, Burghardt B, Gebauer G, Berveiller D, Damesin C, Selosse MA (2005) Mixotrophy in orchids: insights from a comparative study of green individuals and nonphotosynthetic individuals of Cephalanthera damasonium. New Phytologist 166, 639–653.
Mixotrophy in orchids: insights from a comparative study of green individuals and nonphotosynthetic individuals of Cephalanthera damasonium.Crossref | GoogleScholarGoogle Scholar | 15819926PubMed |

Juniper BE, Robins RJ, Joel DM (1989) ‘The carnivorous plants.’ (Academic Press Limited: London)

Kilburn MR, Jones DL, Clode PL, Cliff JB, Stockdale EA, Herrmann AM, Murphy DV (2010) Application of nanoscale secondary ion mass spectrometry to plant cell research. Plant Signaling & Behavior 5, 760–762.
Application of nanoscale secondary ion mass spectrometry to plant cell research.Crossref | GoogleScholarGoogle Scholar |

Komarova NY, Thor K, Gubler A, Meier S, Dietrich D, Weichert A, Suter Grotemeyer M, Tegeder M, Rentsch D (2008) AtPTR1 and AtPTR5 transport dipeptides in planta. Plant Physiology 148, 856–869.
AtPTR1 and AtPTR5 transport dipeptides in planta.Crossref | GoogleScholarGoogle Scholar | 18753286PubMed |

Król E, Płachno B, Adamec L, Stolarz M, Dziubińska H, Trębacz K (2012) Quite a few reasons for calling carnivores ‘the most wonderful plants in the world’. Annals of Botany 109, 47–64.
Quite a few reasons for calling carnivores ‘the most wonderful plants in the world’.Crossref | GoogleScholarGoogle Scholar | 21937485PubMed |

Lambers H, Shanes MW, Cramer MD, Perse SJ, Veneklaas EJ (2006) Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Annals of Botany 98, 693–713.
Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits.Crossref | GoogleScholarGoogle Scholar | 16769731PubMed |

Lambers H, Raven JA, Shaver GR, Smith SE (2008) Plant nutrient-acquisition strategies change with soil age. Trends in Ecology & Evolution 23, 95–103.
Plant nutrient-acquisition strategies change with soil age.Crossref | GoogleScholarGoogle Scholar |

Lauter FR, Ninnemann O, Bucher M, Riesmeier JW, Frommer WB (1996) Preferential expression of an ammonium transporter and of two putative nitrate transporters in root hairs of tomato. Proceedings of the National Academy of Sciences of the United States of America 93, 8139–8144.
Preferential expression of an ammonium transporter and of two putative nitrate transporters in root hairs of tomato.Crossref | GoogleScholarGoogle Scholar | 8755617PubMed |

Leake JR (2004) Myco-heterotroph/epiparasitic plant interactions with ectomycorrhizal and arbuscular mycorrhizal fungi. Current Opinion in Plant Biology 7, 422–428.
Myco-heterotroph/epiparasitic plant interactions with ectomycorrhizal and arbuscular mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar | 15231265PubMed |

Leake JR, Cameron DD (2010) Physiological ecology of mycoheterotrophy. New Phytologist 185, 601–605.
Physiological ecology of mycoheterotrophy.Crossref | GoogleScholarGoogle Scholar | 20356334PubMed |

Lee Y-H, Foster J, Chen J, Voll LM, Weber APM, Tegeder M (2007) AAP1 transports uncharged amino acids into roots of Arabidopsis. The Plant Journal 50, 305–319.
AAP1 transports uncharged amino acids into roots of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 17419840PubMed |

Lima JE, Kojima S, Takahashi H, von Wiren N (2010) Ammonium triggers lateral root branching in Arabidopsis in an ammonium transporter1;3-dependent manner. The Plant Cell 22, 3621–3633.
Ammonium triggers lateral root branching in Arabidopsis in an ammonium transporter1;3-dependent manner.Crossref | GoogleScholarGoogle Scholar | 21119058PubMed |

Lonhienne TGA, Sagulenko E, Webb RI, Lee KC, Franke J, Devos DP, Nouwens A, Carrolla BJ, Fuerst JA (2010) Endocytosis-like protein uptake in the bacterium Gemmata obscuriglobus. Proceedings of the National Academy of Sciences of the United States of America 107, 12883–12888.
Endocytosis-like protein uptake in the bacterium Gemmata obscuriglobus.Crossref | GoogleScholarGoogle Scholar |

Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, Glavina del Rio T, et al (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488, 86–90.
Defining the core Arabidopsis thaliana root microbiome.Crossref | GoogleScholarGoogle Scholar | 22859206PubMed |

Ma Z, Bielenberg DG, Brown KM, Lynch JP (2001) Regulation of root hair density by phosphorus availability in Arabidopsis thaliana. Plant, Cell & Environment 24, 459–467.
Regulation of root hair density by phosphorus availability in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Ma L, Velthof GL, Wang FH, Qin W, Zhang WF, Liu Z, Zhang Y, Wei J, Lesschen JP, Ma WQ, Oenema O, Zhang FS (2012) Nitrogen and phosphorus use efficiencies and losses in the food chain in China at regional scales in 1980 and 2005. Science of the Total Environment 434, 51–61.
Nitrogen and phosphorus use efficiencies and losses in the food chain in China at regional scales in 1980 and 2005.Crossref | GoogleScholarGoogle Scholar | 22542299PubMed |

Mandyam KG, Roe J, Jumpponen A (2013) Arabidopsis thaliana model system reveals a continuum of responses to root endophyte colonization. Fungal Biology
Arabidopsis thaliana model system reveals a continuum of responses to root endophyte colonization.Crossref | GoogleScholarGoogle Scholar | in press

Marschner H (1995) ‘Mineral nutrition of higher plants.’ (Academic Press Ltd.: London)

Marschner P, Neumann G, Kania A, Weiskopf L, Lieberei R (2002) Spatial and temporal dynamics of the microbial community structure in the rhizosphere of cluster roots of white lupin (Lupinus albus L.). Plant and Soil 246, 167–174.
Spatial and temporal dynamics of the microbial community structure in the rhizosphere of cluster roots of white lupin (Lupinus albus L.).Crossref | GoogleScholarGoogle Scholar |

Marshall JD, Ehleringer JR (1990) Are xylem-tapping mistletoes partially heterotrophic? Oecologia 84, 244–248.

McCarren J, DeLong EF (2007) Proteorhodopsin photosystem gene clusters exhibit co-evolutionary trends and shared ancestry among diverse marine microbial phyla. Environmental Microbiology 9, 846–858.
Proteorhodopsin photosystem gene clusters exhibit co-evolutionary trends and shared ancestry among diverse marine microbial phyla.Crossref | GoogleScholarGoogle Scholar | 17359257PubMed |

McCutcheon JP, von Dohlen CD (2011) An interdependent metabolic patchwork in the nested symbiosis of mealybugs. Current Biology 21, 1366–1372.
An interdependent metabolic patchwork in the nested symbiosis of mealybugs.Crossref | GoogleScholarGoogle Scholar | 21835622PubMed |

Mercado-Blanco J, Prieto P (2012) Bacterial endophytes and root hairs. Plant and Soil 361, 301–306.
Bacterial endophytes and root hairs.Crossref | GoogleScholarGoogle Scholar |

Mudge S, Rae A, Diatloff E, Smith F (2002) Expression analysis suggests novel roles for members of the Pht1 family of phosphate transporters in Arabidopsis. The Plant Journal 31, 341–353.
Expression analysis suggests novel roles for members of the Pht1 family of phosphate transporters in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 12164813PubMed |

Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiologia Plantarum 15, 473–497.
A revised medium for rapid growth and bioassays with tobacco tissue cultures.Crossref | GoogleScholarGoogle Scholar |

Näsholm T, Ekblad A, Nordin A, Giesler R, Hogberg M, Hogberg P (1998) Boreal forest plants take up organic nitrogen. Nature 392, 914–916.
Boreal forest plants take up organic nitrogen.Crossref | GoogleScholarGoogle Scholar |

Näsholm T, Kielland K, Ganeteg U (2009) Uptake of organic nitrogen by plants. New Phytologist 182, 31–48.
Uptake of organic nitrogen by plants.Crossref | GoogleScholarGoogle Scholar | 19210725PubMed |

Neumann G, Martinoia E (2002) Cluster roots – an underground adaptation for survival in extreme environments. Trends in Plant Science 7, 162–167.
Cluster roots – an underground adaptation for survival in extreme environments.Crossref | GoogleScholarGoogle Scholar | 11950612PubMed |

Ovečka M, Lang I, Baluška F, Ismail A, Illeš P, Lichtscheidl IK (2005) Endocytosis and vesicle trafficking during tip growth of root hairs. Protoplasma 226, 39–54.
Endocytosis and vesicle trafficking during tip growth of root hairs.Crossref | GoogleScholarGoogle Scholar | 16231100PubMed |

Paungfoo-Lonhienne C, Lonhienne TGA, Rentsch D, Robinson N, Christie M, Webb RI, Gamage HK, Carroll BJ, Schenk PM, Schmidt S (2008) Plants can use protein as a nitrogen source without assistance from other organisms. Proceedings of the National Academy of Sciences of the United States of America 105, 4524–4529.
Plants can use protein as a nitrogen source without assistance from other organisms.Crossref | GoogleScholarGoogle Scholar | 18334638PubMed |

Paungfoo-Lonhienne C, Schenk PM, Lonhienne TGA, Brackin R, Meier S, Rentsch D, Schmidt S (2009) Nitrogen affects cluster root formation and expression of putative peptide transporters. Journal of Experimental Botany 60, 2665–2676.
Nitrogen affects cluster root formation and expression of putative peptide transporters.Crossref | GoogleScholarGoogle Scholar | 19380419PubMed |

Paungfoo-Lonhienne C, Lonhienne TGA, Mudge SR, Schenk PM, Christie M, Carroll BJ, Schmidt S (2010a) DNA is taken up by root hairs and pollen, and stimulates root and pollen tube growth. Plant Physiology 153, 799–805.
DNA is taken up by root hairs and pollen, and stimulates root and pollen tube growth.Crossref | GoogleScholarGoogle Scholar | 20388669PubMed |

Paungfoo-Lonhienne C, Rentsch D, Robatzek S, Webb R, Sagulenko E, Näsholm T, Schmidt S, Lonhienne T (2010b) Turning the table: plants consume microbes as a source of nutrients. PLoS ONE 5, e11915
Turning the table: plants consume microbes as a source of nutrients.Crossref | GoogleScholarGoogle Scholar | 20689833PubMed |

Paungfoo-Lonhienne C, Visser J, Lonhienne TGA, Schmidt S (2012) Past, present and future of organic nutrients. Plant and Soil 359, 1–18.
Past, present and future of organic nutrients.Crossref | GoogleScholarGoogle Scholar |

Peltzer D, Wardle D, Allison V, Baisden W, Bardgett R, Chadwick O, Condron L, Parfitt R, Porder S, Richardson S, Turner B, Vitousek P, Walker J, Walker L (2010) Understanding ecosystem retrogression. Ecological Monographs 80, 509–529.
Understanding ecosystem retrogression.Crossref | GoogleScholarGoogle Scholar |

Pérez-Gómez J, Moore I (2007) Plant endocytosis: it is clathrin after all. Current Biology 17, R217–R219.
Plant endocytosis: it is clathrin after all.Crossref | GoogleScholarGoogle Scholar | 17371763PubMed |

Pillet L, Pawlowski J (2013) Transcriptome analysis of foraminiferan Elphidium margaritaceum questions the role of gene transfer in kleptoplastidy. Molecular Biology and Evolution 30, 66–69.
Transcriptome analysis of foraminiferan Elphidium margaritaceum questions the role of gene transfer in kleptoplastidy.Crossref | GoogleScholarGoogle Scholar | 22993235PubMed |

Poretsky RS, Sun SL, Mou XZ, Moran MA (2010) Transporter genes expressed by coastal bacterioplankton in response to dissolved organic carbon. Environmental Microbiology 12, 616–627.
Transporter genes expressed by coastal bacterioplankton in response to dissolved organic carbon.Crossref | GoogleScholarGoogle Scholar | 19930445PubMed |

Prieto P, Schiliro E, Maldonado-Gonzalez MM, Valderrama R, Barroso-Albarracin JB, Mercado-Blanco J (2011) Root hairs play a key role in the endophytic colonization of olive roots by Pseudomonas spp. with biocontrol activity. Microbial Ecology 62, 435–445.
Root hairs play a key role in the endophytic colonization of olive roots by Pseudomonas spp. with biocontrol activity.Crossref | GoogleScholarGoogle Scholar | 21347721PubMed |

Raven JA (1983) Phytophages of xylem and phloem: a comparison of animal and plantsap-feeders. Advances in Ecological Research 13, 135–234.
Phytophages of xylem and phloem: a comparison of animal and plantsap-feeders.Crossref | GoogleScholarGoogle Scholar |

Raven JA (1987) The role of vacuoles. New Phytologist 106, 357–422.

Raven JA (1997) Phagotrophy in phototrophs. Limnology and Oceanography 42, 198–205.
Phagotrophy in phototrophs.Crossref | GoogleScholarGoogle Scholar |

Raven JA (2012) Carbon. In ‘Ecology of cyanobacteria’. 2nd edn. (Ed. B Whitton) pp. 443–460. (Springer: Berlin)

Raven JA, Donnelly S (2013) Brown dwarfs and black smokers. The potential for photosynthesis using the radiation from low-temperature black bodies. In ‘Habitability of other planets and satellites’. (Ed. J-P Devera) (Springer: Berlin) (In press)

Raven JA, Beardall J, Flynn KJ, Maberly SC (2009) Phagotrophy in the origins of photosynthesis in eukaryotes and as a complementary mode of nutrition in phototrophs: relation to Darwin’s insectivorous plants. Journal of Experimental Botany 60, 3975–3987.
Phagotrophy in the origins of photosynthesis in eukaryotes and as a complementary mode of nutrition in phototrophs: relation to Darwin’s insectivorous plants.Crossref | GoogleScholarGoogle Scholar | 19767306PubMed |

Read DJ, Perez-Moreno J (2003) Mycorrhizas and nutrient cycling in ecosystems – a journey towards relevance? New Phytologist 157, 475–492.
Mycorrhizas and nutrient cycling in ecosystems – a journey towards relevance?Crossref | GoogleScholarGoogle Scholar |

Richardson AE, Hadobas PA, Hayes JE (2000) Acid phosphomonoesterase and phytase activities of wheat (Triticum aestivum L.) roots and utilization of organic phosphorus substrates by seedlings grown in sterile culture. Plant, Cell & Environment 23, 397–405.
Acid phosphomonoesterase and phytase activities of wheat (Triticum aestivum L.) roots and utilization of organic phosphorus substrates by seedlings grown in sterile culture.Crossref | GoogleScholarGoogle Scholar |

Richardson AE, Hocking PJ, Simpson RJ, George TS (2009) Plant mechanisms to optimise access to soil phosphorus. Crop and Pasture Science 60, 124–143.
Plant mechanisms to optimise access to soil phosphorus.Crossref | GoogleScholarGoogle Scholar |

Robinson DG (2005) Plant and fungal endocytosis. Protoplasma 226, 1

Robinson DG, Jiang LW, Schumacher K (2008) The endosomal system of plants: charting new and familiar territories. Plant Physiology 147, 1482–1492.
The endosomal system of plants: charting new and familiar territories.Crossref | GoogleScholarGoogle Scholar | 18678740PubMed |

Šamaj J, Baluška F, Voigt B, Schlicht M, Volkmann D, Menzel D (2004) Endocytosis, actin cytoskeleton, and signaling. Plant Physiology 135, 1150–1161.
Endocytosis, actin cytoskeleton, and signaling.Crossref | GoogleScholarGoogle Scholar | 15266049PubMed |

Šamaj J, Read ND, Volkmann D, Menzel D, Baluska F (2005) The endocytic network in plants. Trends in Cell Biology 15, 425–433.
The endocytic network in plants.Crossref | GoogleScholarGoogle Scholar | 16006126PubMed |

Sauer N (2007) Molecular physiology of higher plant sucrose transporters. FEBS Letters 581, 2309–2317.
Molecular physiology of higher plant sucrose transporters.Crossref | GoogleScholarGoogle Scholar | 17434165PubMed |

Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85, 591–602.
Nitrogen mineralization: challenges of a changing paradigm.Crossref | GoogleScholarGoogle Scholar |

Schulte EE, Kelling KA (1999) ‘Understand plant nutrients – soil and applied sulfur A2525.’ (University of Wisconsin-Extension) Available at www.soils.wisc.edu/extension/pubs/A2525.pdf

Schulten HR, Schnitzer M (1997) The chemistry of soil organic nitrogen: a review. Biology and Fertility of Soils 26, 1–15.
The chemistry of soil organic nitrogen: a review.Crossref | GoogleScholarGoogle Scholar |

Schulze W, Frommer WB, Ward JM (1999) Transporters for ammonium, amino acids and peptides are expressed in pitchers of the carnivorous plant Nepenthes. The Plant Journal 17, 637–646.
Transporters for ammonium, amino acids and peptides are expressed in pitchers of the carnivorous plant Nepenthes.Crossref | GoogleScholarGoogle Scholar | 10230062PubMed |

Schunmann P, Richardson A, Vickers C, Delhaize E (2004) Promoter analysis of the barley Pht1;1 phosphate transporter gene identifies regions controlling root expression and responsiveness to phosphate deprivation. Plant Physiology 136, 4205–4214.
Promoter analysis of the barley Pht1;1 phosphate transporter gene identifies regions controlling root expression and responsiveness to phosphate deprivation.Crossref | GoogleScholarGoogle Scholar | 15542491PubMed |

Selosse MA, Roy M (2009) Green plants that feed on fungi: facts and questions about mixotrophy. Trends in Plant Science 14, 64–70.
Green plants that feed on fungi: facts and questions about mixotrophy.Crossref | GoogleScholarGoogle Scholar | 19162524PubMed |

Shane MW, Lambers H (2005) Cluster roots: a curiosity in context. Plant and Soil 274, 101–125.
Cluster roots: a curiosity in context.Crossref | GoogleScholarGoogle Scholar |

Silberbush M (2013) Root study: why is it behind other plant studies? American Journal of Plant Sciences 4, 198–203.
Root study: why is it behind other plant studies?Crossref | GoogleScholarGoogle Scholar |

Sirová D, Borovec J, Picek T, Adamec L, Nedbalová L, Vrba J (2011) Ecological implications of organic carbon dynamics in the traps of aquatic carnivorous Utricularia plants. Functional Plant Biology 38, 583–593.
Ecological implications of organic carbon dynamics in the traps of aquatic carnivorous Utricularia plants.Crossref | GoogleScholarGoogle Scholar |

Smith SE, Read DJ (2008) ‘Mycorrhizal symbiosis.’ (Academic Press: Amsterdam)

Smith FW, Mudge SR, Rae AL, Glassop D (2003) Phosphate transport in plants. Plant and Soil 248, 71–83.
Phosphate transport in plants.Crossref | GoogleScholarGoogle Scholar |

Soper FM, Paungfoo-Lonhienne C, Brackin R, Rentsch D, Schmidt S, Robinson N (2011) Arabidopsis and Lobelia anceps access small peptides as a nitrogen source for growth. Functional Plant Biology 38, 788–796.
Arabidopsis and Lobelia anceps access small peptides as a nitrogen source for growth.Crossref | GoogleScholarGoogle Scholar |

Sprent JI (2001) ‘Nodulation in legumes.’ (The Cromwell Press: Royal Botanical Gardens, Kew)

Stoecker DK (1998) Conceptual models of mixotrophy in planktonic protists and some ecological and evolutionary implications. European Journal of Protistology 34, 281–290.
Conceptual models of mixotrophy in planktonic protists and some ecological and evolutionary implications.Crossref | GoogleScholarGoogle Scholar |

Stoelken G, Simon J, Ehlting B, Rennenberg H (2010) The presence of amino acids affects inorganic N uptake in non-mycorrhizal seedlings of European beech (Fagus sylvaticus). Tree Physiology 30, 1118–1128.
The presence of amino acids affects inorganic N uptake in non-mycorrhizal seedlings of European beech (Fagus sylvaticus).Crossref | GoogleScholarGoogle Scholar | 20595637PubMed |

Svennerstam H, Ganeteg U, Bellini C, Näsholm T (2007) Comprehensive screening of Arabidopsis mutants suggests the lysine histidine transporter 1 to be involved in plant uptake of amino acids. Plant Physiology 145, 1853–1860.

Svennerstam H, Jämtgård S, Ahmad I, Huss-Danell K, Näsholm T, Ganeteg U (2011) Transporters in Arabidopsis roots mediating uptake of amino acids at naturally occurring concentrations. New Phytologist 191, 459–467.

Tedersoo L, Pellet P, Koljalg U, Selosse MA (2007) Parallel evolutionary paths to mycoheterotrophy in understorey Ericaceae and Orchidaceae: ecological evidence for mixotrophy in Pyroleae. Oecologia 151, 206–217.
Parallel evolutionary paths to mycoheterotrophy in understorey Ericaceae and Orchidaceae: ecological evidence for mixotrophy in Pyroleae.Crossref | GoogleScholarGoogle Scholar | 17089139PubMed |

Tester M, Smith SE, Smith FA (1987) The phenomenon of nonmycorrhizal plants. Canadian Journal of Botany 65, 419–431.
The phenomenon of nonmycorrhizal plants.Crossref | GoogleScholarGoogle Scholar |

Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S (2002) Agricultural sustainability and intensive production practices. Nature 418, 671–677.
Agricultural sustainability and intensive production practices.Crossref | GoogleScholarGoogle Scholar | 12167873PubMed |

Tittel J, Bissinger V, Zippel B, Gaedke U, Bell E, Lorke A, Kamjunke N (2003) Mixotrophs combine resource use to outcompete specialists: implications for aquatic food webs. Proceedings of the National Academy of Sciences of the United States of America 100, 12776–12781.
Mixotrophs combine resource use to outcompete specialists: implications for aquatic food webs.Crossref | GoogleScholarGoogle Scholar | 14569026PubMed |

Tornero P, Conejero V, Vera P (1996) Primary structure and expression of a pathogen-induced protease (PR-P69) in tomato plants: similarity of functional domains to subtilisin-like endoproteases. Proceedings of the National Academy of Sciences of the United States of America 93, 6332–6337.
Primary structure and expression of a pathogen-induced protease (PR-P69) in tomato plants: similarity of functional domains to subtilisin-like endoproteases.Crossref | GoogleScholarGoogle Scholar | 8692815PubMed |

Venterink HO (2011) Legumes have a higher root phosphatase activity than other forbs, particularly under low inorganic P and N supply. Plant and Soil 347, 137–146.
Legumes have a higher root phosphatase activity than other forbs, particularly under low inorganic P and N supply.Crossref | GoogleScholarGoogle Scholar |

Voigt B, Timmers ACJ, Samaj J, Hlavacka A, Ueda T, Preuss M, Nielsen E, Mathur J, Emans N, Stenmark H (2005) Actin-based motility of endosomes is linked to the polar tip growth of root hairs. European Journal of Cell Biology 84, 609–621.
Actin-based motility of endosomes is linked to the polar tip growth of root hairs.Crossref | GoogleScholarGoogle Scholar | 16032929PubMed |

Wagele H, Deusch O, Handeler K, Martin R, Schmitt V, Christa G, Pinzger B, Gould SB, Dagan T, Klussmann-Kolb A, Martin W (2011) Transcriptomic evidence that longevity of acquired plastids in the photosynthetic slugs Elysia timida and Plakobranchus ocellatus does not entail lateral transfer of algal nuclear genes. Molecular Biology and Evolution 28, 699–706.
Transcriptomic evidence that longevity of acquired plastids in the photosynthetic slugs Elysia timida and Plakobranchus ocellatus does not entail lateral transfer of algal nuclear genes.Crossref | GoogleScholarGoogle Scholar | 20829345PubMed |

Walch-Liu P, Ivanov II, Filleur S, Gan YB, Remans T, Forde BG (2006a) Nitrogen regulation of root branching. Annals of Botany 97, 875–881.
Nitrogen regulation of root branching.Crossref | GoogleScholarGoogle Scholar | 16339770PubMed |

Walch-Liu P, Liu LH, Remans T, Tester M, Forde BG (2006b) Evidence that L-glutamate can act as an exogenous signal to modulate root growth and branching in Arabidopsis thaliana. Plant & Cell Physiology 47, 1045–1057.
Evidence that L-glutamate can act as an exogenous signal to modulate root growth and branching in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiology 132, 44–51.
Root exudation and rhizosphere biology.Crossref | GoogleScholarGoogle Scholar | 12746510PubMed |

Warren CR (2013) High diversity of small organic N observed in soil water. Soil Biology & Biochemistry 57, 444–450.
High diversity of small organic N observed in soil water.Crossref | GoogleScholarGoogle Scholar |

Wasaki J, Yamamura T, Shinano T, Osaki M (2003) Secreted acid phosphatase is expressed in cluster roots of lupin in response to phosphorus deficiency. Plant and Soil 248, 129–136.
Secreted acid phosphatase is expressed in cluster roots of lupin in response to phosphorus deficiency.Crossref | GoogleScholarGoogle Scholar |

Weisskopf L, Heller S, Eberl L (2011) Burkholderia species are major inhabitants of white lupin cluster roots. Applied and Environmental Microbiology 77, 7715–7720.
Burkholderia species are major inhabitants of white lupin cluster roots.Crossref | GoogleScholarGoogle Scholar | 21908626PubMed |

Whiteside MD, Treseder KK, Atsatt PR (2009) The brighter side of soils: quantum dots track organic nitrogen through fungi and plants. Ecology 90, 100–108.
The brighter side of soils: quantum dots track organic nitrogen through fungi and plants.Crossref | GoogleScholarGoogle Scholar | 19294917PubMed |

Yamamura T, Wasaki J, Shinano T, Osaki M (2002) Expression of acid phosphatase gene in cluster roots of white lupin. Plant & Cell Physiology 43, S112–S112.

Zhang F, Cui Z, Chen X, Ju X, Shen J, Chen Q, Liu X, Zhang W, Mi G, Fan M, Jiang R (2013) Integrated nutrient management for food security and environment quality in China. In ‘Advances in agronomy. Vol. 116’. (Ed. DL Sparks) pp. 1–40. (Academic Press) (In Press)

Zubkov MV (2009) Photoheterotrophy in marine prokaryotes. Journal of Plankton Research 31, 933–938.
Photoheterotrophy in marine prokaryotes.Crossref | GoogleScholarGoogle Scholar |

Zubkov MV, Tarran GA, Mary I, Fuchs BM (2008) Differential microbial uptake of dissolved amino acids and amino sugars in surface waters of the Atlantic Ocean. Journal of Plankton Research 30, 211–220.
Differential microbial uptake of dissolved amino acids and amino sugars in surface waters of the Atlantic Ocean.Crossref | GoogleScholarGoogle Scholar |