Disentangling who is who during rhizosphere acidification in root interactions: Combining fluorescence with optode techniques

Frontiers in Plant Science

Volumn 4, Issue OCT, 2013, Pages

  Faget, Marc ^a   Blossfeldt, Stephan ^a   Von Gillhaussen, Philipp ^a   Schurr, Ulrich ^a   Temperton, Vicky M ^a  

^a FORSCHUNGSZENTRUM JÜLICH   (Germany)

Author keywords

Bean; Green fluorescent protein; Interaction; Maize; Ph planar optodes; Plant roots; Rhizosphere; Rhizotrons

Indexed keywords

EID: 84901038349     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00392     Document Type: Article

References (47)

1. Blossfeld, S. (2013). Light for the dark side of plant life: planar optodes visualizing rhizosphere processes. Plant Soil 369, 29-32. doi: 10.1007/s11104-11013-11767-11100.
2. Blossfeld, S., and Gansert, D. (2007). A novel non-invasive optical method for quantitative visualization of pH dynamics in the rhizosphere of plants. Plant Cell Environ. 30, 176-186. doi: 10.1111/j.1365-3040.2006.01616.x
3. Blossfeld, S., and Gansert, D. (2012). The Use of Planar Optodes in Root Studiesfor QuantitativeImaging. New York: Springer.
4. Blossfeld, S., Gansert, D., Thiele, B., Kuhn, A. J., and Losch, R. (2011). The dynamics of oxygen concentration, pH value, and organic acids in the rhizosphere of Juncus spp. Soil Biol. Biochem. 43, 1186-1197. doi: 10.1016/j.soilbio.2011.02.007.
5. Blossfeld, S., Schreiber, C. M., Lieb-sch, G., Kuhn, A. J., and Hinsinger, P. (2013). Quantitative imaging of rhizosphere pH and CO2 dynamics with planar optodes. Ann. Bot. 112, 267-276. doi: 10.1093/aob/ mct047.
6. Bolan, N. S., Hedley, M. J., and White, R. E. (1991). Processes of soil acidification during nitrogen cycling with emphasis on legume based pastures. Plant Soil 134, 53-63. doi: 10.1007/BF00010717.
7. Bonkowski, M., Villenave, C., and Griffiths, B. (2009). Rhizosphere fauna: the functional and structural diversity of intimate interactions of soil fauna with plant roots. PlantSoil 321, 213-233. doi: 10.1007/s11104-009- 0013-2.
8. Brooker, R. W., Maestre, F. T., Callaway, R. M., Lortie, C. L., Cavieres, L. A., Kunstler, G., et al. (2008). Facilitation in plant communities: the past, the present, and the future. J. Ecol. 96, 18-34. doi: 10.1111/j.1365-2745.2007.01295.x
9. Cahill, J. F., Mcnickle, G. G., Haag, J. J., Lamb, E. G., Nyanumba, S. M., and Clair, C. C. S. (2010). Plants integrate information about nutrients and neighbors. Science 328, 1657-1657. doi: 10.1126/science.1189736.
10. Callaway, R. M., Brooker, R. W., Choler, P., Kikvidze, Z., Lortie, C. J., Michalet, R., et al. (2002). Positive interactions among alpine plants increase with stress. Nature 417, 844-848. doi: 10.1038/nature00812.
11. Colmer, T.D., and Bloom, A.J. (1998). A comparison of NH4+ and NO3- net fluxes along roots of rice and maize. PlantCell Environ. 21, 240-246. doi: 10.1046/j.1365-3040.1998.00261.x
12. Cousins, A. B., and Bloom, A. J. (2003). Influence of elevated CO2 and nitrogen nutrition on photosynthesis and nitrate photo-assimilation in maize (Zea mays L.). Plant Cell Environ. 26, 1525-1530. doi: 10.1046/j.1365-3040.2003.01075.x
13. Darwin, C. R. (1880). The Power of Movements in Plants. London: John Murray.
14. de Kroon, H. (2007). Ecology - how do roots interact? Science 318, 1562-1563. doi: 10.1126/science.1150726
15. de Kroon, H., Hendriks, M., Van Ruijven, J., Ravenek, J., Padilla, F. M., Jongejans, E., et al. (2012). Root responses to nutrients and soil biota: drivers of species coexistence and ecosystem productivity. J. Ecol. 100, 6-15. doi: 10.1111/j.1365-2745.2011.01906.x
16. de Kroon, H., and Mommer, L. (2006). Root foraging theory put to the test. Trends Ecol. Evol. 21, 113-116. doi: 10.1016/j.tree.2005.11.021.
17. Dudley, S. A., and File, A. L. (2007). Kin recognition in an annual plant. Biol. Lett. 3, 435-438. doi: 10.1098/rsbl.2007.0232.
18. Dudley, S. A., Murphy, G. P., and File, A. L. (2013). Kin recognition and competition in plants. Funct. Ecol. 27, 898-906. doi: 10.1111/13652435.12121.
19. Faget, M., Herrera, J. M., Stamp, P., Aulinger-Leipner, I., Frossard, E., and Liedgens, M. (2009). The use of green fluorescent protein as a tool to identify roots in mixed plant stands. Funct. Plant Biol. 36, 930-937. doi: 10.1071/FP09125.
20. Faget, M., Liedgens, M., Feil, B., Stamp, P., and Herrera, J. M. (2012). Root growth of maize in an Italian ryegrass living mulch studied with a nondestructive method. Eur. J. Agron. 36, 1-8. doi: 10.1016/j.eja.2011. 08.002.
21. Faget, M., Liedgens, M., Stamp, P., Flutsch, P., and Herrera, J. M. (2010). A minirhizotron imaging system to identify roots expressing the green fluorescent protein. Comput. Electron. Agric. 74, 163-167. doi: 10.1016/j.compag.2010.06.010.
22. Faget, M., Nagel, K. A., Walter, A., Herrera, J. M., Jahnke, S., Schurr, U., et al. (2013). Root-root interactions: extending our perspective to be more inclusive of the range of theories in ecology and agriculture using in vivo analyses. Ann. Bot. 112,253-266. doi: 10.1093/aob/mcs296.
23. Fang, C. X., Zhuang, Y. E., Xu, T. C., Li, Y. Z., Li, Y., and Lin, W. X. (2013). Changes in rice allelopathy and rhizo-sphere microflora by inhibiting rice phenylalanine ammonia-lyase gene expression. J. Chem. Ecol. 39, 204-212. doi: 10.1007/s10886-013-0249-4.
24. Fiorani, F., and Schurr, U. (2013). Future scenarios for plant phenotyp-ing. Annu. Rev. Plant. Biol. 64, 267-291. doi: 10.1146/annurev-arplant-050312-120137.
25. Gagliano, M., Renton, M., Duvde-vani, N., Timmins, M., and Man-cuso, S. (2012). Out of sight but not out of mind: alternative means of communication in plants. PLoS ONE 7:e37382. doi: 10.1371/jour-nal.pone.0037382.
26. Gansert, D., and Blossfeld, S. (2008). "The application of novel optical sensors (optodes) in experimental plant ecology," in Progress in Botany, eds U. Lüttge, W. Beyschlag, and J. Murata (Berlin: Springer), 333-358. doi: 10.1007/978-3-540-72954-9_14.
27. Hiltner, L. (1904). Über neuere Erfahrungen und Probleme auf dem Gebiet der Bodenbakteriologie und unter besonderer Berücksichtigung der Grunddüngung und Brache. Arb. Deutsche. Landwirt. Ges. 98, 59-78.
28. Hinsinger, P., Bengough, A. G., Vet-terlein, D., and Young, I. M. (2009). Rhizosphere: biophysics, biogeochemistry and ecological relevance. Plant Soil 321, 117-152. doi: 10.1007/s11104-008-9885-9.
29. Hinsinger, P., Gobran, G. R., Gregory, P. J., and Wenzel, W. W. (2005). Rhi-zosphere geometryand heterogeneity arising from root-mediated physical and chemical processes. New Phytol. 168, 293-303. doi: 10.1111/j.1469-8137.2005.01512.x
30. Hinsinger, P., Plassard, C., Tang, C. X., and Jaillard, B. (2003). Origins ofroot-mediated pH changes in the rhizosphere and their responses to environmental constraints: a review. Plant Soil 248, 43-59. doi: 10.1023/A:1022371130939.
31. Hodge, A. (2004). The plastic plant: root responses to heterogeneous supplies of nutrients. New Phy-tol. 162, 9-24. doi: 10.1111/j.1469-8137.2004.01015.x
32. Holst, G., and Grunwald, B. (2001). Luminescence lifetime imaging with transparent oxygen optodes. Sens. Actuators B Chem. 74, 7890. doi: 10.1016/S0925-4005(00) 00715-2.
33. Hurlbert, S. H. (1984). Pseudoreplication and the design of ecological field experiments. Ecol. Monogr. 54, 187-211. doi: 10.2307/1942661.
34. Jones, D. L., Dennis, P. G., Owen, A. G., and Van Hees, P. A. W. (2003). Organic acid behavior in soils - misconceptions and knowledge gaps. Plant Soil 248, 31-41. doi: 10.1023/A:1022304332313.
35. Klemens, J. A. (2008). Kin recognition in plants? Biol. Lett. 4, 67-68. doi: 10.1098/rsbl.2007.0518.
36. Lambers, H., Shane, M. W., Cramer, M. D., Pearse, S. J., and Veneklaas, E. J. (2006). Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann. Bot. 98, 693-713. doi: 10.1093/aob/mcl114.
37. Li, L., Li, S.-M., Sun, J.-H., Zhou, L.-L., Bao, X.-G., Zhang, H.-G., et al. (2007). Diversity enhances agricultural productivity via rhizosphere phosphorus facilitation on phosphorus-deficient soils. Proc. Natl. Acad. Sci. U.S.A. 104, 11192-11196. doi: 10.1073/pnas. 0704591104.
38. Marschner, H., and Romheld, V.(1983). In vivo measurement of root-induced pH changes at the soil-root interface: effect of plant species and nitrogen source. Z. Pflanzenphysiol. 111, 241-251.
39. Nagel, K. A., Putz, A., Gilmer, F., Heinz, K., Fischbach, A., Pfeifer, J., et al. (2012). GROWSCREEN-Rhizo isanovel phenotypingrobot enabling simultaneous measurements of root and shoot growth for plants grown in soil-filled rhizotrons. Funct. Plant Biol. 39, 891-904. doi: 10.1071/FP12023.
40. Postma, J. A., and Lynch, J. P. (2012). Complementarity in root architecture for nutrient uptake in ancient maize/bean and maize/bean/squash polycultures. Ann. Bot. 110, 521-534. doi: 10.1093/aob/mcs082.
41. Rascher, U., Blossfeld, S., Fio-rani, F., Jahnke, S., Jansen, M., Kuhn, A. J., et al. (2011). Non-invasive approaches for phenotyping of enhanced performance traits in bean. Funct. Plant Biol. 38, 968-983. doi: 10.1071/FP11164.
42. Rewald, B., Meinen, C., Trockenbrodt, M., Ephrath, J. E., and Rachmilevitch, S. (2012). Root taxa identification in plant mixtures - current techniques and future challenges. Plant Soil 359, 165-182. doi: 10.1007/s11104-012-1164-0.
43. Schreiber, C. M., Zeng, B., Temperton, V. M., Rascher, U., Kazda, M., Schurr, U., et al. (2011). Dynamics of organic acid occurrence under flooding stress in the rhizosphere of three plant species from the water fluctuation zone of the Three Gorges Reservoir, P.R. China. Plant Soil 344, 111-129. doi: 10.1007/s11104-011-0732-z
44. Stahl, H., Glud, A., Schroder, C. R., Klimant, I., Tengberg, A., and Glud, R. N. (2006). Time-resolved pH imaging in marine sediments with a luminescent planar optode. Limnol. Oceanogr. Methods 4, 336-345. doi: 10.4319/lom.2006.4.336.
45. Stromberg, N. (2008). Determination of ammonium turnover and flow patterns close to roots using Imaging optodes. Environ. Sci. Tech-nol. 42, 1630-1637. doi: 10.1021/es 071400q
46. Temperton, V. M., Mwangi, P. N., Scherer-Lorenzen, M., Schmid, B., and Buchmann, N. (2007). Positive interactions between nitrogen-fixing legumes and four different neighbouring species in a biodiversity experiment. Oecologia 151, 190-205. doi: 10.1007/s00442-006-0576-z
47. Zavala, J. A., and Baldwin, I. T. (2006). Jasmonic acid signalling and herbivore resistance traits constrain regrowth after herbivore attack in Nicotiana attenuata. Plant Cell Environ. 29, 1751-1760. doi: 10.1111/j.1365-3040.2006.01551.x