Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-15T01:30:51.358Z Has data issue: false hasContentIssue false
  • English
  • Français

Gene expression and nitrogen loss in senescing root systems of red clover (Trifolium pratense)

Published online by Cambridge University Press:  06 July 2010

K. J. WEBB ,
E. F. JENSEN ,
S. HEYWOOD ,
S. M. MORRIS ,
P. E. LINTON  and
J. E. HOOKER
K. J. WEBB*
Affiliation:
Institute of Biological, Environmental and Rural Sciences, Gogerddan, Aberystwyth, CeredigionSY23 3EB, UK
E. F. JENSEN
Affiliation:
Institute of Biological, Environmental and Rural Sciences, Gogerddan, Aberystwyth, CeredigionSY23 3EB, UK
S. HEYWOOD
Affiliation:
Institute of Biological, Environmental and Rural Sciences, Gogerddan, Aberystwyth, CeredigionSY23 3EB, UK
S. M. MORRIS
Affiliation:
Institute of Biological, Environmental and Rural Sciences, Gogerddan, Aberystwyth, CeredigionSY23 3EB, UK
P. E. LINTON
Affiliation:
Department of Environmental and Geographical Sciences, Manchester Metropolitan University, ManchesterM1 5GD, UK
*
*To whom all correspondence should be addressed. Email: judith.webb@aber.ac.uk
Get access Rights & Permissions [Opens in a new window]

Summary

Root system senescence and nitrogen (N) release from red clover (Trifolium pratense L.) plants, grown under semi-sterile conditions and a controlled environment, were studied for 28 days following temporary or prolonged abiotic stress. Plants stressed temporarily, to simulate grazing, recovered with no additional N lost in leachate. In contrast, plants subjected to prolonged stress that simulated overwintering conditions and inhibited shoot re-growth survived stress lasting 7 days, but plant viability was reduced to 50% by 14 days and 0% at 21 days. There were no significant differences in root protein, catalase activity, root death index or total N loss in leachate over 21 days, but by 28 days total N loss in leachate increased to 214% above control levels, with a 433% increase in total oxidized N. This increase in N loss between 21 and 28 days indicated the start of cellular breakdown of the root system, coinciding with the failure of plants to recover.

Key enzyme activities and protein concentrations in nodules decreased rapidly over 10 days' prolonged stress. cDNA–amplified fragment length polymorphism (AFLP) analysis identified contaminating bacterial and fungal genes, along with plant gene sequences with consistent or altered expression profiles. Four plant sequences, glyceraldehyde-3-phosphate dehydrogenase (Tp-gapdh1), nodule senescence reduced (Tp-nsr1), nodule senescence enhanced (Tp-nse1) and a cysteine protease gene (Tp-cp8) were differentially expressed throughout the plant: Tp-nsr1 and Tp-nse1 have potential as molecular markers for nodule senescence.

Root and nodule death in agricultural legumes, such as red clover, are implicated in N release into watercourses and the wider environment. Differences in the ability of these plants to survive prolonged stress lasting 14 days, and the delayed release of root N into leachate until 28 days after the stress, highlight the potential for the development of new red clover varieties with different rates of root system senescence.

Type
Crops and Soils
Information
The Journal of Agricultural Science , Volume 148 , Issue 5 , October 2010 , pp. 579 - 591
Copyright
Copyright © Cambridge University Press 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abberton, M. T. & Marshall, A. H. (2005). Progress in breeding perennial clovers for temperate agriculture. Journal of Agricultural Science 143, 117–135.CrossRefGoogle Scholar
Alesandrini, F., Frendo, P., Puppo, A. & Herouart, D. (2003). Isolation of a molecular marker of soybean nodule senescence. Plant Physiology and Biochemistry 41, 727–732.CrossRefGoogle Scholar
Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J. H., Zhang, Z., Miller, W. & Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25, 3389–3402.CrossRefGoogle ScholarPubMed
Asp, T., Bowra, S., Borg, S. & Holm, P. B. (2004). Cloning and characterisation of three groups of cysteine protease genes expressed in the senescing zone of white clover (Trifolium repens) nodules. Plant Science 167, 825–837.CrossRefGoogle Scholar
Baker, C. J. & Mock, N. M. (1994). An improved method for monitoring cell-death in cell-suspension and leaf disc assays using Evans Blue. Plant Cell Tissue and Organ Culture 39, 7–12.CrossRefGoogle Scholar
Baskin, T. I., Busby, C. H., Fowke, L. C., Sammut, M. & Gubler, F. (1992). Improvements in immunostaining samples embedded in methacrylate – localization of microtubules and other antigens throughout developing organs in plants of diverse taxa. Planta 187, 405–413.CrossRefGoogle ScholarPubMed
Bert, P. F., Charmet, G., Sourdille, P., Hayward, M. D. & Balfourier, F. (1999). A high-density molecular map for ryegrass (Lolium perenne) using AFLP markers. Theoretical and Applied Genetics 99, 445–452.CrossRefGoogle ScholarPubMed
Bingham, I. J. & Rees, R. M. (2008). Senescence and N release from clover roots following permanent excision of the shoot. Plant and Soil 303, 229–240.CrossRefGoogle Scholar
Bingham, I. J. & Stevenson, E. A. (1993). Control of root-growth – effects of carbohydrates on the extension, branching and rate of respiration of different fractions of wheat roots. Physiologia Plantarum 88, 149–158.CrossRefGoogle Scholar
Bradford, M. M. (1976). Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Analytical Biochemistry 72, 248–254.CrossRefGoogle ScholarPubMed
BRAN+LUEBBE GMBH W, 22844 Norderstedt, Germany. Nitrate and nitrite in water, waste water and soil extracts and other aqueous samples. Method No. G-109–94 Rev.5.Google Scholar
Brouquisse, R., Gaudillere, J. P. & Raymond, P. (1998). Induction of a carbon-starvation-related proteolysis in whole maize plants submitted to light/dark cycles and to extended darkness. Plant Physiology 117, 1281–1291.CrossRefGoogle ScholarPubMed
Butler, G. W., Greenwood, R. M. & Soper, K. (1959). Effects of shading and defoliation on the turnover of root and nodule tissue of plants of Trifolium repens, Trifolium pratense and Lotus uliginosus. New Zealand Journal of Agricultural Research 2, 415–426.CrossRefGoogle Scholar
Corre, N., Bouchart, V., Ourry, A. & Boucaud, J. (1996). Mobilization of nitrogen reserves during regrowth of defoliated Trifolium repens L and identification of potential vegetative storage proteins. Journal of Experimental Botany 47, 1111–1118.CrossRefGoogle Scholar
Curioni, P. M. G., Reidy, B., Flura, T., Vogeli-Lange, R., Nosberger, J. & Hartwig, U. A. (2000). Increased abundance of MTD1 and MTD2 mRNAs in nodules of decapitated Medicago truncatula. Plant Molecular Biology 44, 477–485.CrossRefGoogle Scholar
Dar, G., Zargar, M. Y. & Beigh, G. M. (1997). Biocontrol of Fusarium root rot in the common bean (Phaseolus vulgaris L) by using symbiotic Glomus mosseae and Rhizobium leguminosarum. Microbial Ecology 34, 74–80.Google Scholar
Devaux, C., Baldet, P., Joubes, J., Dieuaide-Noubhani, M., Just, D., Chevalier, C. & Raymond, P. (2003). Physiological, biochemical and molecular analysis of sugar-starvation responses in tomato roots. Journal of Experimental Botany 54, 1143–1151.CrossRefGoogle ScholarPubMed
Doulis, A. G., Debian, N., Kingston-Smith, A. H. & Foyer, C. H. (1997). Differential localization of antioxidants in maize leaves. Plant Physiology 114, 1031–1037.CrossRefGoogle ScholarPubMed
Doyle, C. J. & Topp, C. F. E. (2004). The economic opportunities for increasing the use of forage legumes in north European livestock systems under both conventional and organic management. Renewable Agriculture and Food Systems 19, 15–22.CrossRefGoogle Scholar
Gallagher, J. A., Volenec, J. J., Turner, L. B. & Pollock, C. J. (1997). Starch hydrolytic enzyme activities following defoliation of white clover. Crop Science 37, 1812–1818.CrossRefGoogle Scholar
Gordon, A. J., Kessler, W. & Minchin, F. R. (1990). Defoliation-induced stress in nodules of white clover. I. Changes in physiological parameters and protein synthesis. Journal of Experimental Botany 41, 1245–1253.CrossRefGoogle Scholar
Gordon, A. J., Minchin, F. R., James, C. L. & Komina, O. (1999). Sucrose synthase in legume nodules is essential for nitrogen fixation. Plant Physiology 120, 867–878.CrossRefGoogle ScholarPubMed
Hanselle, T., Ichinoseb, Y. & Barz, W. (2001). Biochemical and molecular biological studies on infection (Ascochyta rabiei)-induced thaumatin-like proteins from chickpea plants (Cicer arietinum L.). Zeitschrift Fur Naturforschung C-A Journal of Biosciences 56, 1095–1107.CrossRefGoogle ScholarPubMed
Isobe, S., Klimenko, I., Ivashuta, S., Gau, M. & Kozlov, N. N. (2003). First RFLP linkage map of red clover (Trifolium pratense L.) based on cDNA probes and its transferability to other red clover germplasm. Theoretical and Applied Genetics 108, 105–112.CrossRefGoogle ScholarPubMed
Lesuffleur, F., Paynel, F., Bataille, M. P., LE Deunff, E. & Cliquet, J. B. (2007). Root amino acid exudation: measurement of high efflux rates of glycine and serine from six different plant species. Plant and Soil 294, 235–246.CrossRefGoogle Scholar
Liu, W. T., Marsh, T. L., Cheng, H. & Forney, L. J. (1997). Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA. Applied and Environmental Microbiology 63, 4516–4522.CrossRefGoogle ScholarPubMed
Muyzer, G., Dewaal, E. C. & Uitterlinden, A. G. (1993). Profiling of complex microbial-populations by denaturing gradient gel-electrophoresis analysis of polymerase chain reaction-amplified genes-coding for 16S ribosomal-RNA.Applied and Environmental Microbiology 59, 695–700.CrossRefGoogle Scholar
Naito, Y., Fujie, M., Usami, S., Murooka, Y. & Yamada, T. (2000). The involvement of a cysteine proteinase in the nodule development in Chinese milk vetch infected with Mesohizobium huakuii subsp rengei. Plant Physiology 124, 1087–1095.CrossRefGoogle ScholarPubMed
Ougham, H. J. & Davies, T. G. E. (1990). Leaf development in Lolium temulentum: Gradients of RNA complement and plastid and non-plastid transcripts. Physiologia Plantarum 79, 331–338.CrossRefGoogle Scholar
Payne, R. W., Murray, D. A., Harding, S. A., Baird, D. B. & Soutar, D. M. (2008). GenStat® for Windows™, 11th edn. Hemel Hempstead, UK: VSN International.Google Scholar
Puppo, A., Groten, K., Bastian, F., Carzaniga, R., Soussi, M., Lucas, M. M., De Felipe, M. R., Harrison, J., Vanacker, H. & Foyer, C. H. (2005). Legume nodule senescence: roles for redox and hormone signalling in the orchestration of the natural aging process. New Phytologist 165, 683–701.CrossRefGoogle ScholarPubMed
Ridley, A. M., Mele, P. M. & Beverly, C. R. (2003). Legume-based farming in southern Australia: developing sustainable systems to meet environmental challenges: 13th Australian Nitrogen Fixation Conference, Adelaide, Australia. Soil Biology and Biochemistry 36, 1213–1221.CrossRefGoogle Scholar
Ryle, G. J. A., Powell, C. E. & Gordon, A. J. (1978). The effect of source of nitrogen on the growth of Fiskeby soyabean: the carbon economy of whole plants. Annals of Botany 42, 637–648.CrossRefGoogle Scholar
Scholefield, D., Halling, M., Tuori, M., Isolahti, M., Soelter, U. & Stone, A. C. (2002). Assessment of nitrate leaching from beneath forage legumes. In Legume Silages for Animal Production – Legsil (Ed. Wilkins, R. J. & Paul, C.), pp. 17–25. Braunschweig, Germany: Institute of Crop and Grassland Science.Google Scholar
Tixier, M. H., Sourdille, P., Roder, M., Leroy, P. & Bernard, M. (1997). Detection of wheat microsatellites using a non radioactive silver-nitrate staining method. Journal of Genetics and Breeding 51, 175–177.Google Scholar
Van de Velde, W., Guerra, J. C. P., De Keyser, A., De Rycke, R., Rombauts, S., Maunoury, N., Mergaert, P., Kondorosi, E., Holsters, M. & Goormachtig, S. (2006). Aging in legume symbiosis. A molecular view on nodule senescence in Medicago truncatula. Plant Physiology 141, 711–720.CrossRefGoogle ScholarPubMed
Van Elsas, J. D., Duarte, G. F., Keijzer-Wolters, A. & Smit, E. (2000). Analysis of the dynamics of fungal communities in soil via fungal-specific PCR of soil DNA followed by denaturing gradient gel electrophoresis. Journal of Microbiological Methods 43, 133–151.CrossRefGoogle ScholarPubMed
Watson, C. A., Ross, J. M., Bagnaresi, U., Minotta, G. F., Roffi, F., Atkinson, D., Black, K. E. & Hooker, J. E. (2000). Environment-induced modifications to root longevity in Lolium perenne and Trifolium repens. Annals of Botany 85, 397–401.CrossRefGoogle Scholar
Weir, B. S., Turner, S. J., Silvester, W. B., Park, D. C. & Young, J. A. (2004). Unexpectedly diverse Mesorhizobium strains and Rhizobium leguminosarum nodulate native legume genera of New Zealand, while introduced legume weeds are nodulated by Bradyrhizobium species. Applied and Environmental Microbiology 70, 5980–5987.CrossRefGoogle ScholarPubMed
Winters, A., Heywood, S., Farrar, K., Donnison, I., Thomas, A. & Webb, K. J. (2009). Identification of an extensive gene cluster among a family of PPOs in Trifolium pratense L. (red clover) using a large insert BAC library. BMC Plant Biology 9, 94.CrossRefGoogle ScholarPubMed
Winters, A. L., Lloyd, J. D., Jones, R. & Merry, R. J. (2002). Evaluation of a rapid method for estimating free amino acids in silages. Animal Feed Science and Technology 99, 177–187.CrossRefGoogle Scholar