Grass cells ingested by ruminants undergo autolysis which differs from senescence: Implications for grass breeding targets and livestock production

Plant, Cell and Environment

Volumn 25, Issue 10, 2002, Pages 1299-1312

  Beha, E M ^a,b   Theodorou, M K ^a   Thomas, B J ^a   Kingston Smith, A H ^a  

^a ABERYSTWYTH UNIVERSITY   (United Kingdom)

^b ABERYSTWYTH UNIVERSITY   (United Kingdom)

Author keywords

Agriculture; Cell death; Chloroplasts; Lolium perenne; Proteolysis; Rubisco; Ruminant

Indexed keywords

SENESCENCE;

BOVIDAE; LOLIUM; LOLIUM PERENNE;

EID: 0036788113     PISSN: 01407791     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-3040.2002.00908.x     Document Type: Article

References (80)

1. Adam Z. (1996) Protein stability and degradation in chloroplasts. Plant Molecular Biology 32, 773-783.
2. Aldrich H.C., Fel R.J., Hils M.H. & Akin D.E. (1985) Ultrastructure correlates of anaerobic stress in corn roots. Tissue Cell 17, 341-346.
3. Andersson B. & Aro E.-M. (1997) Proteolytic activities and proteases of plant chloroplasts. Physiologia Plantarum 100, 780-793.
4. Andreev V.Y., Generozova I.P. & Vartapetian B.B. (1991) Energy status and mitochondrial ultrastructure of excised pea root and anoxia and postanoxia. Plant Physiology and Biochemistry 29, 171-176.
5. Arnon D.L. (1949) Copper enzymes in isolated chloroplasts. Polyphenol oxidase in Beta vulgaris. Plant Physiology 24, 1-15.
6. Beever D.E. (1986) Nutrient intake and metabolism in grazing animals. Animal Production 42, 448.
7. Beha E.M. (2000) Plant enzyme mediated proteolysis in fresh grass in an in vitro incubation system simulating the rumen. PhD Thesis. University of Wales, Aberystwyth, UK.
8. Bird I.F., Cornelius M.J. & Keys A.J. (1982) Affinity of RuBP carboxylases for carbon dioxide of ribulose bisphosphate carboxylase. Journal of Experimental Botany 31, 365-369.
9. Boudon A. & Peyraud J.-L. (2001) The release of intracellular constituents from fresh ryegrass (Lolium perenne L.) during ingestive mastication in dairy cows: effect of intracellular constituent, season and stage of maturity. Animal Feed Science and Technology 93, 229-245.
10. Bradford M.M. (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248-254.
11. Broderick G.A. & Cochran R.C. (2000) In vitro and in situ methods for estimating digestibility with reference to protein degradability. In Feeding Systems and Feed Evaluation Models (eds M.K. Theodorou & J. France), pp. 53-85. CABI Publishing, Oxford, UK.
12. Bushnell T.P., Bushnell D. & Jagendorf A.T. (1993) A purified zinc protease of pea choroplasts, EP1, degrades the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase. Plant Physiology 103, 585-591.
13. Cheng K.-J., Fay J.P., Howarth R.E. & Costerton J.W. (1980) Sequence of events in the digestion of fresh legume leaves by rumen bacteria. Applied and Environmental Microbiology 40, 613-625.
14. Dalling M.J., Tang A.B. & Huffaker R.C. (1983) Evidence for the existence of peptide hydrolase activity associated with chloroplasts isolated from barley mesophyll protoplasts. Zeitschrift für Pflanzenphysiologie 111, 311-318.
15. Delorme V.G.R., McCabe P.F., Kim D.J. & Leaver C.J. (2000) A matrix metalloproteinase gene is expressed at the boundary of senescence and programmed cell death in cucumber. Plant Physiology 123, 917-927.
16. Desimone M., Henke A. & Wagner E. (1996) Oxidative stress induces partial degradation of the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase in isolated chloroplasts of barley. Plant Physiology 111, 789-796.
17. Dewhurst R.J., Mitton A.M., Offer N.W. & Thomas C. (1996) Effects of the composition of grass silages on milk production and nitrogen utilization by dairy cows. Animal Science 62, 25-43.
18. Drew M.C. (1997) Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia. Annual Review of Plant Physiology and Plant Molecular Biology 48, 223-250.
19. 3-induced degradation of rubisco protein and loss of rubisco messenger RNA in relation to leaf age in Solanum tuberosum L. New Phytologist 127, 741-748.
20. Feller U. (1986) Proteolytic enzymes in relation to leaf senescence. In Plant Proteolytic Enzymes (ed. M.J. Dalling) Vol. II, pp. 49-68. CRC Press, Boca Raton, FL, USA.
21. Ferreira R.B. & Shaw N.M. (1989) Effect of osmotic-stress on protein-turnover in Lemna minor fronds. Planta 179, 456-465.
22. Grover A., Sabat S.C. & Mohanty P. (1987) Does the loss of leaf chlorophyll during senescence of primary wheat leaf arise due to loss in chloroplast number or chlorophyll content? Biochemie and Physiologie der Pflanzen 182, 481-484.
23. Harrak H., Azelmat S., Baker E.N. & Tabaeizadeh Z. (2001) Isolation and characterisation of a gene encoding a drought-induced cysteine protease in tomato (Lycopersicon esculentum). Genome 44, 368-374.
24. Heber U. & Heldt H.W. (1981) The chloroplast envelope: structure, function and role in leaf metabolism. Annual Review of Plant Physiology 32, 139-168.
25. Hildbrand M., Fischer A. & Feller U. (1994) Protein catabolism in leaf discs: accumulation of a soluble fragment of ribulose-1,5-bisphosphate carboxylase/oxygenase under oxygen deficiency. Journal of Experimental Botany 45, 1197-1204.
26. Hill G.M., Gates R.N. & Burton G.W. (1993) Forage quality and grazing steer performance from Tifton-85 and Tifton-78 bermudagrass pastures. Journal of Animal Science 71, 3219-3225.
27. Hobson (1988) The Rumen Microbial Ecosystem. Elsevier, Amsterdam, The Netherlands.
28. Holden L.A., Muller L.D., Varga G.A. & Hillard P.J. (1994) Ruminal digestion and duodenal nutrient flows in dairy-cows consuming grass as pasture, hay, or silage. Journal of Dairy Science 77, 3034-3042.
29. Howarth C.J. & Ougham H.J. (1993) Tansley Review. 51. Gene-expression under temperature stress. New Phytologist 125, 1-26.
30. Hristov A.N. (1998) Nitrogen fractions and in sacco dry matter and crude protein degradability of fresh and frozen alfalfa. Animal Feed Science and Technology 71, 351-355.
31. Huffaker R.C. (1990) Proteolytic activity during senescence of plants. New Phytologist 116, 199-231.
32. Ishibashi M., Usuda H. & Terashima I. (1996) The loss of ribulose-1,5-bisphosphate carboxylase/oxygenase caused by 24h rain treatment fully explains the decrease in the photosynthetic rate in bean leaves. Plant Physiology 111, 635-640.
33. Ishida H., Makino A. & Mae T. (1999) Fragmentation of the large subunit of Ribulose bisphosphate carboxylase by reactive oxygen species occurs near Gly-329. Journal of Biological Chemistry 274, 5222-5226.
34. Ishida H., Shimizu S., Making A. & Mae T. (1998) Light-dependent fragmentation of the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase in chloroplasts isolated from wheat leaves. Planta 204, 305-309.
35. Ishida K., Suzuki K. & Hogestsu T. (1992) Spreading of nuclear degradation in Pinus thunbergii Parl cuttings under water stress. Plant and Cell Physiology 33, 897-907.
36. Kapuscinski J. (1995) DAPI: a DNA-specific fluorescent probe. Biotechnical Histochemistry 70, 220-233.
37. Kennedy R.A., Rumpho M.E. & Fox T.C. (1992) Anaerobic metabolism in plants. Plant Physiology 100, 1-6.
38. Kingston-Smith A.H. (1992) Dephosphorylation of 2′carboxyarabinitol-1-phosphate and the regulation of Rubisco activity. PhD Thesis. Imperial College, London, UK.
39. Kingston-Smith A.H. & Theodorou M.K. (2000) Post-ingestion metabolism of fresh forage. New Phytologist 148, 37-55.
40. Laemmli U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
41. Lai F.M., Senaratna T. & McKersie B.D. (1992) Anaerobic stress in Medicago sativa cell suspensions. Journal of Plant Physiology 139, 331-338.
42. MacRae J.C., Smith J.S., Dewey P.J.S., Brewer A.C., Brown D.S. & Walker A. (1985) The efficiency of utilization of metabolizable energy and apparent absorption of amino acids in sheep given spring- and autumn-harvested dried grass. British Journal of Nutrition 54, 197-209.
43. Mae T., Kai N., Making A. & Ohira K. (1984) Relation between ribulose bisphosphate carboxylase content and chloroplast number in naturally senescing primary leaves of wheat. Plant Cell Physiology 25, 333-336.
44. Marschner H. & Mix G. (1973) The effect of sodium chloride and myostatin on the mineral content of leaf tissues and on the fine structure of chloroplasts. Zeitschrift für Pflanzenernährung und Bodenkunde 136, 203-219.
45. Marschner H., Handley R. & Overstreet R. (1966) Potassium loss and changes in the fine structure of corn root tips induced by H-ion. Plant Physiology 41, 1725-1735.
46. Martinoia E., Heck U., Dalling M.J. & Matile P. (1983) Changes in chloroplast number and chloroplast constituents in senescing barley leaves. Biochemie and Physiologie der Pflanzen 178, 147-155.
47. Matile P. (1982) Protein degradation. In Encyclopedia of Plant Physiology 14A: Nucleic Acids and Proteins in Plants (eds D. Boulter & B. Parthier), pp. 169-188. Springer Verlag, Berlin, Germany.
48. Matile P. (1997) The vacuole and cell senescence. In The Plant Vacuole: Advances in Botanical Research (eds R.A. Leigh & D. Sanders) Vol. 25, pp. 87-112. Academic Press, London, UK.
49. Matile P., Hortensteiner S. & Thomas H. (1999) Chlorophyll degradation. Annual Review of Plant Physiology and Plant Molecular Biology 50, 67-95.
50. Mehta R.A., Fawcett T.W., Porath D. & Mattoo A.K. (1992) Oxidative stress causes rapid membrane translocation and in vivo degradation of ribulose-1,5-biphosphate carboxylase oxygenase. Journal of Biological Chemistry 267, 2810-2816.
51. Mehta R.A., Warmbardt R.D. & Mattoo A.K. (1996) Tomato (Lycopersicon esculentum cv. Pik Red) leaf carboxypeptidase: identification, N-terminal sequence, stress regulation and specific localisation in the paraveinal mesophyll vacuoles. Plant and Cell Physiology 37, 806-815.
52. Miller B.L. & Huffaker R.C. (1985) Differential induction of endoproteinases during senescence of attached and detached barley leaves. Plant Physiologist 78, 442-446.
53. Mitsuhashi W., Crafts-Brandner S.J. & Feller U. (1992) Ribulose-1,5-bis-phosphate carboxylase/oxygenase degradation in isolated pea chloroplasts incubated in the light or in the dark. Journal of Plant Physiology 139, 653-658.
54. Morris K., Thomas H. & Rogers L.J. (1996) Endopeptidases during the development and senescence of Lolium temulentum leaves. Phytochemistry 41, 377-384.
55. Otto S. & Feierabend J. (1994) Assay and comparative characterization of the proteolytic degradation of isolated small-subunit and holoenzyme of ribulose-1,5-bisphosphate carboxylase/oxygenase in chloroplasts from rye leaves. Journal of Plant Physiology 144, 26-33.
56. Penning P.D., Parsons A.J., Orr R.J., Harvey A. & Champion R.A. (1995) Intake and behaviour responses by sheep in different physiological states, when grazing monocultures of grass or white clover. Applied Animal Behaviour Science 45, 63-78.
57. Pfister-Sieber M. & Brandle R. (1994) Aspects of plant behaviour under anoxia and postanoxia. Proceedings of the Royal Society Edinburgh B 102, 313-324.
58. Ricard B., Couee I., Raymond P., Saglio P.H., Saintges V. & Pradet A. (1994) Plant-metabolism under hypoxia and anoxia. Plant Physiology and Biochemistry 32, 1-10.
59. Rogers J.C., Dean D. & Heck G.R. (1985) Aleurain - a barley thiol protease closely related to mammalian cathepsin-H. Proceedings of the National Academy of Sciences of the USA 82, 6512-6516.
60. Rosen H. (1957) A modified ninhydrin colorimetric analysis for amino acids. Archives of Biochemistry and Biophysics 67, 10-15.
61. Roulin S. & Feller U. (1998) Light-independent degradation of stromal proteins in intact chloroplasts isolated from Pisum sativum L. leaves: requirement for divalent cations. Planta 205, 297-304.
62. Salvucci M.E., Portis A.R. & Ogren W. (1986) Purification of ribulose-1,5-bis-phosphate carboxylase/oxygenase with high specific activity by fast protein liquid chromatography. Analytical Biochemistry 153, 97-101.
63. Siddons R.C., Paradine J., Gale D.L. & Evans R.T. (1985) Estimation of the degradability of dietary-protein in the sheep rumen by in vivo and in vitro procedures. British Journal of Nutrition 54, 545-561.
64. Smart C.M. (1994) Gene expression during leaf senescence. New Phytologist 126, 419-448.
65. Sokolenko A., Altschmied L. & Herrmann R. (1997) Sodium dodecyl sulfate-stable proteases in chloroplasts. Plant Physiology 115, 827-832.
66. Thayer S.S. & Huffaker R.C. (1984) Vacuolar localization of endoproteinases EP1 and EP2 in barley mesophyll cells. Plant Physiology 75, 70-73.
67. Thayer S.S., Choe H.T., Rausser S. & Huffaker R.C. (1988) Characterization and subcellular localization of aminopeptidases in senescing barley leaves. Plant Physiology 87, 894-897.
68. Theodorou M.K., Merry R.J. & Thomas H. (1996) Is proteolysis in the rumen of grazing animals mediated by plant enzymes? British Journal of Nutrition 75, 507-510.
69. Thomas H. (1978) Enzymes of nitrogen mobilization in detached leaves of Lolium temulentum during senescence. Planta 142, 161-169.
70. Thomas H. & Donnison I. (2000) Back from the brink: plant senescence and its reversibility. In Programmed Cell Death in Health and Disease (eds J. Bryant, S.G. Hughes & J.M. Garland), pp. 149-162. Bios Scientific Press, Oxford, UK
71. Thomas H. & Stoddart J.L. (1980) Leaf senescence. Annual Review of Plant Physiology 31, 83-111.
72. Thomas H. & Stoddart J.L. (1982) Leaf senescence. In: Encyclopedia of Plant Physiology 14A: Nucleic Acids and Proteins in Plants (eds D. Boulter & B. Parthier), pp. 592-636. Springer Verlag, Berlin, Germany.
73. Vierling E. (1991) The roles of heat-shock proteins in plants. Annual Review of Plant Physiology 42, 579-620.
74. Wallace R.J. & Cotta M.A. (1988) Metabolism of nitrogen containing compounds. In The Rumen Microbial Ecosystem (ed. P. N. Hobson). Elsevier, Amsterdam, The Netherlands.
75. Wetherall J.A., Armstrong D.G., Finlayson H.J. & Rooke J.A. (1995) Reduction of proteolysis during ensilage of perennial ryegrass by protease inhibitors. Journal of the Science of Food and Agriculture 68, 497-505.
76. Wilson J.R. & Mertens D.R. (1995) Cell-wall accessibility and cell structure limitations to microbial digestion of forage. Crop Science 35, 251-259.
77. Wittenbach V.A. (1978) breakdown of ribulose bisphosphate carboxylase and change in proteolytic activity during dark-induced senescence of wheat seedlings. Plant Physiology 62, 604-608.
78. Yoshida T. & Minamikawa T. (1996) Successive amino-terminal proteolysis of the large subunit of ribulose 1,5-bisphosphate carboxylase/oxygenase by vacuolar enzymes from French bean leaves. European Journal of Biochemistry 238, 317-324.
79. Zavaleta-Mancera H.A., Thomas B.J., Thomas H. & Scott I.M. (1999) Regreening of senescent Nicotiana leaves II. Redifferentiation of plastids. Journal of Experimental Botany 50, 1683-1689.
80. Zhu W.-Y., Kingston-Smith A.H., Troncoso D., Merry R.J., Davies D.R., Pichard G., Thomas H. & Theodorou M.K. (1999) Evidence of a role for plant proteases in the degradation of herbage proteins in the rumen of grazing cattle. Journal of Dairy Science 82, 2651-2658.