The impact of light intensity on shade-induced leaf senescence

Plant, Cell and Environment

Volumn 35, Issue 6, 2012, Pages 1084-1098

  Brouwer, Bastiaan ^a   Ziolkowska, Agnieszka ^a   Bagard, Matthieu ^b   Keech, Olivier ^a   Gardeström, Per ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b UNIVERSITÉ PARIS EST CRÉTEIL   (France)

Author keywords

Arabidopsis thaliana; Light compensation point (LCP); Photosynthetic acclimation; Photosynthetic resource partitioning; Phytochrome A (PHYA); R FR ratio

Indexed keywords

ARABIDOPSIS PROTEIN; CHLOROPHYLL; PHYA PROTEIN, ARABIDOPSIS; PHYTOCHROME A;

CHLOROPHYLL; DICOTYLEDON; GENE EXPRESSION; HISTOLOGY; LIGHT INTENSITY; METABOLISM; NICHE PARTITIONING; PHOTOSYNTHESIS; PHYSIOLOGICAL RESPONSE; PHYTOCHEMISTRY; PROTEIN; RESPIRATION; SENESCENCE;

ACCLIMATIZATION; ARABIDOPSIS; ARTICLE; CELL RESPIRATION; GENE EXPRESSION REGULATION; GENETICS; LIGHT; METABOLISM; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT LEAF; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ACCLIMATIZATION; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL RESPIRATION; CHLOROPHYLL; GENE EXPRESSION REGULATION, PLANT; LIGHT; MICROSCOPY, ELECTRON, TRANSMISSION; PHOTOSYNTHESIS; PHYTOCHROME A; PLANT LEAVES;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 84860228569     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2011.02474.x     Document Type: Article

References (82)

1. Anderson J.M., Chow W.S. & Park Y.-I. (1995) The grand design of photosynthesis: acclimation of the photosynthetic apparatus to environmental cues. Photosynthesis Research 46, 129-139.
2. Andersson A., Keskitalo J., Sjödin A., etal. (2004) A transcriptional timetable of autumn senescence. Genome Biology 5, R24.
3. Barreiro R., Guiamét J.J., Beltrano J. & Montaldi E.R. (1992) Regulation of the photosynthetic capacity of primary bean leaves by the red:far-red ratio and photosynthetic photon flux density of incident light. Physiologia Plantarum 85, 97-101.
4. Bhalerao R., Keskitalo J., Sterky F., etal. (2003) Gene expression in autumn leaves. Plant Physiology 131, 430-442.
5. Biswal U.C. & Biswal B. (1984) Photocontrol of leaf senescence. Photochemistry and Photobiology 39, 875-879.
6. Boonman A., Anten N.P.R., Dueck T.A., Jordi W.J.R.M., Werf A.K., Voesenek L.A.C.J. & Pons T.L. (2006) Functional significance of shade-induced leaf senescence in dense canopies: anexperimental test using transgenic tobacco. The American Naturalist 168, 597-607.
7. Boonman A., Prinsen E., Gilmer F., Schurr U., Peeters A.J.M., Voesenek L.A.C.J. & Pons T.L. (2007) Cytokinin import rate as a signal for photosynthetic acclimation to canopy light gradients. Plant Physiology 143, 1841-1852.
8. Borrás L., Maddonni G.A. & Otegui M.E. (2003) Leaf senescence in maize hybrids: plant population, row spacing and kernel set effects. Field Crops Research 82, 13-26.
9. Buchanan-Wollaston V., Earl S., Harrison E., Mathas E., Navabpour S., Page T. & Pink D. (2003) The molecular analysis of leaf senescence - a genomics approach. Plant Biotechnology Journal 1, 3-22.
10. Cherry J.R., Hershey H.P. & Vierstra R.D. (1991) Characterization of tobacco expressing functional oat phytochrome: domains responsible for the rapid degradation of Pfr are conserved between monocots and dicots. Plant Physiology 96, 775-785.
11. Davies T.G.E., Thomas H., Thomas B.J. & Rogers L.J. (1990) Leaf senescence in a non-yellowing mutant of Festuca pratensis: metabolism of cytochrome f. Plant Physiology 93, 588-595.
12. van Doorn W.G. (2005) Plant programmed cell death and the point of no return. Trends in Plant Science 10, 478-483.
13. van Doorn W.G. & Woltering E.J. (2010) What about the role of autophagy in PCD? Trends in Plant Science 15, 361-362.
14. Evans I.M., Rus A.M., Belanger E.M., Kimoto M. & Brusslan J.A. (2010) Dismantling of Arabidopsis thaliana mesophyll cell chloroplasts during natural leaf senescence. Plant Biology 12, 1-12.
15. Evans J. (1993) Photosynthetic acclimation and nitrogen partitioning within a Lucerne canopy. II. Stability through time and comparison with a theoretical optimum. Functional Plant Biology 20, 69-82.
16. Fracheboud Y., Luquez V., Björkén L., Sjödin A., Tuominen H. & Jansson S. (2009) The control of autumn senescence in European Aspen. Plant Physiology 149, 1982-1991.
17. Franklin K.A. (2008) Shade avoidance. New Phytologist 179, 930-944.
18. Franklin K.A. & Quail P.H. (2010) Phytochrome functions in Arabidopsis development. Journal of Experimental Botany 61, 11-24.
19. Gan S. & Amasino R.M. (1997) Making sense of senescence (molecular genetic regulation and manipulation of leaf senescence). Plant Physiology 113, 313-319.
20. van der Graaff E., Schwacke R., Schneider A., Desimone M., Flugge U.-I. & Kunze R. (2006) Transcription analysis of Arabidopsis membrane transporters and hormone pathways during developmental and induced leaf senescence. Plant Physiology 141, 776-792.
21. Grbic V. & Bleecker A.B. (1995) Ethylene regulates the timing of leaf senescence in Arabidopsis. The Plant Journal 8, 595-602.
22. Gutierrez L., Mauriat M., Gunin S., etal. (2008) The lack of a systematic validation of reference genes: a serious pitfall undervalued in reverse transcription-polymerase chain reaction (RT-PCR) analysis in plants. Plant Biotechnology Journal 6, 609-618.
23. Hennig L., Büche C. & Schäfer E. (2000) Degradation of phytochrome A and the high irradiance response in Arabidopsis: a kinetic analysis. Plant, Cell & Environment 23, 727-734.
24. Hensel L.L., Grbic V., Baumgarten D.A. & Bleecker A.B. (1993) Developmental and age-related processes that influence the longevity and senescence of photosynthetic tissues in Arabidopsis. The Plant Cell 5, 553-564.
25. Hidema J., Makino A., Mae T. & Ojima K. (1991) Photosynthetic characteristics of rice leaves aged under different irradiances from full expansion through senescence. Plant Physiology 97, 1287-1293.
26. Hikosaka K. (1996) Effects of leaf age, nitrogen nutrition and photon flux density on the organization of the photosynthetic apparatus in leaves of a vine (Ipomoea tricolor Cav.) grown horizontally to avoid mutual shading of leaves. Planta 198, 144-150.
27. Hikosaka K. (2005) Leaf canopy as a dynamic system: ecophysiology and optimality in leaf turnover. Annals of Botany 95, 521-533.
28. Hörtensteiner S. & Feller U. (2002) Nitrogen metabolism and remobilization during senescence. Journal of Experimental Botany 53, 927-937.
29. Kawakami N. & Watanabe A. (1988) Senescence-specific increase in cytosolic glutamine synthetase and its mRNA in radish cotyledons. Plant Physiology 88, 1430-1434.
30. Keech O., Pesquet E., Ahad A., Askne A., Nordvall D., Vodnala S.M., Tuominen H., Hurry V., Dizengremel P. & Gardeström P. (2007) The different fates of mitochondria and chloroplasts during dark-induced senescence in Arabidopsis leaves. Plant, Cell & Environment 30, 1523-1534.
31. Keech O., Pesquet E., Gutierrez L., Ahad A., Bellini C., Smith S.M. & Gardeström P. (2010) Leaf senescence is accompanied by an early disruption of the microtubule network in Arabidopsis. Plant Physiology 154, 1710-1720.
32. Keskitalo J., Bergquist G., Gardestrom P. & Jansson S. (2005) A cellular timetable of autumn senescence. Plant Physiology 139, 1635-1648.
33. Kozaki A. & Takeba G. (1996) Photorespiration protects C3 plants from photooxidation. Nature 384, 557-560.
34. Lam E. (2004) Controlled cell death, plant survival and development. Nature Reviews. Molecular Cell Biology 5, 305-315.
35. Leopold A.C. (1961) Senescence in plant development: the death of plants or plant parts may be of positive ecological or physiological value. Science 134, 1727-1732.
36. Lim P.O., Kim H.J. & Nam H.G. (2007) Leaf senescence. Annual Review of Plant Biology 58, 115-136.
37. Mae T., Thomas H., Gay A.P., Makino A. & Hidema J. (1993) Leaf development in Lolium temulentum: photosynthesis and photosynthetic proteins in leaves senescing under different irradiances. Plant and Cell Physiology 34, 391-399.
38. Martínez D.E., Costa M.L. & Guiamet J.J. (2008a) Senescence-associated degradation of chloroplast proteins inside and outside the organelle. Plant Biology 10, 15-22.
39. Martínez D.E., Costa M.L., Gomez F.M., Otegui M.S. & Guiamet J.J. (2008b) 'Senescence-associated vacuoles' are involved in the degradation of chloroplast proteins in tobacco leaves. The Plant Journal 56, 196-206.
40. Masclaux C., Valadier M.-H., Brugière N., Morot-Gaudry J.-F. & Hirel B. (2000) Characterization of the sink/source transition in tobacco (Nicotiana tabacum L.) shoots in relation to nitrogen management and leaf senescence. Planta 211, 510-518.
41. Masclaux-Daubresse C., Reisdorf-Cren M. & Orsel M. (2008) Leaf nitrogen remobilisation for plant development and grain filling. Plant Biology 10, 23-36.
42. Melis A. & Harvey G.W. (1981) Regulation of photosystem stoichiometry, chlorophyll a and chlorophyll b content and relation to chloroplast ultrastructure. Biochimica et Biophysica Acta (BBA) - Bioenergetics 637, 138-145.
43. Miller J.D., Arteca R.N. & Pell E.J. (1999) Senescence-associated gene expression during ozone-induced leaf senescence in Arabidopsis. Plant Physiology 120, 1015-1024.
44. Mothes K. (1960) Über das Altern der Blätter und die Möglichkeit ihrer Wiederverjüngung. Die Naturwissenschaften 47, 337-351.
45. Niinemets Ü. (2007) Photosynthesis and resource distribution through plant canopies. Plant, Cell & Environment 30, 1052-1071.
46. Nooden L.D., Hillsberg J.W. & Schneider M.J. (1996) Induction of leaf senescence in Arabidopsis thaliana by long days through a light-dosage effect. Physiologia Plantarum 96, 491-495.
47. Okada K. & Katoh S. (1998) Two long-term effects of light that control the stability of proteins related to photosynthesis during senescence of rice leaves. Plant Cell Physiology 39, 394-404.
48. Ono K., Terashima I. & Watanabe A. (1996) Interaction between nitrogen deficit of a plant and nitrogen content in the old leaves. Plant and Cell Physiology 37, 1083-1089.
49. Otegui M.S., Noh Y.-S., Martínez D.E., Vila Petroff M.G., Staehelin L.A., Amasino R.M. & Guiamet J.J. (2005) Senescence-associated vacuoles with intense proteolytic activity develop in leaves of Arabidopsis and soybean. The Plant Journal 41, 831-844.
50. Pearcy R.W. & Seemann J.R. (1990) Photosynthetic induction state of leaves in a soybean canopy in relation to light regulation of ribulose-1-5-bisphosphate carboxylase and stomatal conductance. Plant Physiology 94, 628-633.
51. Pons T.L. & Bergkotte M. (1996) Nitrogen allocation in response to partial shading of a plant: possible mechanisms. Physiologia Plantarum 98, 571-577.
52. Pons T.L. & de Jong-van Berkel Y.E.M. (2004) Species-specific variation in the importance of the spectral quality gradient in canopies as a signal for photosynthetic resource partitioning. Annals of Botany 94, 725-732.
53. Porra R.J., Thompson W.A. & Kriedemann P.E. (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochimica et Biophysica Acta (BBA) - Bioenergetics 975, 384-394.
54. Pruzinska A., Tanner G., Aubry S., etal. (2005) Chlorophyll breakdown in senescent Arabidopsis leaves. Characterization of chlorophyll catabolites and of chlorophyll catabolic enzymes involved in the degreening reaction. Plant Physiology 139, 52-63.
55. Rausenberger J., Tscheuschler A., Nordmeier W., Wüst F., Timmer J., Schäfer E., Fleck C. & Hiltbrunner A. (2011) Photoconversion and nuclear trafficking cycles determine phytochrome A's response profile to far-red light. Cell 146, 813-825.
56. Reynolds E.S. (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. The Journal of Cell Biology 17, 208-212.
57. Rivero R.M., Kojima M., Gepstein A., Sakakibara H., Mittler R., Gepstein S. & Blumwald E. (2007) Delayed leaf senescence induces extreme drought tolerance in a flowering plant. Proceedings of the National Academy of Sciences 104, 19631-19636.
58. Rousseaux M.C., Hall A.J. & Sanchez R.A. (1996) Far-red enrichment and photosynthetically active radiation level influence leaf senescence in field-grown sunflower. Physiologia Plantarum 96, 217-224.
59. Rousseaux M.C., Ballare C.L., Jordan E.T. & Vierstra R.D. (1997) Directed overexpression of PHYA locally suppresses stem elongation and leaf senescence responses to far-red radiation. Plant, Cell and Environment 20, 1551-1558.
60. Rousseaux M.C., Hall A.J. & Sánchez R.A. (2000) Basal leaf senescence in a sunflower (Helianthus annuus) canopy: responses to increased R/FR ratio. Physiologia Plantarum 110, 477-482.
61. Schelbert S., Aubry S., Burla B., Agne B., Kessler F., Krupinska K. & Hortensteiner S. (2009) Pheophytin pheophorbide hydrolase (pheophytinase) is involved in chlorophyll breakdown during leaf senescence in Arabidopsis. The Plant Cell 21, 767-785.
62. Schmid M., Davison T.S., Henz S.R., Pape U.J., Demar M., Vingron M., Scholkopf B., Weigel D. & Lohmann J.U. (2005) A gene expression map of Arabidopsis thaliana development. Nature Genetics 37, 501-506.
63. Simeonova E., Garstka M., Kozioł-Lipińska J. & Mostowska A. (2004) Monitoring the mitochondrial transmembrane potential with the JC-1 fluorochrome in programmed cell death during mesophyll leaf senescence. Protoplasma 223, 143-153.
64. Smart C.M. (1994) Gene expression during leaf senescence. New Phytologist 126, 419-448.
65. Smith H., Xu Y. & Quail P.H. (1997) Antagonistic but complementary actions of phytochromes A and B allow optimum seedling de-etiolation. Plant Physiology 114, 637-641.
66. Sugiura M. (1963) Effect of red and far-red light on protein and phosphate metabolism in tobacco leaf discs. Botanical Magazine Tokyo 76, 174-180.
67. Terashima I., Araya T., Miyazawa S.-I., Sone K. & Yano S. (2005) Construction and maintenance of the optimal photosynthetic systems of the leaf, herbaceous plant and tree: an eco-developmental treatise. Annals of Botany 95, 507-519.
68. Tevini M. & Steinmüller D. (1985) Composition and function of plastoglobuli. Planta 163, 91-96.
69. Tucker D.J. (1981) Phytochrome regulation of leaf senescence in cucumber and tomato. Plant Science Letters 23, 103-108.
70. Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A. & Speleman F. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3, R34.
71. Veierskov B. (1987) Irradiance-dependent senescence of isolated leaves. Physiologia Plantarum 71, 316-320.
72. Wada S., Ishida H., Izumi M., Yoshimoto K., Ohsumi Y., Mae T. & Makino A. (2009) Autophagy plays a role in chloroplast degradation during senescence in individually darkened leaves. Plant Physiology 149, 885-893.
73. Wagner R., Dietzel L., Bräutigam K., Fischer W. & Pfannschmidt T. (2008) The long-term response to fluctuating light quality is an important and distinct light acclimation mechanism that supports survival of Arabidopsis thaliana under low light conditions. Planta 228, 573-587.
74. Wagstaff C., Yang T.J.W., Stead A.D., Buchanan-Wollaston V. & Roberts J.A. (2009) A molecular and structural characterization of senescing Arabidopsis siliques and comparison of transcriptional profiles with senescing petals and leaves. The Plant Journal 57, 690-705.
75. Walters R.G. (2005) Towards an understanding of photosynthetic acclimation. Journal of Experimental Botany 56, 435-447.
76. Weaver L.M. & Amasino R.M. (2001) Senescence is induced in individually darkened Arabidopsis leaves, but inhibited in whole darkened plants. Plant Physiology 127, 876-886.
77. Weaver L.M., Gan S., Quirino B. & Amasino R.M. (1998) A comparison of the expression patterns of several senescence-associated genes in response to stress and hormone treatment. Plant Molecular Biology 37, 455-469.
78. Winter D., Vinegar B., Nahal H., Ammar R., Wilson G.V. & Provart N.J. (2007) An 'Electronic Fluorescent Pictograph' browser for exploring and analyzing large-scale biological data sets. PLoS One 2, e718.
79. Yanovski M.J., Casal J.J. & Whitelam G.C. (1995) Phytochrome A, phytochrome B and HY4 are involved in hypocotyl growth responses to natural radiation in Arabidopsis: weak de-etiolation of the phyA mutant under dense canopies. Plant, Cell & Environment 18, 788-794.
80. Yoshida Y. (1962) Nuclear control of chloroplast activity in Elodea leaf cells. Protoplasma 54, 476-492.
81. 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.
82. Zottini M., Barizza E., Bastianelli F., Carimi F. & Lo Schiavo F. (2006) Growth and senescence of Medicago truncatula cultured cells are associated with characteristic mitochondrial morphology. New Phytologist 172, 239-247.