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A cellular timetable of autumn senescence
Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).ORCID iD: 0000-0001-5900-7395
Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).ORCID iD: 0000-0002-7906-6891
2005 (English)In: Plant Physiology, ISSN 0032-0889, E-ISSN 1532-2548, Vol. 139, no 4, 1635-1648 p.Article in journal (Refereed) Published
Abstract [en]

We have studied autumn leaf senescence in a free-growing aspen (Populus tremula) by following changes in pigment, metabolite and nutrient content, photosynthesis, and cell and organelle integrity. The senescence process started on September 11, 2003, apparently initiated solely by the photoperiod, and progressed steadily without any obvious influence of other environmental signals. For example, after this date, senescing leaves accumulated anthocyanins in response to conditions inducing photooxidative stress, but at the beginning of September the leaves did not. Degradation of leaf constituents took place over an 18-d period, and, although the cells in each leaf did not all senesce in parallel, senescence in the tree as a whole was synchronous. Lutein and {beta}-carotene were degraded in parallel with chlorophyll, whereas neoxanthin and the xanthophyll cycle pigments were retained longer. Chloroplasts in each cell were rapidly converted to gerontoplasts and many, although not all, cells died. From September 19, when chlorophyll levels had dropped by 50%, mitochondrial respiration provided the energy for nutrient remobilization. Remobilization seemed to stop on September 29, probably due to the cessation of phloem transport, but, up to abscission of the last leaves (over 1 week later), some cells were metabolically active and had chlorophyll-containing gerontoplasts. About 80% of the nitrogen and phosphorus was remobilized, and on September 29 a sudden change occurred in the {delta}15N of the cellular content, indicating that volatile compounds may have been released.

Place, publisher, year, edition, pages
2005. Vol. 139, no 4, 1635-1648 p.
Keyword [en]
Anthocyanins/metabolism, Carotenoids/metabolism, Chlorophyll/metabolism, Chloroplasts/metabolism, Microscopy; Electron, Mitochondria/metabolism, Nitrogen/metabolism, Phosphorus/metabolism, Photobiology, Photoperiod, Photosynthesis, Pigments; Biological/metabolism, Plant Leaves/cytology/*growth & development/metabolism, Populus/cytology/*growth & development/metabolism, Seasons
Identifiers
URN: urn:nbn:se:umu:diva-5066DOI: doi:10.1104/pp.105.066845OAI: oai:DiVA.org:umu-5066DiVA: diva2:144427
Available from: 2006-04-12 Created: 2006-04-12 Last updated: 2017-12-14Bibliographically approved
In thesis
1. Constructing a timetable of autumn senescence in aspen
Open this publication in new window or tab >>Constructing a timetable of autumn senescence in aspen
2006 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

During the development and lifecycle of multicellular organisms, cells have to die, and this occurs by a process called programmed cell death or PCD, which can be separated from necrosis or accidental cell death (Pennell and Lamb, 1997). Senescence is the terminal phase in the development of an organism, organ, tissue or cell, where nutrients are remobilized from the senescing parts of the plant into other parts, and the cells of the senescing organ or tissue undergo PCD if the process is not reversed in time. Leaf senescence involves cessation of photosynthesis, loss of pigments and proteins, nutrient remobilization, and degradation of the plant cells (Smart, 1994). Initiation of leaf senescence is triggered by a wide range of endogenous and environmental factors, that through unknown pathways controls the process, and regulates the expression of senescence-associated genes (SAGs) (Buchanan-Wollaston, 1997). Autumn leaf senescence in deciduous trees is regulated by photoperiod and temperature, and is an attractive experimental system for studies on senescence in perennial plants.

We have studied the process of autumn senescence in a free-growing aspen (Populus tremula) by following changes in pigment, metabolite and nutrient content, photosynthesis, and cell and organelle integrity. All data were combined in a cellular timetable of autumn senescence in aspen. The senescence process started on September 11 with degradation of pigments and other leaf constituents, and once initiated, progressed steadily without being affected by the environment. Chloroplasts were rapidly degraded, and mitochondria took over energy production after chlorophyll levels had dropped by 50%. At the end of remobilization, around 29th of September, some cells were still metabolically active and had chlorophyll-containing plastids. Over 80% of nitrogen and phosphorus was remobilized, and a sudden change in the 15N of the cellular content on September 29, indicated that volatile compounds may have been released.

We have also studied gene expression in autumn leaves by analysing EST sequences from two different cDNA libraries, one from autumn leaves of a field-grown aspen and the other from young, but fully expanded leaves of a green-house grown aspen. In the autumn leaf library, ESTs encoding metallothioneins, proteases, stress-related proteins and proteins involved in respiration and breakdown of macromolecules were abundant, while genes coding for photosynthetic proteins were massively downregulated. We have also identified homologues to many known senescence-associated genes in annual plants.

By using Populus cDNA microarrays, we could follow changes in gene expression during the autumn over four years in the same free-growing aspen tree. We also followed changes in chlorophyll content to monitor the progression of leaf senescence. We observed a major shift in gene expression, occuring at different times the four years, that reflected a metabolic shift from photosynthetic competence to energy generation by mitochondrial respiration. Even though autumn senescence was initiated almost at the same date each year, the transcriptional timetables were different from year to year, especially for 2004, which indicates that there is no strict correlation between the transcriptional and the cellular timetables of leaf senescence.

Place, publisher, year, edition, pages
Umeå: Fysiologisk botanik, 2006. 30 p.
Keyword
Populus tremula, autumn senescence, senescence-associated genes, cellular timetable, transcriptional timetable, cDNA microarrays, EST sequencing
National Category
Botany
Identifiers
urn:nbn:se:umu:diva-752 (URN)91-7264-075-8 (ISBN)
Public defence
2006-05-05, KB3B1, KBC-huset, universitetsområdet, Umeå, 10:00
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Supervisors
Available from: 2006-04-12 Created: 2006-04-12Bibliographically approved

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Keskitalo, JohannaGardeström, PerJansson, Stefan
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