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Is each light-harvesting complex protein important for plant fitness?
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, Department of Plant Physiology.ORCID iD: 0000-0002-7906-6891
2004 (English)In: Plant Physiology, ISSN 0032-0889, E-ISSN 1532-2548, Vol. 134, no 1, 502-509 p.Article in journal (Refereed) Published
Abstract [en]

Many of the photosynthetic genes are conserved among all higher plants, indicating that there is strong selective pressure to maintain the genes of each protein. However, mutants of these genes often lack visible growth phenotypes, suggesting that they are important only under certain conditions or have overlapping functions. To assess the importance of specific genes encoding the light-harvesting complex (LHC) proteins for the survival of the plant in the natural environment, we have combined two different scientific traditions by using an ecological fitness assay on a set of genetically modified Arabidopsis plants with differing LHC protein contents. The fitness of all of the LHC-deficient plants was reduced in some of the growth environments, supporting the hypothesis that each of the genes has been conserved because they provide ecological flexibility, which is of great adaptive value given the highly variable conditions encountered in nature.

Place, publisher, year, edition, pages
Rockville, Md.: American Society of Plant Physiologists , 2004. Vol. 134, no 1, 502-509 p.
Keyword [en]
Arabidopsis/genetics/growth & development/*physiology, Genes; Plant, Light-Harvesting Protein Complexes/genetics/*physiology, Models; Biological, Mutation, Plant Proteins/genetics/*physiology
URN: urn:nbn:se:umu:diva-11796DOI: 10.1104/pp.103.033324PubMedID: 14730076OAI: diva2:151467
Available from: 2007-08-09 Created: 2007-08-09 Last updated: 2015-04-29Bibliographically approved
In thesis
1. The light-harvesting antenna of higher plant photosystem I
Open this publication in new window or tab >>The light-harvesting antenna of higher plant photosystem I
2004 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

During photosynthesis, two multi-protein complexes, photosystems (PS) I and II work in tandem to convert the light-energy absorbed by the light-harvesting antennae into chemical energy, which is subsequently used to assimilate atmospheric carbon dioxide into organic carbon compounds. This is the main nutritional basis for life on Earth.

The photosynthetic antenna of higher plants comprises at least ten different pigment-binding proteins (LHC), which play important roles in photosynthesis. Chlorophyll and carotenoid molecules associated with the LHC proteins are organised into an array, which can be modulated, thereby optimising light-harvesting processes and protection against oxidative damage under conditions of excessive light absorption. All ten LHC proteins have been conserved through eons of evolution, suggesting that there are strong evolutionary pressures to retain all ten proteins, and hence that each protein has a unique function.

The light-harvesting antenna of higher plant PSI consists of at least four proteins, Lhca1-4, collectively called LHCI. By constructing transgenic Arabidopsis thaliana plants in which each Lhca gene has been individually repressed or knocked-out, a collection of plants with different Lhca protein contents was obtained. The objective was to use these plants to study the structure, function and regulation of the Lhca proteins in vivo. The major findings of this work are as follows.

Removing single Lhca proteins influenced the stability of the other Lhca proteins, showing that there is a high degree of inter-dependency between the polypeptides in LHCI, and hence that a full set of Lhca proteins is important for maintaining the structural integrity of LHCI. This has provided insight into the organisation of LHCI by revealing clues about the relative positions of each Lhca protein in the antenna complex. The physiological consequences of removing individual Lhca proteins were dependent on the degree of antenna depletion. Plants with relatively small antenna changes could compensate, to some extent, for the loss of LHCI, while larger depletions had profound effects on whole plant resulting in growth reductions.

The fitness of each Lhca plant was assessed by measuring their seed production in the harsh conditions in the field. We found that all Lhca-deficient plants produced fewer seeds under some conditions, with seed-production compared to wild type varying between 10-80% depending on the extent of LHCI reduction. Therefore, we conclude that each Lhca protein is important for plant fitness, and hence for the survival of the species.

PSI is characterised by a pool of pigments absorbing light in the red end of the solar visible spectrum, thought to be especially important for plants in dense vegetation systems where the incident light is enriched in wavelengths higher than 690 nm. A majority of these pigments are situated on LHCI and, based on in-vitro studies, were thought to be mainly associated with Lhca4. Using our plants, we have established that red pigments are indeed present on all Lhca proteins and that these pigments become even more red upon association with PSI.

Place, publisher, year, edition, pages
Umeå: Umeå universitet, 2004. 67 p.
Plant physiology, antisense, Arabidopsis thaliana, chlorophyll, fitness, LHC, photosynthesis, Växtfysiologi
National Category
urn:nbn:se:umu:diva-209 (URN)91-7305-625-1 (ISBN)
Public defence
2004-04-02, Umeå, 10:00
Available from: 2004-03-12 Created: 2004-03-12 Last updated: 2011-03-10Bibliographically approved
2. The significance of feedback de-excitation
Open this publication in new window or tab >>The significance of feedback de-excitation
2005 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

During photosynthesis sunlight is absorbed by photosynthetic pigments and converted into organic compounds, such as carbohydrates. Photosynthesis needs to be highly regulated, since both too much and too little light are harmful to plant. If too little light is absorbed, a plant cannot store enough energy, which will have effects on growth and fitness of the plant. With too much light absorbed, a dangerous side reaction of photosynthesis, the production of reactive oxygen species can happen. These reactive oxygen species can damage the proteins in the chloroplast and the lipids of the chloroplast.

To avoid the production of reactive oxygen species, plants have evolved many mechanisms, which act on different time-scales and different levels of organization. As a first measure, when the absorbed light is exceeding the capacity for its utilization, is to switch the light-harvesting antenna from efficient light harvesting to energy dissipation. This process is called feedback de-excitation (FDE). The protein PsbS is essential for this process as well as a functioning xanthophylls cycle with the enzyme violaxanthin de-epoxidase (VDE).

I have investigated the effects of plants with changes in their ability to dissipate excess excitation energy in the model plants species Arabidopsis thaliana. Three genotypes with either increased or decreased capacity for FDE were used during my experiments. The first genotype over-expresses the PsbS gene, having approximately two-fold increased amounts of PsbS and FDE. The second is a PsbS deletion mutant with no PsbS protein and no FDE. The third genotype cannot perform the conversion of violaxanthin to zeaxanthin, because the enzyme VDE is missing. This mutant has some FDE left.

Arabidopsis thaliana is an annual plant, which flowers only once in its lifetime. Therefore, when counting the seeds produced an estimation of fitness can be made from the amount of seeds produced. This was done during my experiments and shown that FDE is a trait and that plants with increased FDE have a higher fitness and vice versa.

This was also the case for a collection of plants lacking a single protein from the light harvesting antenna. All of these genotypes had a fitness reduction, proving that their function is not redundant.

In an attempt to explain why the fitness is reduced in plants with altered FDE, photosynthetic measurements, as well as a determination of the transcriptome and the metabolome was performed. Plants lacking FDE had higher levels of photoinhibition, leading both to lower rates of photosynthesis and to higher repair cost. This could in part explain the reduction in fitness. These plants also had major changes in their transcriptome and their metabolome. Primary metabolism was most effected, for example carbohydrate and amino acid metabolism. But there were also changes in secondary metabolism such as an up regulation of the biosynthesis of anthocyanins.

Place, publisher, year, edition, pages
Umeå: Fysiologisk botanik, 2005. 59 p.
Arabidopsis thaliana, photosynthesis, feedback de-excitation, fitness, metabolomics, transcriptomics
National Category
urn:nbn:se:umu:diva-581 (URN)91-7305-931-5 (ISBN)
Public defence
2005-09-23, 00:00
Available from: 2005-09-05 Created: 2005-09-05 Last updated: 2011-03-10Bibliographically approved

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