Altered levels of LIL3 isoforms in Arabidopsis lead to disturbed pigment–protein assembly and chlorophyll synthesis, chlorotic phenotype and impaired photosynthetic performance

Light‐harvesting complex (LHC)‐like (LIL) proteins contain two transmembrane helices of which the first bears a chlorophyll (Chl)‐binding motif. They are widespread in photosynthetic organisms, but almost nothing is known about their expression and physiological functions. We show that two LIL3 para...

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Bibliographic Details
Published in:Plant, cell and environment cell and environment, 2015-10, Vol.38 (10), p.2115-2127
Main Authors: Lohscheider, Jens N., Rojas‐Stütz, Marc C., Rothbart, Maxi, Andersson, Ulrica, Funck, Dietmar, Mendgen, Kurt, Grimm, Bernhard, Adamska, Iwona
Format: Article
Language:English
Subjects:
Arabidopsis
Arabidopsis - genetics
Arabidopsis - radiation effects
Arabidopsis Proteins - genetics
Arabidopsis Proteins - metabolism
Arabidopsis thaliana
Chlorophyll - metabolism
Chlorophyll synthesis
Chloroplast Proteins - genetics
Chloroplast Proteins - metabolism
geranylgeranyl reductase
high light
light‐harvesting complex
Oxidoreductases - genetics
Oxidoreductases - metabolism
Phenotype
Photosynthesis - physiology
photosynthetic pigment–protein assembly
Photosystem II Protein Complex - genetics
Photosystem II Protein Complex - metabolism
Plant Leaves - metabolism
Plants, Genetically Modified
Protein Isoforms
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Summary:Light‐harvesting complex (LHC)‐like (LIL) proteins contain two transmembrane helices of which the first bears a chlorophyll (Chl)‐binding motif. They are widespread in photosynthetic organisms, but almost nothing is known about their expression and physiological functions. We show that two LIL3 paralogues (LIL3:1 and LIL3:2) in Arabidopsis thaliana are expressed in photosynthetically active tissues and their expression is differentially influenced by light stress. Localization studies demonstrate that both isoforms are associated with subcomplexes of LHC antenna of photosystem II. Transgenic plants with reduced amounts of LIL3:1 exhibited a slightly impaired growth and have reduced Chl and carotenoid contents as compared to wild‐type plants. Ectopic overexpression of either paralogue led to a developmentally regulated switch to co‐suppression of both LIL3 isoforms, resulting in a circular chlorosis of the leaf rosettes. Chlorotic sectors show severely diminished levels of LIL3 isoforms and other proteins, and thylakoid morphology was changed. Additionally, the levels of enzymes involved in Chl biosynthesis are altered in lil3 mutant plants. Our data support a role of LIL3 paralogues in the regulation of Chl biosynthesis under light stress and under standard growth conditions as well as in a coordinated ligation of newly synthesized and/or rescued Chl molecules to their target apoproteins. The assembly of pigment‐protein complexes of the thylakoid membrane during de‐novo‐synthesis or repair requires a tight coordination of pigment synthesis and delivery with translation. Members of the LHC‐like protein family may play crucial roles in these processes. We demonstrate differential expression patterns of the two paralogous LHC‐like 3 proteins (LIL3:1 and LIL3:2) under standard growth conditions and in high light treatments as well as slightly different suborganellar localisation in the thylakoid membrane. Our data show functional redundancy of the two proteins under standard growth conditions, but indicate differential functions when the plant is exposed to high light stress. In transgenic plants with altered expression of the LIL3 isoforms, thylakoid architecture, Chl synthesis and the regulation of proteins involved in tetrapyrrole synthesis are disturbed. Thus, LIL3 proteins may play an important role in retrograde signalling, orchestrating nuclear and chloroplast gene expression and translation.
ISSN:0140-7791
1365-3040
DOI:10.1111/pce.12540