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Chlorophylls, ligands and assembly of light-harvesting complexes in chloroplasts.

Hoober JK, Eggink LL, Chen M - Photosyn. Res. (2007)

Bottom Line: Important modifications are introduction of oxygen atoms at specific locations and reduction or desaturation of sidechains.The coordination bonds are enhanced by H-bonds between the protein and the 7-formyl group.These additional strong interactions with Chl b are necessary to achieve assembly of stable LHCs.

View Article: PubMed Central - PubMed

Affiliation: School of Life Sciences, Arizona State University, Tempe, AZ 85287-4501, USA. khoober@asu.edu

ABSTRACT
Chlorophyll (Chl) b serves an essential function in accumulation of light-harvesting complexes (LHCs) in plants. In this article, this role of Chl b is explored by considering the properties of Chls and the ligands with which they interact in the complexes. The overall properties of the Chls, not only their spectral features, are altered as consequences of chemical modifications on the periphery of the molecules. Important modifications are introduction of oxygen atoms at specific locations and reduction or desaturation of sidechains. These modifications influence formation of coordination bonds by which the central Mg atom, the Lewis acid, of Chl molecules interacts with amino acid sidechains, as the Lewis base, in proteins. Chl a is a versatile Lewis acid and interacts principally with imidazole groups but also with sidechain amides and water. The 7-formyl group on Chl b withdraws electron density toward the periphery of the molecule and consequently the positive Mg is less shielded by the molecular electron cloud than in Chl a. Chl b thus tends to form electrostatic bonds with Lewis bases with a fixed dipole, such as water and, in particular, peptide backbone carbonyl groups. The coordination bonds are enhanced by H-bonds between the protein and the 7-formyl group. These additional strong interactions with Chl b are necessary to achieve assembly of stable LHCs.

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Related in: MedlinePlus

Model of LHCII assembly in the chloroplast envelope and the proposed role of Chl b. Several proposed intermediates are shown in the sequence, left to right. After synthesis in the cytosol, a LHCP precursor is imported sufficiently into the chloroplast stroma for removal of the transit sequence from the N-terminus and for the first membrane-spanning region to engage the inner membrane. Chl a (dark green rectangles) binds to ligands in the motif provided by the ion-pair of the sidechains of glutamate and arginine and the imidazole group of histidine (dotted line, a). However, binding to these sites is not sufficient to retain the protein in the envelope. Without Chl b the protein slips back into the cytosol for transfer to vacuoles and subsequent degradation. Chl b (light green rectangles) forms a strong coordination bond with the peptide bond carbonyl of Tyr24, near the N-terminus, and provides an additional hold on the protein (solid line, a + b). Along with the Chl a molecules that bind to the motifs in membrane-spanning helix 1, Chl b binds to Try24 and the peptide carbonyl of Val119 at the lumenal end of helix-2. These Chls retain the protein in the membrane sufficiently long for the remainder of the protein, including the conserved motif in membrane-spanning helix-3, to enter the membrane, bind additional Chl and xanthophylls molecules, and complete assembly (LHC). Other proteins in the membrane and stroma apparently assist assembly of the complete complex (see text)
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Fig4: Model of LHCII assembly in the chloroplast envelope and the proposed role of Chl b. Several proposed intermediates are shown in the sequence, left to right. After synthesis in the cytosol, a LHCP precursor is imported sufficiently into the chloroplast stroma for removal of the transit sequence from the N-terminus and for the first membrane-spanning region to engage the inner membrane. Chl a (dark green rectangles) binds to ligands in the motif provided by the ion-pair of the sidechains of glutamate and arginine and the imidazole group of histidine (dotted line, a). However, binding to these sites is not sufficient to retain the protein in the envelope. Without Chl b the protein slips back into the cytosol for transfer to vacuoles and subsequent degradation. Chl b (light green rectangles) forms a strong coordination bond with the peptide bond carbonyl of Tyr24, near the N-terminus, and provides an additional hold on the protein (solid line, a + b). Along with the Chl a molecules that bind to the motifs in membrane-spanning helix 1, Chl b binds to Try24 and the peptide carbonyl of Val119 at the lumenal end of helix-2. These Chls retain the protein in the membrane sufficiently long for the remainder of the protein, including the conserved motif in membrane-spanning helix-3, to enter the membrane, bind additional Chl and xanthophylls molecules, and complete assembly (LHC). Other proteins in the membrane and stroma apparently assist assembly of the complete complex (see text)

Mentions: A possible ligand for the Chl b molecule that is necessary for retention of the protein in the plastid was suggested by the crystal structure of LHCII. Several backbone carbonyls near the N-terminus are precluded from H-bonding and formation of an α-helix because of the richness of proline residues in this region of the LHCP. The carbonyl of tyrosine (Tyr24 in spinach Lhcb1) resides three positions distant in the amino acid sequence from a proline residue and is thus free to form a coordination bond with Chl b (Liu et al. 2004; Standfuss et al. 2005). The unusual abundance of proline in the N-terminal domain also extends to an iron-deficiency-induced (Tidi) protein, a homolog of the light-harvesting Chl a/b proteins, in Dunaliella, which increases the probability of interaction with Chl b during this stress condition that leads to chlorosis (Varsano et al. 2006). The strong electrostatic bond formed by further polarization of the carbonyl dipole through interaction with Chl b may be essential to anchor a LHCP in the envelope membrane sufficiently long for the remainder of the protein to be transported from the cytosol to complete assembly (Fig. 4).Fig. 4


Chlorophylls, ligands and assembly of light-harvesting complexes in chloroplasts.

Hoober JK, Eggink LL, Chen M - Photosyn. Res. (2007)

Model of LHCII assembly in the chloroplast envelope and the proposed role of Chl b. Several proposed intermediates are shown in the sequence, left to right. After synthesis in the cytosol, a LHCP precursor is imported sufficiently into the chloroplast stroma for removal of the transit sequence from the N-terminus and for the first membrane-spanning region to engage the inner membrane. Chl a (dark green rectangles) binds to ligands in the motif provided by the ion-pair of the sidechains of glutamate and arginine and the imidazole group of histidine (dotted line, a). However, binding to these sites is not sufficient to retain the protein in the envelope. Without Chl b the protein slips back into the cytosol for transfer to vacuoles and subsequent degradation. Chl b (light green rectangles) forms a strong coordination bond with the peptide bond carbonyl of Tyr24, near the N-terminus, and provides an additional hold on the protein (solid line, a + b). Along with the Chl a molecules that bind to the motifs in membrane-spanning helix 1, Chl b binds to Try24 and the peptide carbonyl of Val119 at the lumenal end of helix-2. These Chls retain the protein in the membrane sufficiently long for the remainder of the protein, including the conserved motif in membrane-spanning helix-3, to enter the membrane, bind additional Chl and xanthophylls molecules, and complete assembly (LHC). Other proteins in the membrane and stroma apparently assist assembly of the complete complex (see text)
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2117338&req=5

Fig4: Model of LHCII assembly in the chloroplast envelope and the proposed role of Chl b. Several proposed intermediates are shown in the sequence, left to right. After synthesis in the cytosol, a LHCP precursor is imported sufficiently into the chloroplast stroma for removal of the transit sequence from the N-terminus and for the first membrane-spanning region to engage the inner membrane. Chl a (dark green rectangles) binds to ligands in the motif provided by the ion-pair of the sidechains of glutamate and arginine and the imidazole group of histidine (dotted line, a). However, binding to these sites is not sufficient to retain the protein in the envelope. Without Chl b the protein slips back into the cytosol for transfer to vacuoles and subsequent degradation. Chl b (light green rectangles) forms a strong coordination bond with the peptide bond carbonyl of Tyr24, near the N-terminus, and provides an additional hold on the protein (solid line, a + b). Along with the Chl a molecules that bind to the motifs in membrane-spanning helix 1, Chl b binds to Try24 and the peptide carbonyl of Val119 at the lumenal end of helix-2. These Chls retain the protein in the membrane sufficiently long for the remainder of the protein, including the conserved motif in membrane-spanning helix-3, to enter the membrane, bind additional Chl and xanthophylls molecules, and complete assembly (LHC). Other proteins in the membrane and stroma apparently assist assembly of the complete complex (see text)
Mentions: A possible ligand for the Chl b molecule that is necessary for retention of the protein in the plastid was suggested by the crystal structure of LHCII. Several backbone carbonyls near the N-terminus are precluded from H-bonding and formation of an α-helix because of the richness of proline residues in this region of the LHCP. The carbonyl of tyrosine (Tyr24 in spinach Lhcb1) resides three positions distant in the amino acid sequence from a proline residue and is thus free to form a coordination bond with Chl b (Liu et al. 2004; Standfuss et al. 2005). The unusual abundance of proline in the N-terminal domain also extends to an iron-deficiency-induced (Tidi) protein, a homolog of the light-harvesting Chl a/b proteins, in Dunaliella, which increases the probability of interaction with Chl b during this stress condition that leads to chlorosis (Varsano et al. 2006). The strong electrostatic bond formed by further polarization of the carbonyl dipole through interaction with Chl b may be essential to anchor a LHCP in the envelope membrane sufficiently long for the remainder of the protein to be transported from the cytosol to complete assembly (Fig. 4).Fig. 4

Bottom Line: Important modifications are introduction of oxygen atoms at specific locations and reduction or desaturation of sidechains.The coordination bonds are enhanced by H-bonds between the protein and the 7-formyl group.These additional strong interactions with Chl b are necessary to achieve assembly of stable LHCs.

View Article: PubMed Central - PubMed

Affiliation: School of Life Sciences, Arizona State University, Tempe, AZ 85287-4501, USA. khoober@asu.edu

ABSTRACT
Chlorophyll (Chl) b serves an essential function in accumulation of light-harvesting complexes (LHCs) in plants. In this article, this role of Chl b is explored by considering the properties of Chls and the ligands with which they interact in the complexes. The overall properties of the Chls, not only their spectral features, are altered as consequences of chemical modifications on the periphery of the molecules. Important modifications are introduction of oxygen atoms at specific locations and reduction or desaturation of sidechains. These modifications influence formation of coordination bonds by which the central Mg atom, the Lewis acid, of Chl molecules interacts with amino acid sidechains, as the Lewis base, in proteins. Chl a is a versatile Lewis acid and interacts principally with imidazole groups but also with sidechain amides and water. The 7-formyl group on Chl b withdraws electron density toward the periphery of the molecule and consequently the positive Mg is less shielded by the molecular electron cloud than in Chl a. Chl b thus tends to form electrostatic bonds with Lewis bases with a fixed dipole, such as water and, in particular, peptide backbone carbonyl groups. The coordination bonds are enhanced by H-bonds between the protein and the 7-formyl group. These additional strong interactions with Chl b are necessary to achieve assembly of stable LHCs.

Show MeSH
Related in: MedlinePlus