Altered xanthophyll compositions adversely affect chlorophyll accumulation and nonphotochemical quenching in Arabidopsis mutants.

Collectively, the xanthophyll class of carotenoids perform a variety of critical roles in light harvesting antenna assembly and function. The xanthophyll composition of higher plant photosystems (lutein, violaxanthin, and neoxanthin) is remarkably conserved, suggesting important functional roles for each. We have taken a molecular genetic approach in Arabidopsis toward defining the respective roles of individual xanthophylls in vivo by using a series of mutant lines that selectively eliminate and substitute a range of xanthophylls. The mutations, lut1 and lut2 (lut = lutein deficient), disrupt lutein biosynthesis. In lut2, lutein is replaced mainly by a stoichiometric increase in violaxanthin and antheraxanthin. A third mutant, aba1, accumulates normal levels of lutein and substitutes zeaxanthin for violaxanthin and neoxanthin. The lut2aba1 double mutant completely lacks lutein, violaxanthin, and neoxanthin and instead accumulates zeaxanthin. All mutants were viable in soil and had chlorophyll a/b ratios ranging from 2.9 to 3.5 and near wild-type rates of photosynthesis. However, mutants accumulating zeaxanthin exhibited a delayed greening virescent phenotype, which was most severe and often lethal when zeaxanthin was the only xanthophyll present. Chlorophyll fluorescence quenching kinetics indicated that both zeaxanthin and lutein contribute to nonphotochemical quenching; specifically, lutein contributes, directly or indirectly, to the rapid rise of nonphotochemical quenching. The results suggest that the normal complement of xanthophylls, while not essential, is required for optimal assembly and function of the light harvesting antenna in higher plants.

[1]  K. Niyogi,et al.  Arabidopsis Mutants Define a Central Role for the Xanthophyll Cycle in the Regulation of Photosynthetic Energy Conversion , 1998, Plant Cell.

[2]  R. Goss,et al.  The xanthophyll cycle of Mantoniella squamata converts violaxanthin into antheraxanthin but not to zeaxanthin: consequences for the mechanism of enhanced non-photochemical energy dissipation , 1998, Planta.

[3]  K. Niyogi,et al.  The roles of specific xanthophylls in photoprotection. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[4]  K. Niyogi,et al.  Chlamydomonas Xanthophyll Cycle Mutants Identified by Video Imaging of Chlorophyll Fluorescence Quenching. , 1997, The Plant cell.

[5]  I. Ohad,et al.  Redox‐controlled thylakoid protein phosphorylation. News and views , 1997 .

[6]  E. Pfündel,et al.  Assembly of light harvesting complexes II (LHC-II) in the absence of lutein , 1997 .

[7]  J. Anderson,et al.  Accumulation of Zeaxanthin in Abscisic Acid-Deficient Mutants of Arabidopsis Does Not Affect Chlorophyll Fluorescence Quenching or Sensitivity to Photoinhibition in Vivo , 1997, Plant physiology.

[8]  J. P. Connelly,et al.  Femtosecond transient absorption study of carotenoid to chlorophyll energy transfer in the light-harvesting complex II of photosystem II. , 1997, Biochemistry.

[9]  N. Bishop.  The β,ϵ-carotenoid, lutein, is specifically required for the formation of the oligomeric forms of the light harvesting complex in the green alga, scenedesmus obliquus , 1996 .

[10]  P. Horton,et al.  Identification of proton-active residues in a higher plant light-harvesting complex. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[11]  B. Pogson,et al.  Functional analysis of the beta and epsilon lycopene cyclase enzymes of Arabidopsis reveals a mechanism for control of cyclic carotenoid formation. , 1996, The Plant cell.

[12]  G. Britton,et al.  Arabidopsis carotenoid mutants demonstrate that lutein is not essential for photosynthesis in higher plants. , 1996, The Plant cell.

[13]  P. Horton,et al.  REGULATION OF LIGHT HARVESTING IN GREEN PLANTS. , 1996, Annual review of plant physiology and plant molecular biology.

[14]  M. Havaux,et al.  Photosynthesis, chlorophyll fluorescence, light-harvesting system and photoinhibition resistance of a zeaxanthin-accumulating mutant of Arabidopsis thaliana. , 1996, Journal of photochemistry and photobiology. B, Biology.

[15]  B. Green,et al.  THE CHLOROPHYLL-CAROTENOID PROTEINS OF OXYGENIC PHOTOSYNTHESIS. , 1996, Annual review of plant physiology and plant molecular biology.

[16]  T. Barrette,et al.  Genetic dissection of carotenoid synthesis in arabidopsis defines plastoquinone as an essential component of phytoene desaturation. , 1995, The Plant cell.

[17]  N. Bishop,et al.  Complete separation of the β,ε‐ and β,β‐carotenoid biosynthetic pathways by a unique mutation of the lycopene cyclase in the green alga, Scenedesmus obliquus , 1995 .

[18]  B. W. Dreyfuss,et al.  Assembly of the Light-Harvesting Complexes (LHCs) of Photosystem II (Monomeric LHC IIb Complexes Are Intermediates in the Formation of Oligomeric LHC IIb Complexes) , 1994, Plant physiology.

[19]  B. W. Dreyfuss,et al.  Organization of the Light-Harvesting Complex of Photosystem I and Its Assembly during Plastid Development , 1994, Plant physiology.

[20]  Yoshinori Fujiyoshi,et al.  Atomic model of plant light-harvesting complex by electron crystallography , 1994, Nature.

[21]  S. Jansson.  The light-harvesting chlorophyll a/b-binding proteins. , 1994, Biochimica et biophysica acta.

[22]  H. Paulsen,et al.  Pigments induce folding of light-harvesting chlorophyll a/b-binding protein. , 1993, European journal of biochemistry.

[23]  R. Bassi,et al.  Carotenoid-binding proteins of photosystem II. , 1993, European journal of biochemistry.

[24]  A. Sukenik,et al.  Purification and Characterization of a Light-Harvesting Chlorophyll-Protein Complex from the Marine Eustigmatophyte Nannochloropsis sp. , 1992 .

[25]  G. Peter,et al.  Biochemical composition and organization of higher plant photosystem II light-harvesting pigment-proteins. , 1991, The Journal of biological chemistry.

[26]  C. Rock,et al.  The aba mutant of Arabidopsis thaliana is impaired in epoxy-carotenoid biosynthesis. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[27]  R. Linforth,et al.  Abscisic-acid-deficient mutants at the aba gene locus of Arabidopsis thaliana are impaired in the epoxidation of zeaxanthin , 1991 .

[28]  T. G. Owens,et al.  Femtosecond energy-transfer processes in the B800-850 light-harvesting complex of Rhodobacter sphaeroides 2.4.1. , 1991, Biochimica et biophysica acta.

[29]  R. J. Porra,et al.  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 , 1989 .

[30]  D. Siefermann-Harms.  The light-harvesting and protective functions of carotenoids in photosynthetic membranes , 1987 .

[31]  J. Brown,et al.  Functional Organization of Chlorophyll a and Carotenoids in the Alga, Nannochloropsis salina. , 1987, Plant physiology.

[32]  R. Cogdell.  Carotenoids in photosynthesis , 1978, Photochemistry and photobiology.

[33]  A. Gilmore,et al.  Mechanistic aspects of xanthophyll cycle‐dependent photoprotection in higher plant chloroplasts and leaves , 1997 .

[34]  B. Demmig‐Adams,et al.  The role of xanthophyll cycle carotenoids in the protection of photosynthesis , 1996 .

[35]  D. Bhaya,et al.  Light-harvesting complexes in oxygenic photosynthesis: diversity, control, and evolution. , 1995, Annual review of genetics.

[36]  T. G. Owens,et al.  Femtosecond dynamics of energy transfer in B800-850 light-harvesting complexes of Rhodobacter sphaeroides. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[37]  G. Schmidt,et al.  Reconstitution of chlorophyll a/b light-harvesting complexes: Xanthophyll-dependent assembly and energy transfer. , 1987, Proceedings of the National Academy of Sciences of the United States of America.