Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Regulation of lutein biosynthesis and prolamellar body formation in Arabidopsis

Abby J. Cuttriss A , Alexandra C. Chubb A , Ali Alawady A B , Bernhard Grimm B and Barry J. Pogson A C
+ Author Affiliations
- Author Affiliations

A ARC Centre of Excellence in Plant Energy Biology, School of Biochemistry and Molecular Biology, The Australian National University, Canberra, ACT 0200, Australia.

B Institute of Biology/Plant Physiology, Humboldt University, Philippstrasse 13 Building 12, 10115 Berlin, Germany.

C Corresponding author. Email: barry.pogson@anu.edu.au

Functional Plant Biology 34(8) 663-672 https://doi.org/10.1071/FP07034
Submitted: 14 February 2007  Accepted: 9 May 2007   Published: 23 July 2007

Abstract

Carotenoids are critical for photosynthetic function in chloroplasts, and are essential for the formation of the prolamellar body in the etioplasts of dark-grown (etiolated) seedlings. They are also precursors for plant hormones in both types of plastids. Lutein is one of the most abundant carotenoids found in both plastids. In this study we examine the regulation of lutein biosynthesis and investigate the effect of perturbing carotenoid biosynthesis on the formation of the lattice-like membranous structure of etioplasts, the prolamellar body (PLB). Analysis of mRNA abundance in wildtype and lutein-deficient mutants, lut2 and ccr2, in response to light transitions and herbicide treatments demonstrated that the mRNA abundance of the carotenoid isomerase (CRTISO) and epsilon-cyclase (ϵLCY) can be rate limiting steps in lutein biosynthesis. We show that accumulation of tetra-cis-lycopene and all-trans-lycopene correlates with the abundance of mRNA of several carotenoid biosynthetic genes. Herbicide treatments that inhibit carotenoid biosynthetic enzymes in wildtype and ccr2 etiolated seedlings were used to demonstrate that the loss of the PLB in ccr2 mutants is a result of perturbations in carotenoid accumulation, not indirect secondary effects, as PLB formation could be restored in ccr2 mutants treated with norflurazon.


Acknowledgements

We acknowledge the support of the Australian Research Council via Centre of Excellence in Plant Energy Biology (CE0561495) to B.J.P.; D.E.S.T and D.A.A.D support to B.J.P. and B.G. and the A.N.U. Endowment of Excellence grant to A.J.C. We thank the ANU electron microscope unit and biomolecular resource facility for assistance with TEM and sequencing, respectively.


References


Adams WW, Demmig-Adams B, Rosenstiel TN, Brightwell AK, Ebbert V (2002) Photosynthesis and photoprotection in overwintering plants. Plant Biology 4, 545–557.
Crossref | GoogleScholarGoogle Scholar | open url image1

Axelsson L, Dahlin C, Ryberg H (1982) The function of carotenoids during chloroplast development. 5. Correlation between carotenoid content, ultrastructure and chlorophyll-b to chlorophyll-a ratio. Physiologia Plantarum 55, 111–116.
Crossref | GoogleScholarGoogle Scholar | open url image1

Barry P, Pallett KE (1990) Herbicidal inhibition of carotenogenesis detected by HPLC. Zeitschrift Fur Naturforschung C. 45, 492–497. open url image1

Bouvier F, Backhaus RA, Camara B (1998) Induction and control of chromoplast-specific carotenoid genes by oxidative stress. Journal of Biological Chemistry 273, 30651–30659.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bramley PM (1993) Inhibition of carotenoid biosynthesis. In ‘Carotenoids in photosynthesis’. (Eds AJ Young, G Britton) pp. 127–159. (Chapman and Hall: London)

Bramley PM (2002) Regulation of carotenoid formation during tomato fruit ripening and development. Journal of Experimental Botany 53, 2107–2113.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal 16, 735–743.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Cunningham FJ, Gantt E (1998) Genes and enzymes of carotenoid biosynthesis in plants. Annual Review of Plant Physiology and Plant Molecular Biology 49, 557–583.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Cunningham FX (2002) Regulation of carotenoid synthesis and accumulation in plants. Pure and Applied Chemistry 74, 1409–1417. open url image1

Curtis M, Grossniklaus U (2003) A Gateway TM cloning vector set for high-throughput functional analysis of genes in plants. Plant Physiology 133, 462–469.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Cuttriss AJ , Mimica J , Howitt C , Pogson BJ (2006) Carotenoid metabolism. In ‘The structure and function of plastids’. (Eds JK Hoober, RR Wise) pp. 315–334. (Springer-Verlag: Dordrecht, The Netherlands)

Dalla Vecchia F, Barbato R, La Rocca N, Moro I, Rascio N (2001) Responses to bleaching herbicides by leaf chloroplasts of maize plants grown at different temperatures. Journal of Experimental Botany 52, 811–820.
PubMed |
open url image1

Davison PA, Hunter CN, Horton P (2002) Overexpression of beta-carotene hydroxylase enhances stress tolerance in Arabidopsis. Nature 418, 203–206.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

DellaPenna D, Pogson BJ (2006) Vitamin synthesis in plants: tocopherols and carotenoids. Annual Review of Plant Biology 57, 711–738.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Denev ID, Yahubyan GT, Minkov IN, Sundqvist C (2005) Organization of protochlorophyllide oxidoreductase in prolamellar bodies isolated from etiolated carotenoid-deficient wheat leaves as revealed by fluorescence probes. Biochimica et Biophysica Acta-Biomembranes 1716, 97–103.
Crossref | GoogleScholarGoogle Scholar | open url image1

Di Baccio D, Quartacci MF, Dalla Vecchia F, La Rocca N, Rascio N, Navari-Izzo F (2002) Bleaching herbicide effects on plastids of dark-grown plants: lipid composition of etioplasts in amitrole and norflurazon-treated barley leaves. Journal of Experimental Botany 53, 1857–1865.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ducreux LJM, Morris WL, Hedley PE, Shepherd T, Davies HV, Millam S, Taylor MA (2005) Metabolic engineering of high carotenoid potato tubers containing enhanced levels of beta-carotene and lutein. Journal of Experimental Botany 56, 81–89.
PubMed |
open url image1

Goodwin TW , Britton G (1988) Distribution and analysis of carotenoids. In ‘Plant pigments’. (Ed. TW Goodwin) pp. 61–132. (Academic Press Limited: San Diego)

Grunewald K, Eckert M, Hirschberg J, Hagen C (2000) Phytoene desaturase is localized exclusively in the chloroplast and up-regulated at the mRNA level during accumulation of secondary carotenoids in Haematococcus pluvialis (Volvocales, Chlorophyceae). Plant Physiology 122, 1261–1268.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Heim DR, Larrinua IM (1989) Primary site of action of amitrole in Arabidopsis thaliana involves inhibition of root elongation but not of histidine or pigment biosynthesis. Plant Physiology 91, 1226–1231.
PubMed |
open url image1

Herman CA, Im CS, Beale SI (1999) Light-regulated expression of the GSA gene encoding the chlorophyll biosynthetic enzyme glutamate 1-semialdehyde aminotransferase in carotenoid-deficient Chlamydomonas reinhardtii cells. Plant Molecular Biology 39, 289–297.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Herrin DL, Battey JF, Greer K, Schmidt GW (1992) Regulation of chlorophyll apoprotein expression and accumulation. Requirements for carotenoids and chlorophyll. Journal of Biological Chemistry 267, 8260–8269.
PubMed |
open url image1

Hirschberg J (2001) Carotenoid biosynthesis in flowering plants. Current Opinion in Plant Biology 4, 210–218.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hoaglands DR, Arnon DA (1950) The water culture method of growing plants without soil. California Agricultural Experiment Station Bulletin , 1–39. open url image1

Hoober JK, Eggink LL (1999) Assembly of light-harvesting complex II and biogenesis of thylakoid membranes in chloroplasts. Photosynthesis Research 61, 197–215.
Crossref | GoogleScholarGoogle Scholar | open url image1

Isaacson T, Ronen G, Zamir D, Hirschberg J (2002) Cloning of tangerine from tomato reveals a carotenoid isomerase essential for the production of beta-carotene and xanthophylls in plants. The Plant Cell 14, 333–342.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Jensen PE, Gibson LCD, Henningsen KW, Hunter CN (1996) Expression of the chlI, chlD, and chlH genes from the cyanobacterium Synechocystis PCC6803 in Escherichia coli and demonstration that the three cognate proteins are required for magnesium-protoporphyrin chelatase activity. Journal of Biological Chemistry 271, 16662–16667.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Johnson GN, Scholes JD, Horton P, Young AJ (1993) Relationships between carotenoid composition and growth habit in British plant species. Plant, Cell & Environment 16, 681–686.
Crossref | GoogleScholarGoogle Scholar | open url image1

Külheim C, Ågren J, Jansson S (2002) Rapid regulation of light harvesting and plant fitness in the field. Science 297, 91–93.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

von Lintig J, Welsch R, Bonk M, Giuliano G, Batschauer A, Kleinig H (1997) Light-dependent regulation of carotenoid biosynthesis occurs at the level of phytoene synthase expression and is mediated by phytochrome in Sinapis alba and Arabidopsis thaliana seedlings. The Plant Journal 12, 625–634.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Logan BA, Barker DH, Demmig Adams B, Adams WW (1996) Acclimation of leaf carotenoid composition and ascorbate levels to gradients in the light environment within an Australian rainforest. Plant, Cell & Environment 19, 1083–1090.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lu S, Van Eck JV, Zhou X, Lopez AB, O”Halloran DM , et al. (2006) The cauliflower Or gene encodes a DnaJ cysteine-rich domain-containing protein that mediates high levels of β-carotene accumulation. The Plant Cell 18, 3594–3605.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Matile P, Hortensteiner S, Thomas H (1999) Chlorophyll degradation. Annual Review of Plant Physiology and Plant Molecular Biology 50, 67–95.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Matsubara S, Morosinotto T, Bassi R, Christian AL, Fischer-Schliebs E , et al. (2003) Occurrence of the lutein-epoxide cycle in mistletoes of the Loranthaceae and Viscaceae. Planta 217, 868–879.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Moehs CP, Tian L, Osteryoung KW, DellaPenna D (2001) Analysis of carotenoid biosynthetic gene expression during marigold petal development. Plant Molecular Biology 45, 281–293.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Moro I, Dalla Vecchia F, La Rocca N, Navari-Izzo F, Quartacci MF, Di Baccio D, Rudiger W, Rascio N (2004) Impaired carotenogenesis can affect organization and functionality of etioplast membranes. Physiologia Plantarum 122, 123–132.
Crossref | GoogleScholarGoogle Scholar | open url image1

Nogaj LA, Srivastava A, van Lis R, Beale SI (2005) Cellular levels of glutamyl-tRNA reductase and glutamate-1-semialdehyde aminotransferase do not control chlorophyll synthesis in Chlamydomonas reinhardtii. Plant Physiology 139, 389–396.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Park H, Kreunen SS, Cuttriss AJ, DellaPenna D, Pogson BJ (2002) Identification of the carotenoid isomerase provides insight into carotenoid biosynthesis, prolamellar body formation, and photomorphogenesis. The Plant Cell 14, 321–332.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Phillip DM, Young AJ (2006) Preferential inhibition of the lycopene ϵ-cyclase by the substituted triethylamine compound MPTA in higher plants. Journal of Plant Physiology 163, 383–391.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Pogson BJ, Rissler HM (2000) Genetic manipulation of carotenoid biosynthesis and photoprotection. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 355, 1395–1403.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Pogson B, McDonald K, Truong M, Britton G, DellaPenna D (1996) Arabidopsis carotenoid mutants demonstrate that lutein is not essential for photosynthesis in higher plants. The Plant Cell 8, 1627–1639.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Pogson BJ, Niyogi KK, Bjorkman O, DellaPenna D (1998) Altered xanthophyll compositions adversely affect chlorophyll accumulation and nonphotochemical quenching in Arabidopsis mutants. Proceedings of the National Academy of Sciences USA 95, 13324–13329.
Crossref | GoogleScholarGoogle Scholar | open url image1

Pogson BJ , Rissler HM , Frank HA (2005) The roles of carotenoids in photosystem II of higher plants. In ‘Photosystem II: the light-driven water : plastoquinone oxidoreductase’. (Eds K Satoh, TJ Wydrzynski) pp. 515–537. (Springer-Verlag: Dordrecht, The Netherlands)

Rascio N, DallaVecchia F, Agnolucci L, Barbato R, Tassani V, Casadoro G (1996) Amitrole effects on barley etioplasts. Journal of Plant Physiology 149, 295–300. open url image1

Rissler HM, Pogson BJ (2001) Antisense inhibition of the beta-carotene hydroxylase enzyme in Arabidopsis and the implications for carotenoid accumulation, photoprotection and antenna assembly. Photosynthesis Research 67, 127–137.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ronen G, Cohen M, Zamir D, Hirschberg J (1999) Regulation of carotenoid biosynthesis during tomato fruit development: Expression of the gene for lycopene epsilon-cyclase is down-regulated during ripening and is elevated in the mutant delta. The Plant Journal 17, 341–351.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Rossel JB, Wilson IW, Pogson BJ (2002) Global changes in gene expression in response to high light in Arabidopsis. Plant Physiology 130, 1109–1120.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Selstam E, Sandelius AS (1984) A comparison between prolamellar bodies and prothylakoid membranes of etioplasts of dark-grown wheat concerning lipid and polypeptide composition. Plant Physiology 76, 1036–1040.
PubMed |
open url image1

Sperling U, Franck F, van Cleve B, Frick G, Apel K, Armstrong GA (1998) Etioplast differentiation in Arabidopsis: both PORA and PORB restore the prolamellar body and photoactive protochlorophyllide-F655 to the cop1 photomorphogenic mutant. The Plant Cell 10, 283–296.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Steinbrenner J, Linden H (2003) Light induction of carotenoid biosynthesis genes in the green alga Haematococcus pluvialis: regulation by photosynthetic redox control. Plant Molecular Biology 52, 343–356.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Strand A, Asami T, Alonso J, Ecker JR, Chory J (2003) Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrinIX. Nature 421, 79–83.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sundqvist C, Dahlin C (1997) With chlorophyll pigments from prolamellar bodies to light-harvesting complexes. Physiologia Plantarum 100, 748–759.
Crossref | GoogleScholarGoogle Scholar | open url image1

Susek RE, Ausubel FM, Chory J (1993) Signal transduction mutants of Arabidopsis uncouple nuclear CAB and RBCS gene expression from chloroplast development. Cell 74, 787–799.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Suzuki Y, Shioi Y (2004) Changes in chlorophyll and carotenoid contents in radish (Raphanus sativus) cotyledons show different time courses during senescence. Physiologia Plantarum 122, 291–296.
Crossref | GoogleScholarGoogle Scholar | open url image1

Tada S, Hatano M, Nakayama Y, Volrath S, Guyer D, Ward E, Ohta D (1995) Insect-cell expression of recombinant imidazoleglycerolphosphate dehydratase of Arabidopsis and wheat and inhibition by triazole herbicides. Plant Physiology 109, 153–159.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Welsch R, Beyer P, Hugueney P, Kleinig H, von Lintig J (2000) Regulation and activation of phytoene synthase, a key enzyme in carotenoid biosynthesis, during photomorphogenesis. Planta 211, 846–854.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Welsch R, Medina J, Giuliano G, Beyer P, von Lintig J (2003) Structural and functional characterization of the phytoene synthase promoter from Arabidopsis thaliana. Planta 216, 523–534.
PubMed |
open url image1

Woitsch S, Römer S (2003) Expression of xanthophyll biosynthetic genes during light-dependant chloroplast differentiation. Plant Physiology 132, 1508–1517.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Young AJ (1993) Factors that affect the carotenoid composition of higher plants and algae. In ‘Carotenoids in photosynthesis’. (Eds AJ Young, G Britton) pp. 161–205. (Chapman and Hall: London)

Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiology 136, 2621–2632.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1