Review
The regulation of carotenoid pigmentation in flowers

https://doi.org/10.1016/j.abb.2010.07.028Get rights and content

Abstract

Carotenoids fulfill many processes that are essential for normal growth and development in plants, but they are also responsible for the breathtaking variety of red-to-yellow colors we see in flowers and fruits. Although such visual diversity helps to attract pollinators and encourages herbivores to distribute seeds, humans also benefit from the aesthetic properties of flowers and an entire floriculture industry has developed on the basis that new and attractive varieties can be produced. Over the last decade, much has been learned about the impact of carotenoid metabolism on flower color development and the molecular basis of flower color. A number of different regulatory mechanisms have been described ranging from the transcriptional regulation of genes involved in carotenoid synthesis to the control of carotenoid storage in sink organs. This means we can now explain many of the natural colorful varieties we see around us and also engineer plants to produce flowers with novel and exciting varieties that are not provided by nature.

Research highlights

► Carotenoids are responsible for the variety of red-to-yellow colors in flowers. ► Biosynthesis can be controlled by transcriptional/post-transcriptional regulation. ► Lipoprotein-sequestering structures can act as carotenoid sinks. ► The accumulation of carotenoids can also be regulated by carotenoid degradation. ► Flower color can be controlled by the genetic modulation of carotenoid metabolism.

Section snippets

Overview of carotenoid synthesis and metabolism in plants

In plants, carotenoids are synthesized de novo from the isomeric C5 precursors isopentenyl diphosphate (IPP) and dimethylallyl diphosphate (DMAPP) [21]. The reaction occurs in plastids and both precursors are derived primarily from the plastidial methylerythritol 4-phosphate (MEP) pathway [22], [23] as shown in Fig. 1. The condensation of three IPP units and one molecule of DMAPP produces geranylgeranyl diphosphate (GGPP, C20), a reaction catalyzed by the enzyme GGPP synthase (GGPPS). The first

Carotenoid biosynthesis and accumulation controlled by transcription of carotenogenic genes

The transcriptional regulation of carotenogenic genes is an important mechanism that contributes to the accumulation of specific carotenoids during flower development. The next section looks at specific case studies to illustrate how transcriptional regulation affects carotenoid accumulation in the flowers of different species.

Carotenoid biosynthesis and accumulation controlled by carotenogenic enzyme levels

Post-transcriptional regulation of carotenogenic enzyme activity also plays a role in controlling carotenoid biosynthesis and accumulation in flowers. The yellow flowers of the wild daffodil Narcissus pseudonarcissus reflect the accumulation of large amounts of lutein and lower amounts of β-carotene and its derivatives [58]. Isolated chromoplasts can be used to synthesize β-carotene when fed with IPP, but upon disintegration they also yield significant amounts of α-carotene and ζ-carotene [76].

The abundance of CCDs

The enzyme 9-cis-epoxycarotenoid dioxygenase (NCED) has been isolated from many different plants, the first being the corn viviparous14 (vp14) gene product [6], [83]. It is not yet clear whether this enzyme significantly affects carotenoid metabolism in flowers. For example, Zhu et al. [84] recently cloned two NCED cDNAs from gentian, one of which (GlNCED1) was expressed in flowers (strongly in the stamens, less strongly in the petals) but its impact on carotenoid accumulation is unknown. There

Extended ketocarotenoid synthesis in Adonis

Adonis (A. aestivalis), also known as Summer pheasant’s-eye, has long petals which are orange for most of their length but have a deep red basal patch which gives the flower a striking, ocellar appearance. The color is caused by carotenoid accumulation, but unlike all other known flowering plants the pigments that accumulate are ketocarotenoids (Fig. 2) [68], [69], predominantly astaxanthin (3,3′-dihydroxy-4,4′-diketo-β,β-carotene) with lesser amounts of 3-hydroxyechinenone

Coupling carotenogenesis to chromoplast development and carotenoid storage

As stated above, Moehs et al. [42] cloned many of the carotenogenic genes from marigold to investigate their impact on flower color, and also found that the MinD and FtsZ genes were upregulated in the most pigmented varieties during development while remaining at basal levels in paler varieties, suggesting a correlation between carotenogenesis and plastid replication. A full-length FtsZ cDNA has also been isolated from gentian petals but in this case the opposite expression profile was

Modulating the existing carotenoid pathway

Flowers evolved to attract pollinators but they are also aesthetically pleasing to humans, and breeding flowers to generate visually appealing color varieties has been an important aspect of floriculture for hundreds of years [20]. One of the obstacles faced by flower breeders is that, for many species, there are colors that cannot be accessed by conventional breeding because the pigments cannot be synthesized using available genotypes, e.g. vivid red petunias and delphiniums, and the elusive

Outlook and conclusions

Over the last decade we have learned a great deal about the accumulation of carotenoid pigments in flowers, the genes and enzymes responsible for carotenoid synthesis and degradation, the cellular mechanisms responsible for carotenoid storage, and how all these processes are regulated during development and in response to external stimuli. The availability of efficient genetic transformation methods for commercially important cut flower varieties and flower-specific promoters [54], [55], [124]

Acknowledgments

We would like to thank Prof. G. Sandmann for permission to use an unpublished photograph in Fig. 3. This research was supported by the Ministry of Science and Innovation, Spain (BFU2007-61413 and BIO2007-30738-E) and European Research Council Advanced Grant (BIOFORCE) to P.C., C.Z. and L.S. are supported in part by grants from the National Natural Science Foundation of China (Nos. 30870222 and 30370123). S.N. and G.F. are supported by Ministry of Science and Innovation (Spain) Ph.D.

References (129)

  • J. Von Lintig et al.

    J. Nutr.

    (2004)
  • G. Farré et al.

    Plant Sci.

    (2010)
  • C. Zhu et al.

    Trends Plant Sci.

    (2007)
  • C. Zhu et al.

    Arch. Biochem. Biophys.

    (2009)
  • G. Sandmann et al.

    Metab. Eng.

    (2006)
  • P.D. Fraser et al.

    Arch. Biochem. Biophys.

    (2009)
  • C.I. Cazzonelli et al.

    Trends Plant Sci.

    (2010)
  • W. Eisenreich et al.

    Trends Plant Sci.

    (2001)
  • Z. Sun et al.

    J. Biol. Chem.

    (1996)
  • F. Bouvier et al.

    Biochim. Biophys. Acta

    (1998)
  • R.F. Quinlan et al.

    Arch. Biochem. Biophys.

    (2007)
  • J.E. Kim et al.

    Phytochemistry

    (2010)
  • S. Al-Babili et al.

    FEBS Lett.

    (2000)
  • M. Seo et al.

    Trends Plant Sci.

    (2002)
  • G.E. Bartley et al.

    J. Biol. Chem.

    (1992)
  • G.E. Bartley et al.

    J. Biol. Chem.

    (1993)
  • C. Zhu et al.

    Biochem. Biophys. Acta

    (2003)
  • K. Egger

    Phytochemistry

    (1965)
  • M.I. Scott et al.

    Poult. Sci.

    (1968)
  • A.A. Del Villar-Martinez et al.

    J. Plant Physiol.

    (2005)
  • C. Zhu et al.

    J. Plant Physiol.

    (2007)
  • A. Rubio et al.

    J. Biol. Chem.

    (2008)
  • F.C. Huang et al.

    Phytochemistry

    (2009)
  • P.A. Tarantilis et al.

    J. Chromatogr.

    (1994)
  • H. Pfander et al.

    Phytochemistry

    (1982)
  • G. Britton et al.

    Carotenoids Handbook

    (2004)
  • H.A. Frank et al.

    Photochem. Photobiol.

    (1996)
  • B. Demmig-Adams et al.

    Science

    (2002)
  • G.E. Bartley et al.

    Plant Cell

    (1995)
  • S.H. Schwartz et al.

    Science

    (1997)
  • V. Gomez-Roldan et al.

    Nature

    (2008)
  • M. Umehara et al.

    Nature

    (2008)
  • F. Bouvier et al.

    Plant Cell

    (2003)
  • F. Bouvier et al.

    Science

    (2003)
  • A.J. Simkin et al.

    Plant Physiol.

    (2004)
  • A.J. Simkin et al.

    Plant J.

    (2004)
  • S. Lu et al.

    J. Integr. Plant Biol.

    (2008)
  • Y. Tanaka et al.

    Plant J.

    (2008)
  • J. Chappell

    Annu. Rev. Plant Physiol. Plant Mol. Biol.

    (1995)
  • H.K. Lichtenthaler

    Annu. Rev. Plant Physiol. Plant Mol. Biol.

    (1999)
  • N. Misawa et al.

    J. Biochem.

    (1994)
  • Y. Chen et al.

    Plant Physiol.

    (2010)
  • J. Breitenbach et al.

    Planta

    (2005)
  • T. Isaacson et al.

    Plant Physiol.

    (2004)
  • L. Tian et al.

    Plant Cell

    (2003)
  • J. Kim et al.

    Proc. Natl Acad. Sci. USA

    (2006)
  • L. Tian et al.

    Plant Mol. Biol.

    (2001)
  • B. Demmig-Adams et al.

    FASEB J.

    (1996)
  • F. Bouvier et al.

    Eur. J. Biochem.

    (2000)
  • S.H. Schwartz et al.

    Plant Physiol.

    (2003)

    • Cited by (0)

    View full text
    Copyright © 2010 Elsevier Inc. All rights reserved.