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Biosynthesis, accumulation and emission of carotenoids, α-tocopherol, plastoquinone, and isoprene in leaves under high photosynthetic irradiance

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Abstract

The localization of isoprenoid lipids in chloroplasts, the accumulation of particular isoprenoids under high irradiance conditions, and channelling of photosynthetically fixed carbon into plastidic thylakoid isoprenoids, volatile isoprenoids, and cytosolic sterols are reviewed. During leaf and chloroplast development in spring plastidic isoprenoid biosynthesis provides primarily thylakoid carotenoids, the phytyl side-chain of chlorophylls and the electron carriers phylloquinone K1, α-tocoquinone and α-tocopherol, as well as the nona-prenyl side-chain of plastoquinone-9. Under high irradiance, plants develop sun leaves and high light (HL) leaves with sun-type chloroplasts that possess, besides higher photosynthetic CO2 assimilation rates, different quantitative levels of pigments and prenylquinones as compared to shade leaves and low light (LL) leaves. After completion of chloroplast thylakoid synthesis plastidic isoprenoid biosynthesis continues at high irradiance conditions, constantly accumulating α-tocopherol (α-T) and the reduced form of plastoquinone-9 (PQ-9H2) deposited in the steadily enlarging osmiophilic plastoglobuli, the lipid reservoir of the chloroplast stroma. In sun leaves of beech (Fagus) and in 3-year-old sunlit Ficus leaves the level of α-T and PQ-9 can exceed that of chlorophyll b. Most plants respond to HL conditions (sun leaves, leaves suddenly lit by the sun) with a 1.4–2-fold increase of xanthophyll cycle carotenoids (violaxanthin, zeaxanthin, neoxanthin), an enhanced operation of the xanthophyll cycle and an increase of β-carotene levels. This is documented by significantly lower values for the weight ratio chlorophylls to carotenoids (range: 3.6–4.6) as compared to shade and LL leaves (range: 4.8–7.0). Many plant leaves emit under HL and high temperature conditions at high rates the volatile compounds isoprene (broadleaf trees) or methylbutenol (American ponderosa pines), both of which are formed via the plastidic 1-deoxy-d-xylulose-phosphate/2-C-methylerythritol 5-phosphate (DOXP/MEP) pathway. Other plants by contrast, accumulate particular mono- and diterpenes. Under adequate photosynthetic conditions the chloroplastidic DOXP/MEP isoprenoid pathway essentially contributes, with its C5 isoprenoid precusors, to cytosolic sterol biosynthesis. The possible cross-talk between the two cellular isoprenoid pathways, the acetate/MVA and the DOXP/MEP pathways, that preferentially proceeds in a plastid-to-cytosol direction, is shortly discussed.

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Notes

  1. At that time I was a post-doc with Melvin Calvin and, after the thylakoid lipid table had been published (Lichtenthaler and Park 1963), Andy Benson became quite interested in the functional organization of membrane lipids and contacted me in Berkeley. During my subsequent visit to his laboratory in La Jolla/San Diego in the summer of 1963, I had on basis of the thylakoid lipid table an extensive discussion with Andy Benson on the arrangement of phospho- and glycolipids in photosynthetic biomembranes. From the dimensions of the double lines seen for thylakoid membranes in electron microscopic observations at high magnification and the length of the fatty acid chains in the glycerolipid molecules, the two of us agreed that a bilayer was spatially possible and that the thylakoid membrane most probably consisted of a bilayer of glycerolipids in which various functional proteins were embedded and attached. We also discussed in a very stimulating approach how chlorophylls with their porphyrin ring and phytyl side-chain were oriented in such a lipid bilayer and how plastidic prenylquinones with their phytyl or nona-prenyl side-chain might be embedded, together with the carotenoids, as C40-isoprenoids to give a possible thylakoid lipid bilayer structure. The thylakoid lipid table and various aspects of our discussion subsequently became essential parts of Andy Benson’s review paper, “Plant Lipid Membranes” (Benson 1964), in which he showed various possibilities for the arrangement of glycerolipids in biomembranes and pointed out the kind of information and research needed to make progress in our understanding of the functional organization of plant and thylakoid membrane lipids. This topic was further advanced by Weier and Benson (1967). In this context, one has to consider that our present knowledge that all cellular membranes are composed of a basic lipid bilayer structure was not known at that time. Likewise, in the early 1960s, it was not known that photosynthetic pigments are bound to particular chlorophyll–carotenoid–protein complexes, such as the light-harvesting Chl a/b complexes, LHCPs (or LHCII), photosystem II (CPa) and photosystem I pigment–protein complexes (CPI and CPIa) (Bennett 1983; Lichtenthaler et al. 1982a; Thornber 1975). Further, that the pigments are not packed together with glycerolipids in the thylakoid bilayer. (H. K. Lichtenthaler, March 2007).

  2. As post-doc in Berkeley at beginning of December 1963, I actually detected the rapid flow of 14C-label from photosynthetically fixed 14CO2, not only into the plastidic isoprenoids β-carotene, plastoquinone-9, phylloquinone K1 and chlorophylls, but also into cytosolic sterols in Chlorella after an exposure time of 2 min. In this experiment Chlorella suspensions were fed 14CO2 in the original ‘Lollipop’ vessel set up by Andy Benson in Melvin Calvin’s photosynthesis laboratory in Berkeley in the early 1950s for studies of the path of carbon in photosynthesis. Due to my return to Germany at the end of December 1963, this work could not be continued. However, feeding 13C-labeled glucose to illuminated Chlorella suspensions in my Karlruhe laboratory 42 years later led to the detection of the chloroplastidic DOXP/MEP pathway for isoprenoid biosynthesis and its responsibility for the biosynthesis of the cytosolic sterols in unicellular green algae (Schwender et al. 1996). (H. K. Lichtenthaler, March 2007).

  3. In addition to isoprenoid compounds, plants emit substantial amounts of phytogenic volatile organic compounds (PVOCS) comprising alkanes, alkenes, alcohols, aldehydes, ethers, esters and carboxylic acids (e.g., Penuelas and Llusia 2004). Plants not only metabolize methanol as shown in a paper co-authored by Andy Benson (Gout et al. 2000), but they also emit substantial amounts of methanol (Nonomura and Benson 1992a, b) via stomates (Nemecek-Marshall et al. 1995) during the early stages of leaf expansion due to pectin demethylation (see review by Fall and Benson, 1996).

Abbreviations

a + b:

Total chlorophylls

a/b:

Ratio of chlorophyll a to b

Chl:

Chlorophyll

(a + b)/(x + c):

Weight ratio of chlorophylls to carotenoids

A:

Antheraxanthin

c:

Carotenes

DMAPP:

Dimethylallyldiphosphate

DOXP/MEP pathway:

Plastidic 1-deoxy-d-xylulose-4-phosphate/2-C-methylerythritol 5-phosphate pathway

GAP:

Glyceraldehyde-3-phosphate

IPP:

Isopentenyl diphosphate

MBO:

2-methyl-3-buten-2-ol

MEP:

2-C-methylerythritol 5-phosphate

MVA:

Mevalonic acid

PPFD:

Photosynthetic photon flux density

V:

Violaxanthin

x + c:

Total carotenoids

x:

Xanthophylls

Z:

Zeaxanthin

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Acknowledgments

I am grateful to former Ph.D students and group members who carried out parts of the research on plant isoprenoid biosynthesis (T. J. Bach, C. Müller, J. Schwender, J. Zeidler) and chloroplast adaptation to high irradiance conditions (C. Buschmann, M. Knapp, G. Langsdorf, D. Meier, U. Rinderle-Zimmer). I wish to thank Professor Bob Buchanan for helpful comments on this manuscript, Ms Sabine Zeiler for long-term excellent implementation of pigment determinations, and Ms Gabrielle Johnson for English language assistance.

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  1. Botanisches Institut (Molecular Biology and Biochemistry of Plants), University of Karlsruhe, Kaiserstr. 12, 76133, Karlsruhe, Germany

    Hartmut K. Lichtenthaler

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Lichtenthaler, H.K. Biosynthesis, accumulation and emission of carotenoids, α-tocopherol, plastoquinone, and isoprene in leaves under high photosynthetic irradiance. Photosynth Res 92, 163–179 (2007). https://doi.org/10.1007/s11120-007-9204-y

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