Phytol derived from chlorophyll hydrolysis in plants is metabolized via phytenal

Abstract

Phytol is the isoprenoid alcohol bound in ester linkage to chlorophyll, the most abundant photosynthetic pigment in plants. During leaf senescence, large amounts of phytol are released by chlorophyll degradation. However, the pathway of phytol catabolism in plants is unknown. We hypothesized that phytol degradation in plants might involve its oxidation into the long-chain aldehyde phytenal. Using GC-MS for aldehyde quantification after derivatization with methylhydroxylamine, phytenal was identified in leaves, whereas other long-chain aldehydes (phytanal and pristanal) were barely detectable. We found that phytenal accumulates during chlorotic stresses, for example, salt stress, dark-induced senescence, and nitrogen deprivation. The increase in the phytenal content is mediated at least in part independently of enzyme activities, and it is independent of light. Characterization of phytenal accumulation in the pao1 mutant affected in chlorophyll degradation revealed that phytenal is an authentic phytol metabolite derived from chlorophyll breakdown. The increase in phytenal was even stronger in mutants affected in the production of other phytol metabolites including vte5-2 (tocopherol deficient) and pes1 pes2 (fatty acid phytyl ester deficient). Therefore, phytenal accumulation is controlled by competing, alternative pathways of phosphorylation (leading to tocopherol production) or esterification (fatty acid phytyl ester production). As a consequence, the content of phytenal is maintained at low levels, presumably to minimize its toxic effects caused by its highly reactive aldehyde group that can form covalent bonds with and inactivate the amino groups of proteins. Phytol is the isoprenoid alcohol bound in ester linkage to chlorophyll, the most abundant photosynthetic pigment in plants. During leaf senescence, large amounts of phytol are released by chlorophyll degradation. However, the pathway of phytol catabolism in plants is unknown. We hypothesized that phytol degradation in plants might involve its oxidation into the long-chain aldehyde phytenal. Using GC-MS for aldehyde quantification after derivatization with methylhydroxylamine, phytenal was identified in leaves, whereas other long-chain aldehydes (phytanal and pristanal) were barely detectable. We found that phytenal accumulates during chlorotic stresses, for example, salt stress, dark-induced senescence, and nitrogen deprivation. The increase in the phytenal content is mediated at least in part independently of enzyme activities, and it is independent of light. Characterization of phytenal accumulation in the pao1 mutant affected in chlorophyll degradation revealed that phytenal is an authentic phytol metabolite derived from chlorophyll breakdown. The increase in phytenal was even stronger in mutants affected in the production of other phytol metabolites including vte5-2 (tocopherol deficient) and pes1 pes2 (fatty acid phytyl ester deficient). Therefore, phytenal accumulation is controlled by competing, alternative pathways of phosphorylation (leading to tocopherol production) or esterification (fatty acid phytyl ester production). As a consequence, the content of phytenal is maintained at low levels, presumably to minimize its toxic effects caused by its highly reactive aldehyde group that can form covalent bonds with and inactivate the amino groups of proteins. The tail of chlorophyll: Fates for phytolJournal of Biological ChemistryVol. 296PreviewUnderstanding the pathways involved in chlorophyll breakdown provides a molecular map to the color changes observed in plant life on a global scale each fall. Surprisingly, little is known about the fate of phytol, chlorophyll’s 20-carbon branched-chain tail, during this process. A recent study from Gutbrod et al. provides evidence using physiological, genetic, and exquisitely sensitive analytical approaches that phytenal is an intermediate in plant phytol catabolism. These insights and techniques open the door to further investigation of this complicated metabolic system, with implications for plant health and agriculture. Full-Text PDF Open Access Chlorophyll is the most important photosynthetic pigment in plants, and it is crucial for light harvesting and channeling of photons to the reaction centers of photosystems I and II. Chlorophyll is subject to constant turnover, and chlorophyll degradation is stimulated during stress or senescence (1Hörtensteiner S. Kräutler B. Chlorophyll breakdown in higher plants.Biochim. Biophys. Acta. 2011; 1807: 977-988Crossref PubMed Scopus (537) Google Scholar). The degradation of chlorophyll by enzymes of chlorophyll catabolism is important as some chlorophyll catabolites can produce radicals after illumination, which are highly toxic to the cell (1Hörtensteiner S. Kräutler B. Chlorophyll breakdown in higher plants.Biochim. Biophys. Acta. 2011; 1807: 977-988Crossref PubMed Scopus (537) Google Scholar). The chlorophyll molecule is composed of the chlorophyllide head group derived from the porphyrin biosynthetic pathway and the phytyl side chain from the isoprenoid pathway. The phytyl chain is linked in an ester bond to the carboxylate group of the chlorophyllide, and it can be hydrolyzed by pheophytin pheophorbide hydrolase or chlorophyll dephytylase 1 during chlorophyll breakdown (2Schelbert S. Aubry S. Burla B. Agne B. Kessler F. Krupinska K. Hörtensteiner S. Pheophytin pheophorbide hydrolase (pheophytinase) is involved in chlorophyll breakdown during leaf senescence in Arabidopsis.Plant Cell. 2009; 21: 767-785Crossref PubMed Scopus (440) Google Scholar, 3Lin Y.-P. Wu M.-C. Charng Y.-Y. Identification of a chlorophyll dephytylase involved in chlorophyll turnover in Arabidopsis.Plant Cell. 2016; 28: 2974-2990Crossref PubMed Scopus (53) Google Scholar). Phytol serves as a precursor for the synthesis of different chloroplast lipids. It can be converted into fatty acid phytyl esters (FAPEs), which accumulate in the plastoglobules of chloroplasts during stress (4Ischebeck T. Zbierzak A.M. Kanwischer M. Dörmann P. A salvage pathway for phytol metabolism in Arabidopsis.J. Biol. Chem. 2006; 281: 2470-2477Abstract Full Text Full Text PDF PubMed Scopus (145) Google Scholar, 5Gaude N. Bréhélin C. Tischendorf G. Kessler F. Dörmann P. Nitrogen deficiency in Arabidopsis affects galactolipid composition and gene expression and results in accumulation of fatty acid phytyl esters.Plant J. 2007; 49: 729-739Crossref PubMed Scopus (156) Google Scholar). Two acyltransferases, PES1 and PES2, are involved in transferring activated fatty acids onto free phytol, thereby producing FAPEs in Arabidopsis (6Lippold F. vom Dorp K. Abraham M. Hölzl G. Wewer V. Lindberg Yilmaz J. Lager I. Montandon C. Besagni C. Kessler F. Stymne S. Dörmann P. Fatty acid phytyl ester synthesis in chloroplasts of Arabidopsis.Plant Cell. 2012; 24: 2001-2014Crossref PubMed Scopus (166) Google Scholar). Alternatively, free phytol can be phosphorylated by phytol kinase (VTE5) yielding phytyl phosphate, which can be further phosphorylated to phytyl diphosphate (phytyl-PP) by VTE6 (7Valentin H.E. Lincoln K. Moshiri F. Jensen P.K. Qi Q. Venkatesh T.V. Karunanandaa B. Baszis S.R. Norris S.R. Savidge B. Gruys K.J. Last R.L. The Arabidopsis vitamin E pathway gene5-1 mutant reveals a critical role for phytol kinase in seed tocopherol biosynthesis.Plant Cell. 2006; 18: 212-224Crossref PubMed Scopus (157) Google Scholar, 8vom Dorp K. Hölzl G. Plohmann C. Eisenhut M. Abraham M. Weber A.P.M. Hanson A.D. Dörmann P. Remobilization of phytol from chlorophyll degradation is essential for tocopherol synthesis and growth of Arabidopsis.Plant Cell. 2015; 27: 2846-2859PubMed Google Scholar). Phytyl-PP is the substrate for the synthesis of tocopherol (vitamin E) and phylloquinone (vitamin K1) (9Collakova E. DellaPenna D. Isolation and functional analysis of homogentisate phytyltransferase from Synechocystis sp PCC 6803 and Arabidopsis.Plant Physiol. 2001; 127: 1113-1124Crossref PubMed Scopus (200) Google Scholar, 10Shimada H. Ohno R. Shibata M. Ikegami I. Onai K. Ohto M.-A. Takamiya K.-I. Inactivation and deficiency of core proteins of photosystems I and II caused by genetical phylloquinone and plastoquinone deficiency but retained lamellar structure in a T-DNA mutant of Arabidopsis.Plant J. 2005; 41: 627-637Crossref PubMed Scopus (61) Google Scholar). Because phytyl-PP derived from phytol phosphorylation is the main source for tocopherol synthesis, the vte5 and vte6 mutants of Arabidopsis are tocopherol deficient. The pathway of phytol degradation in plants is largely unknown. In humans, phytol taken up from the diet is converted into phytenal and phytanoyl-CoA, which is degraded via α- and β-oxidation including the synthesis of the intermediate pristanal, another C19 isoprenoid aldehyde (Fig. 1) J. S. acid metabolism in health and Biophys. Acta. 2011; PubMed Scopus Google Scholar). in that a pathway to the pathway might in plants K. N. The critical role of Arabidopsis during dark-induced Cell. 2005; PubMed Scopus Google Scholar, K. T. I. S. T. N. Identification of the and as alternative catabolism to the chain of Arabidopsis Cell. PubMed Scopus Google Scholar). In phytenal was identified in P. V. of chlorophyll phytyl chain in of higher Scopus Google Scholar). The of phytol into phytenal was to be mediated via P. V. of chlorophyll phytyl chain in of higher Scopus Google Scholar). The analysis of the phytol degradation pathway is by the that phytol catabolites are low abundant and highly The analysis of long-chain aldehydes as and is are to oxidation during P. V. of chlorophyll phytyl chain in of higher Scopus Google Scholar). study phytol metabolism in plants, highly sensitive for quantification of phytenal and other chain aldehydes on GC-MS and were of form Arabidopsis plants revealed that phytenal can be and the most abundant long-chain long-chain including and pristanal, are barely in The of phytenal in and mutant plants of Arabidopsis and stress that phytenal an authentic intermediate of phytol catabolism. in plants are complicated by the that are highly reactive and to can the functional group of thereby the from plant We as the derivatization it aldehydes into of long-chain aldehydes are and can be by GC-MS C. of the acid Identification of as of the of Biophys. PubMed Scopus Google Scholar). The analysis of of and phytenal revealed for and for phytenal (Fig. The of the were and the molecular of of and an to the of the It is known that form that by the of the which is or further from the chain (Fig. T. K. of of via of Chem. Scopus Google Scholar). were identified in the GC-MS for the with the molecular of and an The of can be by the that the phytenal a of derived from the phytol for its synthesis, and each of the to after derivatization (Fig. a from of Arabidopsis was with However, be via GC-MS of the in the We the that as a degradation of phytol, might accumulate during chlorophyll breakdown and plants nitrogen to leaf However, it was to phytenal or other aldehydes after derivatization by In the the from leaf were via on a from leaves, it was to phytenal in plants by GC-MS after derivatization and (Fig. was the long-chain aldehyde in the GC-MS of plants. other or branched-chain aldehydes were of phytenal was using as the the of a known of phytenal was into a leaf and after and by The was as the of phytenal in the leaf in to the after derivatization of the of phytenal in the of the leaf and The was (Fig. The was by quantification of phytenal in independent on different The of phytenal in the by and this was (Fig. the of the GC-MS by different amounts of phytenal to leaf by and quantification by The of phytenal phytenal was in the from to with an of (Fig. The as by the of was in to phytenal other long-chain aldehydes can be in were by of a with was derivatization and each to the were identified in the for the of and phytenal each with large at of and (Fig. increase the even were using a highly sensitive reaction for the derived from the were for and for phytenal (Fig. The was to for other long-chain aldehydes in the that and aldehydes with to including and branched-chain aldehydes derived from or isoprenoid The were derived from the of (Fig. of and The of and that and in with the of the aldehydes and Therefore, and and The aldehydes in each with the as and but the aldehydes from Arabidopsis to nitrogen were by for the of or However, in were observed that the that the long-chain aldehydes pristanal, and be identified in Arabidopsis phytenal accumulates stress Arabidopsis plants were on and to or Chlorophyll was to the stress was with chlorophyll breakdown and phytenal was by GC-MS (Fig. or stress caused a in the chlorophyll with an increase in phytenal. In or stress to large changes in chlorophyll and at the the amounts of phytenal These results that phytenal accumulates during chlorotic stress, by oxidation of phytol which is released by chlorophyll but it increase stress that are with chlorophyll breakdown. the free phytol can be converted into Arabidopsis plants were in the in the of It that phytol can be taken up by Arabidopsis plants and that it can be for the synthesis of FAPEs (6Lippold F. vom Dorp K. Abraham M. Hölzl G. Wewer V. Lindberg Yilmaz J. Lager I. Montandon C. Besagni C. Kessler F. Stymne S. Dörmann P. Fatty acid phytyl ester synthesis in chloroplasts of Arabidopsis.Plant Cell. 2012; 24: 2001-2014Crossref PubMed Scopus (166) Google Scholar). During phytol the of phytenal to amounts the chlorophyll content (Fig. The increase in phytenal during phytol was observed plants were in the a on the of that phytol is to phytenal in the plant in a independent of in to P. V. of chlorophyll phytyl chain in of higher Scopus Google Scholar). the plants were by for at to of the plants in the of phytol in an increase in to a plants. Therefore, the of phytol to phytenal in the plants is in part mediated by oxidation but might be in part to In the further metabolism of phytenal in a were in the of phytol for the plants were further in the of phytol, and phytenal after that the of phytenal was to after that it was presumably by oxidation aldehyde The pao1 mutant of Arabidopsis is in pheophorbide a which pheophorbide the form of chlorophyllide, into chlorophyll G. Aubry S. I. S. T. Kräutler B. Hörtensteiner S. Chlorophyll breakdown in Arabidopsis Characterization of chlorophyll catabolites and of chlorophyll enzymes involved in the Physiol. 2005; PubMed Scopus Google Scholar). As a consequence, chlorophyll in the pao1 mutant is and the plants a (Fig. Dorp K. Hölzl G. Plohmann C. Eisenhut M. Abraham M. Weber A.P.M. Hanson A.D. Dörmann P. Remobilization of phytol from chlorophyll degradation is essential for tocopherol synthesis and growth of Arabidopsis.Plant Cell. 2015; 27: 2846-2859PubMed Google Scholar, G. Aubry S. I. S. T. Kräutler B. Hörtensteiner S. Chlorophyll breakdown in Arabidopsis Characterization of chlorophyll catabolites and of chlorophyll enzymes involved in the Physiol. 2005; PubMed Scopus Google Scholar). of and pao1 were for 1 to senescence (Fig. chlorophyll and phytenal were and chlorophyll amounts with phytenal of the pao1 and the chlorophyll content was phytenal in pao1 mutant in the These results that phytenal is derived from phytol from chlorophyll degradation. study the role of phytenal during phytol Arabidopsis plants were on and and to a It is known that nitrogen chlorophyll breakdown with the of phytol and an increase in tocopherol and FAPEs (6Lippold F. vom Dorp K. Abraham M. Hölzl G. Wewer V. Lindberg Yilmaz J. Lager I. Montandon C. Besagni C. Kessler F. Stymne S. Dörmann P. Fatty acid phytyl ester synthesis in chloroplasts of Arabidopsis.Plant Cell. 2012; 24: 2001-2014Crossref PubMed Scopus (166) Google Scholar, 8vom Dorp K. Hölzl G. Plohmann C. Eisenhut M. Abraham M. Weber A.P.M. Hanson A.D. Dörmann P. Remobilization of phytol from chlorophyll degradation is essential for tocopherol synthesis and growth of Arabidopsis.Plant Cell. 2015; 27: 2846-2859PubMed Google Scholar). were from the for the of chlorophyll, phytol, and phytenal at different The amounts of chlorophyll and phytol the of nitrogen (Fig. the other the amounts of and phytenal during nitrogen and The increase in phytenal was the after of nitrogen However, the of phytenal were low with the amounts of the other that phytenal a of the of a of phytol derived from chlorophyll degradation is in the form of FAPEs and the of phytenal The of metabolites the of nitrogen (Fig. Therefore, most of the phytol which is released from chlorophyll during nitrogen is in the form of or converted into to phytenal. synthesis is by PES1 and Phytol phosphorylation which is mediated by and results in the synthesis of phytyl-PP which is the substrate for tocopherol synthesis (6Lippold F. vom Dorp K. Abraham M. Hölzl G. Wewer V. Lindberg Yilmaz J. Lager I. Montandon C. Besagni C. Kessler F. Stymne S. Dörmann P. Fatty acid phytyl ester synthesis in chloroplasts of Arabidopsis.Plant Cell. 2012; 24: 2001-2014Crossref PubMed Scopus (166) Google Scholar, H.E. Lincoln K. Moshiri F. Jensen P.K. Qi Q. Venkatesh T.V. Karunanandaa B. Baszis S.R. Norris S.R. Savidge B. Gruys K.J. Last R.L. The Arabidopsis vitamin E pathway gene5-1 mutant reveals a critical role for phytol kinase in seed tocopherol biosynthesis.Plant Cell. 2006; 18: 212-224Crossref PubMed Scopus (157) Google Scholar, 8vom Dorp K. Hölzl G. Plohmann C. Eisenhut M. Abraham M. Weber A.P.M. Hanson A.D. Dörmann P. Remobilization of phytol from chlorophyll degradation is essential for tocopherol synthesis and growth of Arabidopsis.Plant Cell. 2015; 27: 2846-2859PubMed Google Scholar). The pathways on phytol that is released from phytenal synthesis with phytol esterification or phytol metabolites were in the pes1 pes2 and in the vte5 mutant plants after nitrogen (Fig. The pes1 pes2 mutant is of of a in the PES1 and (6Lippold F. vom Dorp K. Abraham M. Hölzl G. Wewer V. Lindberg Yilmaz J. Lager I. Montandon C. Besagni C. Kessler F. Stymne S. Dörmann P. Fatty acid phytyl ester synthesis in chloroplasts of Arabidopsis.Plant Cell. 2012; 24: 2001-2014Crossref PubMed Scopus (166) Google Scholar). The vte5 mutant an in the tocopherol content in the of in the phytol kinase (7Valentin H.E. Lincoln K. Moshiri F. Jensen P.K. Qi Q. Venkatesh T.V. Karunanandaa B. Baszis S.R. Norris S.R. Savidge B. Gruys K.J. Last R.L. The Arabidopsis vitamin E pathway gene5-1 mutant reveals a critical role for phytol kinase in seed tocopherol biosynthesis.Plant Cell. 2006; 18: 212-224Crossref PubMed Scopus (157) Google Scholar). of nitrogen the amounts of chlorophyll in vte5 plants were to in the whereas chlorophyll was in pes1 were in the mutant as with the that phytenal synthesis with the esterification and phosphorylation pathways for In the highly sensitive for the of long-chain aldehydes in Arabidopsis long-chain that was whereas other aldehydes were are highly reactive form with amino including amino acids and proteins. Therefore, plant presumably the content of free aldehydes at a low by of aldehyde to toxic with other N. D. in Arabidopsis metabolic and functional 2011; PubMed Scopus Google Scholar). the oxidation of phytol, and it was to be part of the phytol degradation pathway in J. S. acid metabolism in health and Biophys. Acta. 2011; PubMed Scopus Google Scholar, C. of the acid Identification of as of the of Biophys. PubMed Scopus Google (Fig. We the that other long-chain aldehydes as or involved in phytol degradation be in leaf Therefore, with a or a to long-chain aldehydes in leaf However, and were barely in the It is that is an intermediate of phytol to the pathway. free acid is an intermediate of phytol and phytanoyl-CoA, but free was in Arabidopsis plants, that the pathway including and free acid is in plants (Fig. 1) J. S. acid metabolism in health and Biophys. Acta. 2011; PubMed Scopus Google Scholar, K. N. The critical role of Arabidopsis during dark-induced Cell. 2005; PubMed Scopus Google Scholar). the other might be degraded that it accumulate to in Arabidopsis is derived from phytol which in from chlorophyll breakdown. Therefore, phytenal a intermediate of phytol degradation. is on the results that phytenal accumulates during which are with chlorophyll breakdown nitrogen but during that are chlorotic and the pao1 mutant which a accumulates low amounts of phytenal stress (Fig. and phytenal amounts in mutants alternative of phytol metabolites are pes1 (Fig. In this it be that amounts of phytenal after the chlorotic but after senescence stimulated by of plants (Fig. or (Fig. the other a of plants senescence but to an increase in the chlorophyll content (Fig. is in with results that of plants senescence, whereas of senescence is in Arabidopsis leaves, but in Physiol. 2001; 127: PubMed Scopus Google Scholar, K. D. K. C. effects of on pigment composition and I and II in and of 2009; Scopus Google The of phytol or phytenal during chlorophyll breakdown in Arabidopsis with the chlorophyll content (Fig. of nitrogen of chlorophyll was but the of phytol and phytenal In the amounts of tocopherol were FAPEs that most of the phytol derived from chlorophyll breakdown was in the form of Nitrogen a stress phytol is in an intermediate of phytyl esters which is for growth Dorp K. Hölzl G. Plohmann C. Eisenhut M. Abraham M. Weber A.P.M. Hanson A.D. Dörmann P. Remobilization of phytol from chlorophyll degradation is essential for tocopherol synthesis and growth of Arabidopsis.Plant Cell. 2015; 27: 2846-2859PubMed Google Scholar). However, the that the of phytenal are low the that it an authentic intermediate of phytol catabolism. The that the pes1 pes2 or vte5 mutants phytenal nitrogen that free phytol for esterification or phosphorylation can be to phytenal. that of phytol from metabolism via esterification or phosphorylation is important to the of phytenal in the plant cell Phytol to the plants is taken up and can be for synthesis (6Lippold F. vom Dorp K. Abraham M. Hölzl G. Wewer V. Lindberg Yilmaz J. Lager I. Montandon C. Besagni C. Kessler F. Stymne S. Dörmann P. Fatty acid phytyl ester synthesis in chloroplasts of Arabidopsis.Plant Cell. 2012; 24: 2001-2014Crossref PubMed Scopus (166) Google Scholar). We observed a increase in phytenal in plants after phytol that phytol is taken up and in the plants. The increase in phytenal was independent of light as it in (Fig. Therefore, the of phytol into phytenal in plants is mediated via P. V. of chlorophyll phytyl chain in of higher Scopus Google Scholar). the oxidation of phytol to phytenal was observed with plants which were the However, the of phytol into phytenal was after Therefore, a large of phytol is presumably in the plant independently from It be that phytol is by other in the plant for example, the of the oxidation of phytol to phytenal and its further metabolism in the plant to be The Arabidopsis pao1 in chlorophyll vte5-2 in and pes1 pes2 mutants in were (6Lippold F. vom Dorp K. Abraham M. Hölzl G. Wewer V. Lindberg Yilmaz J. Lager I. Montandon C. Besagni C. Kessler F. Stymne S. Dörmann P. Fatty acid phytyl ester synthesis in chloroplasts of Arabidopsis.Plant Cell. 2012; 24: 2001-2014Crossref PubMed Scopus (166) Google Scholar, 8vom Dorp K. Hölzl G. Plohmann C. Eisenhut M. Abraham M. Weber A.P.M. Hanson A.D. Dörmann P. Remobilization of phytol from chlorophyll degradation is essential for tocopherol synthesis and growth of Arabidopsis.Plant Cell. 2015; 27: 2846-2859PubMed Google Scholar, G. Aubry S. I. S. T. Kräutler B. Hörtensteiner S. Chlorophyll breakdown in Arabidopsis Characterization of chlorophyll catabolites and of chlorophyll enzymes involved in the Physiol. 2005; PubMed Scopus Google Scholar). Arabidopsis plants were for on and and to for growth of another T. F. A for growth and with Scopus Google Scholar). were a at and a light of stress the plants on were or stress was by the plants into in the growth salt stress, plants were with stress was by the plants at for 1 each on and The plants were by transferring to a growth at were after the stress nitrogen plants were on with plants were to a with or nitrogen N. Bréhélin C. Tischendorf G. Kessler F. Dörmann P. Nitrogen deficiency in Arabidopsis affects galactolipid composition and gene expression and results in accumulation of fatty acid phytyl esters.Plant J. 2007; 49: 729-739Crossref PubMed Scopus (156) Google Scholar). was from Phytol and was from was by oxidation of phytol with R. C. V. M. analysis of plant long-chain Scopus Google Scholar, H. of and acids in the of Biophys. Acta. PubMed Scopus Google Scholar). a of phytol and a of in was for The reaction was a The reaction was in the and with was from acid as acid ester was by with 1 at for The esters were after of 1 and The was and the ester to with K. T. T. K. oxidation of the isoprenoid Biol. Chem. Scholar). was from by oxidation with as for phytenal. and were from the fatty acids from acid from The fatty acids were converted into esters and to the with and the with as were on with plants were to Phytol and were to of and were for in a in the some were with Chlorophyll was of and for a and with different of the of chlorophyll by Biophys. Acta. Scopus Google Scholar). was by using a and a A.M. Kanwischer M. C. P. I. S. Bréhélin C. Kessler F. Dörmann P. of the tocopherol and metabolic pathways at the J. Scopus Google Scholar). FAPEs were by Dorp K. Hölzl G. Plohmann C. Eisenhut M. Abraham M. Weber A.P.M. Hanson A.D. Dörmann P. Remobilization of phytol from chlorophyll degradation is essential for tocopherol synthesis and growth of Arabidopsis.Plant Cell. 2015; 27: 2846-2859PubMed Google Scholar). phytol was with and by GC-MS using as the Dorp K. Hölzl G. Plohmann C. Eisenhut M. Abraham M. Weber A.P.M. Hanson A.D. Dörmann P. Remobilization of phytol from chlorophyll degradation is essential for tocopherol synthesis and growth of Arabidopsis.Plant Cell. 2015; 27: 2846-2859PubMed Google Scholar). were in nitrogen and with in a the and for and of were C. J. analysis of metabolites in by J. PubMed Google Scholar, J. N. J. metabolite in 2006; PubMed Scopus Google Scholar). were for at and the were with 1 of and the The was a of nitrogen The aldehydes were with in for 1 at C. of the acid Identification of as of the of Biophys. PubMed Scopus Google Scholar). The was the were in 1 of and onto an of The was with 1 of were with of The was a of The were in and to The were with an GC-MS using an with as the at a of The was at the with to for 1 at to with the of the a of phytenal was with a leaf by and quantification by The of phytenal after with the leaf was with the phytenal content of a phytenal the leaf and and the The of the phytenal analytical was by the phytenal in independent quantification on different The of phytenal quantification was by different amounts of phytenal in the of the of the of and The of was for with a of were in the of 1 converted into and by as The were with nitrogen and in were on a II with The was The to was A and The content of was to at and to at were by with a The were in the with of and of V. the were by using the and to a in by with a of V. The was The for the different and branched-chain are in are the The that of with the of this We Hörtensteiner of in for the of the Arabidopsis pao1 P. G. and P. D. P. 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