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First published online June 26, 2009; 10.1104/pp.109.140491 Plant Physiology 150:1981-1989 (2009) © 2009 American Society of Plant Biologists OPEN ACCESS ARTICLE
Turnover of Fatty Acids during Natural Senescence of Arabidopsis, Brachypodium, and Switchgrass and in Arabidopsis β-Oxidation Mutants1,[C],[W],[OA]Department of Plant Biology, Michigan State University, East Lansing, Michigan 48824 (Z.Y., J.B.O.); and Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China (Z.Y.)
During leaf senescence, macromolecule breakdown occurs and nutrients are translocated to support growth of new vegetative tissues, seeds, or other storage organs. In this study, we determined the fatty acid levels and profiles in Arabidopsis (Arabidopsis thaliana), Brachypodium distachyon, and switchgrass (Panicum virgatum) leaves during natural senescence. In young leaves, fatty acids represent 4% to 5% of dry weight and approximately 10% of the chemical energy content of the leaf tissues. In all three species, fatty acid levels in leaves began to decline at the onset of leaf senescence and progressively decreased as senescence advanced, resulting in a greater than 80% decline in fatty acids on a dry weight basis. During senescence, Arabidopsis leaves lost 1.6% of fatty acids per day at a rate of 2.1 µg per leaf (0.6 µg mg–1 dry weight). Triacylglycerol levels remained less than 1% of total lipids at all stages. In contrast to glycerolipids, aliphatic surface waxes of Arabidopsis leaves were much more stable, showing only minor reduction during senescence. We also examined three Arabidopsis mutants, acx1acx2, lacs6lacs7, and kat2, which are blocked in enzyme activities of β-oxidation and are defective in lipid mobilization during seed germination. In each case, no major differences in the fatty acid contents of leaves were observed between these mutants and the wild type, indicating that several mutations in β-oxidation that cause reduced breakdown of reserve oil in seeds do not substantially reduce the degradation of fatty acids during leaf senescence.
Leaf senescence is considered the last stage of leaf development that leads to leaf death (Lim et al., 2007  ). During senescence, the catabolism of macromolecules such as proteins, carbohydrates, lipids, and nucleic acids becomes predominant in leaves, while anabolic activities are strongly decreased, with some even lost. But leaf senescence is not just a passive degradation process, since senescence is also a way to remobilize nutrients from old and photosynthetically less efficient leaves to new vegetative tissues, developing seeds, or storage organs (Himelblau and Amasino, 2001; Lim et al., 2007). In addition to age, leaf senescence can also be induced by many biotic and abiotic factors, including darkness, extreme temperature, drought, and nutrient deficiency. Plant hormones also affect leaf senescence. For example, ethylene, abscisic acid, jasmonate, salicylic acid, and sugar promote senescence, whereas cytokinins, auxin, and gibberellins delay senescence (Gan and Amasino, 1997).
Membrane degradation is one of the early and major manifestations of leaf senescence (Thompson et al., 1998
Many lipid-degrading enzymes are involved in the degradation of membrane lipids. A transcriptome study of Arabidopsis leaves revealed that 2,491 senescence-associated genes, based on analysis of 6,200 senescence-associated ESTs, were up-regulated during senescence (Guo et al., 2004
Most previous studies of lipid changes during leaf senescence have been short term or have used hormones or other treatments to induce senescence. In this study, we characterized fatty acid changes in leaves during natural senescence over the life cycle of Arabidopsis, Brachypodium, and switchgrass (Panicum virgatum). Young leaves have approximately 5% lipids by dry weight. Because a typical lipid has 2 times more energy per weight than carbohydrates or protein, lipids can represent 10% of the energy content of the leaves. If high-energy lipids could be retained in leaves while proteins, carbohydrates, and nucleic acids were mobilized, it can be estimated that the energy content of leaves could be increased approximately 20%. Therefore, an additional rationale behind this study was to test the possibility of preventing the breakdown of fatty acids during leaf senescence by mutations of β-oxidation, so that the energy content of plant leaves at harvest might be increased. To this end, we examined three Arabidopsis β-oxidation mutants, acx1acx2 (ecotype Columbia [Col-0] background; Adham et al., 2005
Breakdown of Fatty Acids in Arabidopsis Leaves during Senescence
Phenotype of Arabidopsis Leaves at Different Ages Figure 1 shows the typical rosette leaves of Arabidopsis at varying developmental stages, in which the changing appearance of the leaves can be easily observed. Leaf yellowing is a typically visible symptom of leaf senescence, caused mainly by chlorophyll turnover, and is considered a signal of the early disintegration of the photosynthetic machinery. Age-dependent changes in chlorophyll content of Arabidopsis leaves during growth and senescence are shown in Figure 2. Leaves from 25 to 51 d after planting retained similar high levels of chlorophyll, with an average value of 1.6 mg g–1 fresh weight. Thereafter, from day 57 onward, the amount of leaf chlorophyll began to decline, until at the end of senescence the leaves contained only 6% of the maximum chlorophyll content.
In the life cycle of the plants, the leaf weight also varied with time. During leaf development, the dry weight on a per leaf basis initially increased continually to a maximum value of 3.7 mg at 65 d. Subsequently, leaf weight decreased gradually to the end of senescence, at which time leaves abscised off the plant.
Fatty Acid Changes in Arabidopsis Leaves during Growth and Senescence
The relative contents (mol %) of 16:0 and 18:3 are given in the inset of Figure 3, which indicates a decline in the percentage of 18:3 and a relative increase in 16:0 with increased senescence. At late senescence, 16:0 became the most abundant fatty acid in leaves, nearly reaching 40% of the total fatty acids. Accordingly, these changes resulted in a decrease in the ratio of unsaturated to saturated fatty acids of leaves during senescence (data not shown).
As shown in Figure 4,
the total fatty acid content, expressed on leaf dry weight, had a maximum level of about 40 µg mg–1 dry weight in the 31- to 51-d period, the stage having the highest growth rate. After that phase, fatty acids decreased abruptly. At the end of senescence (104 d), fatty acid content was only 7 µg mg–1 dry weight. The contents of total fatty acids were reduced by 83%, and the average rate of fatty acid turnover was 0.6 µg mg–1 dry weight d–1 during senescence, corresponding to a loss of 1.6% of leaf fatty acids per day. The rate of fatty acid turnover in senescing leaf is much slower than the rates of fatty acid and TAG breakdown in geminating seeds (see inset of Fig. 4). During germination, between day 0 and day 5, seeds lost 14% of all fatty acids per day at a rate of 50 µg mg–1 dry weight and 11% of eicosenoic acid (20:1), which is considered representative of TAG in Arabidopsis seeds (Germain et al., 2001
When expressed on a per leaf basis (Supplemental Fig. S1A), it appears that leaf experienced two phases of fatty acid changes. Up to day 51, fatty acid in leaves increased with growth time. The net rate of synthesis of fatty acids was 4.0 µg per leaf per day (1.5 x 10–2 µmol fatty acid per leaf per day), equal to a value of about 0.16 µmol carbon mg–1 chlorophyll h–1. This value is severalfold lower than maximum rates obtained by short-term isotope labeling of very young Arabidopsis leaves (Bao et al., 2000 ; Bonaventure et al., 2004). After senescence began, the net rate of fatty acid breakdown was found to be 2.1 µg per leaf per day, or approximately half the rate of synthesis that occurred during leaf expansion. We also determined the fatty acid contents on a leaf area (cm2) basis (Supplemental Fig. S1B). The results showed that during leaf expansion (days 33–53), there is a slight increase in the fatty acid per area of leaves until an inflection point at day 53, where the fatty acid level is highest with a value of 43 µg cm–2 leaf area. During this period of fatty acid gain, the mean rate of fatty acid synthesis based on leaf area is 0.11 µg fatty acid cm–2 per day. After this stage, the content of fatty acids decreased, leading to a loss of approximately 30% in fatty acids at the end of senescence. The mean rate of fatty acid breakdown is 0.33 µg fatty acid cm–2 per day. In sharp contrast to the glycerolipids, the chloroform-soluble aliphatic surface lipids in Arabidopsis leaves remained comparatively constant during the plant life cycle (Supplemental Fig. S2). For example, the wax levels in Arabidopsis leaves at 26, 50, and 77d were found to be 1.7, 1.3, and 1.3 µg mg–1 dry weight, respectively. Therefore, the soluble aliphatic surface lipids became an increasing proportion of total leaf lipids, increasing from about 4% at 26 d to 9% at 77 d.
Fatty Acid Changes in Brachypodium and Switchgrass Leaves during Senescence In Brachypodium leaves, 18:3 is the most abundant fatty acid, followed by 16:0 and 18:2 in this order (data not shown). At leaf maturity (days 58–105), 18:3 reached 70% of total fatty acids, higher than its counterpart in Arabidopsis leaves, in which the content of 18:3 is not more than 60%. Another notable difference between Brachypodium and Arabidopsis is that Brachypodium has no detectable 16:3 in leaves, which reflects that the biosynthesis of plastidial lipids follows a eukaryotic pathway; consequently, Brachypodium, like other grasses, is a "C18:3" plant. The maximal content of total fatty acids in Brachypodium leaves is around 40 µg mg–1 dry weight, very close to the counterpart level in Arabidopsis leaves. During the growth time of 37 to 96 d, the levels of total fatty acids in leaves generally increased (Fig. 5). After that, the fatty acids in leaves declined with time. At day 139, the fatty acid level dropped to only 20% of that at day 96. The degradation rate of fatty acids in Brachypodium leaves was about 0.70 µg mg–1 dry weight per day on average, corresponding to 1.9%, similar to the values observed in Arabidopsis leaves (Fig. 5).
Like Brachypodium, switchgrass is also a C18:3 plant, since no C16:3 was found in leaves (data not shown). On a dry weight basis, the maximum amount of fatty acids in switchgrass leaves is around 55 µg mg–1 dry weight, higher than in Arabidopsis and Brachypodium (Fig. 5). Senescence also caused a reduction of fatty acids in switchgrass leaves. After day 60, the total fatty acids in the grass leaves began to drop. At the late senescence stage of 121 d, the leaves had lost 80% of fatty acids, to 10.6 µg mg–1 dry weight. The average degradation rate of fatty acids was about 0.69 µg mg–1 dry weight per day, close to those of Arabidopsis and Brachypodium.
TAG Levels in Plant Leaves
Figure 6
shows the TLC of neutral lipid extracts from plant leaves of Arabidopsis (Col-0; 58 d) Brachypodium (58 d), switchgrass (58 d), and crabapple (2 and 20 weeks old). All of these leaves were freeze dried for 24 h and are of the same dry weight (10 mg). As can be seen from Figure 6, although lipids from equal dry weight of leaves were applied, the size and intensity of TAG bands on the TLC plate varied with plant species, suggesting varying concentrations of TAG in different plant leaves. Particularly in older leaves, based on iodine staining, bands with greater abundance than TAG comigrated with a wax ester standard. These were not further identified but may be sterol esters or phytol esters (Hugly et al., 1990
To provide definitive identification of TAG, neutral lipid extracts of leaves were analyzed by ESI-MS (Supplemental Fig. S3). We found that the TAG levels in dry leaves of 58-d Arabidopsis were 0.12 µg mg–1 dry weight, a little higher than Brachypodium leaves (0.08 µg mg–1 dry weight) but much lower than switchgrass leaves (0.76 µg mg–1 dry weight). TAG fatty acid equivalents in these plant leaves were only 0.35%, 0.19%, and 1.23% of the corresponding total fatty acids (determined by GC) for Arabidopsis, Brachypodium, and switchgrass, respectively. The TAG content determined by ESI-MS in dry leaves of 20-week-old crabapple was about 1.3 µg mg–1 dry weight. This value is similar to that determined by GC, where the TAG content is 1.8 µg mg–1 dry weight. For 2-week-old crabapple, the TAG content determined by ESI-MS is 1.4 µg mg–1 dry weight in dry leaves. In addition, a low amount of TAG was observed to accumulate in 20-week-old Cirsium vulgare leaves, with only 0.12 µg mg–1 dry weight. For Arabidopsis, TAG levels in leaves were very low at all stages, not more than 0.5 µg mg–1 dry weight (Supplemental Fig. S4). Even in senescent leaves, TAG contents remained less than 1% of total lipids (see inset of Supplemental Fig. S4).
It is well established that β-oxidation is critical in the turnover of storage oil and that the supply of carbon and energy from β-oxidation of fatty acid in peroxisomes is essential for seed germination and early postgermination growth. However, although it has been suggested that β-oxidation plays a general housekeeping role in lipid catabolism throughout the plant life cycle (Graham and Eastmond, 2002 We used three β-oxidation mutants, acx1acx2, lacs6lacs7, and kat2, to test the influence of β-oxidation on the breakdown of fatty acids during leaf senescence. The activities of the peroxisomal enzymes long-chain acyl-CoA synthetase in lacs6lacs7, acyl-CoA oxidase in acx1acx2, and ketoacyl thiolase in kat2 are defective, which results in an almost complete lack of storage TAG mobilization during seedling growth. Our results showed that blocking β-oxidation in the double mutants acx1acx2 and lacs6lacs7 and the single mutant kat2 had almost no effect on the breakdown of fatty acids during leaf senescence, as indicated in Figure 7. In leaves of various ages, the levels of fatty acids in these β-oxidation mutants were not substantially different from those in the wild type. For example, the lacs6lacs7 mutant in the Ws background showed a similar rate of fatty acid degradation to the wild type. In the 28-d period of leaf senescence, lacs6lacs7 was decreased by 45% in the amount of fatty acids, comparable to the changes in the wild type that lost 49% of fatty acids.
Fatty acid catabolism is best characterized as a major metabolic pathway during seed germination and seedling growth (Graham, 2008 ), but it is also active throughout the plant life cycle. Although a less predominant metabolic flux during plant senescence, fatty acid degradation is an important metabolism, since it can mobilize carbon stored in leaves for utilization during seed filling and can eliminate deteriorative effects of free fatty acids released from lipid turnover (Gerhardt, 1992).
In this investigation, we systematically studied the fatty acid profiles of Arabidopsis, Brachypodium, and switchgrass leaves during natural senescence. Although similar results with other plants have been presented in earlier studies (Hirayama and Oido, 1969
Our results revealed that during their senescence (days 51–104), Arabidopsis leaves lost about 1.6% of fatty acids every day, resulting in 83% lower fatty acid contents per dry weight at the end of senescence. In the same plants, a 94% loss of chlorophyll was observed; thus, the degradation rate of chlorophyll was approximately 1.8% per day. In a previous study, it was reported that during leaf senescence, nitrogen was decreased by 85.4% over a period of 10 d (Himelblau and Amasino, 2001
During seed germination, the rate of fatty acid breakdown in seeds is 50 µg dry weight d–1 (inset of Fig. 4). Thus, during leaf senescence, the rate of fatty acid turnover is approximately 80-fold lower on a dry weight basis than fatty acid breakdown during seed germination. These large differences in fluxes are consistent with the level of expression of genes during seedling growth and in leaves (Graham, 2008
Among the major fatty acid classes, 18:3 showed the largest decline and 16:0 showed the least (Fig. 3). The ratio of unsaturated to saturated fatty acids at the end of senescence was only 1.5, much lower than the value of 6 during leaf expansion. Thus, there is a preferential degeneration of unsaturated fatty acids in the senescing leaves. Although in part this likely reflects the earlier degradation of the highly unsaturated plastid galactolipids (Fong and Heath, 1977
The importance of fatty acid β-oxidation for seed germination and postgerminative growth has been demonstrated in many β-oxidation mutants (Graham, 2008
However, our results have shown that the breakdown of total fatty acids as well as each fatty acid class (data not shown) still occurred in β-oxidation mutants of acx1acx2, lacs6lacs7, and kat2 during leaf senescence. There was no substantial reduction in loss of fatty acids in Arabidopsis senescent leaves compared with the wild type, although the activities of ACX1, ACX2, LACS6, LACS7, and KAT2 were inhibited in the mutants. ACX1 exhibits medium- to long-chain activity ranging from C12:0 and C16:0 (Hooks et al., 1999
Although previous studies have reported substantial accumulation of TAG in senescent leaves (Kaup et al., 2002
The soluble aliphatic surface lipids of Arabidopsis proved much more stable during senescence than the membrane fatty acids. To our knowledge, this is the first study to compare the turnover of both membrane and surface lipids. The greater stability of the extracellular and predominantly saturated structures is not surprising, but it highlights the fact that one strategy to increase the energy content of biofuel crops might be to enhance surface lipid production. This has been achieved in principle by different transgenic strategies (Broun et al., 2004
Plant Materials and Growth Conditions Seeds of wild-type and β-oxidation mutants of Arabidopsis (Arabidopsis thaliana ecotypes Col-0 and Ws) were surface sterilized for 20 min in 20% (v/v) bleach and 0.5% Triton X-100 and rinsed at least four times with excess sterile water. Seeds were then sown on plates containing Murashige and Skoog medium, 1% Suc, and 1.2% agar (pH 5.6). After preincubation for 3 d in the dark at 4°C, plates containing seeds were placed into an environmentally controlled growth chamber at 22°C, 40% to 60% relative humidity, with a 16-h-light/8-h-dark cycle with moderate light intensity (80–100 µmol m–2 s–1). After 10 to 15 d, wild-type and mutant seedlings were transplanted to soil containing a mixture of vermiculite:peat moss:perlite (1:1:1). The growth conditions for Brachypodium distachyon and switchgrass (Panicum virgatum) on the same soil were 20-h-light/4-h-dark photoperiod, 24°C during the day and 18°C at night, 40% to 60% relative humidity, with cool-white fluorescent lighting at a level of 150 µE m–2 s–1. Plants were watered once per week with nutrient solution [5 mM KNO3, 2.5 mM KPO4, 2.0 mM MgSO4, 2.0 mM Ca(NO3)2, 50 µM Fe-EDTA, 70 µM boric acid, 14 µM MnCl2, 0.5 µM CuSO4, 1 µM ZnSO4, 0.2 µM Na2MoO4, 10 µM NaCl, and 0.01 µM CoCl2, pH 6.5].
The rosette leaves of Arabidopsis are numbered from the bottom (Guo and Gan, 2006
Direct transmethylation of fatty acids into fatty acid methyl esters for GC analysis was performed according to the modified method of Browse et al. (1986)
Lipid extractions followed the method of Hara and Radin (1978)
TAG, free fatty acid, and diacylglycerol were separated on silica gel G plates (20 x 20 cm K6 silica, 60 Å plates; Whatman) using hexane:diethylether:acetic acid (70:30:1, v/v/v; Mangold, 1961 Individual lipid bands were scraped off the TLC plate and eluted with chloroform:methanol (2:1, v/v). The eluate was evaporated to dryness under N2, and the lipids were stored in toluene at –20°C prior to GC or ESI-MS analysis.
Neutral lipids were separated from total lipids by liquid column chromatography. A short column (approximately 7 cm in length) of silica gel was prepared from 1 g of silica acid (100–200 mesh) in a glass disposable Pasteur pipette (22.3 cm length x 0.6 cm i.d.) plugged with solvent-washed glass wool. The column was conditioned by elution with 5 mL of chloroform, after which the lipid samples were applied to the top of the column. Samples were eluted with 10 mL of chloroform, and neutral lipid fractions were collected and dried under nitrogen. Before analysis by ESI-MS, tritridecanoin (triC13:0) was added as an internal standard to the resulting neutral lipid samples. Then, 1 µL of the samples was directly injected into the ESI source. ESI-MS experiments were conducted with a Micromass Quattro LCZ quadrupole mass spectrometer. In MS mode, fragmentation was achieved by introducing argon into the reaction chamber in front of the second quadrupole.
Leaves were dipped in chloroform (20 mL) for 30 s twice. n-Octacosane, docosanoic acid, and 1-tricosanol (20 µg each) were added as internal standards. After removal of chloroform under nitrogen, the resulting waxes were silylated to convert free alcohols and carboxylic acids to their trimethylsilyl ethers and esters, respectively, by heating the sample at 110°C for 10 min in medium of 100 µL of pyridine and 100 µL of bis(trimethylsilyl)-trifluoroacetamide. After cooling, the solvent was evaporated under nitrogen and the product was resuspended in mixed solvent of heptane:toluene (1:1, v/v) for GC-MS analysis (Li et al., 2007
Fresh leaves were weighed and then ground in liquid nitrogen using a mortar and pestle. The pulverized leaf tissue was added to 80% acetone (0.1 mL mg–1 leaf tissue), vortexed, and incubated for 30 min in the dark at room temperature. The solution was vortexed and centrifuged (3,000g, 10 min), and the absorbance of the supernatant was measured at 663 and 645 nm to determine chlorophyll based on fresh weight (Lichtenthaler and Wellburn, 1983
The following materials are available in the online version of this article.
We are grateful to Professors John Browse (Washington State University), Bethany Zolman (University of Missouri), and Steven Footitt (University of Warwick) for their gifts of β-oxidation mutants lacs6lacs7, acx1acx2, and kat2, respectively. We thank John Sedbrook (Illinois State University) for providing seeds of Brachypodium and David Oliver (Iowa State University) for kind donation of leaf samples of crabapple and Cirsium vulgare. We are deeply indebted to Timothy P. Durrett (Michigan State University) for assistance with the ESI-MS experiments and to Mike Pollard (Michigan State University) for advice and help with GC and GC-MS analysis. We also thank Kurt Thelen and Stephanie Smith (Michigan State University) for providing us with switchgrass seeds and Iqbal Munir (Michigan State University) for testing methods to assay fatty acid oxidation. Received April 27, 2009; accepted June 22, 2009; published June 26, 2009.
1 This work was supported by the Great Lakes Bioenergy Research Center through the U.S. Department of Energy (Cooperative Agreement no. DE–FC02–07ER64494).  The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: John B. Ohlrogge (ohlrogge{at}msu.edu).
[C] Some figures in this article are displayed in color online but in black and white in the print edition.
[W] The online version of this article contains Web-only data.
[OA] Open Access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.109.140491 * Corresponding author; e-mail ohlrogge{at}msu.edu.
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