Journal of Experimental Botany, Vol. 53, No. 376, pp. 1857-1865,
September 1, 2002
© 2002 Oxford University Press
Bleaching herbicide effects on plastids of dark-grown plants: lipid composition of etioplasts in amitrole and norflurazon-treated barley leaves
Received 7 February 2002; Accepted 10 May 2002
1 Dipartimento di Chimica e Biotecnologie Agrarie, Università di Pisa, Via del Borghetto 80, 56124 Pisa, Italy
2 Dipartimento di Biologia, Università di Padova, Via U. Bassi 58/B, 35131 Padova, Italy
Abbreviations: DGDG, digalactosyldiacylglycerol; GL, glycolipids; MGDG, monogalactosyldiacylglycerol; NF, norflurazon, PG, phosphatidylglycerol; PL, phospholipids; PLB, prolamellar body; POR, protochlorophyllide oxidoreductase; SQDG, sulphoquinovosyldiacylglycerol.
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Abstract |
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The effects of the bleaching herbicides amitrole (125 µM) and norflurazon (100 µM) on etioplast lipids were studied in barley plants (Hordeum vulgare L. cv. Express) grown for 7 d either at 20°C or 30°C in darkness. Total lipid, glycolipid and phospholipid contents of control etioplasts were increased at 30°C in comparison with those at 20°C. The two herbicides caused a decrease in the total lipid, glycolipid and phospholipid amounts compared to the untreated etioplasts and lowered the lipid to protein ratio. In the controls, monogalactosyldiacylglycerol (MGDG) and digalactosyldiacylglycerol (DGDG) accounted for about 66 mol% of the etioplast polar lipids, while the remainder was represented by sulphoquinovosyldiacylglycerol (SQDG) and phosphatidylglycerol (PG), in approximately equal proportions. Both amitrole and norflurazon increased MGDG at both temperatures, but decreased DGDG except with norflurazon at 30°C. As a consequence, the MGDG to DGDG molar ratio was higher in the herbicide-treated etioplasts compared to the controls at both the growth temperatures. The amount of the negatively charged polar lipids SQDG and PG were decreased by treatments with amitrole at 20°C and norflurazon at 30°C. The two herbicides determined different responses in the fatty acid unsaturation of the individual polar lipids. Changes in the lipid composition of etioplasts and the interaction between the pigment–protein complex, protochlorophyllide–NADPH–protochlorophyllide oxidoreductase, and polar lipids are discussed.
Key words: Key words: Amitrole, etioplasts, Hordeum vulgare, lipids, norflurazon.
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Introduction |
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Amitrole (2-amino-1,2,4-triazole) and norflurazon [NF, (4-chloro-5-methylamino-2-(3-trifluoromethylphenyl)-pyri dazin-3(2H)one)] are chlorosis-inducing herbicides. Ami trole has two target sites in carotenoid biosynthesis: the desaturation reactions leading from phytoene to lycopene, and the cyclization reactions that lead to the formation of ß-carotene and the xanthophylls (Young, 1991). Norflurazon is a non-competitive inhibitor of phytoene desaturase interrupting the carotenogenic pathway with accumulation of phytoene (Muraja Ljubicic et al., 1999; La Rocca et al., 1998; Sandmann and Albrecht, 1990). Colourless carotenes such as phytoene have short chromophores which cannot protect the plants against photo-oxidation (Jung et al., 2000). Furthermore, phenylpyridazinones, such as NF, exert striking effects on the composition of polar lipids, especially glycolipids (Lem and Williams, 1983). Norflurazon has a specific action on the
15-desaturase present within the plastids, where the enzyme uses both prokaryotic and eukaryotic molecular species of monogalactosyldiacylglycerol (MGDG) as substrates (Abrous et al., 1998; Ohlrogge and Browse, 1995). Some studies have investigated the effect of temperature on bleaching herbicides in plants that are blocked in carotenoid biosynthesis either because of mutations or due to the use of compounds such as amitrole and NF (Dalla Vecchia et al., 2001; Agnolucci et al., 1996; Rascio et al., 1996; Casadoro et al., 1983). In the presence of light amitrole-treated plants of barley and maize grown at 20°C showed a dramatic impairment of carotenogenesis and reduction in the thylakoid system compared with the same plants grown at 30°C (Dalla Vecchia et al., 2001; Agnolucci et al., 1996). This suggested the existence of alternative thermo-modulated steps with different sensitivity to temperature and to the herbicide in the carotenoid biosynthetic pathway. Also, in darkness, barley plants grown at 20°C with amitrole were characterized by carotenoid reduction and extensive disorganization of etioplast ultrastructure (Rascio et al., 1996). The protochlorophyllide oxidoreductase (POR) level did not suffer any change compared with the control, while the amount of protochlorophyllide was greatly increased and the pigment was mainly present in the non-phototransformable state (La Rocca et al., 2001; Rascio et al., 1996). The growth temperature of 30°C caused an increase in the amount of carotenoids and a normalization of the etioplast ultrastructure suggesting that carotenoids might be one of the factors that play a role in the build-up and maintenance of the organization of the etioplast inner membrane system (Rascio et al., 1996).
In a study on the effects of temperature on etioplasts from NF-treated barley leaves (Agnolucci et al., 1994) no differences in the ultrastructure and amount of protochlorophyllide and POR were detected at 20°C, while severe damages to the ultrastructural organization of plastids occurred at 30°C. At both temperatures carotenoid biosynthesis was dramatically affected.
It is known that carotenoid functions are determined by the neighbouring protein and lipid molecules (Vishnevetsky et al., 1999), and that correct organization and functionality of plastids are also due to the structure and properties of the membrane lipid matrix (Gounaris et al., 1986). In order to clarify the role of lipids and their relationship with carotenoids and POR in the complex organization of the etioplast membrane system, the lipid composition of etioplasts in barley leaves treated with amitrole or NF either at 20°C or 30°C was analysed. The knowledge of the effects of amitrole and NF on etioplast lipids at the two different temperatures could help to explain the ultrastructural changes observed in the organelles under these conditions (Agnolucci et al., 1994; Rascio et al., 1996) and to identify a thermo-dependence in the primary mechanism of action of the two herbicides. The results are discussed in relation to the importance of the etioplast lipid composition for the formation of the PLB structure and the correct functionality of the main etioplast protein complex, the protochlorophyllide oxidoreductase.
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Materials and methods |
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Plant material
Grains of barley (Hordeum vulgare L. cv. Express) were germinated and grown in vermiculite on water (control) or on a solution containing 125 µM amitrole or 100 µM NF. All the analyses were performed on 7-d-old seedlings grown in the dark at 20 °C or 30 °C and 80% RH. The analyses were carried out on the first leaf from which the tip and basal regions were cut. All handling of the material was done in dim green light.
Etioplast isolation
First leaves of etiolated seedlings were homogenized according to Ryberg and Sundqvist (1982), but without adding TES [N-tris(hydroxymethyl)methyl-2-aminomethanesulphonic acid]. The isolation medium consisted of 0.5 M sucrose, 1 mM MgCl2, 1 mM EDTA, and 10 mM HEPES-KOH adjusted to pH 7.2. Leaf material (25 g) was homogenized for 5 s in a Waring blender at the highest speed in 230 ml of isolation medium, filtered through four layers of Miracloth and centrifuged at 270 g for 5 min. After discarding the pellet, the supernatant was centrifuged at 1000 g for 10 min. The pellet was resuspended in 35 ml of the isolation medium, centrifuged at 1000 g for 10 min and again suspended in 3–5 ml of the isolation medium. All the operations were performed at 4°C.
Extraction and determination of etioplast proteins
Etioplast proteins were solubilized by incubating the pellets at 100 °C for 5 min in 1 ml TRIS-HCl (pH 6.8) containing 2% (w/v) SDS. Protein amounts were determined according to Bradford (1976), using bovine serum albumin as standard.
Extraction and analysis of etioplast lipids
Etioplast membranes were first boiled in isopropanol for 5 min. Lipids were then extracted with chloroform:methanol (2:1, v/v) containing butylhydroxytoluol as an antioxidant. The combined lipid extracts were washed and separated into neutral lipid, glycolipid (GL) and phospholipid (PL) fractions on Sep-Pak cartridges (Waters) as described by Quartacci et al. (2001). Quantitative analyses of GL and PL were performed as reported earlier (Navari-Izzo et al., 1993) using galactose and KH2PO4 as standards, respectively. All procedures were performed in the presence of silica gel from TLC. The fatty acid methyl ester derivatives were obtained by transmethylation with a mixture containing methanol:benzene:sulphuric acid (100:5:5, by vol.) after heating at 70 °C for 1 h (Douce et al., 1990). A known amount of heptadecanoic acid as an internal standard for quantitative determination was added before transmethylation. The fatty acid methyl esters were analysed by a Dani 86.10 HT chromatograph equipped with a flame ionization detector. A capillary column (i.d.=0.32 mm, length=60 m) with SP 2340 as stationary phase was used. The operating conditions were: column, 175°C; injector and detector, 250°C; split ratio 1:70. Nitrogen was used as the carrier gas with a flux of 0.9 ml min–1.
Statistical analysis
A two-way analysis of variance (ANOVA) was applied to the data in order to evaluate the effect of the chemicals (amitrole and NF), the temperatures (20°C and 30°C) and the interaction between chemicals and temperatures. Comparisons between treatments were performed by the ‘Duncan’s Multiple Range Test’ (DMRT).
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Results |
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The total lipid content of etioplasts of barley leaves (Table 1) was affected by both the growth temperatures and the herbicide treatments. At 30 °C, there was a general increase in the membrane total lipids compared with that observed at 20 °C (+28%, +27% and +74% for control, amitrole and NF, respectively). As regards the herbicides, the most striking effect on total lipids was induced by NF.
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0.001.
The GL and PL contents of etioplasts were influenced by the growth temperatures, the herbicide treatments and their interaction (Table 1). The amount of GL was higher at 30°C than at 20°C, except in the presence of amitrole where no change between the two temperatures was detected. There was a 48% increase in GL at the higher temperature. Amitrole caused a remarkable decrease in GL while NF application had no significant effect.
At both temperatures amitrole caused a remarkable decrease in PL content compared with the controls (–58% at 20°C and –44% at 30°C), whereas NF caused a reduction only at 30°C (–48%). In general, the growth temperature of 30°C determined an increase of 33% in the total amount of PL (Table 1). The amitrole-treated plants showed the highest decrease in PL, independently of the temperature. In fact, the mean values following amitrole and NF treatments were one-half and two-thirds, respectively, compared with the control.
The temperatures, the herbicides and their interaction also had a significant effect on the lipid to protein ratio (Table 1). At 20°C the amitrole and NF treatments lowered the ratio from 3.19 (control) to 2.87 and 2.27, respectively. At 30°C the lipid to protein ratio was affected by a 40% reduction in the presence of amitrole, whereas a 28% increase in the NF-treated samples was observed. Both the herbicides, as well as the higher temperature, lowered the lipid to protein ratio compared with the control.
In the controls, galactolipids (MGDG and DGDG) accounted for about 66 mol% of the etioplast polar lipids (Fig. 1). The growth temperatures, the herbicide treatments and the interaction temperaturexherbicide significantly influenced the levels of both MGDG and DGDG, and their molar ratio (Figs 1A, B, 2). The two different temperatures did not cause any change in the MGDG levels of the controls (Fig. 1A). In the presence of amitrole, MGDG doubled at 20°C and increased by 1.4-fold at 30°C compared with the controls. The amount of MGDG in the NF-treated plants was not influenced by the two growth temperatures. However, compared with the control, the NF treatment determined an increase of about 50% in MGDG at both temperatures. As a consequence of the remarkable increase in MGDG of amitrole-treated etioplasts at 20°C, the mean value at the lower temperature (37.4 mol%) was 1.2-fold higher than that at 30°C (30 .8 mol%). Both the herbicide treatments determined an increase in the MGDG level compared with the control.
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The control etioplasts grown at 30°C showed a very slight increase in DGDG compared with those grown at 20°C (Fig. 1B). At 20°C both the amitrole and NF treatments induced a 30% decrease in this galactolipid. At 30°C DGDG dropped from 43.1 (control) to 22.6 mol% in the presence of amitrole, while NF restored a DGDG amount comparable with the control level. Due to these variations, the herbicide which caused the major decrease in DGDG was amitrole, independently of the growth temperatures.
Compared with the control, at 20°C the MGDG to DGDG molar ratio increased by 2.8-fold following the amitrole treatment and by about 2-fold following NF (Fig. 2). At 30°C amitrole increased the ratio from 0.55 (control) to 1.45, while NF increased the ratio from 0.55 to 0.83. The two-way analysis of variance showed that the increase in the growth temperatures reduced the MGDG to DGDG ratio compared with the control, while the two herbicide treatments raised it.
SQDG and PG were detected in approximately equal proportion of 17 mol% (Fig. 3). These negatively charged lipids were present at about the same level in the etioplasts of the controls grown either at 20°C or 30°C (Fig. 3A, B). The temperatures, the herbicides and their interaction had a significant effect on these lipids. At 20°C the SQDG content of etioplasts from amitrole-treated leaves suffered a 42% reduction compared with the control, whereas plants grown at the same temperature, but in the presence of NF, did not show any change (Fig. 3A). At 30°C amitrole caused a 58% increase in SQDG, by contrast with NF which determined a 35% decrease. At 20°C PG decreased by 1.7-fold following the amitrole treatment, while it did not show any significant difference in the presence of NF, compared with the control (Fig. 3B). By contrast, at 30°C amitrole caused a slight increase (+7%) in PG, while NF determined a 1.8-fold decrease.
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The main fatty acids of MGDG and DGDG were linolenic and palmitic acids, while those of SQDG and PG were palmitic, stearic and oleic acids (Table 2). In addition, PG of barley etioplasts had significant amounts of the unusual trans-
3-hexadecenoic acid. At both temperatures the two herbicide treatments caused different responses in the fatty acid composition of individual PL and GL. At 20°C amitrole caused a 20% decrease in the double bond index (DBI) of MGDG, while the NF treatment did not cause significant differences compared with the control (Table 2). At 20°C either amitrole or NF induced a significant reduction in the DBI of DGDG and SQDG. By contrast, at 20°C the DBI of PG was increased from 0.55 (controls) to 0.74 by the action of NF. At the higher temperature the two galactolipids showed an increase in DBI following the treatment with NF (+77% and +66% for MGDG and DGDG, respectively). Compared with the control, at both temperatures NF determined a higher or not significantly different 18:2/18:3 ratio in all the lipid classes analysed. The increase in temperature lowered the DBI of MGDG and DGDG of control plants, but had no significant effect on the DBI of SQDG and PG (Table 2). At 20°C amitrole determined the disappearance of trans-3-hexadecenoic acid, while at 30°C both herbicides caused its dramatic reduction. The two-way analysis of variance indicated a significant effect of temperatures, herbicides and their interaction upon the DBI, with the exception of temperature in the case of PG.
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Discussion |
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Studies on pigment and protein composition of barley etioplasts treated with inhibitors of carotenogenesis at different temperatures (Agnolucci et al., 1994, 1996; Rascio et al., 1996) led to the conclusion that the membrane lipid moiety plays an essential role in the formation of the paracrystalline PLB structure. Although data on etioplast lipids are scanty, according to Selstam and Widell-Wigge (1993) the lipid composition of etioplast membranes is similar to that of the chloroplast. In these experiments the lipid content of etioplasts (Table 1) and, at least in the untreated leaves, the typical relative proportions among polar lipids were maintained (Figs 1, 2, 3) (Webb and Green, 1991; Gounaris et al., 1986). This agrees with the observation that, in the dark, lipid biosynthesis does not suffer any alteration but only a slowing down of the production (Somerville and Browse, 1991). In the controls, the higher temperature induced a greater production of lipids than at 20°C. The simplest explanation of this fact may lie in the increase of temperature that accelerates the activity of enzymes involved in lipid metabolism (Ohlrogge and Browse, 1995). With regard to the herbicide treatments, the fact that NF determined the more remarkable reductions compared with amitrole at both temperatures may be related to its direct action on lipid biosynthesis (Abrous et al., 1998).
The change in GL and PL proportions at 20°C in the amitrole-treated etioplasts (90 mol% and 10 mol%, respectively) compared to the untreated leaves (83 mol% and 17 mol%) may account, at least in part, for the damage to the ultrastructural organization previously observed at the same temperature (Rascio et al., 1996). The increase in the MGDG to DGDG molar ratio that was also observed at 20°C in etioplasts of amitrole-treated barley (Fig. 2) could partially explain the anomalies observed by Rascio et al. (1996) in the same growth conditions. In their study, amitrole caused dramatic alterations of the plastid inner membrane system, but did not prevent the organization of the PLB tubular membranes. Indeed, the non-bilayer-forming lipid MGDG has been seen to favour the formation of anastomosing tubules of granal thylakoids and PLBs (Webb and Green, 1991; Lindblom and Rilfors, 1989). At 30°C amitrole-treated etioplast ultrastructure was characterized by regularly arranged networks of PLB and prothylakoids, although vesicles were present in the stroma (Rascio et al., 1996). At that temperature, significant changes in GL and PL proportions compared with the control (Figs 1, 3) were not observed, and the MGDG to DGDG ratio was similar to that detected in the presence of amitrole at 20°C (Fig. 2). This may be explained by the assumption that two factors favour the building and stability of the bicontinuous cubic phase in the etioplast inner membranes: the lipid proportions and the high MGDG to DGDG molar ratio (Ryberg et al., 1983).
The maintained GL and PL proportions did not affect the ultrastructural organization of NF-treated etioplasts, which at 20°C did not exhibit apparent alterations compared to the control (Agnolucci et al., 1994). Under the same conditions, this study showed an increase in the MGDG to DGDG molar ratio (Fig. 2), which favours the formation of the typical bicontinuous cubic phase of branched membrane tubules (Selstam and Widell-Wigge, 1993; Lindblom and Rilfors, 1989). On the other hand, at 30°C, when the etioplast membrane system showed extensive ultrastructural alterations (Agnolucci et al., 1994) the MGDG to DGDG molar ratio of NF-treated etioplasts suffered a remarkable reduction in comparison with that at 20°C (Fig. 2).
The molecular bases which determine the formation of the unusual paracrystalline structure of PLBs in darkness are still unknown, although membrane lipids, especially GL, seem to play an essential role in the aggregation of tubular elements in the PLB network (Selstam and Sandelius, 1984; Tönissen and Lütz, 1984; Ryberg et al., 1983). However, there is some evidence that the enzymatic complex protochlorophyllide–NADPH–POR, which catalyses the only known light-requiring step of chlorophyll biosynthesis, may be important for the formation of the PLB structure (Böddi et al., 1989; Ryberg and Sundqvist, 1982). The protein–lipid interactions between the POR complex and membrane lipids are due to the presence of polar regions in their molecular structures (Dahlin et al., 1995). Some structural lipids carry electric charges which confer relative hydrophobicity/hydrophilicity and permit lipid–lipid and lipid–protein interactions in cellular and subcellular structures (Webb and Green, 1991; Gounaris et al., 1986). At physiological pH, both SQDG and PG have a net negative charge, which may interact with the basic protochlorophyllide oxidoreductase in POR complexes, stabilizing the PLB structure. A remarkable reduction in both SQDG and PG in the etioplasts of leaves treated with amitrole at 20°C and with NF at 30°C was observed (Fig. 3A, B). These are the two experimental conditions under which the most relevant alterations of plastids were detected (Agnolucci et al., 1994; Rascio et al., 1996).
Membrane fluidity is regulated by the relative proportion of lipids and proteins, as well as by the length and the unsaturation of fatty acids (Siegenthaler and Trémolières, 1998). Previous studies on the paracrystalline structure of PLBs showed that an enhancement of its molecular order and rigidity stabilizes the whole tubular system (Lindstedt and Liljenberg, 1990; Rascio et al., 1986), even though for PLBs an interpretation of the lipid to protein ratio (Table 1) in terms of fluidity may not be so strictly linked as in other membranes. However, among the herbicide-treated etioplasts an increased lipid to protein ratio and, as a consequence, increased fluidity (Quartacci et al., 2001), was observed, coincident with the altered ultrastructural organization of etioplasts (Table 1).
In the presence of NF at 30°C some unusual inclusions described as large clusters of lightly-stained droplets were observed (Agnolucci et al., 1994). These non-osmiophilic bodies were certainly the indication of degenerative processes, which occur during stress conditions (Quartacci et al., 1997; Navari-Izzo et al., 1989; Rascio et al., 1993). They could be interpreted as lipid-like inclusions, similar to the extra thylakoidal plastoglobuli containing triacylglycerols and lipophilic prenyl quinones observed by Steinmüller and Tevini (1985), in which products of degradation as free fatty acids and diacylglycerols were accumulated as a consequence of stressful treatments (Navari-Izzo et al., 1989).
A high degree of unsaturation increases the MGDG tendency to adopt an hexagonal HII configuration (Selstam et al., 1990). Compared with the control, at 30°C, MGDG of etioplasts from NF-treated plants showed a remarkable increase in DBI due to oleic and linoleic acid accumulation (Table 2). In accordance with lipid molecular shapes, linolenic acid is the fatty acid esterified to MGDG which mainly favours the MGDG ability to form non-bilayer arrangements (Webb and Green, 1991). Thus, in NF-treated etioplasts the reduction at 30°C of the linolenic acid level compared with the one at 20°C could contribute to an explanation of the impairment of etioplast organization in the presence of the herbicide at the higher temperature. In general, the 18:2 to 18:3 ratio of all the lipids analysed was higher in the NF-treated etioplasts, which agrees with the inhibition of the activity of 15–desaturase caused by the herbicide (Abrous et al., 1998). The disappearance or the low amount of the trans-3-hexadecenoic acid following the amitrole and norflurazon treatments at 20°C and 30°C, respectively, could support the role of this fatty acid in grana formation and stabilization during chloroplast biogenesis (Kruse et al., 2000).
In conclusion, the results show that lipid composition plays a major role in determining the characteristic organization of the etioplast inner membrane system. In this context, particularly noteworthy might be the interaction between the pigment–protein complex, proto chlorophyllide–NADPH–POR, and the polar regions of the membrane. As regards the amitrole-treated etioplasts at 20°C, in particular (Rascio et al., 1996), these interactions might influence not only the correct organization of PLBs, but also the activity of the ternary complex, as recently observed by Klement et al. (2000).
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Acknowledgement |
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This study was funded by the University of Pisa (Fondi di Ateneo 2000).
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