Plant and Cell Physiology

Li, Hsou-min;Yu, Chun-Wei

2018 Plant and Cell Physiology

doi: 10.1093/pcp/pcy088pmid: 29727004

Abstract Monogalactosyldiacylglycerol (MGDG) and digalactosyldiacylglycerol (DGDG) together constitute approximately 80% of chloroplast lipids. Apart from facilitating the photosynthesis light reaction in the thylakoid membrane, these two lipids are important for maintaining chloroplast morphology and for plant survival under abiotic stresses such as phosphate starvation and freezing. Recently it was shown that severe growth retardation phenotypes of the DGDG-deficient mutant dgd1 were due to jasmonate overproduction, linking MGDG and DGDG homeostasis with phytohormone production and suggesting MGDG as a major substrate for jasmonate biosynthesis. Induction of jasmonate synthesis and jasmonic acid (JA) signaling was also observed under conditions of phosphate starvation. We hypothesize that when DGDG is recruited to substitute for phospholipids in extraplastidic membranes during phosphate deficiency, the altered MGDG to DGDG ratio in the chloroplast envelope triggers the conversion of galactolipids into jasmonates. The conversion may contribute to rebalancing the MGDG to DGDG ratio rapidly to maintain chloroplast shape, and jasmonate production can reduce the growth rate and enhance predator deterrence. We also hypothesize that other conditions, such as suppression of dgd1 phenotypes by trigalactosyldiacylglycerol (tgd) mutations, may all be linked to altered jasmonate production, indicating that caution should be exercised when interpreting phenotypes caused by conditions that may alter the MGDG to DGDG ratio at the chloroplast envelope. Introduction The major lipid constituents of the chloroplast membrane are two galactolipids, monogalactosyldiacylglycerol (MGDG) and digalactosyldiacylglycerol (DGDG), which possess one or two galactose residues as the headgroup, an 18-carbon unsaturated fatty acyl chain at the sn-1 position and an 18-carbon or 16-carbon unsaturated acyl chain at the sn-2 position (Fig. 1). In Arabidopsis, the enzyme MGDG synthase1 (MGD1) transfers a galactose from UDP-galactose to diacylglycerol (DAG) to produce MGDG (Jarvis et al. 2000), which is further converted to DGDG through the addition of a second galactose by the enzyme DGDG synthase1 (DGD1) (Dörmann et al. 1995) (Fig. 2). Under normal growth conditions, MGDG and DGDG are exclusively present in chloroplasts. This special lipid composition is inherited from the cyanobacterial ancestor of chloroplasts and is preserved in all oxygenic photosynthetic membranes, from cyanobacteria to plants. Aspects of galactolipid biosynthesis, regulation, evolution and transport have been comprehensively reviewed elsewhere (Moellering and Benning 2011, Dörmann 2012, Nakamura et al. 2012, Block and Jouhet 2015, Kobayashi and Wada 2016, Sato and Awai 2016). This review highlights the large array of functions these two lipids assume. As a result of their multiple functions, they provide direct biochemical links between photosynthesis, chloroplast shape maintenance, jasmonate synthesis, phosphate starvation responses, freezing tolerance and probably other reactions. Fig. 1 View largeDownload slide Structure and predicted shape and packing phase of MGDG and DGDG. R1 and R2 represent the hydrocarbon chains of fatty acids at the sn-1 and sn-2 positions, respectively. Fig. 1 View largeDownload slide Structure and predicted shape and packing phase of MGDG and DGDG. R1 and R2 represent the hydrocarbon chains of fatty acids at the sn-1 and sn-2 positions, respectively. Fig. 2 View largeDownload slide Multiple functions of MGDG and DGDG. Biosynthesis pathways for MGDG and DGDG, the enzymes responsible, and their subcellular localizations are drawn. Functions of lipids at various locations are indicated with red arrows. Fig. 2 View largeDownload slide Multiple functions of MGDG and DGDG. Biosynthesis pathways for MGDG and DGDG, the enzymes responsible, and their subcellular localizations are drawn. Functions of lipids at various locations are indicated with red arrows. Galactolipids in Photosynthesis Apart from MGDG and DGDG being the major constituents of the thylakoid membranes housing the photosynthesis light reaction electron transport chain, crystallography has also shown that MGDG is present in both PSI and PSII, and in the Cyt b6f complex, and that DGDG is present in PSII (Picot et al. 1994, Stroebel et al. 2003, Guskov et al. 2009). Both galactolipids are important for various aspects of the photosynthesis light reaction (reviewed in Boudière et al. 2014, Kobayashi and Wada 2016, Kobayashi et al. 2016). Knockout mutations in Arabidopsis MGD1 cause embryonic lethality, and knockdown of MGD1 by microRNA or by a chemical inhibitor results in albino or extremely pale seedlings with severe defects in chloroplast and leaf development, most probably due to MGDG’s function in supporting photosynthesis and thylakoid development (Jarvis et al. 2000, Kobayashi et al. 2007, Botté et al. 2011, Fujii et al. 2014). DGD1-knockout mutants exhibit a small reduction in photosynthesis that can be directly attributed to DGDG deficiency (Dörmann et al. 1995, Hölzl et al. 2006, Hölzl et al. 2009, Lin et al. 2016). Thylakoid membranes could be considered the most abundant membranes in nature. To facilitate the production of massive amounts of membrane for oxygenic photosynthesis, a change from phospholipids to glyceroglycolipids may have endowed cyanobacteria with an evolutionary advantage since phosphate is more likely to be limited. Why the galactose headgroup is exclusively used in photosynthetic membranes is not clear. Chloroplasts and cyanobacteria also seem to differ in whether the galactose headgroup can be substituted by glucose. In Arabidopsis, accumulation of glucosylgalactosyldiacylglycerol in DGDG-deficient mutants restored trimerization of the light-harvesting complex of PSII (LHC-II), but the PSII quantum yield was not fully restored (Hölzl et al. 2006, Hölzl et al. 2009). However, in Synechocystis sp. PCC 6803, a mutant with only monoglucosyldiacylglycerol (MGlcDG) and no MGDG or DGDG, due to a mutation in the epimerase converting MGlcDG to MGDG, is almost normal in photosynthesis (Awai et al. 2014). Galactolipids in Chloroplast Morphology Biological membranes are usually organized as lipid bilayers, but many of the lipids found in biological membranes are known to prefer to adopt a non-bilayer phase. The galactose headgroup and the two unsaturated fatty acyl chains of MGDG give the lipid a cone shape, so MGDG can pack into inverted micelles—the so-called hexagonal HII structure (Jouhet 2013) (Fig. 1A). Nonetheless, LHC-II associates with MGDG (Kuhlbrandt et al. 1994), and the three hydrophobic transmembrane α-helices of LHC-II force MGDG to adopt a bilayer structure (Simidjiev et al. 2000). In contrast, the headgroup of DGDG is larger than that of MGDG and, together with the two unsaturated fatty acyl chains, DGDG exhibits a cylindrical shape (Fig. 1B) and only forms bilayers (Sen et al. 1981, Lee 2000). Both MGDG and DGDG are considered to be important for the stacking of the thylakoid membrane bilayers to form grana (Simidjiev et al. 2000, Deme et al. 2014). Hence, the amounts of non-bilayer-forming MGDG and bilayer-forming DGDG and/or the ratio between these two lipids, as well as the ratio of these two lipids to thylakoid membrane proteins, most probably play a critical role in controlling chloroplast membrane morphology (Murphy 1982, Deme et al. 2014). Indeed, it has been shown that reduced MGDG, both in an Arabidopsis MGD1-knockdown mutant caused by T-DNA insertion and in a transgenic tobacco line with post-transcriptional gene silencing of the tobacco MGD1 gene, leads to altered thylakoid architecture (Jarvis et al. 2000, Wu et al. 2013). Recent studies have also revealed that, under electron microscopy, chloroplasts in Arabidopsis transgenic lines with a severely reduced amount of MGDG had oval or flattened shapes, differing from the lens-shaped chloroplasts of wild-type plants (Fujii et al. 2014). However, these altered chloroplast shapes could be the result of severely reduced thylakoid developement in the mutant plants. In Arabidopsis dgd1 mutants with severely reduced DGDG content and highly elevated MGDG to DGDG ratios, chloroplast thylakoid membranes were highly curved and the envelope membranes were much more rounded, resulting in balloon-like chloroplasts with large thylakoid-free stromal areas (Dörmann et al. 1995). The ‘balloon-like chloroplast’ phenotype was rescued by expressing a bacterial glycosyltransferase in the mutant plants to produce sufficient amounts of glucosylgalactosyldiacylglycerol to substitute for DGDG (Hölzl et al. 2006, Hölzl et al. 2009). This finding suggests that adequate amounts of lipids with a similar headgroup size, and not strictly DGDG itself, is sufficient to restore chloroplast membrane morphology. MGDG as a Major Substrate for Jasmonate Biosynthesis Jasmonic acid (JA) is an important phytohormone in many aspects of plant development and stress responses, for example pollen maturation and defense against insect attacks (Wasternack and Song 2017). JA and its derivatives, collectively called jasmonates, are lipid-derived signaling compounds. During stresses, the 18:3 or 16:3 fatty acids from chloroplast membrane lipids are sequentially metabolized by lipoxygenase, allene oxide synthase (AOS) and allene oxide cyclase into 12-oxo-phytodienoic acid (OPDA) or dinor-12-oxo-phytodienoic acid (dnOPDA), respectively. OPDA and dnOPDA are exported from chloroplasts into peroxisomes for further steps of JA biosynthesis (Feussner and Wasternack 2002, Wasternack and Hause 2013). In Arabidopsis, OPDA and dnOPDA can be directly esterified in the sn-1 and/or sn-2 position of MGDG and DGDG, producing arabidopsides (Stelmach et al. 2001, Mosblech et al. 2009, Acosta and Farmer 2010,, Wasternack and Hause 2013). MGDG seems to be the primary substrate for arabidopside production because high levels of arabidopsides, in particular those synthesized from MGDG, are produced upon wounding (Ibrahim et al. 2011, Nilsson et al. 2012, Vu et al. 2012). However, the exact lipid source for free OPDA synthesis has not been clearly demonstrated since the lipase(s) for producing the fatty acid substrates remain enigmatic. There seem to be redundant but also stimuli- and pathway-specific lipases to generate fatty acid substrates for JA production (Ellinger et al. 2010, Wasternack and Song 2017). The lipase DEFECTIVE IN ANTHER DEHISCENCE1 (DAD1) is required for male fertility, but displays a 4-fold higher substrate preference for phosphatidylcholine over MGDG (Ishiguro et al. 2001). Overexpression of the lipase DONGLE (DGL) results in JA overproduction in leaves (Hyun et al. 2008), but DGL shows much higher activity toward DGDG than toward MGDG (Hyun et al. 2008, Seo et al. 2009) and it is localized in the cytosol (Ellinger et al. 2010). It was recently found that the visible phenotypes of dgd1 mutants are caused by JA overproduction (Lin et al. 2016). Elevated levels of jasmonates were observed in the dgd1 mutants. Disrupting JA production or signaling in the dgd1 mutants by knockout mutations in the AOS enzyme or in the JA receptor CORONATINE INSENSITIVE1 (COI1) fully eradicated the dgd1 mutant growth phenotypes, including short inflorescence stems and petioles, lignification of phloem-cap cells and ruffled leaves, without changing the lipid profiles. These data indicate that the dgd1 mutant phenotypes originally attributed to slow growth caused by reduced photosynthesis are actually the result of abnormal activation of JA signaling. However, the reduced photosynthesis and balloon-like chloroplast phenotypes were not rescued (Lin et al. 2016), indicating that proper photosynthesis and chloroplast morphology directly require DGDG or similar lipids, as we describe in previous sections. JA overproduction in dgd1 mutants also agrees with arabidopside production upon wounding in supporting that MGDG is the major substrate for jasmonate biosynthesis since, in the dgd1 mutants, MGDG is in excess either in total amounts or in its ratio to DGDG. Interestingly, it was recently shown that the amount of MGDG in dgd1 mutants is actually reduced compared with the MGDG level in wild-type plants (Kelly et al. 2016). This finding suggests that JA production in the dgd1 mutants is triggered by an increased ratio of MGDG to DGDG, not by increased amounts of MGDG. It has also been shown that when the amounts of both MGDG and DGDG are increased, resulting in a slightly reduced MGDG to DGDG ratio, JA overproduction was not observed (Wang et al. 2014). These data suggest that tight control of the ratio of MGDG to DGDG is important not only for chloroplast morphology but also for JA homeostasis (Fig. 2). DGDG as a Substitute for Phospholipids in Extraplastidic Membranes during Phosphate Starvation Phosphate is an essential macronutrient. Most phosphates in cells occur as phospholipids in endomembrane systems and mitochondrial membranes. During phosphate starvation, phosphate is released from these membrane lipids by lipases, and the resulting DAG is probably transported to the chloroplast outer membrane where it is converted to DGDG by the enzymes MGD2, MGD3, DGD1 and DGD2 (Fig. 2) (Arabidopsis MGD2/3 and DGD2 are phosphate deficiency-induced isozymes of MGD1 and DGD1, respectively) (Nakamura 2013). DGDG is then translocated to plasma membranes as well as tonoplast and mitochondrial membranes to substitute for the digested phospholipids (Hartel et al. 2000, Andersson et al. 2003, Jouhet et al. 2004, Andersson et al. 2005,,Moellering and Benning 2011). Interestingly, under phosphate-limited conditions or in the pho1 mutant, which is defective in phosphate loading into the root xylem so its shoots suffer from phosphate starvation (Hamburger et al. 2002), JA-responsive genes are up-regulated and JA production is increased in the absence of wounding (Khan et al. 2016). The pho1 mutant exhibits an array of phenotypes that were originally attributed to phosphate deficiency. However, pho1 aos and pho1 coi1 double mutants have revealed that the short petiole and anthocyanin accumulation phenotypes are entirely caused by JA overproduction, and that the small plant size phenotype is also partly caused by JA (Khan et al. 2016). Why and how phosphate starvation induces JA production is not clear. It is conceivable that under conditions of phosphate starvation or in the pho1 mutant, the ratio of MGDG to DGDG in the chloroplast envelope may be significantly altered due to elevated synthesis and export of DGDG. Although it has been shown that the ratio of MGDG to DGDG in the chloroplast fraction, represented by a low-speed centrifugation pellet from the total cell lysate, does not change significantly during phosphate starvation, the pellet fraction mostly reflects the relative amounts in the thylakoid membranes. The chloroplast envelope membranes remain in the supernatant fraction together with the extraplastidic membranes after low-speed centrifugation (Hartel et al. 2000), so the actual MGDG to DGDG ratio in the chloroplast envelope is not known. We hypothesize that JA induction during phosphate starvation may work according to the same mechanism that operates in the dgd1 mutants, i.e. JA biosynthesis is activated due to an altered ratio of MGDG to DGDG at the chloroplast envelope, particularly at the inner envelope membrane where the lipases and most of the OPDA biosynthesis enzymes are localized (Froehlich et al. 2001, Joyard et al. 2010). While the dgd1 mutations are unlikely to be encountered in nature, triggering JA biosynthesis through an imbalanced MGDG to DGDG ratio at the chloroplast envelope, after mobilization of DGDG to extraplastidic membranes during phosphate starvation, may have evolved to retard growth during nutrient limitation and to deter insect predators during slow growth. Galactolipids in Freezing Tolerance The gene SENSITIVE TO FREEZING 2 (SFR2) encodes a galactolipid:galactolipid galactosyltransferase that transfers a galactose from MGDG to either MGDG, DGDG or higher oligogalactoglycerolipids (OGDGs) to produce DAG and DGDG or OGDGs (Fig. 2). SFR2 does not contribute significantly to DGDG synthesis during normal growth, but it is required for freezing tolerance in cold-acclimated Arabidopsis. It has been proposed that reducing the level of MGDG, which has a higher tendency to form the cylindrical non-lamellar hexagonal phase (HII phase, Fig. 1A), may facilitate the maintenance of the lamellar chloroplast outer envelope membrane and prevent the outer membrane from fusing with other cellular membranes during freezing stress (Moellering et al. 2010, Moellering and Benning 2011). Indeed, in Arabidopsis, the level of MGDG was decreased during freezing, and in the post-freezing recovery stage the level of MGDG decreased even further while the level of DGDG was stable in both stages (Li et al. 2008). Similarly, in Arabidopsis, oat, sunflower and several other species, the amount of MGDG was greatly decreased after freeze–thawing of leaves (Nilsson et al. 2015). In addition, SFR2-generated DAG can be further converted to triacylglycerol, a non-polar storage lipid. This may further contribute to freezing tolerance by removing excess membrane lipids resulting from chloroplast shrinkage due to dehydration from freezing (Moellering et al. 2010, Moellering and Benning 2011). The tgd1 (trigalactosyldiacylglycerol 1) to tgd4 mutants were originally isolated as genetic suppressors of the dgd1 mutant. In tgd dgd1 double mutants, SFR2 is somehow constitutively activated, resulting in a small increase in DGDG content, production of a sustainable amount of trigalactosyldiacylglycerol (TGDG) and partial rescue of the dgd1 mutant growth phenotypes (Xu et al. 2003). Since it is now known that the dgd1 mutant growth phenotypes are caused by JA overproduction (Lin et al. 2016), it is therefore reasonable to propose that the suppression of dgd1 phenotypes in the tgd dgd1 double mutants is due to SFR2 processing of MGDG to produce DGDG and TGDG, thereby moderately rebalancing the ratio of MGDG to DGDG at the chloroplast envelope and hence reducing JA production in the dgd1 mutant. Other Functions As the major structural constituent of plastids, MGDG and DGDG may also be important for tolerance to other abiotic stresses. For example, it has been shown in many plant species that during drought stress MGDG is hydrolyzed and the ratio of MGDG to DGDG is reduced (Stevanovic et al. 1992, Quartacci et al. 1997, Gigon et al. 2004, Torres-Franklin et al. 2007, Gasulla et al. 2013), which is suggested to stabilize chloroplast membranes through the same mechanism proposed for membrane protection during freezing (Gasulla et al. 2013). Furthermore, overexpression of rice MGD1 in tobacco results in increased salt and aluminum tolerance (Wang et al. 2014, Zhang et al. 2016). In addition, lipids have been shown to be important for the process of protein import into mitochondria and also for bacterial protein secretion (De Vrije et al. 1988, Rietveld et al. 1995, Bottinger et al. 2016). Several in vitro studies have suggested that lipids may also be important for protein import into chloroplasts (Bruce 1998) and, indeed, it has been shown that chloroplasts isolated from the dgd1 mutant exhibit a deficiency in importing proteins into the chloroplast stroma (Chen and Li 1998). Whether these functions are due to direct or indirect effects of MGDG and DGDG, as well as what the functional mechanisms are, remain to be investigated. Funding This work was supported by Academia Sinica of Taiwan [funding to H.-m.L. and a post-doctoral fellowship to C.-W.Y.]. Acknowledgment We thank Yuki Nakamura for reading the manuscript. 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