Skip to main content
NCBI home page
Plant Signaling & Behavior logoLink to Plant Signaling & Behavior
. 2009 Feb;4(2):94–99. doi: 10.4161/psb.4.2.7580

Very long chain fatty acid and lipid signaling in the response of plants to pathogens

Sylvain Raffaele 1,†, Amandine Leger 1, Dominique Roby 1,✉
PMCID: PMC2637489  PMID: 19649180

Abstract

Recent findings indicate that lipid signaling is essential for plant resistance to pathogens. Besides oxylipins and unsaturated fatty acids known to play important signaling functions during plant-pathogen interactions, the very long chain fatty acid (VLCFA) biosynthesis pathway has been recently associated to plant defense through different aspects. VLCFAs are indeed required for the biosynthesis of the plant cuticle and the generation of sphingolipids. Elucidation of the roles of these lipids in biotic stress responses is the result of the use of genetic approaches together with the identification of the genes/proteins involved in their biosynthesis. This review focuses on recent observations which revealed the complex function of the cuticle and cuticle-derived signals, and the key role of sphingolipids as bioactive molecules involved in signal transduction and cell death regulation during plant-pathogen interactions.

Key words: very long chain fatty acids (VLCFAs), plant-pathogen interactions, lipid signaling, sphingolipids, epicuticular waxes, lipid rafts, cuticle, plant defense

Introduction

In response to pathogen attack, plants have evolved various mechanisms, both constitutive and inducible, in order to defend themselves. During the past 10 years, a number of studies have revealed the role of lipids and lipid metabolites during plant-pathogen interactions: (i) through the lipoxygenase pathway with the production of oxylipins and for example jasmonic acid (JA), which are important signaling molecules for defense regulation,1,2 (ii) through the unsaturated fatty acid pathway by the remodeling of membrane lipid composition and defense signaling,3 and finally (iii) through the very long chain fatty acid (VLCFA) pathway. The VLCFAs are fatty acids containing 20 to 36 carbons synthesized in the endoplasmic reticulum, which are crucial for a wide range of biological processes in plants. Their role in water-loss control or organ shape has been well studied. These lipids are indeed required for the biosynthesis of the plant cuticle,4,5 and the generation of sphingolipids,6,7 which can be bioactive molecules on their own.8,9 This review focuses on recent studies that highlight the involvement of VLCFAs and VLCFA derivatives in the response of plants to pathogen attack. It will first describe the general pathway and the regulation of VLCFA and VLCFA derivative biosynthesis; then the role of these lipids in cell signaling and pathogen resistance through different aspects will be discussed.

VLCFA Biosynthesis, Regulation and Use for Wax and Sphingolipid Production

The elongation of the C16 and C18 fatty acids into VLCFAs (C20-C36 chains) takes place in the endoplasmic reticulum. Elongase complexes consisting in four enzymes mediate this step: a β-keto acylcoA synthase condensing enzyme (KCS), a β-keto acyl-coA reductase (KCR), an enoyl-coA reductase (ECR) and a β-hydroxyacyl-coA dehydratase (HCD). Three different pathways then lead to the transformation of VLCFAs: in the epidermis, (i) through the “acylreduction pathway”, primary alcohols and wax-esters are formed by fatty acyl-coA reductases (FAR) and wax synthases (WS), respectively, (ii) in the “decarbonylation pathway”, VLCFAs are reduced to alkanes, which in stems are oxidised by mid-chain alkane hydroxylase (MAH1) to form secondary alcohols and ketones (Fig. 1, reviewed in ref. 5). Finally, (iii) in all cells, VLCFAs and long chain bases (LCBs) (generated from C16 and C18 fatty acids) are the precursors for the synthesis of sphingolipids9 (Fig. 1).

Figure 1.

Figure 1

Open in a new tab

Simplified pathways for VLCFA and VLCFA derivative biosynthesis and transport in Arabidopsis. Regulators of these pathways and their putative action are indicated in red. PM: plasma membrane; CW: cell wall.

The identification of the genes encoding VLCFA biosynthetic enzymes has been achieved mainly through mutational approaches. FAE1 (fatty acid elongase 1) was the first identified enzyme by the isolation of the fae1mutant altered in VLCFA accumulation in seeds.10 Several KCS genes have also been identified through wax or cuticle mutants,11–14 then by homology searches. They belong to a large gene family in Arabidopsis with 21 members,15,16 hypothesized to drive the specificity (chain length, tissue…) of the elongation reaction. Concerning the other enzymes of the elongase complex, all of them have been recently found in plants, and in contrast to KCS, they are encoded by single genes: AtYBR159 codes for the first reductase,17 PAS2 revealed to be a 3-hydroxacyl-CoA dehydratase18 and CER10, the homologue of the yeast gene TSC13, encodes the trans-2,3-enoyl-CoA reductase.19

Concerning wax biosynthesis, most of the genes have been screened by forward genetics in wax-deficient (cer) mutants. In the “acyl-reduction pathway”, CER4 is the major fatty acyl-CoA reductase responsible for primary alcohol formation20 while WSD1 produces wax esters in Arabidopsis stems.21 In the “decarbonylation pathway”, CER1 and CER3 are involved in alkane synthesis22,23 while secondary alcohols and ketones are produced by the mid-chain alkane hydroxylase MAH1.24 Finally, ABC transporters such as CER5 and WBC11 were shown to be involved in the transport of wax constituents through the plasma membrane.25,26

This is only recently that the genes controlling the biosynthesis of plant sphingolipids have been identified. In Arabidopsis, the gene AtLCB1, encoding the first subunit of the serine palmitoyltransferase (SPT), has been recently characterized.27 The second subunit of SPT was also identified; however, 2 genes (AtLCB2a and AtLCB2b) encode functional isoforms of the LCB2 subunit.28 Recently, two sphingoid base hydroxylase genes (SBH1 and SBH2) have also been identified in Arabidopsis,29 together with an inositolphosphorylceramide synthase30 and a ceramidase from rice (OsCDase).31 This enzyme, localized in the ER, catalyses the formation of phytoceramide.

Regulation of these biosynthesis pathways remains largely unknown. We have recently shown that AtMYB30, a MYB transcription factor, behaves as a transcriptional activator of several genes encoding the four enzymes forming the fatty acid elongase complex, responsible for VLCFA biosynthesis.32 Interestingly, this regulator acts as a positive regulator of a form of programmed cell death (PCD) in plants, the Hypersensitive Response (HR).33 Concerning wax synthesis, the only transcription factors known to affect this pathway belong to the WAX INDUCER (WIN)/SHINE family in Arabidopsis.34 The WIN1/SHN1 transcription factor activates genes encoding cutin biosynthetic enzymes for instance LACS2, and wax biosynthetic genes. However, the control of wax formation by WIN1/SHN1 may be indirect and may require additional transcription factors acting downstream of WIN1/SHN1. Finally, a new regulatory pathway controlling cuticular wax accumulation was recently discovered in Arabidopsis.35 The key component of this pathway is the CER7 ribonuclease, a core subunit of the exosome involved in RNA processing and degradation. The putative target of this ribonuclease is an mRNA encoding a repressor of transcription of the key wax biosynthetic gene CER3.

Plant Sphingolipids as Key Signals during Plant-Pathogen Interactions?

Recent studies indicate that sphingolipids, as in animals, may play in plants a major signaling role in diverse fundamental processes. In terms of biotic stresses, the fungal Alternaria alternata f. sp. lycopersici (AAL) toxin has been shown to trigger cell death by disruption of sphingolipid metabolism.36 Tomato plants sensitive to AAL-toxin accumulate more sphingolipid precursors due to a mutation in the Asc gene, encoding a component of the key enzyme ceramide synthase. Treatment with another mycotoxin, fumonisin, which is a specific inhibitor of ceramide synthase, leads to a dramatic accumulation of LCB and LCB-P in plant tissues. Lack of AtDPL1 lyase activity in the mutant lines enhances sphingolipid precursors accumulation and exacerbates fumonisin toxicity.37 An Arabidopsis mutant, which is fumonisin B1 resistant (fbr 11-1), fails to generate reactive oxygen intermediates (ROIs), and cannot initiate PCD when the mutant is challenged by fumonisin B1.38 FBR11 encodes a long-chain base 1 (LCB1) subunit of serine palmitoyltransferase (SPT).39 Consequently, free sphingoid bases are involved in the control of PCD in Arabidopsis, presumably through the regulation of the ROI level upon receiving different developmental or environmental cues.38

Another evidence in favor of the role of sphingolipids in the control of cell death in the context of plant-pathogen interactions has been the characterization of the mutant accelerated cell death 5 (acd5). The corresponding gene encodes a ceramide kinase (CERK)40 and the mutant exhibits spontaneous cell death, shows enhanced disease symptoms during a pathogen attack and accumulates CERK substrates. This suggests that the balance between the ceramides and their phosphorylated derivatives are involved in the modulation of PCD and in the control of disease susceptibility. As previously mentioned, AtMYB30 has been shown to be a positive regulator of the hypersensitive response, through activation of VLCFA biosynthetic genes and increased sphingolipid production,32,33 suggesting that sphingolipids would act as pro-cell death signals. The recent discovery of the gene ERH1, a gene acting as a negative regulator of the HR dependent on the resistance gene RPW8 in response to powdery mildew infection, is also clearly in favor of a role of sphingolipids in the control of cell death and resistance in plants. Indeed, this gene encodes an inositolphosphorylceramide synthase (IPCS), and is rapidly induced during a pathogen attack, suggesting that it serves to increase GIPC (glucosyl inositolphosphorylceramide) biosynthesis for a defense related function.30

Together, these results show that multiple steps of the sphingolipid biosynthetic pathway are activated by infection, and that programmed cell death and disease resistance are in many cases tightly associated with this regulatory process. LCBs, ceramides and their derivatives might be the critical messengers to control cell death, or other defense mechanisms. Consequently it will be determinant to identify the targets of these bioactive sphingolipids to understand these regulatory mechanisms.

Are Lipid Rafts All-Armed Battleships?

In addition to their possible direct role as signaling components, sphingolipids also count among the constitutive elements of the plasma membrane (PM). They are also hypothesized to play a role in plant defense signaling as such. Sphingolipids were indeed shown to be quantitatively predominant, together with sterols, in the detergent insoluble membrane (DIM) fraction of the PM from tobacco, Arabidopsis and Medicago.41–43 The lipid raft (LR) model44 assumes that because of this distinctive biochemical composition, DIMs are organized in vivo in microdomains, and that the dynamic exclusion/incorporation processes within these domains can regulate signaling events. Consistently, DIMs were found to have specific protein content.45 Some proteins are predominantly DIM-associated like remorins46 or known components of plant defense responses such as the NDR1 GPI-anchored protein, suggesting the involvement of LRs in defense signaling cascades.47

Although direct involvement of LRs in plant defense responses has not been clearly evidenced to date, the cell biology of various plant-pathogen interactions is consistent with the LR theory. Polarization of the cytoskeleton, aggregation of peroxisomes, endoplasmic reticulum and Golgi bodies at the interface with the pathogen are among the first observable responses of a plant cell to a pathogen attack (reviewed in ref. 48). In addition, polarization and focal accumulation processes are not only found inside the cell but also inside the PM itself. Barley and Arabidopsis cells challenged by the powdery mildew pathogen Blumeria graminis, were shown to undergo focal accumulation, beneath the site of appresorium formation, of a subset of GFP-fused PM proteins (the resistance locus O, the protein MLO, the ROR2 syntaxin and its Arabidopsis ortholog PEN1), whereas other PM proteins (aquaporin isoforms, SYP132 syntaxin) were not re-localized upon infection.49 Similarly, the GFP-fused ATP-binding cassette transporter PEN3/PDR8 localizes in the PM of Arabidopsis un-inoculated leaves and showed strongly focused accumulation at sites of Blumeria attempted penetration.50

However, if experimental evidences for filamentous pathogen-induced focal protein clustering at the PM are emerging, the underlying mechanisms remain enigmatic. On the one hand, the filipin antibiotic, which binds sterols, shows enhanced labelling at Blumeria entry sites, suggesting aggregation of plant LRs or the release of sterol-rich fungal material.51 On the other hand, the hexose-proton symporter HUP1 was shown to segregate in the DIM fraction and to show a sterol-dependent spotty distribution in the PM when expressed in yeast.52 These results suggest the existence of detergent-insoluble PM domains in planta. Nevertheless, lateral organization of membrane lipids could not be clearly associated to pathogen-induced protein focal accumulation events to date. Therefore, the precise role of PM domain clustering in plant defense responses remains poorly documented. In addition, it is still not known whether membrane focal accumulation is restricted to response toward filamentous pathogens or to certain types of plant-pathogen interactions.

The Plant Cuticle, More than a Protective Shell against Pathogens

Well-organized cuticle layers, made of cutin and wax polymers, covers aerial plant surfaces. In many plant species, cutin originates from polymerization of C16 and C18 ω-hydroxylated fatty acids. By contrast, wax synthesis requires elongation of C16 and C18 fatty acids into VLCFAs. These compounds form the outermost layer in epidermal cells, and therefore the first barrier encountered by pathogens in the natural environment. Nevertheless the impact of plant cuticle on the outcome of the interaction with a pathogen is beyond a simple barrier effect.

First, the cuticle can be considered as a reservoir of signals telling phytopathogenic fungi that they found a proper host to infect. This hypothesis originates from the observation that fungi often secrete cutinases when reaching a plant, and that cutin monomers induce appresorium formation in Magnaporthe grisea and Erysiphe graminis.53,54 Consistently, removal of cuticular waxes reduces conidial germination of Blumeria graminis on barley,55 and the altered cuticle of the sma4 (allelic to bre1 and lacs2) Arabidopsis mutant inhibits Botrytis cinerea spore germination.56 Therefore, a thinner, more permeable cuticle does not facilitate the entry of these pathogenic fungi but rather arrests their invasion.

In addition to being detrimental to the growth of the pathogen, cuticle alteration also favors the onset of defense by the plant, as plants can perceive modifications of the cuticle. Exogenous expression of a fungal cutinase gene in Arabidopsis provides immunity to B. cinerea due to the release of fungitoxic compounds and activation of other resistance-associated genes. Similarly, release of antifungal compounds and enhanced B. cinerea resistance have been observed in the bgd mutant that exhibits cuticular defects.57 Increased release of antifungal compounds also plays a role in the enhanced resistance to Botrytis and Sclerotinia observed in sma4 mutant.58 Nevertheless, a positive effect of the cuticle on defense processes is also documented. The plant cuticle not only protects from water loss, but also reduces plant-pathogen recognition and efficient release of antifungal compounds in certain cases during the infection process. Double knockouts gpat4/gpat8, with strongly reduced cutin content, are less resistant to Alternaria brassicicola.59 Whereas more resistant to B. cinerea, the sma4 mutant shows a normal susceptible phenotype toward Erysiphe cichoracearum.56 These two examples illustrate the current consensus that cuticle thickness has a negative effect on biotrophic fungal growth. The att1 mutant has a cutin content reduced by 30%, and shows enhanced susceptibility to virulent Pseudomonas syringae.60 This mutant causes enhanced expression of bacterial type III genes, suggesting that cutin-related compounds repress bacterial type III genes expression in the plant apoplast. On the other hand, att1 displays enhanced resistance to B. cinerea.56

Taken together, these data essentially based on analysis of cuticle-defective mutants, indicate that cuticle-derived signals act negatively on necrotrophic fungal infection and positively on biotrophic fungi and virulent bacterial pathogens. However, further investigations involving gain-of-function experiments and various plant-pathogen interactions will be required before reaching a general rule on the contribution of cuticle related genes and cuticle composition to plant defense mechanisms.

Conclusions and Perspectives

Within the past few years, there has been a “burst” of articles in the field of plant pathology which have revealed the various and major roles of lipids, and more recently, the function of very long chain fatty acid-based molecules during plant-pathogen interactions (Fig. 2). Identification of the roles of these lipids in biotic stress responses is the result of the use of genetic approaches together with the rapid progress made in the identification of the genes/proteins involved in lipid biosynthesis. These discoveries highlight the complex function of the cuticle and cuticle-derived signals, and the key role of sphingolipids as bioactive molecules involved in signal transduction and cell death regulation. However, the results are still fragmentary and need further investigations.

Figure 2.

Figure 2

Open in a new tab

Schematic diagram summarizing the contribution of VLCFAs and VLCFA-derived molecules to the molecular dialogue occurring during plant-pathogen interactions. Exchanges between the plant and different pathogens involve (i) VLCFAs and sphingolipid synthesis, (ii) cuticular compounds, and (iii) PM microdomain organization. As a consequence, pathogen growth is differentially affected by the onset of the HR, according to their invasion strategy (e.g., positively for necrotrophic fungi, negatively for biotrophic fungi). Plain red arrows indicate a positive effect; dotted lines with boxed arrowhead, a negative effect, dotted red arrows shows putative positive effect. PM, Plasma Membrane; TTSS, Type Three Secretion System; LCB, Long chain Base; HR, Hypersensitive Response.

Sphingolipids are known to function in all eukaryotic cells as membrane structural and signaling components. Intensive research in the animal field has shown that these compounds play essential regulatory roles in the control of cell death and cell survival.9,61,62 A number of reports described here suggest that plant sphingolipids might be involved in similar regulatory mechanisms. However, this notion that there may be common lipid signaling mechanisms for the control of cell death in plants and in animals often relies on indirect or correlative evidences.63–65 Besides, these compounds being active in low amounts and existing under a large number of different molecular forms, studies on their biochemistry are still limited. Extraction, separation and identification of such compounds remain a challenge, and an accurate picture of the different species and biosynthetic pathways of plant sphingolipids is not yet available. The systematic identification of sphingolipid biosynthesis genes will also face the difficult task of assessing their enzymatic/molecular function and of the identification of their targets. Together with a genetic approach to addressing the question of their importance in defense/cell death signaling, these are keys to understand the role of sphingolipids in plant cell signaling.

After intensive studies in animal systems, lipid rafts start appearing as ubiquitous entry sites for pathogens, in plants as well. Again, the gap between animals and plants in term of PM raft functions should not be filled in prematurely. But in this case, biochemistry is ahead of genetics, and assessing the existence and function of PM microdomains in vivo is a major expectation. A key step toward this achievement could be the identification of plant counterparts of caveolins, or flotillins, that is to say protein markers of lipid rafts that allow detection of rafts in living cells. Pathogen attack would then be a convenient stimulus to study raft dynamics and role in signaling.

Finally, epicuticular waxes are specific to plants, known to play important general functions in the interactions of plants with their environment.66 This key adaptation in the evolution of plants67 has been shown to influence the issue of plant-pathogen interactions in unexpected ways. This is clearly an exciting area of research, and the important question of the signaling function of some components of the cuticle will need future work, using different plants, pathogens and adequate biochemical methods to identify the active molecules and their exact roles. Another intriguing question is related to the putative signaling roles of LTPs (Lipid Transfer Proteins). In favour of this hypothesis is the identification of DIR1, a putative LTP involved in the long distance signaling associated with systemic resistance.68 DIR1 has been recently structurally characterized, sharing some structural and lipid binding properties with LTP2, but displaying some specific features.69 A functional analysis of this protein family in Arabidopsis would bring some light on lipid signaling and transport. Finally, in depth analysis of the functions of VLCFAs and VLCFA derivatives during plant-pathogen interactions will undoubtedly provide access to fundamental functions of these compounds during plant development.

Acknowledgements

We are very grateful to Dr. Frederic Domergue for critical reading and comments on the manuscript.

Abbreviations

VLCFAs

very long chain fatty acids

JA

jasmonic acid

KCS

β-keto acyl-coA synthase condensing enzyme

KCR

β-keto acyl-coA reductase

ECR

enoyl-coA reductase

HCD

β-hydroxyacyl-coA dehydratase

FAR

fatty acyl-coA reductase

WS

wax synthase

LCBs

long chain bases

FAE

fatty acid elongase

MAH

mid-chain alkane hydroxylase

SPT

serine palmitoyltransferase

SBH

sphingoid base hydroxylase

PCD

programmed cell death

IPCS

inositolphosphorylceramide synthase

HR

the hypersensitive response

ROIs

reactive oxygen intermediates

SPT

serine palmitoyltransferase

CERK

ceramide kinase

PM

plasma membrane

DIM

detergent insoluble membrane

LR

lipid raft

GFP

green fluorescent protein

cer

eceriferum (not wax-carrying)

Footnotes

Previously published online as a Plant Signaling & Behavior E-publication: http://www.landesbioscience.com/journals/psb/article/7580

References

  • 1.Feussner I, Wasternack C. The lipoxygenase pathway. Annu Rev Plant Biol. 2002;53:275–297. doi: 10.1146/annurev.arplant.53.100301.135248. [DOI] [PubMed] [Google Scholar]
  • 2.Blee E. Impact of phyto-oxylipins in plant defense. Trends Plant Sci. 2002;7:315–322. doi: 10.1016/s1360-1385(02)02290-2. [DOI] [PubMed] [Google Scholar]
  • 3.Upchurch RG. Fatty acid unsaturation, mobilization and regulation in the response of plants to stress. Biotechnol Letts. 2008 doi: 10.1007/S10529-008-9639-z. [DOI] [PubMed] [Google Scholar]
  • 4.Shepherd T, Wynne Griffiths D. The effects of stress on plant cuticular waxes. New Phytol. 2006;171:469–499. doi: 10.1111/j.1469-8137.2006.01826.x. [DOI] [PubMed] [Google Scholar]
  • 5.Samuels L, Kunst L, Jetter R. Sealing plant surfaces: cuticular wax formation by epidermal cells. Ann Rev Plant Biol. 2008;59:683–707. doi: 10.1146/annurev.arplant.59.103006.093219. [DOI] [PubMed] [Google Scholar]
  • 6.Sperling PaH E. Plant sphingolipids: structural diversity, biosynthesis, first genes and functions. Biochim Biophys Acta. 2003;1632:1–15. doi: 10.1016/s1388-1981(03)00033-7. [DOI] [PubMed] [Google Scholar]
  • 7.Worall D, Ng CK-Y, Hetherington AM. Sphingolipids, new players in plant signaling. Trends Plant Sci. 2003;8:317–320. doi: 10.1016/S1360-1385(03)00128-6. [DOI] [PubMed] [Google Scholar]
  • 8.Dunn TM, Lynch DV, Michaelson LV, Napier JA. A post-genomic approach to understanding sphingolipid metabolism in Arabidopsis thaliana. Ann Bot. 2004;93:483–497. doi: 10.1093/aob/mch071. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Lynch DV, Dunn TM. An introduction to plant sphingolipid and a review of recent advances in understanding their metabolism and function. New Phytol. 2004;161:677–702. doi: 10.1111/j.1469-8137.2004.00992.x. [DOI] [PubMed] [Google Scholar]
  • 10.James DW, Lim E, Keller J, Plooy I, Ralston E, Dooner HK. Directed tagging of the Arabidopsis FATTY ACID ELONGATION1 (FAE1) gene with the maize transposon activator. Plant Cell. 1995;7:309–319. doi: 10.1105/tpc.7.3.309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Todd J, Post-Beittenmiller D, Jaworski JG. KCS1 encodes a fatty acid elongase 3-ketoacyl-CoA synthase affecting wax biosynthesis in Arabidopsis thaliana. Plant J. 1999;17:119–130. doi: 10.1046/j.1365-313x.1999.00352.x. [DOI] [PubMed] [Google Scholar]
  • 12.Millar AA, Clemens S, Zachgo S, Giblin EM, Taylor DC, Kunst L. CUT1, an Arabidopsis gene required for cuticular wax biosynthesis and pollen fertility, encodes a very-long-chain fatty acid condensing enzyme. Plant Cell. 1999;11:825–838. doi: 10.1105/tpc.11.5.825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Yephremov A, Wisman E, Huijser P, Huijser C, Wellesen K, Saedler H. Characterization of the FIDDLEHEAD gene of Arabidopsis reveals a link between adhesion response and cell differentiation in the epidermis. Plant Cell. 1999;11:2187–2201. doi: 10.1105/tpc.11.11.2187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Pruitt RE, Vielle-Calzada JP, Ploense SE, Grossniklaus U, Lolle SJ. FIDDLEHEAD, a gene required to suppress epidermal cell interactions in Arabidopsis, encodes a putative lipid biosynthetic enzyme. Proc Natl Acad Sci USA. 2000;97:1311–1316. doi: 10.1073/pnas.97.3.1311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Balcklock BJ, Jaworski JG. Substrate specificity of Arabidopsis 3-ketoacyl-CoA synthases. Biochem Biophys Res Commun. 2006;346:583–590. doi: 10.1016/j.bbrc.2006.05.162. [DOI] [PubMed] [Google Scholar]
  • 16.Joubes J, Raffaele S, Bourdenx B, Garcia C, Laroche-Traineau J, Moreau P, Domergue F, Lessire R. The VLCFA elongase gene family in Arabidopsis thaliana: phylogenetic analysis, 3D modelling and expression profiling. Plant Mol Biol. 2008;67:547–566. doi: 10.1007/s11103-008-9339-z. [DOI] [PubMed] [Google Scholar]
  • 17.Han G, Gable K, Kohlwein SD, Beaudoin F, Napier JA, Dunn TM. The Saccharomyces cerevisiae YBR159w gene encodes the 3-ketoreductase of the microsomal fatty acid elongase. J Biol Chem. 2002;277:35440–35449. doi: 10.1074/jbc.M205620200. [DOI] [PubMed] [Google Scholar]
  • 18.Bach L, Michaelson LV, Haslam R, Bellec Y, Gissot L, Marion J, Da Costa M, Boutin JP, Miquel M, Tellier F, Domergue F, Markham JE, Beaudoin F, Napier JA, Faure J-D. The very-long-chain hydroxy fatty acyl-CoA dehydratase PASTICCINO2 is essential and limiting for plant development. Proc Natl Acad Sci USA. 2008;105:14727–14731. doi: 10.1073/pnas.0805089105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Zheng H, Rowland O, Kunst L. Disruptions of the Arabidopsis Enoyl-CoA reductase gene reveal an essential role for very-long-chain fatty acid synthesis in cell expansion during plant morphogenesis. Plant Cell. 2005;17:1467–1481. doi: 10.1105/tpc.104.030155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Rowland O, Zheng H, Hepworth SR, Lam P, Jetter R, Kunst L. CER4 encodes an alcohol-forming fatty acyl-coenzyme A reductase involved in cuticular wax production in Arabidopsis. Plant Physiol. 2006;142:866–877. doi: 10.1104/pp.106.086785. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Li F, Wu X, Lam P, Bird D, Zheng H, Samuels L, Jetter R, Kunst L. Identification of the wax ester synthase/acyl-coenzyme A: diacylglycerol acyltransferase WSD1 required for stem wax ester biosynthesis in Arabidopsis. Plant Physiol. 2008;148:97–107. doi: 10.1104/pp.108.123471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Aarts MG, Keijzer CJ, Stiekema WJ, Pereira A. Molecular characterization of the CER1 gene of Arabidopsis involved in epicuticular wax biosynthesis and pollen fertility. Plant Cell. 1995;7:2115–2127. doi: 10.1105/tpc.7.12.2115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Chen X, Goodwin SM, Boroff VL, Liu X, Jenks MA. Cloning and characterization of the WAX2 gene of Arabidopsis involved in cuticle membrane and wax production. Plant Cell. 2003;15:1170–1185. doi: 10.1105/tpc.010926. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Greer S, Wen M, Bird D, Wu X, Samuels L, Kunst L, Jetter R. The cytochrome P450 enzyme CYP96A15 is the midchain alkane hydroxylase responsible for formation of secondary alcohols and ketones in stem cuticular wax of Arabidopsis. Plant Physiol. 2007;145:653–667. doi: 10.1104/pp.107.107300. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.Pighin J, Zheng H, Balakshin LJ, Goodman IP, Western TL, Jetter R, Kunst L, Samuels AL. Plant cuticular lipid export requires an ABC transporter. Science. 2004;306:702–704. doi: 10.1126/science.1102331. [DOI] [PubMed] [Google Scholar]
  • 26.Panikashvili D, Savaldi-Goldstein S, Mandel T, Yifhar T, Franke RB, Höfer R, Schreiber L, Chory J, Aharoni A. The Arabidopsis DESPERADO/AtWBC11 transporter is required for cutin and wax secretion. Plant Physiol. 2007;145:1345–1360. doi: 10.1104/pp.107.105676. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Chen M, Han G, Dietrich CR, Dunn TM, Cahoon EB. The essential nature of sphingolipids in plants as revealed by the functional identification and characterization of the Arabidopsis LCB1 subunit of serine palmitoyltransferase. Plant Cell. 2006;18:3576–3593. doi: 10.1105/tpc.105.040774. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Dietrich C, Han G, Chen M, Berg RH, Dunn TM, Cahoon EB. Loss-of-function mutations and inducible RNAi suppression of Arabidopsis LCB2 genes reveal the critical role of sphingolipids in gametophytic and sporophytic cell viability. Plant J. 2008;54:284–298. doi: 10.1111/j.1365-313X.2008.03420.x. [DOI] [PubMed] [Google Scholar]
  • 29.Chen M, Markham JE, Dietrich CR, Jaworski JG, Cahoon EB. Sphingolipid long-chain base hydroxylation is important for growth and regulation of sphingolipid content and composition in Arabidopsis. Plant Cell. 2008;20:1862–1878. doi: 10.1105/tpc.107.057851. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Wang W, Yang X, Tangchaiburana S, Ndeh R, Markham JE, Tsegaye Y, Dunn TM, Wang G-L, Bellizzi M, Parsons JF, Morrissey D, Bravo JE, Lynch DV, Xiao S. An inositolphosphorylceramide synthase is involved in regulation of plant programmed cell death associated with defense in Arabidopsis. Plant Cell. 2008:1–17. doi: 10.1105/tpc.108.060053. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31.Pata M, Wu BX, Bielawski J, Xiong TC, Hannun YA, Ng CK. Molecular cloning and characterization of OsCDase, a ceramidase enzyme from rice. Plant J. 2008;55:1000–1009. doi: 10.1111/j.1365-313X.2008.03569.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 32.Raffaele S, Vailleau F, Leger A, Joubes J, Miersch O, Huard C, Blee E, Mongrand S, Domergue F, Roby D. A MYB transcription factor regulates very-long-chain fatty acid biosynthesis for activation of the hypersensitive cell death response in Arabidopsis. Plant Cell. 2008;20:752–767. doi: 10.1105/tpc.107.054858. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33.Vailleau F, Daniel X, Tronchet M, Montillet JL, Triantaphylides C, Roby D. A R2R3-MYB gene, AtMYB30, acts as a positive regulator of the hypersensitive cell death program in plants in response to pathogen attack. Proc Natl Acad Sci USA. 2002;99:10179–10184. doi: 10.1073/pnas.152047199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 34.Kannangara R, Branigan C, Liu Y, Penfield T, Rao V, Mouille G, Hofte H, Pauly M, Riechmann JL, Broun P. The transcription factor WIN1/SHN1 regulates cutin biosynthesis in Arabidopsis thaliana. Plant Cell. 2007;19:1278–1294. doi: 10.1105/tpc.106.047076. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 35.Hooker T, Lam P, Zheng H, Kunst L. A core subunit of the RNA-processing/degrading exosome specifically influences cuticular wax biosynthesis in Arabidopsis. Plant Cell. 2007;19:904–913. doi: 10.1105/tpc.106.049304. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 36.Spassieva S, Markham JE, Hille J. The plant disease resistance gene Asc-1 prevents disruption of sphingolipid metabolism during AAL-toxin-induced programmed cell death. Plant J. 2002;32:561–572. doi: 10.1046/j.1365-313x.2002.01444.x. [DOI] [PubMed] [Google Scholar]
  • 37.Tsegaye Y, Richardson CG, Bravo JE, Mulcahy BJ, Lynch DV, Markham JE, Jaworski JG, Chen M, Cahoon EB, Dunn TM. Arabidopsis mutants lacking long chain base phosphate lyase are fumonisin-sensitive and accumulate trihydroxy-18:1 long chain base phosphate. J Biol Chem. 2007;282:28195–28206. doi: 10.1074/jbc.M705074200. [DOI] [PubMed] [Google Scholar]
  • 38.Shi L, Bielawski J, Mu J, Dong H, Teng C, Zhang J, Yang X, Tomishige N, Hanada K, Hannun YA, Zuo J. Involvement of sphingoid bases in mediating reactive oxygen intermediate production and programmed cell death in Arabidopsis. Cell Res. 2007;17:1030–1040. doi: 10.1038/cr.2007.100. [DOI] [PubMed] [Google Scholar]
  • 39.Teng C, Dong H, Shi L, Deng Y, Mu J, Zhang J, Yang X, Zuo J. Serine palmitoyltransferase, a key enzyme for de novo synthesis of sphingolipids, is essential for male gametophyte development in Arabidopsis. Plant Physiol. 2008;146:1322–1332. doi: 10.1104/pp.107.113506. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 40.Liang H, Yao N, Song JT, Luo S, Lu H, Greenberg JT. Ceramides modulate programmed cell death in plants. Genes Dev. 2003;17:2636–2641. doi: 10.1101/gad.1140503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 41.Mongrand S, Morel J, Laroche J, Claverol S, Carde JP, Hartmann MA, Bonneu M, Simon-Plas F, Lessire R, Bessoule JJ. Lipid rafts in higher plant cells: purification and characterization of Triton X-100-insoluble microdomains from tobacco plasma membrane. J Biol Chem. 2004;279:36277–36286. doi: 10.1074/jbc.M403440200. [DOI] [PubMed] [Google Scholar]
  • 42.Borner GHSD, Weimar T, Michaelson LV, Hawkins ND, Macaskill A, Napier JA, Beale MH, Lilley KS, Dupree P. Analysis of detergent-resistant membranes in Arabidopsis. Evidence for plasma membrane lipid rafts. Plant Physiol. 2005;137:104–116. doi: 10.1104/pp.104.053041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 43.Lefebvre B, Furt F, Hartmann MA, Michaelson LV, Carde JP, Sargueil-Boiron F, Rossignol M, Napier JA, Cullimore J, Bessoule JJ, Mongrand S. Characterization of lipid rafts from Medicago truncatula root plasma membranes: a proteomic study reveals the presence of a raft-associated redox system. Plant Physiol. 2007;144:402–418. doi: 10.1104/pp.106.094102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 44.Simons K vMG. Lipid sorting in epithelial cells. Biochemistry. 1988;27:6197–6202. doi: 10.1021/bi00417a001. [DOI] [PubMed] [Google Scholar]
  • 45.Morel JCS, Mongrand S, Furt F, Fromentin J, Bessoule JJ, Blein JP, Simon-Plas F. Proteomics of plant detergent-resistant membranes. Mol Cell Proteom. 2006;5:1396–1411. doi: 10.1074/mcp.M600044-MCP200. [DOI] [PubMed] [Google Scholar]
  • 46.Raffaele S, Gamas P, Niebel A, Ott T. Genome-wide annotation of remorins, a plant-specific protein family: evolutionary and functional perspectives. Plant Physiol. 2007;145:593–600. doi: 10.1104/pp.107.108639. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 47.Shah J. Lipids, lipases and lipid-modifying enzymes in plant disease resistance. Annu Rev Phytopathol. 2005;43 doi: 10.1146/annurev.phyto.43.040204.135951. [DOI] [PubMed] [Google Scholar]
  • 48.Underwood W, Somerville SC. Focal accumulation of defences at sites of fungal pathogen attack. J Exp Bot. 2008;59:3501–3508. doi: 10.1093/jxb/ern205. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 49.Bhat RA, Miklis M, Schmelzer E, Schulze-Lefert P, Panstruga R. Recruitment and interaction dynamics of plant penetration resistance components in a plasma membrane microdomain. Proc Natl Acad Sci USA. 2005;102:3135–3140. doi: 10.1073/pnas.0500012102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 50.Stein M, Dittgen J, Sanchez-Rodriguez C, Hou BH, Molina A, Schulze-Lefert P, Lipka V, Somerville S. Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell. 2006;18:731–746. doi: 10.1105/tpc.105.038372. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 51.Bhat R, Panstruga R. Lipid rafts in plants. Planta. 2005;223:5–19. doi: 10.1007/s00425-005-0096-9. [DOI] [PubMed] [Google Scholar]
  • 52.Grossmann G, Opekarova M, Novakova L, Stolz J, Tanner W. Lipid raft-based membrane compartmentation of a plant transport protein expressed in Saccharomyces cerevisiae. Eukaryot Cell. 2006;5:945–953. doi: 10.1128/EC.00206-05. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 53.Francis S, Dewey FM, Gurr SJ. The role of cutinase in germling development and infection by Erysiphe graminis f sp hordei. Physiol Mol Plant Pathol. 1996;49:201–211. [Google Scholar]
  • 54.Gilbert RD, Johnson AM, Dean RA. Chemical signals responsible for appressorium formation in the rice blast fungus Magnaporthe grisea. Physiol Mol Plant Pathol. 1996;48:335–346. [Google Scholar]
  • 55.Zabka V, Stangl M, Bringmann G, Vogg G, Riederer M, Hildebrandt U. Host surface properties affect prepenetration processes in the barley powdery mildew fungus. New Phytol. 2008;177:251–263. doi: 10.1111/j.1469-8137.2007.02233.x. [DOI] [PubMed] [Google Scholar]
  • 56.Tang D, Simonich MT, Innes RW. Mutations in LACS2, a Long-Chain Acyl-coenzyme a synthetase, enhance susceptibility to avirulent Pseudomonas syringae but confer resistance to Botrytis cinerea in Arabidopsis. Plant Physiol. 2007;144:1093–1103. doi: 10.1104/pp.106.094318. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 57.Chassot C, Nawrath C, Métraux J-P. Cuticular defects lead to full immunity to a major plant pathogen. Plant J. 2007;49:972–980. doi: 10.1111/j.1365-313X.2006.03017.x. [DOI] [PubMed] [Google Scholar]
  • 58.Bessire M, Chassot C, Jacquat AC, Humphry M, Borel S, Petetot JM, Metraux JP, Nawrath C. A permeable cuticle in Arabidopsis leads to a strong resistance to Botrytis cinerea. EMBO J. 2007;26:2158–2168. doi: 10.1038/sj.emboj.7601658. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 59.Li Y, Beisson F, Koo AJ, Molina I, Pollard M, Ohlrogge J. Identification of acyltransferases required for cutin biosynthesis and production of cutin with suberin-like monomers. Proc Natl Acad Sci USA. 2007;104:18339–18344. doi: 10.1073/pnas.0706984104. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 60.Xiao F, Mark Goodwin S, Xiao Y, Sun Z, Baker D, Tang X, Jenks MA, Zhou JM. Arabidopsis CYP86A2 represses Pseudomonas syringae type III genes and is required for cuticle development. EMBO J. 2004;23:2903–2913. doi: 10.1038/sj.emboj.7600290. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 61.Hannun YA, Obeid LM. Principles of bioactive lipid signalling: lessons from sphingolipids. Nat Rev Mol Cell Biol. 2008;9:139–150. doi: 10.1038/nrm2329. [DOI] [PubMed] [Google Scholar]
  • 62.Morales A, Lee H, Kolesnick R, Fernandez-Checa JC. Sphingolipids and cell death. Apoptosis. 2007;12:923–939. doi: 10.1007/s10495-007-0721-0. [DOI] [PubMed] [Google Scholar]
  • 63.Koga J, Yamauchi T, Shimura M, Ogawa N, Oshima K, Umemura K, Kikuchi M, Ogasawara N. Cerebrosides A and C, sphingolipid elicitors of hypersensitive cell death and phytoalexin accumulation in rice plants. J Biol Chem. 1998;273:31985–31991. doi: 10.1074/jbc.273.48.31985. [DOI] [PubMed] [Google Scholar]
  • 64.Chalfant C, Spiegel S. Sphingosine 1-phosphate and ceramide 1-phosphate: expanding roles in cell signaling. J Cell Sci. 2005;118:4605–4620. doi: 10.1242/jcs.02637. [DOI] [PubMed] [Google Scholar]
  • 65.Petersen N, McKinney LV, Pike H, Hofius D, Zakaria A, Brodersen P, Petersen M, Brown RE, Mundy J. Human GLTP and mutant forms of ACD11 suppress cell death in the Arabidopsis acd11 mutant. FEBS J. 2008;275:4378–4388. doi: 10.1111/j.1742-4658.2008.06584.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 66.Nawrath C. Unraveling the complex network of cuticular structure and function. Curr Opin Plant Biol. 2006;9:281–287. doi: 10.1016/j.pbi.2006.03.001. [DOI] [PubMed] [Google Scholar]
  • 67.Raven J, Edwards D. Physiological evolution of lower embryophytes: adaptations to the terrestrial environment. In: Hemsley A, Poole I, editors. The Evolution of Plant Physiology: From Whole Plants to Ecosystems. 2004. pp. 17–41. [Google Scholar]
  • 68.Maldonado AM, Doerner P, Dixon RA, Lamb CJ, Cameron RK. A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature. 2002;419:399–403. doi: 10.1038/nature00962. [DOI] [PubMed] [Google Scholar]
  • 69.Lascombe N, Bakan B, Buhot N, Marion D, Blein JP, Larue V, Lamb C, Prangé T. The structure of “defective in induced resistance” protein of Arabidopsis thaliana, DIR1, reveals a new type of lipid transfer protein. Protein Sci. 2008;17:1522–1530. doi: 10.1110/ps.035972.108. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Plant Signaling & Behavior are provided here courtesy of Taylor & Francis

RESOURCES