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Structural features and regulation of lignin deposited upon biotic and abiotic stresses
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ScienceDirect Structural features and regulation of lignin deposited upon biotic and abiotic stresses Igor Cesarino Lignin is not only important for plant growth and development but is also a major player in the response of plants to various biotic and abiotic stresses. Although the link between lignin and stresses has been widely demonstrated, the chemical nature and especially the molecular mechanisms underlying the biosynthesis of stress lignin remain largely unknown. Recent findings suggest that the structure of the polymer produced de novo seems to largely depend on the type and intensity of the stress and on the plant species. In addition, the control of stress-related lignification might also occur at several regulatory levels, including transcriptional, posttranscriptional, and posttranslational, similar to developmental lignification. This review focuses on the recent advances on the function, structure, and regulation of lignin deposited upon stress. Address Departamento de Botaˆnica, Instituto de Biocieˆncias, Universidade de Sa˜o Paulo, Rua do Mata˜o 277, Sa˜o Paulo, 05590-020, Brazil Corresponding author: Cesarino, Igor ([email protected])
Current Opinion in Biotechnology 2019, 56:209–214 This review comes from a themed issue on Plant biotechnology Edited by Wout Boerjan and John Ralph
https://doi.org/10.1016/j.copbio.2018.12.012 0958-1669/ã 2018 Elsevier Ltd. All rights reserved.
Introduction Lignin is a non-linear phenolic polymer mostly deposited in secondary walls of specialized cell types, making them rigid and waterproof [1]. A tightly controlled developmental program ensures an appropriate timing and localization of lignin deposition during the differentiation of such specialized cells, which is essential for their proper function. Apart from its role in plant development, lignin is also involved in the response to various biotic and abiotic stresses and thus plays an important function in the adaptation of plants to their environment [2,3]. Accordingly, the lignin polymer synthesized in response to stresses is called ‘stress lignin’, ‘defense lignin’ or ‘lignin-like material’ to distinguish it from developmental lignin [3,4]. Although the link between lignin and stresses has been widely demonstrated in a variety of species, www.sciencedirect.com
most studies simply report a direct effect of a given stress on lignin amount and, to a lower extent, lignin composition, without assessing any regulatory mechanism. In addition, the commonly observed stress-induced changes in the expression of phenylpropanoid genes might be basically related to the production of soluble phenolic compounds with antioxidant properties or other defense functions and do not necessarily implicate lignin biosynthesis. Despite the extensive literature on this topic, the chemical nature and especially the molecular mechanisms underlying the biosynthesis of stress lignin remain largely elusive. Here, I summarize the progress in the elucidation of the structural features and regulatory mechanisms underlying lignin biosynthesis in response to biotic and abiotic stresses.
General structural features of stress lignin A product of the phenylpropanoid pathway, the lignin polymer is generated via oxidative coupling of mainly three hydroxycinnamyl alcohols (i.e. monolignols) differing in their degree of methoxylation, p-coumaryl, coniferyl, and sinapyl alcohols, whose incorporation produces p-hydroxyphenyl (H), guaiacyl (G), and syringyl (S) units. Following oxidation, radical–radical coupling results in a mixture of dehydrodimers with both non-condensed C– O–C ether units such as b-aryl ethers (b-O-4) and condensed C–C units such as phenylcoumarans (b-5) and resinols (b-b) [5]. Content, monomeric composition, and frequency of intermonomeric linkages of developmental lignin vary among cell types, developmental stages and plant species. Lignin of non-flowering vascular plants is composed of G units with minor amounts of H units, whereas the lignin of angiosperms contains mainly G and S units [6]. In addition, the b-O-4 linkage type was shown to be prevalent regardless of the analyzed lignin material [2]. Lignins synthesized in response to stresses have been shown to display distinct structural features from those of developmental lignins [4,7,8,9–12], suggesting that the newly synthesized lignins possess different physical properties that allow them to play a role in stress responses. The chemical nature of stress-induced lignin is not well understood because this parameter was actually not assessed in many studies. Although the structure of the polymer produced de novo seems to largely depend on the type and intensity of the stress and on the plant species, some common responses have been observed (Figure 1). Several abiotic stresses such as ozone exposure, high nitrogen fertilization, wounding, and gravitational Current Opinion in Biotechnology 2019, 56:209–214
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Figure 1
WOUNDING
REGULATION
STRUCTURE
ZmMYB11/ZML ZmMYB31/ZML ZmMYB42/ZML
abiotic and biotic stresses in gymnosperms O
H
IbmiR828 NH2
IbMYB1
OH G
phenylalanine
IbsRNA8105 abiotic stresses in angiosperms
ABIOTIC
EjMYB1
H
MdMYB88/124
ZmmiR528 HO
O
MdVND6 MdMYB46
S
G CoA S
biotic stresses in angiosperms
POSTTRANSLATIONAL
TRANSCRIPTIONAL
BIOTIC
AtMYB15 OsMYB30 OsMYB55
POSTTRANSCRIPTIONAL
p-coumaroyl-CoA
H
Hypersensitive Response
O
HO
MeO
coniferaldehyde
G
H
S
Current Opinion in Biotechnology
Regulation and structure of stress lignin. Regulation: several players involved in the multi-leveled regulatory mechanism that controls stress lignin deposition, including transcription factors, microRNAs and interaction partners for protein–protein interactions, were recently characterized in a range of plants species. Structure: different types of stress induce the biosynthesis of lignin with distinct structural features. Induced branches of the monolignol pathway and the final lignin composition for the different types of stress are highlighted in different colors. Double arrows represent more than one catalytic step. Legend: At, Arabidopsis thaliana; Ej, Eriobotrya japonica; Ib, Ipomoea batatas; Md, Malus domestica; Os, Oryza sativa; Zm, Zea mays.
stimulus have been shown to induce the biosynthesis of a more condensed lignin polymer containing a higher proportion of interunit C–C bonds and H units in both angiosperms and gymnosperms [7,11–13]. Similar features were found in the lignin released by suspension cultures of both Norway spruce and Jack pine treated with fungal elicitor preparations [8,14]. Increased amounts of H units are also characteristic to lignin of compression wood (i.e. the reaction wood produced by gymnosperms in response to gravistimulation). Originally, it was thought that lignin of compression wood had also increased proportions of condensed-type linkages compared to that of normal wood, but more recent studies reported no significant differences [15,16]. Lignin enrichment with H units might be a consequence of a rapid induction of lignification in such stresses, which may exhaust the cellular pool of the precursors of coniferyl and, in the case of angiosperms, sinapyl alcohols, favoring the incorporating of a Current Opinion in Biotechnology 2019, 56:209–214
lignin monomer whose biosynthetic pathway requires fewer catalytic steps, allowing a faster response [8]. The higher incorporation of H units might lead to a higher condensation degree because of the lack of methoxy groups at the 3-position and 5-position of the aromatic ring in p-coumaryl alcohol that favors the formation of C– C bonds [16,17]. Additionally, high concentrations of monolignols triggered by stresses have also been shown to favor the formation of b-5 and b–b condensed bonds via dehydrodimerization reactions [17]. Interestingly, these structural features typify early developmental stages of lignification in both gymnosperms and angiosperms, in which highly condensed, H-units enriched lignin is deposited in the compound middle lamella during cell differentiation [18,19]. In addition to the role of the lignin polymer as a physical barrier against the spread of pathogens, unpolymerized www.sciencedirect.com
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monolignols also have antimicrobial activity [20]. Particularly, the involvement of S lignin in response to pathogen infection in angiosperms has been described in several different pathosystems. Two lines of evidence support a more prominent role of S lignin in plant defense against biotic stresses when compared to other lignin monomers: S-enriched lignin has been shown to preferentially accumulate in infected tissues [9,10,21] and engineered high-S-lignin plants have shown increased resistance to pathogen infection [22,23,24]. Consistent with this hypothesis, a different regulatory pathway was shown to control S lignin biosynthesis when compared to that of H and G monomers in both Arabidopsis thaliana and Medicago truncatula [25]. The transcription factor MYB58 directly activates the expression of monolignol biosynthetic genes by binding to the AC elements in their promoter regions [26], except for FERULATE 5HYDROXYLASE (F5H), which encodes the first enzyme committed to the biosynthesis of S lignin and whose promoter has no AC element [27]. Instead, SND1, a NAC master switch that activates the entire program of secondary cell wall deposition, directly regulates F5H but is not able to activate other lignin genes [25]. Because F5H and SND1 orthologs are found almost exclusively in angiosperms, an evolutionary scenario has been proposed, in which S monolignol biosynthesis initially evolved as a defense mechanism following the appearance of F5H and, once its regulator SND1 gained the ability to bind the promoter of MYB46 (a downstream regulator of secondary wall deposition), the new pathway was subsequently recruited for cell wall biosynthesis [25].
Molecular mechanisms underlying stress lignin deposition Lignification represents an irreversible investment of carbon and energy. It is not surprising that developmental lignin deposition is, therefore, tightly controlled at several regulatory levels, including transcriptionally [28], posttranscriptionally [29], posttranslationally [30] and via feedback inhibition of biosynthetic enzymes by pathway intermediates [31]. Comparatively, much less is known regarding the molecular control of lignin deposition during stress responses. Nevertheless, recent findings suggest that, similar to developmental lignification, the control of stress-related lignification also involves several regulatory levels (Figure 1). Recently, experiments using extracellular lignin-forming cultures of Norway spruce have shown that the redox state of the apoplast has a profound effect on phenolic metabolism [32]. Under higher oxidative conditions in the apoplast, the significant amount of H2O2 is perceived by plasma membranelocated receptors and the consequent signal transduction leads to extracellular lignin and flavonoid biosynthesis. Conversely, extracellular lignin formation was severely blocked upon H2O2 scavenging [32]. Therefore, it is likely that changes in redox status caused by ROS accumulation upon biotic and abiotic stresses constitute a first www.sciencedirect.com
layer of regulation during stress lignin formation. Accordingly, stress-induced lignin deposition is reduced in Arabidopsis loss-of-function mutants affected in both ROS biosynthesis and signaling [33]. Many transcription factors (TFs) involved in the regulatory cascade triggering stress lignin biosynthesis have been characterized in recent years. In maize, three lignin repressors belonging to the R2R3-MYB subfamily, MYB11, MYB31, and MYB42, were shown to participate in wound-induced lignification by interacting with ZML2, a protein belonging to the TIFY family. Each of these MYBs physically interacts with ZML2 and the resulting protein complex binds to the promoter of some lignin biosynthetic genes to repress their expression. When wounding occurs, the jasmonate-signaling cascade triggers the degradation of the MYB/ZML complex, resulting in the derepression of lignin genes and, consequently, in the activation of lignin deposition [34]. Another R2R3-type MYB was shown to regulate fruit flesh lignification in loquat (Eriobotrya japonica) in response to chilling. The expression of EjMYB1, a coortholog of the lignin-specific activators AtMYB68/63 in Arabidopsis, is highly activated during low-temperature treatment, when lignin content of the fruit also increased. EjMYB1 was shown to directly activate lignin genes by binding to AC elements found in their corresponding promoters, leading to flesh lignification [35]. In apple (Malus domestica), the paralogue pair MdMYB88/124 was shown to play important roles in maintaining root hydraulic conductivity under long-term drought conditions [36]. These xylem-specific TFs regulate root xylem development under drought by directly binding to MdVND6 and MdMYB46 promoters and, consequently, triggering the deposition of both cellulose and lignin in vessels. In Arabidopsis, MYB15 was shown to be a part of the genetic pathway controlling defense-induced lignification and basal immunity [37]. Treatment with the bioactive epitope of bacterial flagellin flg22 induced MYB15 expression and resulted in ectopic lignification in WT plants but not in myb15 mutants. In addition, myb15 mutants show increased susceptibility to Pseudomonas syringae, whereas an induced expression of MYB15 using a glucocorticoid-inducible system restored basal resistance of myb15 to wild-type levels. Further analyses showed that MYB15 binds to the promoters of genes required for the defense-induced synthesis of G lignin, and that this TF is also necessary for the basal synthesis of the preformed defense metabolite scopoletin [37]. Interestingly, the co-orthologs of AtMYB15 in rice, OsMYB30 and OsMYB55, were also shown to contribute to plant immunity by directly activating monolignol genes and inducing higher accumulation of ferulic acid, which is an important constituent of grass cell walls [38]. Posttranscriptional control of lignin deposition has been demonstrated not only for developmental lignin but also Current Opinion in Biotechnology 2019, 56:209–214
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for stress lignin. A regulatory mechanism involving the wounding-responsive miR828 was described in sweet potato [39]. In response to wounding, miR828 expression is induced and the transcripts of both IbMYB and IbTLD are targeted for degradation. These TFs function in the repression of the phenylpropanoid pathway and in the activation of antioxidant enzymes, respectively. Therefore, miR828 induction results in derepression of phenylpropanoid genes and in lower activity of antioxidant enzymes, leading to the accumulation of lignin and H2O2 as a part of defense mechanisms. Interestingly, the posttranscriptional regulation of wounding-triggered lignin deposition in sweet potato seems to also involve small RNA-8105 [40]. The activity of this sRNA occurs via both RNA degradation and DNA methylation of IbMYB1, as well as via targeting other IbMYB1 family genes by secondary siRNAs. sRNA8105-mediated repression of the IbMYB1 family genes upon wounding induces the expression of monolignol biosynthetic genes and leads to increased lignin deposition. In maize, the monocot-specific miR528 was shown to regulate lignin biosynthesis under luxurious nitrogen fertilization, affecting lodging resistance [41]. Nitrogen luxury induces the expression of ZmmiR528 that, in turn, negatively regulates the expression of the lignin-related laccase genes ZmLAC3 and ZmLAC5, leading to lower lignin levels, decreased S/ G ratio and reduced lodging resistance. Small peptides are important cell-to-cell signaling components in plants, acting as regulators of both developmental processes and in response to the environmental cues [42]. Several classes of such peptides participate in defense mechanisms against pathogens and wounding. In sweet potato, a hydroxyproline-rich glycopeptide (HypSys) is involved in a signaling cascade leading to lignin deposition during defense responses to wounding [43]. Functional IpHypSys is produced in the presence of wounding signals (i.e. jasmonate and H2O2) and induces the expression of lignin biosynthetic genes, leading to lignin deposition and, consequently, contributing to protect plants from herbivores. In Arabidopsis, pathogenrelated cell wall damages induce the expression of the elicitor peptides PROPEP1 and PROPEP3. In the apoplast, PROPEPs are processed to generate AtPeps that are perceived by the receptors PEPR1 and PEPR2, triggering pattern-triggered immunity (PTI) responses that ultimately involve lignin deposition [44]. The involvement of lignin metabolism in response to pathogen attack seems to be beyond the production of a physical barrier. Remarkably, two key enzymes in lignin biosynthesis were recently shown to modulate the defense response independently of their catalytic activity [45,46]. One of the multiple defense mechanisms evolved in plants occurs through the recognition of pathogen effector molecules by resistance (R) genes, whose interaction triggers the activation of a localized cell death Current Opinion in Biotechnology 2019, 56:209–214
at the infection site called hypersensitive response (HR). Several R genes encode nucleotide binding Leu-richrepeat (NLR) proteins, whose activity must be tightly controlled to avoid severe stunting and loss of fitness. Accordingly, NLR proteins are maintained inactive through interaction with other NLRs or other cofactors, which may be called ‘guardees’. Maize lignin-related ZmCCoAOMT2 and ZmHCT1806/ enzymes ZmHCT4918 were shown to physically interact with the NLR protein Rp1-D21 in a heterologous system, suggesting that they might work as guardees. In the proposed scenario, Rp1 proteins are maintained and inhibited by physically interacting with the CCoAOMT/HCT complex. Upon attack, the pathogen effectors would modify the CCoAOMT/HCT complex, disrupting the interaction and activating Rp1 that will further trigger HR [45,46]. The identification of the potential pathogen effectors and the confirmation that this proposed model occurs in maize remains to be determined. Interestingly, ZmCCoAOMT2 was recently mapped as the gene within the quantitative trait locus qMdr9.02 conferring quantitative resistance to both southern leaf blight and gray leaf spot in maize [47].
Perspectives It is widely accepted that lignin is a major player in the response of plants to various biotic and abiotic stresses. Despite the recent progress in the elucidation of key biochemical and molecular features of stress lignin, there is still much to be explored and determined in terms of structure and regulation of lignin deposited upon stress. For instance, due to the contrasting results regarding the composition of stress lignin, it is not clear whether each lignin monomer plays a specific role in response to stresses after the incorporation into the polymer. Noteworthy, the recent discovery of the incorporation of nonconventional lignin monomers in some plant groups, such as the flavone tricin in grasses [48], hydroxystilbenes in palms [49] or highly decorated monolignols in Canary Island date palm [50] advocates for an evaluation on their participation in stress-related responses. In addition, several distinct regulatory mechanisms have been recently implicated in the control of developmental lignin deposition, such as phosphorylation-mediated on/off regulation of monolignol enzymes [51], transcriptional repression via physical interaction of transcription factors with a linker histone variant [52] and monolignol glycosylation [53]. So far, no evidence is available on the involvement of such mechanisms in stress lignin deposition. Finally, as lignin bioengineering is considered a major strategy to improve the conversion of plant biomass into bioproducts in the biorefinery, understanding the biology of stress lignin is essential for the development of optimized feedstock without undesired effects on plant fitness.
Conflict of interest statement Nothing declared. www.sciencedirect.com
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Acknowledgements Work on lignin metabolism is supported by the FAPESP BIOEN Young Investigator Awards no. 2015/02527-1.
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40. Lin J-S, Lin C-C, Li Y-C, Wu M-T, Tsai M-H, Hsing Y-IC, Jeng S-T: Interaction of small RNA–8105 and the intron of IbMYB1 RNA regulates IbMYB1 family genes through secondary siRNAs and DNA methylation after wounding. Plant J 2013, 75:781-794. 41. Sun Q, Liu X, Yang J, Liu W, Du Q, Wang H, Fu C, Li W-X: MicroRNA528 affects lodging resistance of maize by regulating lignin biosynthesis under nitrogen-luxury conditions. Mol Plant 2018, 11:806-814. This work shows that, by regulating the expression of the lignin-related laccasesZmLAC3 and ZmLAC5, ZmmiR528 controls lignin deposition and affects maize lodging resistance under nitrogen-luxury conditions.
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52. Soler M, Plasencia A, Larbat R, Pouzet C, Jauneau A, Rivas S, Pesquet E, Lapierre C, Truchet I, Grima-Pettenati J: The Eucalyptus linker histone variant EgH1.3 cooperates with the transcription factor EgMYB1 to control lignin biosynthesis during wood formation. New Phytol 2017, 213:287-299. 53. Lin J-S, Huang X-X, Li Q, Cao Y, Bao Y, Meng X-F, Li Y-J, Fu C, Hou B-K: UDP-glycosyltransferase 72B1 catalyzes the glucose conjugation of monolignols and is essential for the normal cell wall lignification in Arabidopsis thaliana. Plant J 2016, 88:26-42.
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ScienceDirect Structural features and regulation of lignin deposited upon biotic and abiotic stresses Igor Cesarino Lignin is not only important for plant growth and development but is also a major player in the response of plants to various biotic and abiotic stresses. Although the link between lignin and stresses has been widely demonstrated, the chemical nature and especially the molecular mechanisms underlying the biosynthesis of stress lignin remain largely unknown. Recent findings suggest that the structure of the polymer produced de novo seems to largely depend on the type and intensity of the stress and on the plant species. In addition, the control of stress-related lignification might also occur at several regulatory levels, including transcriptional, posttranscriptional, and posttranslational, similar to developmental lignification. This review focuses on the recent advances on the function, structure, and regulation of lignin deposited upon stress. Address Departamento de Botaˆnica, Instituto de Biocieˆncias, Universidade de Sa˜o Paulo, Rua do Mata˜o 277, Sa˜o Paulo, 05590-020, Brazil Corresponding author: Cesarino, Igor ([email protected])
Current Opinion in Biotechnology 2019, 56:209–214 This review comes from a themed issue on Plant biotechnology Edited by Wout Boerjan and John Ralph
https://doi.org/10.1016/j.copbio.2018.12.012 0958-1669/ã 2018 Elsevier Ltd. All rights reserved.
Introduction Lignin is a non-linear phenolic polymer mostly deposited in secondary walls of specialized cell types, making them rigid and waterproof [1]. A tightly controlled developmental program ensures an appropriate timing and localization of lignin deposition during the differentiation of such specialized cells, which is essential for their proper function. Apart from its role in plant development, lignin is also involved in the response to various biotic and abiotic stresses and thus plays an important function in the adaptation of plants to their environment [2,3]. Accordingly, the lignin polymer synthesized in response to stresses is called ‘stress lignin’, ‘defense lignin’ or ‘lignin-like material’ to distinguish it from developmental lignin [3,4]. Although the link between lignin and stresses has been widely demonstrated in a variety of species, www.sciencedirect.com
most studies simply report a direct effect of a given stress on lignin amount and, to a lower extent, lignin composition, without assessing any regulatory mechanism. In addition, the commonly observed stress-induced changes in the expression of phenylpropanoid genes might be basically related to the production of soluble phenolic compounds with antioxidant properties or other defense functions and do not necessarily implicate lignin biosynthesis. Despite the extensive literature on this topic, the chemical nature and especially the molecular mechanisms underlying the biosynthesis of stress lignin remain largely elusive. Here, I summarize the progress in the elucidation of the structural features and regulatory mechanisms underlying lignin biosynthesis in response to biotic and abiotic stresses.
General structural features of stress lignin A product of the phenylpropanoid pathway, the lignin polymer is generated via oxidative coupling of mainly three hydroxycinnamyl alcohols (i.e. monolignols) differing in their degree of methoxylation, p-coumaryl, coniferyl, and sinapyl alcohols, whose incorporation produces p-hydroxyphenyl (H), guaiacyl (G), and syringyl (S) units. Following oxidation, radical–radical coupling results in a mixture of dehydrodimers with both non-condensed C– O–C ether units such as b-aryl ethers (b-O-4) and condensed C–C units such as phenylcoumarans (b-5) and resinols (b-b) [5]. Content, monomeric composition, and frequency of intermonomeric linkages of developmental lignin vary among cell types, developmental stages and plant species. Lignin of non-flowering vascular plants is composed of G units with minor amounts of H units, whereas the lignin of angiosperms contains mainly G and S units [6]. In addition, the b-O-4 linkage type was shown to be prevalent regardless of the analyzed lignin material [2]. Lignins synthesized in response to stresses have been shown to display distinct structural features from those of developmental lignins [4,7,8,9–12], suggesting that the newly synthesized lignins possess different physical properties that allow them to play a role in stress responses. The chemical nature of stress-induced lignin is not well understood because this parameter was actually not assessed in many studies. Although the structure of the polymer produced de novo seems to largely depend on the type and intensity of the stress and on the plant species, some common responses have been observed (Figure 1). Several abiotic stresses such as ozone exposure, high nitrogen fertilization, wounding, and gravitational Current Opinion in Biotechnology 2019, 56:209–214
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Figure 1
WOUNDING
REGULATION
STRUCTURE
ZmMYB11/ZML ZmMYB31/ZML ZmMYB42/ZML
abiotic and biotic stresses in gymnosperms O
H
IbmiR828 NH2
IbMYB1
OH G
phenylalanine
IbsRNA8105 abiotic stresses in angiosperms
ABIOTIC
EjMYB1
H
MdMYB88/124
ZmmiR528 HO
O
MdVND6 MdMYB46
S
G CoA S
biotic stresses in angiosperms
POSTTRANSLATIONAL
TRANSCRIPTIONAL
BIOTIC
AtMYB15 OsMYB30 OsMYB55
POSTTRANSCRIPTIONAL
p-coumaroyl-CoA
H
Hypersensitive Response
O
HO
MeO
coniferaldehyde
G
H
S
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Regulation and structure of stress lignin. Regulation: several players involved in the multi-leveled regulatory mechanism that controls stress lignin deposition, including transcription factors, microRNAs and interaction partners for protein–protein interactions, were recently characterized in a range of plants species. Structure: different types of stress induce the biosynthesis of lignin with distinct structural features. Induced branches of the monolignol pathway and the final lignin composition for the different types of stress are highlighted in different colors. Double arrows represent more than one catalytic step. Legend: At, Arabidopsis thaliana; Ej, Eriobotrya japonica; Ib, Ipomoea batatas; Md, Malus domestica; Os, Oryza sativa; Zm, Zea mays.
stimulus have been shown to induce the biosynthesis of a more condensed lignin polymer containing a higher proportion of interunit C–C bonds and H units in both angiosperms and gymnosperms [7,11–13]. Similar features were found in the lignin released by suspension cultures of both Norway spruce and Jack pine treated with fungal elicitor preparations [8,14]. Increased amounts of H units are also characteristic to lignin of compression wood (i.e. the reaction wood produced by gymnosperms in response to gravistimulation). Originally, it was thought that lignin of compression wood had also increased proportions of condensed-type linkages compared to that of normal wood, but more recent studies reported no significant differences [15,16]. Lignin enrichment with H units might be a consequence of a rapid induction of lignification in such stresses, which may exhaust the cellular pool of the precursors of coniferyl and, in the case of angiosperms, sinapyl alcohols, favoring the incorporating of a Current Opinion in Biotechnology 2019, 56:209–214
lignin monomer whose biosynthetic pathway requires fewer catalytic steps, allowing a faster response [8]. The higher incorporation of H units might lead to a higher condensation degree because of the lack of methoxy groups at the 3-position and 5-position of the aromatic ring in p-coumaryl alcohol that favors the formation of C– C bonds [16,17]. Additionally, high concentrations of monolignols triggered by stresses have also been shown to favor the formation of b-5 and b–b condensed bonds via dehydrodimerization reactions [17]. Interestingly, these structural features typify early developmental stages of lignification in both gymnosperms and angiosperms, in which highly condensed, H-units enriched lignin is deposited in the compound middle lamella during cell differentiation [18,19]. In addition to the role of the lignin polymer as a physical barrier against the spread of pathogens, unpolymerized www.sciencedirect.com
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monolignols also have antimicrobial activity [20]. Particularly, the involvement of S lignin in response to pathogen infection in angiosperms has been described in several different pathosystems. Two lines of evidence support a more prominent role of S lignin in plant defense against biotic stresses when compared to other lignin monomers: S-enriched lignin has been shown to preferentially accumulate in infected tissues [9,10,21] and engineered high-S-lignin plants have shown increased resistance to pathogen infection [22,23,24]. Consistent with this hypothesis, a different regulatory pathway was shown to control S lignin biosynthesis when compared to that of H and G monomers in both Arabidopsis thaliana and Medicago truncatula [25]. The transcription factor MYB58 directly activates the expression of monolignol biosynthetic genes by binding to the AC elements in their promoter regions [26], except for FERULATE 5HYDROXYLASE (F5H), which encodes the first enzyme committed to the biosynthesis of S lignin and whose promoter has no AC element [27]. Instead, SND1, a NAC master switch that activates the entire program of secondary cell wall deposition, directly regulates F5H but is not able to activate other lignin genes [25]. Because F5H and SND1 orthologs are found almost exclusively in angiosperms, an evolutionary scenario has been proposed, in which S monolignol biosynthesis initially evolved as a defense mechanism following the appearance of F5H and, once its regulator SND1 gained the ability to bind the promoter of MYB46 (a downstream regulator of secondary wall deposition), the new pathway was subsequently recruited for cell wall biosynthesis [25].
Molecular mechanisms underlying stress lignin deposition Lignification represents an irreversible investment of carbon and energy. It is not surprising that developmental lignin deposition is, therefore, tightly controlled at several regulatory levels, including transcriptionally [28], posttranscriptionally [29], posttranslationally [30] and via feedback inhibition of biosynthetic enzymes by pathway intermediates [31]. Comparatively, much less is known regarding the molecular control of lignin deposition during stress responses. Nevertheless, recent findings suggest that, similar to developmental lignification, the control of stress-related lignification also involves several regulatory levels (Figure 1). Recently, experiments using extracellular lignin-forming cultures of Norway spruce have shown that the redox state of the apoplast has a profound effect on phenolic metabolism [32]. Under higher oxidative conditions in the apoplast, the significant amount of H2O2 is perceived by plasma membranelocated receptors and the consequent signal transduction leads to extracellular lignin and flavonoid biosynthesis. Conversely, extracellular lignin formation was severely blocked upon H2O2 scavenging [32]. Therefore, it is likely that changes in redox status caused by ROS accumulation upon biotic and abiotic stresses constitute a first www.sciencedirect.com
layer of regulation during stress lignin formation. Accordingly, stress-induced lignin deposition is reduced in Arabidopsis loss-of-function mutants affected in both ROS biosynthesis and signaling [33]. Many transcription factors (TFs) involved in the regulatory cascade triggering stress lignin biosynthesis have been characterized in recent years. In maize, three lignin repressors belonging to the R2R3-MYB subfamily, MYB11, MYB31, and MYB42, were shown to participate in wound-induced lignification by interacting with ZML2, a protein belonging to the TIFY family. Each of these MYBs physically interacts with ZML2 and the resulting protein complex binds to the promoter of some lignin biosynthetic genes to repress their expression. When wounding occurs, the jasmonate-signaling cascade triggers the degradation of the MYB/ZML complex, resulting in the derepression of lignin genes and, consequently, in the activation of lignin deposition [34]. Another R2R3-type MYB was shown to regulate fruit flesh lignification in loquat (Eriobotrya japonica) in response to chilling. The expression of EjMYB1, a coortholog of the lignin-specific activators AtMYB68/63 in Arabidopsis, is highly activated during low-temperature treatment, when lignin content of the fruit also increased. EjMYB1 was shown to directly activate lignin genes by binding to AC elements found in their corresponding promoters, leading to flesh lignification [35]. In apple (Malus domestica), the paralogue pair MdMYB88/124 was shown to play important roles in maintaining root hydraulic conductivity under long-term drought conditions [36]. These xylem-specific TFs regulate root xylem development under drought by directly binding to MdVND6 and MdMYB46 promoters and, consequently, triggering the deposition of both cellulose and lignin in vessels. In Arabidopsis, MYB15 was shown to be a part of the genetic pathway controlling defense-induced lignification and basal immunity [37]. Treatment with the bioactive epitope of bacterial flagellin flg22 induced MYB15 expression and resulted in ectopic lignification in WT plants but not in myb15 mutants. In addition, myb15 mutants show increased susceptibility to Pseudomonas syringae, whereas an induced expression of MYB15 using a glucocorticoid-inducible system restored basal resistance of myb15 to wild-type levels. Further analyses showed that MYB15 binds to the promoters of genes required for the defense-induced synthesis of G lignin, and that this TF is also necessary for the basal synthesis of the preformed defense metabolite scopoletin [37]. Interestingly, the co-orthologs of AtMYB15 in rice, OsMYB30 and OsMYB55, were also shown to contribute to plant immunity by directly activating monolignol genes and inducing higher accumulation of ferulic acid, which is an important constituent of grass cell walls [38]. Posttranscriptional control of lignin deposition has been demonstrated not only for developmental lignin but also Current Opinion in Biotechnology 2019, 56:209–214
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for stress lignin. A regulatory mechanism involving the wounding-responsive miR828 was described in sweet potato [39]. In response to wounding, miR828 expression is induced and the transcripts of both IbMYB and IbTLD are targeted for degradation. These TFs function in the repression of the phenylpropanoid pathway and in the activation of antioxidant enzymes, respectively. Therefore, miR828 induction results in derepression of phenylpropanoid genes and in lower activity of antioxidant enzymes, leading to the accumulation of lignin and H2O2 as a part of defense mechanisms. Interestingly, the posttranscriptional regulation of wounding-triggered lignin deposition in sweet potato seems to also involve small RNA-8105 [40]. The activity of this sRNA occurs via both RNA degradation and DNA methylation of IbMYB1, as well as via targeting other IbMYB1 family genes by secondary siRNAs. sRNA8105-mediated repression of the IbMYB1 family genes upon wounding induces the expression of monolignol biosynthetic genes and leads to increased lignin deposition. In maize, the monocot-specific miR528 was shown to regulate lignin biosynthesis under luxurious nitrogen fertilization, affecting lodging resistance [41]. Nitrogen luxury induces the expression of ZmmiR528 that, in turn, negatively regulates the expression of the lignin-related laccase genes ZmLAC3 and ZmLAC5, leading to lower lignin levels, decreased S/ G ratio and reduced lodging resistance. Small peptides are important cell-to-cell signaling components in plants, acting as regulators of both developmental processes and in response to the environmental cues [42]. Several classes of such peptides participate in defense mechanisms against pathogens and wounding. In sweet potato, a hydroxyproline-rich glycopeptide (HypSys) is involved in a signaling cascade leading to lignin deposition during defense responses to wounding [43]. Functional IpHypSys is produced in the presence of wounding signals (i.e. jasmonate and H2O2) and induces the expression of lignin biosynthetic genes, leading to lignin deposition and, consequently, contributing to protect plants from herbivores. In Arabidopsis, pathogenrelated cell wall damages induce the expression of the elicitor peptides PROPEP1 and PROPEP3. In the apoplast, PROPEPs are processed to generate AtPeps that are perceived by the receptors PEPR1 and PEPR2, triggering pattern-triggered immunity (PTI) responses that ultimately involve lignin deposition [44]. The involvement of lignin metabolism in response to pathogen attack seems to be beyond the production of a physical barrier. Remarkably, two key enzymes in lignin biosynthesis were recently shown to modulate the defense response independently of their catalytic activity [45,46]. One of the multiple defense mechanisms evolved in plants occurs through the recognition of pathogen effector molecules by resistance (R) genes, whose interaction triggers the activation of a localized cell death Current Opinion in Biotechnology 2019, 56:209–214
at the infection site called hypersensitive response (HR). Several R genes encode nucleotide binding Leu-richrepeat (NLR) proteins, whose activity must be tightly controlled to avoid severe stunting and loss of fitness. Accordingly, NLR proteins are maintained inactive through interaction with other NLRs or other cofactors, which may be called ‘guardees’. Maize lignin-related ZmCCoAOMT2 and ZmHCT1806/ enzymes ZmHCT4918 were shown to physically interact with the NLR protein Rp1-D21 in a heterologous system, suggesting that they might work as guardees. In the proposed scenario, Rp1 proteins are maintained and inhibited by physically interacting with the CCoAOMT/HCT complex. Upon attack, the pathogen effectors would modify the CCoAOMT/HCT complex, disrupting the interaction and activating Rp1 that will further trigger HR [45,46]. The identification of the potential pathogen effectors and the confirmation that this proposed model occurs in maize remains to be determined. Interestingly, ZmCCoAOMT2 was recently mapped as the gene within the quantitative trait locus qMdr9.02 conferring quantitative resistance to both southern leaf blight and gray leaf spot in maize [47].
Perspectives It is widely accepted that lignin is a major player in the response of plants to various biotic and abiotic stresses. Despite the recent progress in the elucidation of key biochemical and molecular features of stress lignin, there is still much to be explored and determined in terms of structure and regulation of lignin deposited upon stress. For instance, due to the contrasting results regarding the composition of stress lignin, it is not clear whether each lignin monomer plays a specific role in response to stresses after the incorporation into the polymer. Noteworthy, the recent discovery of the incorporation of nonconventional lignin monomers in some plant groups, such as the flavone tricin in grasses [48], hydroxystilbenes in palms [49] or highly decorated monolignols in Canary Island date palm [50] advocates for an evaluation on their participation in stress-related responses. In addition, several distinct regulatory mechanisms have been recently implicated in the control of developmental lignin deposition, such as phosphorylation-mediated on/off regulation of monolignol enzymes [51], transcriptional repression via physical interaction of transcription factors with a linker histone variant [52] and monolignol glycosylation [53]. So far, no evidence is available on the involvement of such mechanisms in stress lignin deposition. Finally, as lignin bioengineering is considered a major strategy to improve the conversion of plant biomass into bioproducts in the biorefinery, understanding the biology of stress lignin is essential for the development of optimized feedstock without undesired effects on plant fitness.
Conflict of interest statement Nothing declared. www.sciencedirect.com
Lignin in biotic and abiotic stresses Cesarino 213
Acknowledgements Work on lignin metabolism is supported by the FAPESP BIOEN Young Investigator Awards no. 2015/02527-1.
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