2. Lignin as the Critical Barrier Contributing to Basic Disease Resistance
Lignin is an intricate polymer that serves the physical barrier in the defense response to pathogen infection, as lignin is un-degradable to most microorganisms
[17][18][51,52]. When pathogens invade a cell, they induce lignin deposition in the cell wall which provides a physical barrier to resist pathogen infection by limiting the entry of pathogen toxins and cell wall-degrading enzymes into plants and preventing the nutrient transmission from the host to the pathogen
[19][20][53,54]. It is important to know how lignin accumulation will affect disease resistance in plants. The majority of data shows that the high lignin levels will increase disease resistance, but contrary results were also reported that low lignin content in plants exhibited less disease severity
[21][22][23][55,56,57]. As a highly labile heteropolymer, lignin composition was also proposed to affect the disease severity in plant. Here, the data showed that S, G, or H lignin might affect disease severity. More G and H units were accumulated when soft rot pathogens infected in Chinese cabbage
[24][58]. The S unit concentration was increased in false flax (
Camelina sativa) and wheat upon fungal penetration
[19][25][53,59]. The contradictory results mainly derive from the different plants in study, which are complicated by the many unrestrained genetic and developmental factors possibly impacting defense responses.
3. Lignin Related Chemicals Inducing Immune Reaction
Lignin and some related compounds can play as a signal to activate plant-specific immune response. It has reported that silencing Gh4CL30 will promote caffeic acid and ferulic acid accumulation, which inhibit the growth of fungal hyphal and increase resistance to Verticillium wilt in cotton
[26][61]. Many molecules associated with the lignin pathway can serve as phytoalexins which restrict pathogens
[27][62]. Coumarins (including umbelliferone, esculetin, and scopoletin) are synthesized through
p-coumaryl-CoA and feruloyl-CoA. They have been proposed to be regulators in plant microbiomes
[28][63]. Stilbenes are phenolic phytoalexins. Its skeleton (stilbene skeleton) synthesis is catalyzed by stilbene synthase (STS) through the conversion of
p-coumaryl-CoA. The defensive roles of stilbene against pathogens have also been documented
[29][64]. Recently, a large-scale and in-depth investigation of the phyllosphere microbiome in rice has revealed that 4-hydroxycinnamic acid (4-HCA), a precursor compound in lignin synthesis, is the main driver for enrichment of beneficial
Pseudomonas, and inhibition of harmful bacteria
Xanthomonas. OsPAL02 is responsible for 4-HCA synthesis, and therefore maintains healthy phyllosphere homeostasis in rice. It is proposed that regulating microbiome-shaping genes become a new strategy as ‘M gene breeding’ in plant disease resistance breeding alone with the current strategy known as ‘
R gene breeding strategy’
[30][65].
Lignans are phenylpropanoid dimmers synthesized via the monolignol pathway, with coniferyl alcohol as the direct precursor
[31][66]. Dirigent proteins have been shown to act in initiating lignan synthesis
[32][44]. Both dirigent and lignan are proposed to have vital roles in defense responses
[33][34][35][67,68,69]. Particularly, some dirigent proteins boost disease resistance by directly promoting lignan accumulation
[36][70].
Besides these lignin compounds’ ability to act directly on pathogens, cell wall damage will affect cell wall integrity (CWI) and then release damage-associated molecular patterns (DAMPs) which trigger immunity reactions
[37][71]. Lignin is proposed to play the critical part during this process
[38][72]. The reactive oxygen species (ROS) and stress-related hormones, such as jasmonate (JA) and salicylic acid (SA), are involved in lignin’s action to disease resistance
[39][73]. A dirigent protein DIR7 has been identified which play the important role in response to plant CWI impairment
[40][74].
4. Lignin Related Genes Serving Target in Defense Response
In plants, resistance genes (
R) play a vital part in disease resistance. Most
R genes encode the NLR class of proteins
[41][77]. Upon pathogen recognition of
R genes, it triggers a defense response that includes hypersensitive response (HR). HR leads a rapid cell death in infection site. It has been reported that maize has two NLRs, Rp1-D, and Rp1-dp2. Combination of Rp1-D and Rp1-dp2 will lead to activated HR without pathogen infection. Two key enzymes in lignin biosynthesis, HCT and caffeoyl CoA
O-methyltransferase (CCoAOMT), have been demonstrated to suppress this HR by interacting with the Rp1-D21 complex. The enzymatic activities of HCT and CCoAOMT are not necessary to suppress HR. It is proposed that HCT, CCoAOMT, and Rp1 proteins form a complex. Pathogen effectors may target on the lignin pathway as its importance to plant defense, in turn, NLR proteins will monitor special components during this process
[42][43][78,79]. This model is reminiscent to resistosome, which has been elucidated recently
[44][80].
Pathogenesis is also involved in lignin by targeting its synthetic enzymes. An F-box protein (ZmFBL41) has been identified that confers resistance to banded leaf and sheath blight (BLSB) in maize. ZmFBL41 interacts with cinnamyl alcohol dehydrogenase (CAD), the final enzyme in the monolignol pathway, leading to the ubiquitination and degradation of CAD. Two amino acid substitutions in the natural allele of resistant maize lines prevent this interaction. It is proposed that the pathogen (
Rhizoctonia solani) may deliver effectors to directly or indirectly interact with ZmFBL41 or ZmFBL41-ZmSKP1-ZmCAD complex and increase susceptibility of the host
[45][81]. The protein containing tetratrico-peptide repeats (TPRs) is the largest functional family that maintains protein organization and homeostasis through a complicated chaperone network
[46][82]. A mutant, namely
bsr-k1 (broad-spectrum resistance Kitaake-1), has been identified in rice.
Bsr-k1 confers broad-spectrum resistance against the fungal pathogen (
Magnaportheoryzae)and bacterial pathogen (
Xanthomonasoryzae).
Bsr-k1 encodes a tetratricopeptide repeats (TPRs)-containing protein, which binds to PAL mRNAs (OsPAL1-7) and promotes their turnover. Loss of Bsr-k1 function results in lignin accumulation and increases resistance to rice blast and bacterial blight
[47][83].
5. The Regulating Network Linking Lignin with Immune Reaction
The transcriptional regulation on plant metabolism and development is important, which also participates in immune reaction through lignin metabolism. MYB proteins are one of the largest transcription factor families which play an important part in plant growth and development. Some members of MYB are master regulators in the lignin pathway, usually form MBW ternary complex that consists of MYB, basic helix-loop-helix, and WD40
[48][49][84,85]. A R2R3 MYB transcription factor, namely GhODO1, was isolated from cotton. GhODO1 interacts with the promoters of lignin genes Gh4CL1 and GhCAD3, activates their expression, and increases lignin accumulation and resistance to Verticillium wilt (
Verticillium dahlia). JA-mediated defense signaling is also proposed to be involved in this process
[50][86]. AtMYB15 has been reported to regulate defense-induced lignification and contribute to resistance to
Pseudomonas syringae (Pst DC3000). Furthermore, effector-triggered immunity (ETI) responses to Pst DC3000 challenge are required for AtMYB15-mediated lignification. This suggests that MYB15 plays a central part in pathogen-induced lignification
[51][52][87,88]. BnMYB43 from oilseed rape has been shown to regulate vascular lignification, plant morphology and potential yield, but negatively affect resistance to
Sclerotinia sclerotiorum, therefore being a growth-defense trade-off participant
[53][89].
Small GTP-binding proteins exist ubiquitously in eukaryotes, which regulate different cell functions such as organogenesis, polar growth, cell division, and defense response
[54][55][91,92]. ROP is a subfamily of small GTP-binding proteins that exclusively occur in plants. There are 11 ROPs in
Arabidopsis, 7 in rice, and 6 in wheat
[56][93]. OsRac1, one member of ROP in rice, has been reported to affect on CCR, the first enzyme special to lignin monolignol pathway, and then increase defense responses
[57][94].
6. The Metabolic Flux towards Lignin Affecting Defense Response
The metabolic reprogramming is a common phenomenon in regulating metabolism of plant. Its relation with plant innate immunity and lignin pathway remain largely unknown. A novel glycosyltransferase UGT73C7 was identified from
Arabidopsis. It has shown that UGT73C7 could glycosylate
p-coumaric acid and ferulic acid, the upstream compounds in the lignin pathway. This will up-regulate SNC1 expression, a Toll/interleukin 1 receptor-type
NLR gene, and then activate immunity in the plant. UGT73C7 is an important regulator to redirect lignin metabolism upon pathogen challenge
[58][99]. Recently,
thwe
researchers hhave demonstrated that wheat DFRL exerted disease resistance through shifting NADP pool and lignin synthesis
[59][100].
Hm1 is a first-cloned
R gene from maize, which encodes an enzyme that detoxifies the
Helminthosporium carbonum (HC) toxin from the special pathogen
Cochliobolus carbonum [60][101]. However, the homologous
Hm genes have also been found from other monocot crops, including rice, barley, and wheat, although they are not the host of
C. carbonum.
Hm homologs are similar with dihydroflavonol-4-reductase (DFR) in sequence, an important rate-limiting enzyme in flavonoid pathway; therefore they are named as dihydroflavonol-4-reductase like (DFRL).
The Our
esearchers' studies have shown that wheat TaDFRL has the broad substrate preference, including dihydroflavonol (such as taxifolin), flavonol, and flavones (such as quercetin and apigenin), and use both NAD and NADP as co-enzyme, which is different with DFR. Up-regulated
TaDFRL alters NAD(H) and NADP(H) pools towards high NADPH levels. Subsequently, the expressions of CAD and CCR genes are increased, which required NADPH as reducing equivalent. This leads to the enhancement of lignin accumulation and resistance to broad-spectrum diseases
[59][100]. This provides a novel mechanism about increasing host defense responses by elevating metabolic flux towards lignin biosynthesis.