1. Introduction

2. A brief history of the genus Populus and a list of poplar pathogens

Basidiomycota includes pathogens from the subphylums Pucciniomycotina and Agaricomycotina. The first are about 25 rust fungal species from the genus Melampsora, such as M. larici-populina, M. larici-tremulae, M. medusae, and M. × columbiana, they are biotrophic pathogens causing poplar leaf rusts [59]. Agaricomycotina are represented by necrotrophic macromycetes, often with a wide host range, feeding on wood and usually causing white, brown and yellow heartwood rots. These are members of the orders Agaricales (Pholiota adiposa [60], Hymenochaetales (Inonotus hispidus [61], Phellinus tremulae [62], P. igniarius [63] and Polyporales (Laetiporus sulphureus [64,65], Polyporus squamosus [66], Fomes fomentarius, F. inzegnae [67], Climacodon septentrionalis, Spongipellis litschaueri, S. spumens [68] and Cantharellales (Rhizoctonia solani - a causative agent of root rot and dampling off [69]).

Figure 1. Phylogenetic trees of the main genera of fungal poplar pathogens, and diseases caused by them. The majority of poplar pathogens are fungi from the phylums Ascomycota and Basidiomycota. Among the Basidiomycota representatives, the majority are macromycetes that cause wood rot, as well as rust fungi from the genus Melampsora. Ascomycota pathogens are more diverse, causing powdery mildews, leaf spots, blights, necroses, rots, cankers, etc., among them the most important are representatives of genera Marssonina, Septoria, Dothiorella, Botryosphaeria, Botrytis, Alternaria. To resolve difficulties with the dichotomies, information from NCBI Taxonomy was used as well as data from articles [70,71,72,73,74,75].

Figure 1. Phylogenetic trees of the main genera of fungal poplar pathogens, and diseases caused by them. The majority of poplar pathogens are fungi from the phylums Ascomycota and Basidiomycota. Among the Basidiomycota representatives, the majority are macromycetes that cause wood rot, as well as rust fungi from the genus Melampsora. Ascomycota pathogens are more diverse, causing powdery mildews, leaf spots, blights, necroses, rots, cankers, etc., among them the most important are representatives of genera Marssonina, Septoria, Dothiorella, Botryosphaeria, Botrytis, Alternaria. To resolve difficulties with the dichotomies, information from NCBI Taxonomy was used as well as data from articles [70,71,72,73,74,75].

Poplars are also prone to viral diseases. Poplar mosaic virus (PopMV) from the genus Carlavirus which is a (+)ssRNA virus is one of the most studied viral pathogens, also in Europe [86,87], and a recent study described a new (-)ssRNA Emaravirus from the family Fimoviridae, transmitted by gall mites and causing aspen leaf mosaic in Scandinavian countries [88]. In the middle Rocky Mountain region, (+)ssRNA tobacco necrosis virus (TNV-A) from the family Tombusviridae was found to be able to infect P. tremuloides [89]. One of the largest genera of (+)ssRNA viruses affecting plants is Potyvirus from the family Potyviridae [90], which was isolated from P. x euramericana and P. tremuloides [91]. Bean common mosaic virus (BCMV), which is also from the Potyvirus genus, has also recently been described as the poplar mosaic disease causative agent of P. alba var. pyramidalis in China [92]. P. alba infected with begomoviruses: ToLCuKeV and PaLCuV and their associated satellites: Ageratum alphasatellite, Multan alphasatellite and betasatellite have been detected in Pakistan. The plants did not show disease symptoms, which led to the conclusion that they may be asymptomatic carriers of begomovirus-betasatellite-alphasatellite complexes, contributing to disease in other plants. Begomoviruses belong to the family Geminiviridae, are ssDNA viruses and are capable of causing cotton leaf curl disease, tomato leaf curl disease, etc., being transmitted by arthropods [93,94]. Moreover, it is worth noting that carrying some viruses can be beneficial to poplar: for example, LdNPV (Lymantria dispar nuclear polyhedrosis virus), which is pathogenic to insects but not to plants, affects gypsy moths if they eat infected leaves.

Figure 2. Non-fungal poplar pathogens. One rot-causing oomycete generalist, several pathogenic bacteria usually resulting in cankers, and viruses most of them manifest as mosaics, are shown on there phylograms. Among them, Lonsdalea populi and mosaic viruses cause the most damage and are most actively studied. For phylogenetic difficulties, information from [95], [96] was used.

Figure 2. Non-fungal poplar pathogens. One rot-causing oomycete generalist, several pathogenic bacteria usually resulting in cankers, and viruses most of them manifest as mosaics, are shown on there phylograms. Among them, Lonsdalea populi and mosaic viruses cause the most damage and are most actively studied. For phylogenetic difficulties, information from [95], [96] was used.

3. The Immunity of Poplars

3.3. PRs and Related Defensive Peptides and Proteins in Poplars

In addition to ROS and low-molecular-weight compounds, enzymes and peptides not related to these processes may contribute to defense against pathogens. We will consider them in this section.

Plant pathogenesis-related (PR) proteins are known to be abundant in plants, and what they have in common is that they are involved in providing plant defense against infection. PRs are divided into different families: PR-1s have antifungal activity, PR-2s are β-1,3-glucanases, PR-3s, PR-4s, PR-8s and PR-11s are chitinases, PR-5s are also known as thaumatin-like proteins, PR-6s are proteinase inhibitors, PR-7s are endoproteinases, PR-9s are peroxidases, PR-10s are 'ribonuclease-like proteins', PR-12s are defensins, PR-13s are thionins, PR-14s are lipid transfer proteins, PR-15s are oxalate oxidases, etc. [173]. Many of the proteins and peptides described in this section are poplar PRs or have a similar function in other organisms.

Antimicrobial peptides (AMPs) found in many organisms constitute an important group: cecropins have been isolated from silkworm hemolymph, histatins - from primate saliva, cathelicidins are present in mammals, and defensins are widespread in numerous living species, including plants.

A defensin isolated from P. trichocarpa (PtDef) has in vitro antibacterial and antifungal activity. When added to the plant, it affected bacterial growth similarly to the antibiotic cefotaxime while being less toxic, so one possible practical application of PtDef is to add it to plants instead of antibiotics, which is a more environmentally safe strategy. An alternative approach is to create transgenic poplars overexpressing PtDef gene. Such a line in the experiment had increased resistance to S. populiperda, while the plants had increased content of GA, ABA, SA and JA and activity of the corresponding pathways and decreased concentration of IAA and expression of genes under its control. Probably, the increased content of most PRs and non-specific lipid transfer proteins (nsLTPs) is also associated with the superresistance of PtDef-overexpressing poplars, in addition to defensin itself [42]. Further studies revealed that transgenic P. × euramericana overexpressing PtDef carries out a more "aggressive" HR in response to S. populiperda infection, as the H₂O₂ concentration is higher in the transgenic lines than in WT [174].

The poplar genome contains a number of nsLTPs, the number of which has been increased by tandem and segmental duplications, and in vitro inhibitory activity against pathogens such as S. populiperda has been shown for some of them [175]. However, it is probably more promising to utilize AMPs from medicinal plants to enhance plant resistance, such as nsLTP LJAMP2 from motherwort Leonorus japonicus. Transgenic P. tomentosa with constitutive expression of the LJAMP2 gene had increased resistance to A. alternata and C. gloeosporioides. Likely a part of the properties of LJAMP2 is related to its ability to transport nonpolar molecules, including styrenes, that elicit an immune response [176].

Another recently explored small cationic protein with antifungal properties is rust-inducible secreted protein (RISP). Its gene was discovered when analyzing the P. trichocarpa genome as one of 71 small protein genes of unknown function (SPUFs) lying in the LRR-RLP gene clusters [101]. RISP expression is induced upon wounding, and in earlier work it was described in the transcriptome as a marker of response to Melampsora infection with unknown function [177]. Further studies revealed that recombinant RISP indeed possesses anti-Melampsora activities; it suppresses fungal growth and prevents urediniospore germination by directly binding to them. In plants, RISP undergoes limited proteolysis at maturation, is secreted into the apoplast and leads to an increase in pH in poplar cell culture [178]. However, studies on RISP overexpression in poplar have not yet been conducted, so this could be one of the promising avenues for improving its disease resistance.

Transgenic expression of MsrA2, which is an N-modified host defense peptide (HDP) dermaseptin β1 from the Amazonian poisonous aboreal frog Phyllomedusa bicolor, in P. nigra × P. maximowiczii increased plant resistance to S. musiva infection. MsrA2 has marked toxicity in vitro against fungi, and the putative mechanism of action of it and other dermaseptins is to increase microbial plasmalemma permeability. Although MsrA2 has some phytotoxicity, the first symptoms of it begin to appear at a peptide concentration 3 times the minimum inhibitory concentration required to suppress the growth of S. musiva by 95% [179].

Some of the most important enzymes responsible for defense against fungal pathogens are chitinases. In terms of PRs, the chitinases are PR-3, PR-4, PR-8 and PR-11 [173]. The genome of P. trichocarpa contains 48 genes of different chitinases belonging to 7 different groups and located on 13 different chromosomes, their number was largely increased by tandem duplications; so at the same time, poplar has many more chitinase genes than A. thaliana. Some genes are expressed constitutively, while most can increase expression levels in response to exposure to chitin, chitosan, SA, and MeJA. Poplar chitinases can cleave both chitin and chitosan, although the activity toward them is different [180].

Although poplars possess their own chitinases, it seems more prospective to create a transgenic plant expressing a chitinase from an organism, which is specialized in chitin degradation to create plants with indeed greatly enhanced resistance to fungal infections. Apparently, it was this logic that led to the emergence of transgenic P. tomentosa overexpressing Beauveria bassiana chitinase 1 (BbChit1) gene which demonstrated increased resistance to C. chrysosperma. B. bassiana is an entomopathogenic fungus exploited for biological control of insect pests, so its enzyme is more efficient than homologs from plants, and a strong promoter allows a lot of protein to be accumulated. The use of transgenic chitinases is a valid and environmentally friendly strategy for preventing fungal diseases [181]. Some generalization of the preceding two works was the creation of P. tomentosa overexpressing both BbChit1 and LJAMP2. This double transformant was more resistant to A. alternata than plants overexpressing only BbChit1 or only LJAMP2, while amongst the latter ones plants expressing BbChit1 were more resistant than plants expressing LJAMP2 [182].

The PR-5 protein group includes zeamatin, osmotin and thaumatin-like proteins (TLPs). Many TLPs act as β-1,3-glucanases through a structural motif known as the acidic cleft. P. trichocarpa has 55 TLP genes, which is significantly more than A. thaliana and O. sativa, which have 10 TLP genes each. At least 20 TLPs were under positive selection pressure, and because TLPs possess antifungal activity, the authors of the paper suggest that it is fungal pathogens that have driven the evolution of poplar defense systems more than other biotic stresses [97]. Overexpression of PeTLP from P. deltoides × P. euramericana in the same poplar resulted in a significantly more resistant phenotype to M. brunnea. Although PeTLP, unlike many other TLPs, did not possess antifungal activity in vitro, its role in enhancing resistance probably lies in activation of plant immunity and expression of other defensive proteins [183].

Universal stress proteins (USPs) are important proteins associated with the response to various types of stresses. The P. trichocarpa genome contains 46 USPs, which is significantly more than in A. thaliana, although the genes themselves are highly conserved. In P. davidiana × P. alba var. pyramidalis, the expression of many USPs is significantly induced in response to F. oxyporum infection [184]. Despite the importance of USPs, their mechanism of action in the plant is not fully understood - perhaps they are involved in redox signaling [185].

Heterologous expression of Hsp24 from the fungus Trichoderma asperellum in the hybrid poplar P. davidiana × P. alba var. pyramidalis yielded an interesting result. In T. asperellum, Hsp24 expression is elevated in response to various stresses. Transgenic plants are characterized by lower membrane permeability, higher SOD and POD activity, increased expression of PRs and genes related to the JA (JAR1, MYC1) and SA (NPR, PR1) pathways, and, as a result of all this, greater resistance to C. chrysosperma and A. alternata, compared to the control ones [186].

Proteins associated with the regulation of oxidative stress are worth mentioning briefly, as it is an important part of the response to pathogen invasion. For example, in P. deltoides × P. euroamericana, expression of the PdePrx12 gene encoding peroxidase is reduced in response to infection by B. dothidea and A. alternata. The PdePrx overexpressing poplar line had decreased H₂O₂ and was more susceptible to these pathogens, while plants with reduced PdePrx12 expression, on the contrary, were more resistant to them due to excess H₂O₂ [187]. On the other hand, glutathione, which is a ROS scavenger, is associated with the response to the pathogen. In response to B. dothidea infection in P. tomentosa, the expression of glutathione transferase L3 (GSTL3) and glutathione S-transferase tau7 (GSTU7) is increased, which may be either the plant response to excess H₂O₂ or the result of molecular control of the processes by the pathogenic fungus [188].

Figure 5. Plant defense proteins, including PRs. Both poplar innate proteins, such as chitinases, nsLTP and TLP, and proteins from other organisms the transgenic expression of which in poplars can increase disease resistance are shown. Poplar defence against pathogens is provided by a number of proteins active against fungi and bacteria, many of which belong to the group of PR proteins: chitinases, defensins, nsLTPs, TLPs, RISPs, USPs and others. Overexpression of genes of many of them can increase poplar disease resistance, as can expression of transgenes derived from specially selected organisms: BbChit1 from the chitinolytic fungus B. bassiana, LJAMP2 from the medicinal plant L. japonicus, MsrA2 from the poisonous frog P. bicolor, and Hsp24 from the fungus T. applanatum. The images of organisms are schematic and are not accurate biological drawings.

Figure 5. Plant defense proteins, including PRs. Both poplar innate proteins, such as chitinases, nsLTP and TLP, and proteins from other organisms the transgenic expression of which in poplars can increase disease resistance are shown. Poplar defence against pathogens is provided by a number of proteins active against fungi and bacteria, many of which belong to the group of PR proteins: chitinases, defensins, nsLTPs, TLPs, RISPs, USPs and others. Overexpression of genes of many of them can increase poplar disease resistance, as can expression of transgenes derived from specially selected organisms: BbChit1 from the chitinolytic fungus B. bassiana, LJAMP2 from the medicinal plant L. japonicus, MsrA2 from the poisonous frog P. bicolor, and Hsp24 from the fungus T. applanatum. The images of organisms are schematic and are not accurate biological drawings.

3.4. Transcription Factors Regulating the Immune Response

The regulation of immune response, synthesis of secondary metabolites and other defense-related processes, is carried out in plants by a limited set of families of transcription factors (TFs). In the following, we will consider the representation and role of these families in poplars and how they can be leveraged to enhance resiliency.

One of the most important ones is the WRKY family, named thus for the presence of the WRKYGQK domain within the protein. WRKYGQK, together with the zinc finger domain, binds to the W-box element in the promoter of its target genes, among which many genes for the synthesis of secondary metabolites, including alkaloids and flavonoids, have been found in many plants. WRKY family genes are pivotal in defense against biotic stresses [189]. Representatives of this family are found in algae and land plants and are divided into 4 groups: I, II, III and IV based on their domain structure [189]. Like many other poplar genes, most of the WRKY family genes were amplified as a result of Salicoid WGD [190].

When analyzing the genome of P. trichocarpa, more than 100 representatives of the WRKY family were detected, and the cis-elements W-box, MBS, CGTCA-motif, and TCA-element were found in the vast majority of promoters, capable of responding to signals from WRKY, MYB, MeJA, and SA, respectively. Thus, most of them can be activated by abiotic and biotic stresses, biotrophic and necrotrophic pathogens, TFs of the same and other families. This is in agreement with the experimental data. However, WRKY genes are responsible for different aspects of resistance and have differential expression in plant tissues [189]. Poplar is unlikely to possess more WRKY genes than most other plants, unlike, for example, NBS-LRR genes. When WRKY III family genes were compared in four model plants, 10, 13, 6, and 28 members of this group were found in poplar, arabidopsis, grape, and rice, respectively. At the same time, WRKY III genes in poplar were shown to be under strong purifying selection, indicating their importance [191].

For example, in the same research it was shown that group III member PtrWRKY89 is an SA-inducible gene, so its overexpression in P. tomentosa led to increased expression of several PR genes and resistance to D. gregaria, but at the same time had no effect on genes related to JA signaling [189]. Overexpression of this gene in P. trichocarpa resulted in increased tolerance to Melampsora sp., which is also a biotrophic pathogen. Moreover, it led to increased expression of PtrWRKY18, PtrWRKY35, and PtrWRKY77 because PtrWRKY89 activated them through W-box elements in the promoters [192]. Thus, PtrWRKY89 can be considered as one of the central genes associated with resistance to biotrophic pathogens.

Analogously to PtrWRKY89 in P. trichocarpa, the group III representative PsnWRKY70 has broad potencies in P. simonii × P. nigra hybrid. PsnWRKY70-overexpressing poplars were more resistant to A. alternata infection, and PsnWRKY70-repressed plants were better able to withstand salt stress, so this gene contributes to defense against biotic stresses but reduces fitness to abiotic stresses. PsnWRKY70 is a subject to both self-regulation and regulation by TFs PsnNAM, PsnMYB, PsnGT1, and some MAPK pathway proteins. In the PsnWRKY70-overexpressing line, genes of the MAP kinase cascade, calcium channels, and calcium-dependent protein kinases, as well as homologous genes (WRKY6, WRKY18, WRKY22, and WRKY22-1), LRR domain protein genes, and SA pathway genes were upregulated. Thus, PsnWRKY70 activates crucial defense cascades related to both PTI and ETI [193].

On the other hand, overexpression of PtrWRKY40 in P. tomentosa conferred it increased susceptibility to the biotroph D. gregaria, which correlates with a lower concentration of endogenous SA and decreased expression of SA-dependent genes such as PRs. However, overexpression of PtrWRKY40 in A. thaliana results in its increased resistance to the necrotrophic pathogen B. cinerea, with constitutively higher expression of JA-dependent genes. PtrWRKY40 belongs to group IIa. Thus, PtrWRKY40 increases resilience to necrotrophic pathogens but decreases adaptation to biotrophic pathogens. Moreover, PtrWRKY40 localizes in the nucleus but does not act as a transcription activator [194]. In contrast, another group IIa gene, PtoWRKY60 from P. tomentosa, responds most strongly to SA signaling and weakly to JA, and its overexpression leads to increased resistance to D. gregaria by activating SA-dependent, namely PR5 genes, but does not affect the expression of JA pathway genes such as JAZ8 and JAZ10 [195].

On the contrary to PtrWRKY40, overexpression of the SA-inducible gene PtrWRKY73, which is a I group member, in A. thaliana, increases its resistance to biotrophic pathogens as it was shown on P. syringae but decreases fitness to necrotrophic pathogens such as B. cinerea, and the SA-related defense genes PR1, PR2, PAD4, and CPR5 were upregulated; PtrWRKY73 can be phosphorylated by MAPKs. In contrast to PtrWRKY40, PtrWRKY73 is a transcriptional activator [196].

One of the earliestly and most extensively studied genes of the family was the group IIc member PtWRKY23 from P. tremula × P. alba. PtWRKY23 expression is induced by Melampsora sp. infection, chitosan, SA signaling and wounding and is a typical early response gene. Which is the most important, both poplars overexpressing and underexpressing PtWRKY23 were found to be more susceptible to Melampsora infection than the wild type ones. Transcriptome assay of PtWRKY23 overexpressing plants showed that changes in gene expression were largely consistent with the response to Melampsora infection, but also provided a clue as to which changes were associated with susceptibility of this line. Firstly, in PtWRKY23 overexpressors, genes related to the biosynthesis of lignin and cell-wall related carbohydrates were down-regulated. This reduced cell wall synthesis, hence negatively affecting the plant's ability to build a mechanical barrier. Secondly, the expression of several genes related to flavonoid biosynthesis: PAL, F5H, C4H, and CCR was decreased. Thirdly, the chitinase gene was downregulated. Finally, PtWRKY23 inhibits oxidative burst, also by increasing peroxidase activity, and therefore H₂O₂ concentration was lower in PtWRKY23 overexpressing poplars [197].

Another gene studied in this regard is PsWRKY25 from P. simonii. It was found that sorbitol exposure increased poplar resistance to A. alternata, and PsWRKY25 was one of the most important effectors: it activated the expression of PsCERK1 (ceramide kinase 1) gene, MAPK cascade genes, and secondary metabolites, including phenylpropanoids, biosynthetic genes, etc. Poplar overexpressing PsWRKY25 also had increased resistance to this pathogen [198].

It should also be kept in mind that defense against pathogens is not the only function of poplar WRKYs - rather, they may be associated with the display of a wide range of resistance to biotic and abiotic stresses. For example, PeWRKY41 from P. x euramericana is an SA-, MeJA- and ET-dependent gene, overexpression of which increases the level of peroxidases, chitinases, etc., and the resulting transgenic plants become more resistant to phytophages and salt stress [199]. Similarly, WRKY1 from P. euphratica is induced by HSF1 and contributes to salt tolerance [200].

To summarize the discussion regarding the TFs of the WRKY family, we must note that this is a huge family of very important genes both for plants in general and for poplars in particular, which are extremely important for resistance not only to pathogens but also to abiotic stresses. The exact function of most of them has not yet been studied, which future researchers will need to do. At the same time, when creating transgenic poplars, overexpression of one WRKY gene may increase resistance to some pathogens and decrease resistance to others, such as in the case of biotrophs and necrotrophs. Moreover, many WRKY genes are expressed in wild type plants at exactly the level that gives them maximum protection against infections, as we have seen in the example of PtWRKY23, and attempting to alter their expression will only weaken poplar. Thus, when creating transgenic plants with increased disease resistance, it will be necessary to screen using different pathogens to understand exactly which infections the line has increased resistance to, by how much, and why. It is also necessary to study in more detail the role of other genes of this family and to consciously choose a target for genetic manipulation.

Among the groups of TFs which are important for resistance in plants there are bHLH and MYB families. The name bHLH stands for basic helix-loop-helix and this corresponds to the protein domain structure. This family includes the effector of JA signaling MYC2, and TT8 which will be dicussed below. Members of the MYB family have 1, 2, 3 or 4 repeats of DNA-binding domains and often function as homomultimeric complexes. bHLH and MYB frequently form heterodimeric and heteromultimeric complexes that participate in the regulation of gene expression of biosynthesis of secondary metabolites: flavonoids, anthocyanins and proanthocyanins - for example, this role was shown for the MYB-bHLH-WDR (MBW) complex. The latter protein is WD40 repeat (thus WD40, or WDR) containing TF, for example, TTG1 [201].

It should be first noted that although most MYB TFs positively regulate flavonoid biosynthesis, there are also negative regulators among the representatives of this family, for example, MYB182. Its overexpression in P. tremula × P. alba led to a decrease in transcription of both structural flavonoid biosynthesis genes and their positive regulators from MYB and bHLH families, resulting in a lower content of anthocyanins and PAs in transgenic plants than in WT plants [202]. Two other repressors, MYB165 and MYB194, have a similar function. They both interact with bHLH131 and repress the flavonoid and phenylpropanoid biosynthesis pathways as well as the MYB activators, as was shown in experiments on their overexpression [203]. PtrMYB57 exerts its repressor functions through the C-terminal LxLxL domain, it interacts with bHLH131 and PtrTTG1, and after PtrMYB57 knockout by the CRISPR/Cas system, transgenic plants have higher levels of anthocyanins and PAs [204].

Next, consider the activators of flavonoid biosynthesis. Among them, MYB134, which responds with increased expression to UV-B irradiation, mechanical damage and Melampsora infection, was the first to be studied in detail; hybrid poplars with MYB134 overexpression have increased PA content and decreased content of small phenylpropanoid metabolites [205]. In a more recent study, overexpression of MYB134 in P. tremula × P. alba increased plant resistance to Melampsora rust [170].

MYB115 is another important MYB activator and its overexpression in P. tomentosa led to increased expression of several flavonoid biosynthesis genes, enhanced proanthocyanidin content and made the plant more resistant to D. gregaria infection. Since TT8 and TTG1 interact with MYB115 and form a WDR complex with it, simultaneous coexpression of PtoMYB115, PtoTT8, and PtoTTG1 in Nicotiana benthamiana can lead to increased expression of ANR1 and LAR3 and if they are overexpressed in poplar, this may be a more effective strategy to increase secondary metabolite levels and thus pathogen resisntance compared to sole overexpression of MYB115 [55]. Although this was not tested in the article, it is likely that such transgenic poplar has even higher proanthocyanidin content and is even more resistant to pathogens than poplar overexpressing MYB115 alone.

But what was tested for resistance is a line of transgenic P. alba var. pyramidalis overexpressing both PalbHLH1 and PalMYB90. Upon infection, these plants more efficiently up-regulated the expression of genes related to flavonoid biosynthesis: F3H, DFR, ANS and ANR, and therefore showed increased resistance to B. cinerea and D. gregaria. At the same time basically, transgenic plants had increased levels of total phenols, proanthocyanidins, anthocyanins, quercetin and kaempferol compared to the control ones. This correlates with the observation that P. euphratica, which is superior to P. alba in resistance to D. gregaria, has higher both content of anthocyanins and expression levels of bHLH, DFR and F3H. Overexpressor plants also showed higher ROS content and higher transcription of WRKY70, NAC12, and ERF1 genes compared with WT [206].

Overexpression of PtrMYB119 or PtrMYB120 genes from P. trichocarpa in the hybrid poplar P. alba × P. tremula resulted in upregulation of a large number of flavonoid biosynthesis genes, especially PtrCHS1 and PtrANS2, and enhanced production of anthocyanins such as cyanidin-3-O-glucoside. PtrMYB182, a repressor of anthocyanin and proanthocyanidin biosynthesis, was downregulated in the transgenic plants, and no negative effect on growth was detected despite the increased anthocyanin content [207]. Interestingly, PtrMYB120 is a positive regulator of both flavonoid and lignin biosynthesis, as shown in experiments on its overexpression and suppression in hybrid poplar [208].

In addition to ones discussed above, MYB6, MYB118 and MYB117 were overexpressed in various articles, but the resulting transgenic poplars were not studied for disease resistance. MYB6 overexpression in P. tomentosa increased the biosynthesis rate and flavonoid content in the tree, while through the interaction of MYB6 with KNAT7, a competing pathway of lignin biosynthesis was inhibited by down-regulation of CCR2, CCoAOMT1, F5H, COMT2 and CAD genes, and here is the difference in regulation by MYB6 and MYB120 [209]. PdMYB118 promotes the accumulation of anthocyanins after wounding, and their levels were also increased when PdMYB118 was overexpressed in P. deltoides. Interestingly, PtrJAZ1, which is a repressor of the JA pathway, also suppresses the function of PdMYB118 because it binds PdTT8 and thereby disrupts the MDR complex [210]. MYB117 overexpression in hybrid poplar resulted in increased B-ring hydroxylation of flavonoids but did not alter their total content, but this still can alter their biological activity [211]. In conclusion, none of the MYB119-, MYB120-, MYB6-, MYB118-, or MYB117-overexpressors have been tested for pathogen resistance, and this is an area for future research.

MYB TFs also regulate the biosynthesis of other secondary metabolite classes. For example, PtoMYB142 responds to drought, and its overexpression in P. tomentosa leads to up-regulation of the wax biosynthesis genes CER4 and KCS and thus increased wax accumulation in leaves, which helps to survive water deficit conditions [212]. In the context of pathogen defense, it would be very interesting to overexpress MYB142 and examine whether increasing the amount of wax contributes to improved pathogen defense. It is known that the cuticle can inhibit pathogen penetration both mechanically (in which case the amount of wax may play a crucial role) and biochemically, the latter being relevant for leaf pathogens such as rust fungi penetrating stomata [213].

Thus, MYBs and the transcription factors bHLH and WDR interacting with them are among the most important regulators of the biosynthesis of secondary metabolites, especially flavonoids. By overexpressing activating MYBs, the authors of the studies were able to achieve an increase in flavonoid content in poplars, and in some cases, it was directly shown that such transgenic plants are more resistant to diseases. The increase in flavonoid biosynthesis in double and triple overexpressions is more effective when other components of activatory MBW complexes are overexpressed in addition to MYBs. Thus, obtaining and introducing such overexpressing poplars may be one line of work. Another line of work could be to create knockouts for those MYB genes that reduce flavonoid biosynthesis, such as MYB182 or MYB165.

Figure 6. Transcription factors involved in plant defense. The results of experiments on the effect of overexpression of TFs from the WRKY family on resistance to biotrophic and necrotrophic pathogens, as well as on changes in the composition of secondary metabolites as a result of overexpression of TFs from the MYB, bHKH and WDR family are illustrated (not all MYBs are drawn as part of MBW complexes due to space limitations in the figure). The role of TFs from the ERF and TGA families and the VIP1 protein in the regulation of defense responses is also briefly demonstrated. Plants control defence responses through a number of TF families. WRKY act on SA-dependent and JA-dependent systems, conferring resistance to biotrophs and necrotrophs, respectively (which, however, may work differently in poplar than in Arabidopsis, due to a possible lack of SA-JA antagonism). MYBs, bHLHs, and WDR together form MBW complexes that activate or (less frequently) inhibit the biosynthesis of secondary metabolites, primarily flavonoids. In addition, factors of the TGA, ERF, VIP, etc. families are involved in the regulation of defence reactions.

Figure 6. Transcription factors involved in plant defense. The results of experiments on the effect of overexpression of TFs from the WRKY family on resistance to biotrophic and necrotrophic pathogens, as well as on changes in the composition of secondary metabolites as a result of overexpression of TFs from the MYB, bHKH and WDR family are illustrated (not all MYBs are drawn as part of MBW complexes due to space limitations in the figure). The role of TFs from the ERF and TGA families and the VIP1 protein in the regulation of defense responses is also briefly demonstrated. Plants control defence responses through a number of TF families. WRKY act on SA-dependent and JA-dependent systems, conferring resistance to biotrophs and necrotrophs, respectively (which, however, may work differently in poplar than in Arabidopsis, due to a possible lack of SA-JA antagonism). MYBs, bHLHs, and WDR together form MBW complexes that activate or (less frequently) inhibit the biosynthesis of secondary metabolites, primarily flavonoids. In addition, factors of the TGA, ERF, VIP, etc. families are involved in the regulation of defence reactions.

CAMTAs (calmodulin-binding transcription activators) are a family of TFs which contain Ca²⁺-binding and two DNA-binding domains. They are involved in normal growth and development as well as in reaction to both abiotic and biotic stress and are responsive to ABA, SA and JA. Seven members of this family have been found in the genomes of P. trichocarpa and P. ussuriensis: CAMTA1-7. It is currently known that in response to A. alternata infection, PtCAMTA1 and PtCAMTA2 are induced, the expression of PtCAMTA5 is unchanged and the others are decreased, after some time this kinetics changes [214]. More research is needed to understand how CAMTAs are related to pathogen resistance and whether they can be used to produce improved transgenic plants.

Another family studied in poplar is NAC. NAC proteins contain A, B, C, D, and E domains, and their DNA-binding domain is in the N-terminus. It is known that in some plants these TFs can downregulate the expression of flavonoid and anthocyanin biosynthesis genes [215]. NAC proteins are discussed in more detail in the next section, due to being a target of miRNA164 [216]. One of the NAC TFs is PtATAF1-1 from P. trichocarpa. It is probably involved in the rapid launching of the immune response, since its expression is activated as early as one hour after treatment of poplar cells with Flg22 [217].

Representatives of the AR2/ERF (ET response factor) family have a 60 amino acid DNA-binding domain, which consists of three beta-sheets and one alpha-helix. These TFs affect the biosynthesis of lignin, nicotine, saponins, resveratrol, etc [215]. Whereas 170 ERF genes were initially detected in the P. trichocarpa genome, exploration of the transcriptome of rust susceptible P. nigra x P. deltoides revealed 143 members of this group, of which 21 were up- and 72 were down-regulated 4 days after inoculation with M. larici-populina. Moreover, most defense-related ERF targets were down-regulated in infected leaves and, in contrast, histone deacetylase 1, which is an inhibitor of poplar innate immunity and a target of the ERF40 transcriptional repressor, was up-regulated. Thus, the failure of P. nigra x P. deltoides to up-regulate ERF genes expression in response to infection by the rust fungus and the resulting reduced expression of defense proteins and unblocked immune inhibitor signaling explain the susceptibility of this genotype, emphasizing the importance of ERFs in defense [218]. In another paper, PdPapERF109 was cloned from and overexpressed in the hybrid poplar P. davidiana × P. alba var. pyramidalis (Pdpap). This increased resistance to the fungus F. oxysporum. At the same time, the activity of POD and CAT in transgenic plants was higher than in WT ones, and the content of H₂O₂ and MDA was lower. Thus, overexpression of PdPapERF109 increased ROS scavenging capacity and likely provided a more adequate immune response [219].

The bZIPs are named for their basic and leucine zipper domains, they regulate the production of diterpenoid phytoalexins, anthocyanins, etc. [215]. One well-studied TF from the bZIP family is the VirE2-interaction protein 1 (VIP1), which regulates mitogen-activated protein kinase 3 (MPK3). VIP1 was named because it acts as an adaptor for the VirE2 effector from Agrobacterium tumefaciens, conditioning the interaction of VirE2 with importins and its transport into the nucleus [220]. And although many molecular details of the VIP1 response to pathogenic stress are still unknown, transgenic P. trichocarpa overexpressing either AtVIP1 from A. thaliana or its own PtVIP1 have been shown to have increased resistance to B. salicis, and increased expression of genes from the PR1 group was observed in them [85]. Probably the main reason for the increased resistance of VIP1-overexpressing plants is the VIP1 downstream target MPK3, which, like MPK6, activates NBS-LRR genes expression in plants and allows SA signaling to be triggered [221]. Intriguingly, the MAPK pathway is not only important for plant defense, but also for fungal infection: for example, in C. gloeosporioides, the genes CgSte50, CgSte11, CgSte7 and CgMk1 encode an adaptor protein, MAPKKK, MAPKK and MAPK, respectively, and this whole cascade controls processes such as appressorium formation, invasive growth, melanin biosynthesis, hydrophobicity, conidia germination, response to ROS and overall pathogenicity [222].

Another characterized bZIP protein is PeTGA1, a TGACG-binding (TGA) TF isolated from P. euphratica. PeTGA1 activates the expression of PeSARD1, which is an important regulator of SA biosynthesis. Therefore, transgenic white poplar overexpressing PeTGA1 has increased SA content and responds more efficiently to C. gloeosporioides infection compared to WT [223].

PdPapHB12 gene from the hybrid poplar P. davidiana × P. alba var. pyramidalis encodes a protein that is a TF from the HD-Zip I subfamily. PdPapHB12 expression is induced by abiotic stress and is dependent on biotic stress (it is increased in response to F. oxysporum infection and decreased upon C. chrysosperma invasion), as well as increased in response to JA, SA, and ABA hormone signaling [224]. However, a more detailed study of the role of PdPapHB12 in the regulation of the poplar immune response is required.

Trihelix genes are transcription factors that recognize the GT element. There are a total of 56 trihelix genes (PtrGT1-56) in the P. trichocarpa genome. Expression of most of them increases in response to abiotic stress, pathogen invasion, and signaling by phytohormones (ABA, MeJA, SA) [225].

Transcription factors are closely linked to chromatin function. The alteration of epigenetic markers in response to infection is an important but poorly studied process, as usually sequencing studies focus more on changes in the transcriptome. Infection of poplar Lonsdalea populi was found to decrease DNA methylation levels, especially in CHH islands. The repeats and promoters of protein-coding genes are hypomethylated, leading to increased expression of the latter, especially R-, PR-, and hormone signaling genes; genes encoding microRNAs are also demethylated [226].

3.5. Contribution of microRNAs to the Regulation of Defense Responses

Small non-coding RNAs: both siRNAs and miRNAs - are involved in plant defense responses, with miRNAs being more conservative and usually having a single target, while siRNAs are more variable and may possess multiple targets [227].

Some miRNAs are essential for the proper plant response to pathogen invasion. For instance, expression of miR172b in A. thaliana is increased upon infection and it suppresses TOE, which is a repressor of FLS2 - a component of the PTI system which senses bacterial flagellin [228], while miR393 promotes PTI by repressing auxin signaling which can antagonise SA [229]. In defense, plants can engage the host-induced gene silencing (HIGS) mechanism, which consists in suppression of virulence genes in the pathogen by host miRNAs. For example, in cotton, infection with the fungus Verticillium dahliae induces the expression of miR159 and miR166, which are then exported to hyphae [230]. HIGS is also used against parasitic plants, sometimes resulting in horizontal gene transfer [231].

However, several miRNAs differentially expressed at rest and during infection are not required for activation of the immune response but rather to repress defense responses in the absence of the pathogen. For example, miR472, miR482, and miR2118 suppress NB-LRRs in plants [232]. Upon invasion, SNC1 accumulates in the nucleus and promotes the destruction of these “peacetime” miRNAs [233]. Some pathogens leverage these miRNAs in order to weaken host immune reactions. For example, miR319 is upregulated by virus because it suppresses JA pathway effectors thereby suppressing it [234], while miR528 and miR168 repress AO (ascorbate oxidase) and AGO1, respectively, and are inhibited by AGO18 in plants because they may interfere with antiviral defense [235].

Thus, during infection, miRNAs are utilized by both the plant and the pathogen, with both sides using miRNAs to affect themselves as well as each other. Within a single plant, miRNAs are transmitted through the plasmodesmata system and the phloem, and transit between the plant and the parasitic fungus is often via haustoria. MiRNAs can be transmitted in both "naked" form and as part of extracellular vesicles [227].

One of the first was research, conducted in 2012, where the transcriptome of P. trichocarpa infected with B. dothidea was analyzed. The infection has led to elevated levels of 41 miRNAs from 12 families: miR156, miR319, miR166, miR164, miR408, miR160, miR168, miR159, miR172, miR398, miR1448 and miR1450. Most of them are also known to be involved in responses to different types of abiotic stresses, and miR156 is associated with all types; hence, miR156 may be related to nonselective stress tolerance of poplar trees [236]. In this case, the miR156 - SPL regulatory axis is one of the most important because SPL TFs destabilize the MYB-bHLH-WD40 complex, thereby preventing flavonoid accumulation [237]. A larger study conducted in the same year on P. beijingensis infected with D. gregaria allowed to study not only 37 conserved miRNA families, but also 27 Populus-specific ones. Moreover, the expression of most of the miRNAs studied in both studies changed in the same direction in response to infection [238]. These two works have been excellently reviewed in 2014 [239], so we will move on to more recent studies.

We will now note that already in the first studies it was found that many of the miRNAs differentially expressed in poplar in response to infection target NBS-LRR genes [236]. Subsequent work has shown that a disproportionate number of poplar-specific miRNAs, compared to those miRNAs that are conserved among plants, target specifically R-genes [240]. This is essential for more precise and distinct regulation of the immune response [216].

It may seem counterintuitive that a plant would upregulate microRNAs targeting NBS-LRR genes and thereby block its own defense signaling. However, many microRNAs targeting R genes realize their regulatory functions not by upregulation during infection, but rather by expression at relatively high levels under normal growth conditions, repression of their targets in the absence of disease, and downregulation during infection. One such microRNA is ptc-miR472, which can be down-regulated in P. trichocarpa leaves after treatment with SA, JA, or flagellin. The first experiments on genetic engineering of microRNAs in poplar were also conducted with it: both an overexpression line and a reduced expression line were obtained, the latter being created using the short tandem target mimic (STTM) technology originally proposed for A. thaliana in 2012. In the STMM method, an artificial nucleotide sequence containing two binding sites mimicking the target gene and a linker between them is created; such a transgenic construct is transcribed, then binds to the target small RNA (microRNA or any other type), leading to degradation of the latter by small RNA degrading nucleases and, as a consequence, to its silencing. As a result, the miR472 overexpressor line was the most susceptible to the hemibiotrophic pathogen C. gloeosporioides, as it failed to adequately up-regulate NBS-LRRs, trigger ETI, and activate ROS production, but at the same time it was the most resistant to the necrotroph C. chrysosperma, as it had the most active JA/ET signaling and increased expression of its marker gene ERF1. On the other hand, poplar line STTM472a with reduced levels of ptc-miR472 had maximum resistance to C. gloeosporioides, while its susceptibility to C. chrysosperma was comparable to WT plants [241]. Thus, editing microRNAs that somehow target NBS-LRR genes can increase resistance to either biotrophs or necrotrophs, depending on current needs. Creating a system in which overexpression of such microRNA or STTM, or even both, would be conditional rather than constitutive will allow us more flexibility to artificially modify plant resistance depending on the current needs and type of pathogen.

Several papers in this area have focused on the interaction of poplar with M. larici-populina, a biotrophic pathogen that causes rust. In a relatively recent work, two novel miRNAs were isolated from P. szechuanica. They were named novel_mir_11 and novel_mir_357, they target and negatively regulate the expression of RPM1 and RPS2/5 genes, respectively, while both targets contain NBS and LRR domains, thus being resistance genes. What was most significant in this work is that when the plant was infected with the avirulent M. larici-populina strain Sb052, the expression of both novel_mir_11 and novel_mir_357 declined and the expression of their targets changed only slightly, which appears to be the normal immune response of the plant. If, however, poplar was inoculated with the virulent strain Th053 instead of Sb052, the expression of novel_mir_11 and novel_mir_357 increased, while the expression of their targets decreased steadily during the first 48 h after infection, which corresponds to M. larici-populina growth phase. This probably indicates the ability of this pathogen to utilize the plant's regulatory mechanisms to at least temporarily shut down its immune response [242]. Previously, the same group of researchers had shown that infection of P. szechuanica with strain Sb052 resulted in the upregulation of most microRNAs, while infection with Th053 led to downregulation of most microRNAs, indicating that there are some general differences in microRNA changes in response to avirulent and virulent pathogens [243].

Another study attempted to elucidate the cause of susceptibility of P. nigra × P. deltoides 'Robusta' to rust fungus. In this poplar, PTI was activated after infection, but further R-genes did not respond properly: of 64 TIR-NBS-LRRs and 119 CC-NBS-LRRs, only 1 TIR-NBS-LRR family, which is regulated by miR472b, was up-regulated, whereas members of the miR482 superfamily and their targets from both groups of R-genes hardly responded to rust infection. There was also no proper activation of SA-, JA-, and ET-signaling, which is also possibly due to the dysregulation of microRNAs. Thus, misregulation of microRNAs may be the cause of poplar rust susceptibility [244].

One important regulatory module in the plant response to fungal infection is an axis composed of miRNA164a, NACs, and R genes. NACs are extremely important transcription factors that have been shown in other plants to be up-regulated in response to both biotrophs and necrotrophs, and their overexpression can enhance plant disease resistance. miRNA164a, which regulates NACs, is highly conserved among flowering plants. In poplar, the targets of miRNA164a are two NAC1 genes and one NAC100 gene, and their expression is negatively correlated with miRNA164a expression [216].

Two articles were conducted with the focus on the response of P. tomentosa to infection by the bacterial pathogen, Lonsdalea quercina. One showed that the expression of miR1447 and miR171c was upregulated [245]. In the second one, it was studied how the expression of microRNA targets, instead of microRNAs themselves, is altered during the infection. Among the differentially expressed genes there were many participants of such processes as hormonal signaling pathways, plant-pathogen interactions, and phenylpropanoid biosynthesis. Genes related to auxin, cytokinin, and brassinosteroid signaling were downregulated, and although SA-related TGA and NPR1 genes were also downregulated, PR-1 mRNA levels were increased. Among pathogen interaction genes, the expression of FLS2, calcium-dependent protein kinases, and MYB TFs was upregulated, whereas the expression of various NBS-LRR genes changed differently. As for phenylpropanoid biosynthesis genes, the expression of most of them, especially cinnamoyl-CoA reductase, was upregulated. Although researchers did not measure expression of all microRNA genes, a negative correlation between the expression of microRNAs and of their targets was demonstrated [246].

78 microRNAs from 21 families, the largest of which are miR156, miR395, and miR167, are also differentially expressed in P. alba var. pyramidalis leaves in response to infection with a novel bean mosaic virus (BCMV) from the genus Potyvirus. Representatives of the families miR1444, miR390, miR397, miR398, miR399, miR408 and miR478 were upregulated, while miR1446, miR167, miR169, miR394, miR396 and miR350 were downregulated throughout the duration of infection. Among the miR395 and miR482 families, differences in expression were observed between different members and phases of infection. Since most miR395 representatives were upregulated at the beginning and downregulated at the end of infection, and miR395 is a target of genes associated with protein ubiquitination, it is possible that the manifestation of mosaic symptoms on leaves is also related to miR395, which, requires further experimental confirmation [92].

Changes in miRNA profile occur not only during pathogenesis, but also in the course of establishment of contacts with endophytes. For example, the endophytic strain Streptomyces sp. SSD49 upregulates 25 host miRNAs, including miR156 and miR160, and downregulates 13 miRNAs, including miR168, miR319, miR398, and miR408, when incubated with P. tomentosa seedlings [247]. MiR156a and miR168a may be important for mycorrhizal formation, for example, with the ascomycete fungus Cenococcum geophilum [248]. It is likely that endophytes leverage miRNAs expression regulation the same way that pathogens do, so studying interactions in the poplar-symbiont system can be accurately applied to poplar-pathogen relationships.

Not only miRNAs but also siRNAs are able to respond to infection and provide plant defense. For example, when P. tomentosa was infected with the fungus M. larici-populina, 95% of the fungus genes, including effector genes and other proteins important for the infection process, became targets of poplar sRNAs: siRNAs and miRNAs [240].

Moreover, many microRNAs in plants, which is about 30% in poplar, owe their evolutionary origin to transposons and pseudogenes, which are thus evolutionary catalysts for microRNA formation. For example, miR478e and miR6427 originated from transposons, miR393c and miR6438b are derived from pseudogenes [216]. The same situation is with siRNAs: a great proportion of them is located in transposons and pseudogenes, The main differences in expression in response to different stages of rust fungus infection are attributed to siRNAs derived from the transposon regions [240].

In addition to small RNAs such as miRNAs and siRNAs, lnRNAs are involved in the regulation of defense responses in plants, including poplar. When studying the response of P. × euramericana to M. larici-populina infection, of the 3994 lncRNAs detected, 53 were differentially expressed between healthy and infected tissues: 18 were detected only in control samples, another 18 were down-regulated and 7 were up-regulated during infection, and 10 were present only in infected leaves, with most of the differentially expressed lncRNAs being in close proximity to and likely coexpressed with protein-coding genes. Interestingly, two lncRNAs were predicted to be capable of complementarily binding to microRNAs and thus competing with their protein-coding targets: namely TCONS_00086550 binds to Ptc-miR396a and was downregulated during infection, while TCONS_00025165 binds to Ptc-miR530a and was upregulated in infected leaves [249]. In more recent work, the responses of P. × euramericana in response to the application of exogenous SA were studied. The expression of 606 mRNAs and 49 lncRNAs was altered in SA-treated samples compared with H₂O-treated controls, with DEGs being associated with general responses to stress and light, disease resistance, growth and developmental processes, while mRNA-lncRNA interactions appeared to play an important role in the orchestration of all these responses [250]. Thus, lncRNAs, although still poorly understood in the regulation of plant immune reactions, are extremely important, as they interact with both mRNAs and miRNAs. Further research in this area is required to better understand their role in plant defense.

Figure 7. Differential expression of microRNAs and their targets under the influence of infection. Some interactions between microRNAs and their targets are shown. Defense proteins are blue, TFs are orange, hormone signaling components are yellow and ROS-related proteins are pink. Changes in expression level detected in [236] are indicated by blue arrows, in [238] – by purple arrows, in [246] – by green arrows, in [92] – by pink arrows, and in [249] – by burgundy arrows. Up-regulation is shown by an up-arrow, down-regulation by a down-arrow, and a bidirectional arrow indicates that the expression of different family members changes differently. This scheme is far from exhaustive because of the enormous complexity of microRNA regulation, the lack of data, and our low level of understanding of these processes. Non-coding RNAs can regulate defence responses in plants, including poplars. The large proportion of microRNAs target NBS-LRR genes, primarily TNLs, and under normal conditions these microRNAs repress the expression of their targets, but during infection this repression is attenuated, allowing a strong and robust immune response to be triggered. miR-156 is a highly expressed microRNA, and its up-regulation during infection allows it to suppress SPL TFs and through it auxin signaling, which competes with SA signaling and thus interferes with the immune process. miR-164 - NAC TFs is an important regulatory axis of the immune response that is conserved in many plants. Many miRNAs control gene expression of hormonal pathways. Some lncRNAs are able to bind to miRNAs and repress their activity, representing another level of regulation. siRNAs are able to directly repress pathogen-derived virulence genes. Ptc-miR472a is so far the only example of microRNA engineering in poplar trees in the context of defence against infection that has been both knock-in and knockdown (the latter by STTM technology).

Figure 7. Differential expression of microRNAs and their targets under the influence of infection. Some interactions between microRNAs and their targets are shown. Defense proteins are blue, TFs are orange, hormone signaling components are yellow and ROS-related proteins are pink. Changes in expression level detected in [236] are indicated by blue arrows, in [238] – by purple arrows, in [246] – by green arrows, in [92] – by pink arrows, and in [249] – by burgundy arrows. Up-regulation is shown by an up-arrow, down-regulation by a down-arrow, and a bidirectional arrow indicates that the expression of different family members changes differently. This scheme is far from exhaustive because of the enormous complexity of microRNA regulation, the lack of data, and our low level of understanding of these processes. Non-coding RNAs can regulate defence responses in plants, including poplars. The large proportion of microRNAs target NBS-LRR genes, primarily TNLs, and under normal conditions these microRNAs repress the expression of their targets, but during infection this repression is attenuated, allowing a strong and robust immune response to be triggered. miR-156 is a highly expressed microRNA, and its up-regulation during infection allows it to suppress SPL TFs and through it auxin signaling, which competes with SA signaling and thus interferes with the immune process. miR-164 - NAC TFs is an important regulatory axis of the immune response that is conserved in many plants. Many miRNAs control gene expression of hormonal pathways. Some lncRNAs are able to bind to miRNAs and repress their activity, representing another level of regulation. siRNAs are able to directly repress pathogen-derived virulence genes. Ptc-miR472a is so far the only example of microRNA engineering in poplar trees in the context of defence against infection that has been both knock-in and knockdown (the latter by STTM technology).

3.6. Intra-Population Differences in Resilience and Related Molecular Mechanisms

Like any other population, plant populations are heterogeneous in their susceptibility/resistance to infection. A number of genes are known in poplars, changes in which increase their resistance to disease or, conversely, weaken their immunity.

One good example are MLO (mildew resistance locus O) genes, which are known as plant vulnerability genes to powdery mildew because they are negative regulators of the immune response. P. trichocarpa has 26 MLO genes in its genome: PtMLO1-26, and breakage of PtMLO 17, 18, 19 and 24 may be associated with resistance to powdery mildew, since knockout of homologous genes in A. thaliana confers resistance to a similar disease [251].

Resistance (R) genes are all those plant genes the function of which is related to disease resistance: they include extracellular receptors, including those associated with kinases, intracellular receptors and kinases, etc. The largest group of R-genes are the NBS-LRR genes, of which poplar has more than 400: 64 TNLs, 119 CNLs, 34 BNLs and a large number of genes of other domain composition, such as TNLTs or CNs [252].

One way to classify plant resistance is to divide it into qualitative and quantitative resistance. Qualitative resistance provides complete resistance to a pathogen (i.e. makes the plant a non-host) by inducing a rapid and strong immune response against it, is due to one or more genes (often R genes), but is race-specific and unstable to evolutionary change. In contrast, quantitative resistance is only partial but, due to polygenicity (it is usually controlled by quantitative trait loci (QTLs)), allows the plant to fight a wide range of pathogens and is thus more robust than quantitative resistance. Examples of alleles conferring qualitative and quantitative resistance to M. larici-populina are R_US from P. trichocarpa and R₁ from P. deltoides; cross between these poplar trees produce offspring with the genotypes R_USR₁, R_USr₁, r_USR₁, and r_USr₁ with different resistance to the pathogen; both alleles map to the NBS-LRR-rich region on chromosome 19 [253].

Poplar QTLs have been described in the paper [254]. In P. trichocarpa, 4 QTL intervals containing a total of 38 markers are associated with quantitative control of fungal pathogens, and another 3 QTL intervals with 40 markers are required for defense against phytophagous insects. The QTL intervals contain TNL, lipoxygenase, oxidoreductase, and cytochrome P450 genes, which have undergone numerous tandem duplications in the recent evolutionary past, most of which have led to increased plant resistance.

Disease resistance depends on the status of not only R genes or genes located within the QTL, but also any other genes. In the paper [255] a total of 40 SNPs were found to have a significant effect on rust susceptibility and severity of this disease. Many of them were located, in addition to exons, in introns, intergenic regions, 3' and 5'-UTRs and were associated with a wide range of genes and far not just the R genes. On the other hand, in another study, one constitutively expressed TNL, one constitutively expressed CNL and one G-type lectin receptor-like kinase (G-type lecRLK), the expression of which is induced by pathogens, were described as R-genes, certain allelic variations of which were associated with resistance to Melampsora [256].

Whole-genome sequencing of 1000 P. trichocarpa individuals and testing them for resistance to S. musiva infection in another study [257] found 3 resistance-associated loci: one L-type lecRLK and two receptor-like proteins (RLPs): RLP1 and RLP2, and one vulnerability locus, G-type lecRLK. Accordingly, poplars with a resistant phenotype have higher expression of L-type lecRLK, RLP1, and RLP2, and lower expression of G-type lecRLK, than more susceptible individuals. All these proteins are associated with fungal cell wall receptivity and RLPs interact with RLKs, but whereas some of them activate defense responses (e.g., L-type lecRLK), others are needed to establish symbiotic relationships and then reduce the immune response (G-type lecRLK) [257].

On the other hand, the interaction between plants and pathogens is a long-term arms race, with the latter also possessing a certain genotypic variability that causes their different phenotypes. For example, in 1994, the poplar qualitative resistance gene RMlp7 ceased to confer resistance to some genotypes of rust fungi because a major deletion occurred in the genome of M. larici-populina in the region of the AvrMlp7 effector, to which RMlp7 binds [258]. Similarly, M. brunnea has genotypes that differ in host specificity due to the transcription of different genes and, in particular, the use of different effectors [259].

Resistant and susceptible individuals of P. trichocarpa differ not only genotypically but also in the dynamics and nature of the response to S. musiva infection, as shown by comparative proteomics analysis. For example, susceptible poplar (BESC-801) had an increased amount of S gene products such as G-type lecRLK, which was not observed in the resistant one (BESC-22). Moreover, the levels of proteins associated with SA-dependent responses, including PRs (such as chitinase PR-4), MAPK-dependent and Ca²⁺-dependent signaling compounds, SAR and HR proteins, increased faster and to a greater extent in resistant poplar than in susceptible poplar. It has higher levels of PTI members, such as PRRs (especially important ones such as PtCERK1), PRR coreceptors (such as BAK1 and SOBIR) and HR trigger-related receptors HRLI4 and HIRP, as well as ABC transporters that release phytoalexins. In contrast, ET and JA signals are more active in susceptible poplar [260]. Similar observations were obtained when comparing the response of susceptible P. deltoides and resistant P. tomentosa to Lonsdalea quercina subsp. populi bacteriosis. The expression of genes related to SA signaling (such as PR1s, NPR1s, TGA1,2) was higher in the resistant phenotype, while JA signaling genes showed a more diverse pattern: MYC2s were more actively expressed in the resistant plant, while JAZ1 and COI1s in the susceptible plant [260]. Finally, in a system where the intolerant genotype was P. nigra × P. deltoides and the tolerant ones were P. trichocarpa × P. deltoides hybrids, while theinfection agent was M. larici-populina, a rust-causing biotroph, in intolerant plants, the JA pathway was activated at the early stages and SA was inhibited; in contrast, in tolerant plants, JA was inhibited and the expression of genes associated with the SA response (among which NBS-LRRs, EDS1, NDR1, WRKYs, and PRs) was upregulated. In addition, Kunitz-type trypsin inhibitor (KTI), a gene associated with the development of apoptosis, which is important for the containment of biotrophs, was activated [261]. Thus, a resistant phenotype in different poplar species is often associated with a higher ability to rapidly and strongly activate SA signaling and related processes.

Such a susceptible phenotype with decreased SA and increased JA activity can be reproduced artificially. For example, myo-inositol is an antagonist of SA signaling and galactinol is an agonist of JA signaling. In the normal response of P. alba × P. grandidentata to infection by the biotroph M. aecidiodes, there is a decrease in galactinol levels, activation of SA, calcium, and phosphatide signaling, increased expression of NPR1 and PR1, and increased ROS levels, which does not occur in the mutant line overexpressing Arabidopsis galactinol synthase 3 (AtGolS) and Cucumber sativa raffinose synthase (CsRFS) and therefore more susceptible to rust diseases [262]. On the other hand, overexpression of PdbLOX2, which is the initial enzyme in the JA biosynthesis pathway in the P. davidiana × P. bollena hybrid, enhances its resistance to such a dangerous necrotroph as A. alternata [263]. Thus, both natural and artificially created genotypes with enhanced SA signaling are more resistant to biotrophic pathogens, while those with enhanced JA signaling are more resistant to necrotrophic ones. This consideration can be used both in breeding and in genetic engineering, when it is necessary to obtain trees resistant to a certain type of pathogens.

Metabolomic methods provide another insight into the causes of susceptibility. The genotype of P. trichocarpa resistant to S. musiva accumulated SAR-related metabolites such as trehalose, sucrose, SA and gentisic acid in greater amounts than the susceptible one in response to infection by this fungus, whereas the susceptible poplar did not, and many of its metabolites were catabolized by the fungus [264]. This once again emphasizes the role of SA in defense against biotrophs, but from the metabolomic point of view. The limit of such resistance is P. euphratica, which has almost absolute resistance to biotrophs but is susceptible to a number of necrotrophic pathogens [151].

Interestingly, the results of all these papers are consistent with old ideas about the existence of SA-JA antagonism and contradict the articles we discussed earlier, at the end of Section 3.1, whose authors concluded that in poplar SA- and JA-signaling pathways positively affect each other's activity. This is partly because in the articles supporting antagonism, the evidence was indirect, based on genotype correlation: plants with increased SA signalling activity usually had relatively reduced JA activity, and vice versa [260,261,262,263]. However, these observations may not have a direct causal relationship. Whereas in the paper [120], the authors experimentally proved a positive interaction by applying exogenous SA or JA to poplar, which leads to an increase in the concentration of JA or SA, respectively. However, more research is needed to definitively clarify this contradiction.

Surprisingly, when infected with Lonsdalea populi, the resistant poplar has more active auxin signaling and expression of photosynthesis-related genes, allowing it to maintain its growth, whereas the susceptible one is unable to quickly block the infection and activates more NBS-LRR and PR genes that inhibit growth processes [265]. Thus, paradoxically, in the growth-defense trade-off, growth processes are more important in resistant poplar, while susceptible poplar displays stronger defense reactions. In the same study, it was hypothesized that a likely cause of poplar susceptibility is the delayed accumulation of antimicrobial compounds such as catechin [263].

Some interesting data have recently been obtained to study epigenetic differences - the different pattern of DNA methylation in susceptible (P. x euroamericana) and resistant (P. tomentosa) poplars during infection with the canker-causing bacterium Lonsdalea populi. It was found that during infection there is a decrease in DNA methylation, apparently necessary for the immune response, with the resistant poplar already having a lower basal level of DNA methylation than the susceptible one. DNA hypomethylation in response to infection occurs in both poplar genotypes, but certain patterns of this process differ between them [226].

Another previously discussed reason for susceptibility of poplar to M. larici-populina is impaired regulation by microRNAs: whereas PTI is adequately regulated, microRNA-mediated regulation of ETI, SAR and HR appears to be impaired by the rust strain in susceptible poplar [244].

Finally, within the same species, poplars can differ in the copy number of a particular gene, a phenomenon called gene copy number variations (CNVs). For example, the P. balsamifera from northern and southern Canada studied in paper [266] differed in the number of ~ 1,700 of the nearly 20,000 genes studied: southern populations had more copies of defense genes (chitinases, leucine-rich transmembrane protein kinase, TNLs, etc.) because they were under greater pathogenic pressure, while northern populations were more adapted to withstand abiotic stresses associated with light and water deficiency.

Information on the resistance of certain phenotypes and genotypes to diseases is of great importance, as it allows the production of resistant plants by simple crossing. Often (as in the case of CNVs) a large number of genes are involved in this resistance and selection is more relevant than the use of genetic engineering.

Figure 8. Metabolic, physiological, genetic and populational differences between "susceptible" and "resistant" poplar. "Generally resistant" and "generally susceptible" poplars differ from each other in a number of genes that are still used for breeding purposes. Resistance can be qualitative, which is absolute, highly pathogen-specific and provided by only a single gene, in this case we speak of R-genes, and quantitative, which is not absolute but has a broader spectrum of action and is provided by a group of genes, named quantitative trait loci (QTL). Poplar plants that are more resistant to biotrophs often have more active SA signalling and acquire SAR more rapidly, while those that are more resistant to necrotrophs have more active JA/ET signalling. More resistant plants may have higher concentrations of secondary metabolites and synthesise them more rapidly during infection. They have lower total DNA methylation levels and more adequate regulation by microRNAs. They continue to photosynthesise actively and maintain growth even during infection, maintaining an optimal trade-off between growth and defence. The genome of more resistant plants may contain more copies of defence genes, which is more characteristic of southern populations. It should be noted that the concepts of susceptibility and resistance are used here in a general sense, and in relation to different specific pathogens, these patterns may have a number of nuances.

Figure 8. Metabolic, physiological, genetic and populational differences between "susceptible" and "resistant" poplar. "Generally resistant" and "generally susceptible" poplars differ from each other in a number of genes that are still used for breeding purposes. Resistance can be qualitative, which is absolute, highly pathogen-specific and provided by only a single gene, in this case we speak of R-genes, and quantitative, which is not absolute but has a broader spectrum of action and is provided by a group of genes, named quantitative trait loci (QTL). Poplar plants that are more resistant to biotrophs often have more active SA signalling and acquire SAR more rapidly, while those that are more resistant to necrotrophs have more active JA/ET signalling. More resistant plants may have higher concentrations of secondary metabolites and synthesise them more rapidly during infection. They have lower total DNA methylation levels and more adequate regulation by microRNAs. They continue to photosynthesise actively and maintain growth even during infection, maintaining an optimal trade-off between growth and defence. The genome of more resistant plants may contain more copies of defence genes, which is more characteristic of southern populations. It should be noted that the concepts of susceptibility and resistance are used here in a general sense, and in relation to different specific pathogens, these patterns may have a number of nuances.

4. Environmental Factors Protecting Poplar from Infections: Endophytes, Phytophages and Chemical Elements

4.1. Endophytes

In nature, poplar interacts with a huge number of organisms, not all of which can even be classified as potential pathogens. Organisms from the external environment - usually fungi and bacteria - that interact with the plant on the surface are called rhizosphere in the case of the root and phyllosphere in the case of the leaves. Those that establish a closer symbiotic relationship with the plant by penetrating its tissues are called root and leaf endophytes, respectively. In addition to these, a number of poplar endophytes can live inside the wood of the stem and, taking advantage of the anaerobic conditions created there, fix atmospheric nitrogen [267].

To date, > 5000 endophytic strains, including > 3000 bacteria and > 2000 fungi, have been isolated from members of the genus Populus, with > 550 bacterial and ~ 65 fungal genomes sequenced [268]. One of the best known is the fungus Laccaria bicolor, which forms ectomycorrhiza. Others include the arbuscular mycorrhiza-forming fungus Rhizophagus irregularis, the fungi Atractiella, Phialophora, Illyonectria and Mortierella, and the bacterium P. fluorescens [267]. The poplar microbiome is formed at early stages of ontogenesis under the influence of both selection and stochastic factors. Its composition depends on the genotype, habitat and developmental stage of the plant. While bacteria are influenced by strong homogenizing selection during this process, the fungal part of the community develops under the influence of a mixture of weak selective and stochastic processes [269].

Among others, a very important function of the normal plant microbiome, i.e. the totality of all microorganisms interacting with it, is to protect the plant against pathogenic invasion. In this way, they contribute to the stability of the ecosystem to which they belong. Their combined name is DefenseBiome - a community of bacteria associated with defense against infections [270].

Plants during infection can target changes in their microbiome to provide protection - for example, the "cry for help" strategy involves releasing compounds (benzoxazinoids, aminocyclopropane-1-carboxylic acid (ACC), etc.) into the soil that will attract beneficial microorganisms. Therefore, often the relative abundance of bacteria associated with plant defense is elevated during a pathogen attack [270].

Bacteria and fungi utilize several mechanisms to combat infectious agents: (1) direct microbial antagonism, which includes the secretion of antibiotics and antimicrobial toxins, volatiles, cell-wall degrading enzymes, siderophores, etc., (2) positive effects on plant health, thus indirectly allowing the plant to fight infections more effectively, and (3) interactions with the host immune system: priming and induced systemic resistance (ISR). The terms priming and ISR refer to a state of heightened alertness of the whole plant which allows it to respond more quickly and strongly to pathogenic invasion; this is called priming in the early stages and in the later stages it is known as ISR [271].

A good example of direct microbial antagonism can be provided by recently isolated from wild poplar strains of Burkholderia vietnamiensis WPB, Bacillus velezensis AFE 4A and AFE 21B, Pseudomonas sp. AFE 5 and AFE 8. B. vietnamiensis WPB has strong in vitro antifungal activity due to its ability to produce occidiofungin, and clusters of ornibactin, cepacin A, difficidin, macrolactin, bacillaene, fengycin, bacilysin, bacillibactin, sessilin, viscosin and tolaasin, compounds toxic to fungi, bacteria and oomycetes, were detected in the genomes of these strains [69]. B. velezensis and the closely related species B. amyloliquefaciens are often endophytes of plants and can protect them from infection. For example, B. velezensis strain EB14, according to mass spectrometric analysis data, produces five cyclic lipopeptides: iturins A1, A2 and A9, subtulene A and fengycin, thereby inhibiting the growth of S. musiva. Clusters of antibiotic biosynthesis of surfactin, rhizoactin, difficidin, macrolactin, and bacilysin were detected in its genome, and the possibility of biosynthesis of subtulene and fengycin was also confirmed [272,273]. Also, Streptomyces sp. strain SSD49, originally isolated from Stropanthus divaricatus and which is a growth-promoting endophyte for P. tomentosa, is able to inhibit in vitro the growth of phytopathogenic strains of fungi (Cryphonectri parasitica, S. sclerotiorum, D. gregaria, and B. dothidea) and bacteria (Lonsdalea quercina subsp. populi) [247]. A number of other compounds, including primary metabolites, may also participate in such antagonism. For example, endophytic strains of B. velezensis 33RB and Aspergillus niger 46SF suppress the pathogens C. gloeosporioides BJ02 and F. oxysporum 20RF, and the possible bioactive compounds identified by LC-MS are the fumaric, DL-malic, citric, isobutyric, glutamic, lauric, linoleic, oleic, stearic and myristic acids as well as a number of others, totaling about 30 metabolites with proven antimicrobial activity [54].

Symbiotic fungi isolated from P. alba demonstrate mechanisms of antagonism different from those known in bacteria. Belonging to the orders Pleosporales, Eurotiales, Dothideales and Hypocreales, these leaf endophytes in vitro inhibit the growth of Venturia tremulae, due to (1) parasitism on pathogen mycelia and (2) substrate competition, which suppresses pathogen development, whereas (3) antibiosis was rarely observed and it has a relatively weak effect. In any case, P. alba when treated with suspension of these strains becomes more tolerant to shoot blight caused by V. tremulae [274]. Thus, spraying on leaves is one of the practical possibilities of utilizing these strains.

A very interesting example of the first strategy is Cladosporium oxysporum, which is a hyperparasitic fungus towards M. medusae f. sp. deltoidae. This parasitism consists of three distinct mechanisms involving enzymatic, direct and contact parasitism. Thus, C. oxysporum protects poplar from rust, but has no negative effect on the leaves of the plant itself [275].

B. amyloliquefaciens AW3 is an example of a microorganism that prevents the rot caused by F. oxysporum Fox68 by priming P. davidiana × P. bolleana (PdPap) seedlings. Indeed, B. amyloliquefaciens AW3 stimulated expression of PAL, PPO, SOD, CAT, SA- (PR1 and NPR1), JA- (MYC2 and JAR1), and auxin-related (MP, AUX1, and LAX2) genes in plants, thereby enhancing the natural resistance of poplars and being an eco-friendly biocontrol agent for this fungus [276]. Laccaria bicolor, which is a mycorrhizal fungus, affects the expression of a huge number of genes in the plant and protects it from infection by B. dothidea. Exposure to the fungus alters the activity of pathways related to hormone signaling, plant immune responses, cell wall metabolism and ROS scavenging. For example, when exposed to L. bicolor, ROS clearance is more efficient in infected tissues, which reduces ROS-induced stress in the plant and thus allows it to combat infection more effectively, increases the synthesis of cell wall proteins such as expansins, which physically prevent the fungus from entering, the expression of defensive genes increases, etc. [277]. Fungal foliar endophytes isolated from P. trichocarpa have a more localized and limited effect. Stachybtrys sp., T. atroviride and to a lesser extent Ulocladium atrum and Truncatella angustata reduce the degree of leaf damage by the rust fungus M. x columbiana. At the same time, only those leaves, which were previously inoculated with the endophyte, became resistant, which may indicate local stimulation of immune response as well as direct antagonism. In any case, these strains do not cause a systemic reaction of the plant [278].

Disease development is often associated not with the interaction of a single endophyte and a single pathogen, but with a critical change in the entire microbial community. For example, in healthy heartwood of P. x euramericana the dominant bacterial genera are Proteiniphilum, Dysgonomonas and Bacteroides, while during the development of a poorly studied bacterial wet heartwood disease, Proteiniphilum, Actinotalea and Methanobacterium increase in abundance and become dominant. At the same time, both pathogen and disease-associated bacteria may be among these three genera [279].

The microbiome of poplars, and hence their disease resistance, changes with age. When studying the dynamics of the root community in P. tomentosa from 1 year to 35 years of age, it was found that the representation of Actinobacteria increased with age. This process is closely related to the biosynthesis of flavonoids and their content in the soil surrounding the root, and their biosynthesis in turn depends on the activity of the Transparent Testa 8 (TT8) gene, which is a bHLH TF and a component of the WDR complex, as discussed above. Actinobacteria are beneficial in suppressing plant diseases by synthesizing antibiotics - for example, the Streptomyces andamanensis bj1 strain studied in this work is able to biosynthesize hygromycin B or related substances due to the presence of the hyBl cluster in its genome. It is likely that this age-related accumulation of Actinobacteria may be related to poplar longevity, which should be verified in further studies [280].

Endophyte-pathogen interactions are not purely unidirectional. The anthracnose-causing fungus C. gloeosporioides has been shown to reduce the diversity of both bacterial and fungal phyllosphere communities, with the fungal community changing more dramatically. While in healthy leaves the most abundant genera were Mortierella, Fusarium, Colletotrichum, Aspergillus and Cladosporium, after infection the representation of Colletotrichium increased from about a few-20% to 85-100% as the pathogen itself displaced all other fungi. This trend was replicated on different poplar genotypes: P. x canadensis, P. x beijingensis and P. tomentosa, which have respectively different resistance. At the same time, this effect may be not only a consequence of direct antagonism by C. gloeosporioides, but also mediated by secondary metabolites. gloeosporioides, but also mediated by secondary metabolites, many of which were altered during infection [281].

Figure 9. The role of endophytes in the defense of poplar against infection. Endophytes are beneficial for the plant in terms of defence against diseases. They suppress pathogens both directly (by producing antibiotics, parasitising on pathogen mycelia and competing with them for substrate) and indirectly (by improving plant health and stimulating its immune system, termed priming in the case of more localised responses and induced systemic resistance in the case of more global responses). In turn, pathogens also affect the endophytic community, probably through similar direct mechanisms and by altering the secondary metabolite profile of the host plant.

Figure 9. The role of endophytes in the defense of poplar against infection. Endophytes are beneficial for the plant in terms of defence against diseases. They suppress pathogens both directly (by producing antibiotics, parasitising on pathogen mycelia and competing with them for substrate) and indirectly (by improving plant health and stimulating its immune system, termed priming in the case of more localised responses and induced systemic resistance in the case of more global responses). In turn, pathogens also affect the endophytic community, probably through similar direct mechanisms and by altering the secondary metabolite profile of the host plant.

Not all endophytes are beneficial against infections. Among epiphytes and endophytes isolated from wild P. trichocarpa, antagonists of the rust-causing fungus M. x columbiana were found in the genera Cladosporia, Trichoderma, Chaetomium and Penicillium, whereas pathogen facilitators, which exacerbated the disease pattern although they were not pathogenic themselves, were observed in the genera Epicoccum, Alternaria and Cladosporia [282]. Interestingly, this can be leveraged as another tool of plant competition: for example, Penicillium raistrickii was a pathogen antagonist for P. trichocarpa in this study, but it also was earlier described as a pathogen facilitator for Pinus ponderosa [283].

Figure 10. Indirect competition between plants through microorganisms. Endophytes can be used by plants as another mechanism of interspecific competition. The same species and strains of microorganisms may be beneficial to some plants, but at the same time may either cause diseases themselves or be pathogen facilitators for other plant species, which can be used by plants to suppress each other. Similarly, viruses that are asymptomatic in some plants can cause disease in others, such as begomoviruses in poplar.

Figure 10. Indirect competition between plants through microorganisms. Endophytes can be used by plants as another mechanism of interspecific competition. The same species and strains of microorganisms may be beneficial to some plants, but at the same time may either cause diseases themselves or be pathogen facilitators for other plant species, which can be used by plants to suppress each other. Similarly, viruses that are asymptomatic in some plants can cause disease in others, such as begomoviruses in poplar.

The boundary between the normal microbiome and pathogens is an intriguing one. Indeed, since commensals and symbionts carry the same PAMPs as pathogens, they could be detected by PRRs and trigger PTI, but in reality this does not happen because microbes: (1) mitigate the immune response by producing compounds that capture both ROS and organic acids produced by the plant, (2) modify their PAMPs to reduce their recognition efficiency, and (3) contain fewer trigger molecules on the membrane than their free-living relatives. This indicates a significant co-evolution of plants and their microbial symbionts [270]. It should be realized that endophytes of some plants may be pathogens for others. A F. culmorum strain isolated from P. trichocarpa leaves was identical to that of a wheat pathogen causing blight and rot. In the same research, in the leaf microbiome of P. trichocarpa, sequencing revealed representatives of 56 taxa, including Cryptodiaporthe pulchella, Knufia cryptophialidica, Pyrenophora tritici-repentis, Phaeosphaeria pontiformis, Phaeosphaeria nodorum, Phoma macrostoma, B. cinerea, Elytroderma deformans, Taphrina spp., Ciborinia camelliae, Ramularia pratensis, etc. They are pathogens to other plants in the same region, Pacific Northwest USA, including those in the genera Populus and Salix. It is likely that carrying such strains may be another way that poplars use to compete with other plants [57]. A great number of potential pathogens and saprotrophs were found among fungal genera when analyzing early poplar microbiome assembly [269]. And as discussed above, under certain conditions, such as climate change, endophytes can change their life strategy and become pathogens [284]. And it appears that a similar ecological role may be played by the transfer of some viruses, such as earlier discussed begomoviruses and their satellites, which are asymptomatic to poplar and potentially pathogenic to other plants [93]. Thus, the boundary between poplar endophytes that protect the tree from pathogens and the pathogens themselves is quite blurred.

4.2. Phytophages

Despite the traditional view of the damage phytophages cause to plants, there are examples where plant-eating organisms are beneficial. For poplars, there are several such examples.

In addition to endophytes, phytophagous animals can also perform a protective function. For example, it was shown that caterpillars of Lymantria dispar, which are pests of poplars, are more willing to eat leaves of P. nigra infected with the rust fungus M. larici-populina, and on such leaves they first of all eat sporangia of the fungus. The attractant for caterpillars is mannitol, which is more abundant in infected leaves, and the reason for such behavior is that the spores of the fungus have a higher nitrogen content, a more suitable ratio of amino acids for the insect body and a high concentration of B vitamins: B3, B5, B7 and B10 [285].

Pathogens also affect the arthropod community associated with a plant: in a study on P. fremontii, P. angustifolia and their F1 hybrid on the one hand, and the fungus Drepanopeziza populi on the other, it was found that both species diversity and the number of arthropod individuals were reduced in those plants exposed to the pathogen, and not only first-order consumers but also predators were affected. The main reason for this decline in diversity was infection-induced leaf fall. Thus, there is an "equalization" of poplars in terms of adaptability: more pathogen-resistant plants lose their advantage over less resistant ones under herbivory conditions, as infection significantly reduces phytophagy levels [286]. This may also explain why plants do not develop "absolute" resistance to pathogens. Finally, as we discussed earlier, carrying certain viruses (LdNPVs) may be directly dangerous to the phytophage itself (Lymantria dispar) and thus provide an advantage to the plant [94]. Probably, other microorganisms, including those pathogenic to poplar, may be involved in similar defense mechanisms against phytophages.

Finally, poplars can, with the help of their secondary metabolites, protect associated insects from their pathogens. For example, in a research on the honeybee Apis mellifera, six different 3-acyl-dihydroflavonols, which originate from P. fremontii and several other poplar trees in North America and are incorporated into bee propolis, were found to be active against the bacterium Paenibacillus larvae that causes american foulbrood and the fungus Ascosphaera apis that causes chalkbrood [287].

Thus, on the one hand, phytophagous insects may reduce pathogenic pressure on the plant, and infections may lower phytophagy. The plant can both contribute to the infestation of insects with dangerous diseases and give increased resistance to them. All this demonstrates the immense complexity of the ecosystem consisting of plants, phytopathogens, arthropods and arthropod pathogens and emphasizes the need for its further study.

Figure 11. Ecological interactions between poplar, microorganisms and arthropods. Plants, associated microorganisms and arthropods constitute a complex and multifaceted regulatory network. Phytophagous insects can control the spread of phytopathogens by eating preferentially affected leaves because of their more suitable amino acid composition, vitamin content, etc. In turn, pathogens may limit phytophagy by causing stress-induced leaf loss. At the same time, some viruses in the plant may be pathogenic to phytophages. The plant can protect associated arthropods (e.g. bees) from entomopathogens by synthesising secondary metabolites that the insect obtains with food and thus becomes more protected.

Figure 11. Ecological interactions between poplar, microorganisms and arthropods. Plants, associated microorganisms and arthropods constitute a complex and multifaceted regulatory network. Phytophagous insects can control the spread of phytopathogens by eating preferentially affected leaves because of their more suitable amino acid composition, vitamin content, etc. In turn, pathogens may limit phytophagy by causing stress-induced leaf loss. At the same time, some viruses in the plant may be pathogenic to phytophages. The plant can protect associated arthropods (e.g. bees) from entomopathogens by synthesising secondary metabolites that the insect obtains with food and thus becomes more protected.

4.3. Elemental Defense Hypothesis

Not only living organisms but also abiotic factors may contribute to the resistance of plants, including poplars, to infections. Elemental defense hypothesis claims that plants can use chemical elements to protect themselves against pathogens.

In support of this hypothesis, leaves of P. yunnanensis grown under conditions of excess Cd²⁺ had higher resistance to both phytophages (Spodoptera exigua and Botyodes diniasalis) and the pathogenic fungus Pestalotiopsis microspora, while they did not differ from control ones in the concentration of secondary metabolites [288,289]. It is also interesting that the degree of cadmium protection of poplar from both phytophages and leaf pathogens (Pestalotiopsis microspora) depends on other elements of mineral nutrition: for example, when exogenous nitrogen was applied, the plant accumulated more Cd in leaves, which were thus less eaten by insect larvae or affected by fungus [290].

Very intriguingly, Cd-mediated defense can depend on the gender of the plant. In the experiment, male and female individuals of P. deltoides were grown on Cd-contaminated soil. Moreover, male individuals not only accumulated more Cd in leaves but were also more resistant to the pathogen Pestalotiopsis microspora. This may be due not only to the direct toxicity of Cd, but also to indirect effects through the microbiome, which appeared healthier in male plants than female plants when exposed to Cd [291]. In addition, the species P. deltoides shows that males are more resistant to leaf herbivores and more susceptible to root herbivores compared to their female relatives under soil stress in the presence of this heavy metal. Such sex differences in resistance to herbivores are most likely due to differences in the patterns of Cd accumulation and distribution in plants of different sexes [292].

The opposite situation was reported for the other metal. The authors grew P. simonii seedlings on medium with different zinc concentrations and examined the effect on how vulnerable they will be to rust disease. It turned out that Zn-stress not only reduced seedling biomass, but also increased their susceptibility to the disease, which is probably associated with a decrease in the natural chemical defense of the plant organism [293].

Figure 12. Elemental defence hypothesis. Atoms of heavy metals (zinc, copper, cobalt, nickel, cadmium), which are frequent soil pollutants and are largely absorbed by poplar because of their non-specific toxicity, protect the leaves of the plant (where metals accumulate in high concentrations) from being eaten by phytophages and infected by pathogens. This is called the elemental defence hypothesis. At the same time, heavy metals themselves sometimes make the plant more susceptible to disease by negatively affecting its own biochemical defences and health.

Figure 12. Elemental defence hypothesis. Atoms of heavy metals (zinc, copper, cobalt, nickel, cadmium), which are frequent soil pollutants and are largely absorbed by poplar because of their non-specific toxicity, protect the leaves of the plant (where metals accumulate in high concentrations) from being eaten by phytophages and infected by pathogens. This is called the elemental defence hypothesis. At the same time, heavy metals themselves sometimes make the plant more susceptible to disease by negatively affecting its own biochemical defences and health.

Whether an element protects against pathogens probably depends on the chemical and biological properties of the element itself - for example, Cd²⁺ may be more toxic to phytopathogens than Zn²⁺, but exposure of the plant itself to Zn²⁺ may be sufficient to weaken its own chemical defense mechanisms. It is also possible that different pathogen groups and different poplar genotypes vary in their resistance to different heavy metals. Thus, the elementary defense hypothesis may be appropriate in some cases and completely unacceptable in others, and it all depends on the specifics of a particular system.

5. The Sex of the Tree - as a Factor in Determining the Effectiveness of Plant Protection

6. Conclusions

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