Transcriptional Regulation and Gene Expression of Disease-Responsive Genes in Model Plants and Hevea Brasiliensis

ABSTRACT

Plant immunity relies on coordinated transcriptional reprogramming that integrates pathogen perception, hormone signaling, and redox homeostasis to balance effective defense with growth and development. While these mechanisms have been extensively characterized in model plants, their conservation and diversification in woody perennial crops remain less well understood. Hevea brasiliensis, the primary source of natural rubber, represents a biologically important tree crop in which immune regulation must be tightly coordinated with specialized laticifer metabolism and long life cycles. Here, we review current advances in understanding the transcriptional regulation of immune responses in Hevea, with a focus on major transcription factor (TF) families (WRKY, AP2/ERF, NAC, and MYB) and cis-regulatory elements conserved in defense regulation in model plants. We additionally discuss pathogenesis-related genes and the roles of reactive oxygen species (ROS) biosynthesis and detoxification genes in Hevea immunity. Transcriptomic evidence indicates that Hevea activates core immune modules shared with model plants, while also exhibiting additional layers of distinctive regulatory complexity, including tissue-specific gene expression in laticifers during wounding and pathogen infection. We conclude by discussing current limitations in functional validation and highlight future directions integrating RNA-seq, cis-regulatory elements analysis, and targeted functional genomics to elucidate biotic stress networks. Such advances will be critical for accelerating molecular breeding strategies aimed at improving disease resistance while preserving natural rubber productivity.

1. Introduction

Biotic stressors such as fungi, bacteria, and viruses can infect plants, inhibit plant growth, and reduce yield. To protect against pathogen invasion, plants have developed complex defense systems, controlled by many genes that switch on in response to biotic stress. In the first layer of defense, plant immune responses to pathogens depend on the pathogen-associated molecular patterns (PAMPs) perceived by specific pattern recognition receptors (PRRs). This detection initiates a defense mechanism known as PAMP-triggered immunity (PTI) [1] while the second layer is the effector-triggered immunity (ETI) [2, 3]. The host cells activate transcriptional reprogramming including dynamic regulation of signaling networks, transcription factors (TFs), and effector genes [4]. Advances in high-throughput studies have shown the molecular basis of plant immunity in model plants, such as Arabidopsis and rice [5, 6]. Several reports consistently show that infection triggers the activation of defense-related genes, such as pathogenesis-related (PR) proteins, reactive oxygen species (ROS)-related proteins, and hormone-responsive regulators [7, 8, 9].

Transcriptomic studies examining the responses of tropical tree species to pathogen infection are beginning to emerge, yet a substantial knowledge gap remains compared with the deep understanding obtained from model and non-woody plants. Hevea brasiliensis, a major economic tree crop valued for latex production, is similarly exposed to diverse biotic challenges, but its defense regulatory mechanisms remain poorly characterized. Consequently, mechanistic interpretations in Hevea are often inferred based on findings from related or better-studied species rather than from direct experimental evidence. Recently, transcriptomic studies in Hevea reveal strong activation of WRKY, NAC, ERF, and MYB transcription factors, early ROS accumulation, hormone crosstalk, and induction of PR proteins [10, 11]. As a perennial species, Hevea brasiliensis experiences constant environmental fluctuations, requiring flexible and stimulus-dependent modulation of its defense responses when confronted with pathogen attack. Understanding how transcriptional regulation in Hevea compares with that of model plants is critical for breeding disease-resistant rubber and for elucidating immune mechanisms in woody plants. This review provides current information on the transcriptional regulation and gene expression of disease-responsive genes in model plants and Hevea brasiliensis, and proposes research priorities for the molecular understanding of defense regulation in this important tropical tree crop.

2. Transcriptional regulation during pathogen infection

Transcription factors regulate gene expression by binding to specific cis-regulatory elements in promoter regions, thereby modulating the expression of downstream regulatory and defense-related genes. This coordinated interaction establishes an integrated transcriptional network essential for plant stress responses.

Comparative transcriptomic analyses of two Hevea clones following infection with Corynespora cassiicola revealed distinct gene expression and transcription factor regulatory patterns associated with contrasting levels of disease susceptibility [12]. Notably, genes encoding several transcription factor families, including WRKY, NAC, and GATA, were upregulated during disease development in both clones [12], suggesting their involvement in the core defense response. These transcription factor families are well characterized in model plant systems, where they play central roles in coordinating immune signaling and defense gene expression during pathogen attack. Their conserved induction in Hevea brasiliensis during C. cassiicola infection supports the notion that core transcriptional regulatory frameworks governing biotic stress responses are evolutionary conserved between herbaceous model plants and woody perennial species.

2.1 Transcriptional regulators of defense

Plant defense signaling triggers transcriptional reprogramming mediated by transcription factors that serve as key modulators of plant immune responses. During pathogen infection, defense responses are governed by complex regulatory networks involving multiple signaling cascades and dynamic metabolic reprogramming. Among the transcription factor families involved, WRKY, AP2/ERF, NAC, and MYB are frequently implicated in the regulation of immune responses to biotic stress [13, 14, 15, 16].

2.1.1 WRKY transcription factors

The WRKY transcription factors constitute a prominent family of plant-specific regulatory proteins marked by the conserved WRKY domains and the zinc-finger motif [17]. Members are classified into three groups according to the number of WRKY domains and the nature of their zinc finger motifs. Each WRKY domain consists of an N-terminal DNA-binding domain (DBD) harboring the conserved WRKYGQK heptapeptide and a C-terminal zinc finger motif that is essential for DNA binding and protein stability [18]. WRKY transcription factors can act as activators or repressors depending on the cellular and environmental context [19], and play pivotal roles in plant responses to abiotic and biotic stresses, as well as in development and senescence, primarily by binding to W-box (TTGACC/T) elements in the promoters of defense and stress-responsive genes [18, 20].

In Arabidopsis, AtWRKY18, AtWRKY40, and AtWRKY60 act cooperatively and partially redundantly as negative and positive regulators of resistance to both the hemibiotrophic bacterial pathogen Pseudomonas syringae and necrotrophic fungal pathogen Botrytis cinerea, with AtWRKY18 playing a more crucial role [21]. The contrasting effects of mutations of the three WRKY genes to the microbial pathogens reflect the antagonism between salicylic acid (SA)- and jasmonic acid (JA)-mediated defense signaling pathways [21]. Birkenbihl et al. [22] demonstrated that AtWRKY33 expression is strongly induced during B. cinerea infection. The atwrky33 mutant exhibits increased susceptibility to the pathogen, attributed to a reduction in the JA-regulated expression of PDF1.2 and impaired camalexin biosynthesis [22, 23]. Conversely, overexpression of AtWRKY33 enhanced the resistance against B. cinerea [23].

In maize (Zea mays), WRKY transcription factors comprise approximately 120 members, of which seven show significant transcriptional upregulation in response to infection by Ustilago maydis. These WRKY TFs specifically bind to ZmSWEET4b (the sugar transporter) promoter, either subjecting it to self-activation or enhancing its transcriptional activity [24]. Taken together, WRKY TF functions as either an activator or a repressor in the biotic stressors.

In Hevea, 111 genes have been identified to encode the WRKY proteins. HbWRKY40 is strongly induced by Colletotrichum gloeosporioides and salicylic acid and directly binds to the promoters of MYB and ethylene-responsive transcription factor genes [25], indicating a role in coordinating cross-regulatory transcriptional network during pathogen infection. The overexpression of HbWRKY40 in tobacco triggers ROS burst and enhances resistance to B. cinerea in Arabidopsis [25]. Other HbWRKY TFs, such as HbWRKY1, HbWRKY27, and HbWRKY83, are also involved in wound responses, direct gene regulation, hormone-mediated signaling pathways, drought, salt stress, and natural rubber biosynthesis [26, 27, 28].

2.1.2 AP2/ERF transcription factors

AP2/ERF TF family is classified into four major subfamilies: APETALA2 (AP2), Dehydration-Responsive Element Binding Proteins (DREBs), Related to Abscisic Acid Insensitive 3/ Viviparous 1 (RAV), and Ethylene Responsive Element Binding Factors (ERFs) [29]. The AP2/ERF TFs are involved in the regulation of various downstream target genes related to plant growth, development, response to plant hormones such as abscisic acid (ABA) and ethylene (ET) [30, 31] and mediated responses to both biotic and abiotic stress regulation [31, 32]. However, their downstream regulation does not always confer a beneficial effect in the plant and can also be associated with adverse developmental outcomes [31]. In the context of plant defense, the AP2/ERF TF family is crucial in regulating plant defense mechanisms against biotic stress. Recent studies indicate that AP2/ERF TFs mediate immune signaling via complex regulatory networks, primarily acting downstream of mitogen-activated protein kinase (MAPK) cascades [33]. These TFs coordinate the expression of defense-related genes that are important for systemic acquired resistance (SAR) and localized defense responses against biotrophic and necrotrophic pathogens [33, 34].

Arabidopsis ORA59, an AP2/ERF transcription factor, has been identified as a major regulator of pathogen-induced phytoalexin synthesis that is involved in ET and JA signaling pathways [30, 35] in defense systems against B. cinerea necrotrophic pathogen [30]. Similarly, AtERF014-overexpressing plants exhibited enhanced expression of SA-responsive genes (AtPR1 and AtPR5), and increased ROS accumulation, following infection with Pseudomonas syringae pv. tomato. In contrast, overexpression of AtERF014 suppressed JA-responsive gene AtPDF1.2 during B. cinerea infection [36]. Thus, AP2/ERF transcription factors have dual functions in plant immunity, coordinating antagonistic SA and JA/ET pathway based on the stressors.

The AP2/ERF TFs have also been investigated in transgenic rice for their role in response to biotic stress. Overexpression of OsEREBP1 enhances tolerance to abiotic and biotic stresses, functioning downstream of signaling pathways activated during Xanthomonas oryzae infection. This gene regulates the expression of genes involved in JA and ABA signaling, as well as lipid metabolism [37]. Similarly, OsBIERF3 overexpression enhances immunity against Pyricularia oryzae (syn. Magnaporthe oryzae) and Xanthomona oryzae by activating PRs, MAPK pathways, and cell wall biosynthesis genes, including cellulose synthase genes (OsCes7 and OsCesA9) and glucan endo-1,3-beta-glucosidase genes [38]. In addition, OsERF83 overexpression in plants leads to the upregulation of PR genes, including PR1, PR2, PR3, PR5, and PR10 during P. oryzae infection [39]. In contrast, OsERF922 acts as a negative regulator, its overexpression suppresses defense-related genes, including PRs, PAL, and genes involved in phytoalexin biosynthesis [40]. Collectively, these studies demonstrate that AP2/ERF TFs contribute to pathogen resistance in rice by modulating the expression of key defense-related genes.

Transcriptomic analyses have identified 142 AP2/ERF transcription factor contigs in Hevea, comprising 20 AP2, 115 ERF, 4 RAV, and 3 soloist members [29]. Hevea AP2/ERF transcription factors respond to pathogen attack and are involved in hormone signaling pathways (ET, JA), latex metabolism, and tapping panel dryness [29, 41, 42, 43, 44], although the functional evidence is still limited. Gene expression analyses of HbERF genes following phytohormone treatments revealed that HbERF-IXc4 and HbERF-IXc5 are capable of transactivating the GCC-box, and it is assumed that they may have regulatory roles in modulating defense genes in laticifers [44].

2.1.3 NAC transcription factors

The NAC transcription factor family comprises more than 100 genes in each of Arabidopsis [15], rice [45, 46], maize [47, 48], and wheat [49]. The TFs are classified on basis of a highly conserved DNA-binding domain and by their distinct and sometimes overlapping functional roles in regulating plant development and defense mechanisms [15].

Members of the NAC TF family play important roles in immune response, including plant hormone signaling, hypersensitive response (HR), regulation of defense genes, and interaction with pathogen-derived effectors [14]. AtATAF2, a NAC-domain transcription factor, is induced in response to tobacco mosaic virus (TMV) infection, and its overexpression leads to a reduction in virus accumulation and the upregulation of defense-related marker gene PR1 in infected tissues [50]. In tomato, LeJA2 and LeJA2L genes play distinct roles in the regulation of stomatal movement during pathogen infection. Expression of LeJA2 is induced by the gene LeNCED1, a key gene in the ABA biosynthesis pathway, whereas LeJA2L expression is induced by JA and toxin coronatine (COR) to regulate the transcriptional activation of genes related to metabolism of SA [51].

Genome-wide studies have identified 51 NAC genes in Hevea, of which 11 HbNAC genes are homologous to Arabidopsis NACs [52]. The involvement of HbNAC genes in response to cold and drought stress [52, 53, 54], as well as in infection by C. cassiicola [12] has been documented. Promoter analysis of HbNAC genes by Yang et al. [52] revealed enrichment of cis-regulatory elements associated with environmental stress responses (anaerobic induction, low temperature, drought, defense, and wound responsiveness), hormone responsiveness (ABA, auxin, gibberellin, and SA) and developmental regulation (meristem expression, cell cycle control). Both Arabidopsis and Hevea share conserved NAC subfamilies, although the size of the several subfamilies differs between the two species. Notably, the HbNAC subfamily VIII appears to be specific to Hevea, suggesting species-specific evolutionary divergence that may confer specialized functional role in woody plants.

2.1.4 MYB transcription factor

MYB transcription factors have been identified in eukaryotes, including Arabidopsis, rice, maize, and soybean. The MYB superfamily of TFs is divided into four groups based on the number and position of MYB repeats, namely 1R-MYB, 2R-MYB, 3R-MYB, and 4R-MYB [55]. Among these, the 1R-MYB and 2R-MYB groups represent the largest MYB families in higher plants. The MYB TFs are known to play important roles in growth, development, and stress responses, particularly in signal transduction in response to pathogen invasion [5]. In the context of biotic stress responses, MYB TFs play pivotal roles in plant immunity, functioning as either negative or positive regulators of host defense during fungal pathogenicity [56, 57]. Moreover, the involvement of MYB TFs in hormonal crosstalk, such as SA, JA, and ET pathways, has been investigated as central to the Arabidopsis defense mechanism [5, 58].

In Arabidopsis, numerous MYB TFs, particularly those belonging to the R2R3-MYB subgroup, have been implicated in regulating plant defense responses. For instance, BOTRYTIS SUSCEPTIBLE (BOS1), a R2R3-MYB TF regulate plant responses to biotic stress by mediating signaling from reactive oxygen molecules [59]. Another key member, AtMYB30, is known as one of the HR activators upon pathogen infection [60, 61], modulating the biosynthesis of very-long-chain fatty acids (VLCFAs) and reprogramming toward the other signaling molecules involved in programed cell death [61]. Furthermore, AtMYB15 is involved in reinforcing the plant cell wall through the transcriptional activation of lignin biosynthesis genes upon pathogen challenge [62, 63]. The expression of OsMYB4 in Arabidopsis has been reported to be involved in phenylpropanoid biosynthesis, SAR pathway, and ROS scavenging during P. syringae pv. tomato and B. cinerea infections [64].

In rice, MYB TFs have also been involved in both basal and inducible resistance to various pathogens, including fungal and bacterial infections. For example, OsMYB30, in cooperation with OsMYB55 and OsMYB110, activates the hydroxycinnamic-acid amide (HCAA) in the cinnamate/monolignol pathway, leading to increased HCAA accumulation, such as ferulic acid (FA), which plays important roles in cell-wall reinforcement and exhibits antimicrobial activity against the blast fungus P. oryzae infection [65]. Li et al. [66] revealed that P. oryzae induces the OsMYB30 binding and transactivation of 4-coumarate:coenzyme A ligase (Os4CL3 and Os4CL5) genes, which are responsible for lignin biosynthesis, leading to sclerenchyma thickening.

In Hevea, genome-wide analysis identified over 40 HbMYB proteins from rubber tree laticifer cells, which were grouped into 17 subgroups based on Arabidopsis orthologs. Transient overexpression of Hblmyb19 and Hblmyb44 in tobacco activated the promoter of HbFDPS1 and HbSRPP, which participate in natural rubber biosynthesis [67]. Hbmyb1 expression is reported to be responsive to latex tapping and ethephon stimulation [68]. The effects of wounding and hormonal treatment highlight the pivotal role that MYB factors play in defense regulation. In disease context, the overexpression of Hbmyb1 in transgenic tobacco suppresses stress-induced cell death caused by B. cinerea. In addition, RNA-seq work on wood and lignification in Hevea reported by Meng et al. [69] showed that TFs from the MYB, C2H2, and NAC family are involved in phenylpropanoid biosynthesis pathway, which may be linked to potential stress responses. As a result, the studies on MYB TFs in Hevea during pathogen infection are still limited. The direct role of TFs in the plant-pathogen interaction in disease resistance requires further study. The summary of the involvement of WRKY, AP2/ERF, NAC, and MYB TFs in regulating immune responses to biotic stresses are shown in Table 1.

Table 1: Transcription factors involved in plant responses to biotic stress

Family/ Subfamily	Transcription factor	Plant	Pathogen	Function	Reference
WRKY	AtWRKY18, AtWRKY40, AtWRKY60	Arabidopsis	Pseudomonas Syringae	Negative regulators of resistance; modulate SA-dependent defense signaling.	[21]
	AtWRKY18, AtWRKY40, AtWRKY60	Arabidopsis	Botrytis cinerea	Positive regulators of resistance; associated with JA-mediated defense pathway.	[21]
	AtWRKY33 (mutant)	Arabidopsis	Botrytis cinerea	Reduction in JA-mediated regulation of PDF1.2 in atwrky33 mutant.	[22, 23]
	WRKY TFs	Maize	Ustilago maydis	The WRKY TFs bind to the ZmSWEET4b promoter and self-activate or enhance its transcriptional activity.	[24]
AP2/ERF	AtORA59	Arabidopsis	Botrytis cinerea	pathogen-induced phytoalexin synthesis and involvement in ET and JA-signaling pathways.	[30, 35]
	AtERF15 (overexpression)	Arabidopsis	Pseudomonas Syringae; B. cinerea	Reduction in ROS accumulation in overexpressing plants.	[6]
	AtERF014 (overexpression)	Arabidopsis	Botrytis cinerea	Positively regulates SA-responsive genes (PR1, PR5) while acting as a suppressor of JA gene (PDF1.2).	[36]
	OsEREBP1 (overexpression)	Rice	Xanthomonas oryzae	OsEREBP1 overexpression regulates JA and ABA signaling and also involved in lipid metabolism.	[38]
	OsBIERF3 (overexpression)	Rice	P. oryzae; Xanthomonas oryzae	Enhances plant immunity through the activation of PRs, MAPK pathways, and cell wall biosynthesis genes (OsCes7 and OsCeA9) in overexpressing plants.	[38]
	OsERF83 (overexpression)	Rice	P. oryzae	Overexpressing plants upregulate PR gene transcripts (PR1, PR2, PR3, PR5, PR10).	[39]
	OsERF922 (overexpression)	Rice	P. oryzae	OsERF922 overexpression suppresses the activation of defense-related genes (PRs, PAL), and genes involved in phytoalexin biosynthesis.	[40]
NAC	AtATAF2 (overexpression)	Arabidopsis	Fusarium oxysporum	Enhances resistance to the pathogen.	[50]
	JA2 and JA2-like	Tomato	P. Syringae pv. tomato DC3000	JA2 regulates an ABA biosynthetic gene, whereas JA2-like regulates the activation of genes involved in SA metabolism.	[51]
MYB	BOS1	Arabidopsis	B. cinerea; A. brassicicola	Mediates signaling from reactive oxygen molecules.	[59]
	AtMYB30	Arabidopsis	n.a	It acts as an HR activator, an early regulator in MAMP signaling pathway, and a direct transcriptional target of bri1-EMS-suppressor 1 (BES1) which activates brassinosteroid genes.	[60, 61]
	AtMYB15	Arabidopsis	n.a	Involved in reinforcing the plant cell wall.	[62, 63]
	OsMYB30	Rice	Pyricularia syringae	Acts cooperatively with OsMYB55 and OsMYB110 to increase hydroxycinnamic acid amide (HCCA) accumulation needed for cell-wall reinforcement.	[65]
	OsMYB30	Rice	P. oryzae	Transactivates Os4CL and Os4CL5 which are responsible for lignin biosynthesis, thereby leading to sclerenchyma thickening.	[66]

n.a – not applicable

2.2 Cis-elements in resistance regulation

Plants constantly encounter a diverse array of biotic stressors and have evolved sophisticated defense systems that rely heavily on rapid and large-scale transcriptional reprogramming [70, 71]. Upon perception of pathogen- or damage-associated molecular patterns, immune signaling cascades involving SA, JA, ET, and other hormones channel signals toward the nucleus, where transcription factors orchestrate the activation or repression of defense-related genes [72, 73]. Central to this regulatory rewiring are cis-regulatory elements (CREs) in the promoter region of genes which govern the transcription of genes. CREs represent the primary interface between upstream immune signaling and downstream transcriptional outputs [74], and thus lie at the core of plant immune specificity, speed, and robustness. Despite the differences in gene promoter architecture of genes, the modulation of defense-related transcription by DNA binding proteins has led to the identification of common defense-associated motifs such as the W-box (TTGACC/T, WRKY TF binding), GCC-box (AGCCGCC, AP2/ERF TF binding), TGA/as‑1 elements (TGACG or TGACGTCA, TGA/bZIP binding) and MYB recognition elements (MREs) [20, 75, 76]. Enrichment patterns across promoters induced by different attackers reflect both shared immune circuitry and pathogen-class–specific signaling, permitting plants to balance general defenses with specialized responses. Below we discuss two common CREs as motif signatures enriched in promoters of genes induced by pathogens and wounding.

2.2.1 W-box

The W-box motif (TTGACC/T) is recognized by the WRKY TFs family via a conserved ~60 amino acids WRKY domain and a C2H2 zinc finger [20, 71, 77, 78]. PTI initiated by PRRs rapidly activates MAPK cascades that in turn induce and activate WRKY TF [79] which bind W-boxes in promoters of early defense genes and amplify transcriptional outputs [71, 80]. Promoter analysis of Arabidopsis early flg22-induced genes reveals the overrepresentation of the W-box cis-acting element [80, 81, 82], and this serves as fast-response binding site for WRKY-mediated transcriptional activation during bacterial perception. Enrichment of W-box and few other cis-acting elements have been recorded in rice during pathogen attack [83]. Mutational analyses of W-boxes in promoter regions of PR-1 [84], NPR1 [85], RLK4 [86], AtWRKY33 [87], RPP8 [88] have demonstrated their relevance to immune regulation in Arabidopsis. Evidence suggests that W-box can direct wounding- and pathogen-inducible gene expression in plants [89, 90]. Resistance (R) genes can be induced during ETI, and the majority of the genes encoding R protein contain a nucleotide-binding site and leucine rich repeats (NLR proteins), and W-box is significantly enriched in their promoter [88]. The W-boxes are important regulatory elements in genes that encode redox components, transcriptional regulators of defense, and antimicrobial genes, thus establishing WRKY TFs role in coordinating defense responsiveness (see [78, 91]). The induction of a pathogenesis-related (PR) gene requires W-box [25, 92, 93], an element which also modulates resistance to pathogen attack [85]. The W-box is suggested to be involved in autoregulation as it is statistically enriched in the promoters of activated AtWRKY genes triggered by SA-dependent defense [91, 94].

2.2.2 GCC-box

The GCC-motif (AGCCGCC) is a CRE primarily identified as an ethylene-responsive element in promoters of PR genes and it is bound by members of the AP2/ERF TF family [76, 90, 95, 96, 97, 98, 99]. Over decades of work, the GCC-box has been shown to play a central role in defense gene regulation in response to necrotrophic pathogens, wounding, and combinations of JA and ET signaling [71, 90, 95, 99, 100, 101]. The motif is found to be over-represented in the promoters of many PR genes [83, 95, 101]. Promoter mutagenesis studies have demonstrated the importance of GCC-box element in methyl jasmonate (MeJA) responsiveness of PDF1.2 [100, 102] and ET regulation of PDF1.2 [103]. Overexpression of ERF96 in Arabidopsis induces several defense genes, among which the genes with GCC-box in their promoters were reported to have the strongest activation and are directly bound by ERF96 [95]. ERF96 is JA and ET responsive, triggers the expression of JA/ET-responsive defense genes enriched in GCC elements in their regulatory region [95]. A tetrameric construct of GCC-box has been shown to be responsive to JA and ET [103], wounding and incompatible biotrophic oomycete Peronospora parasitica pv. Cala2 in transgenic plants [90]. A genome-wide survey in rice identified a large number of promoters harboring the GCC-box, as well as other pathogen-inducible cis-elements, and many of those genes encode disease-resistance/susceptibility proteins and transcription factors [83]. OsERF922, a transcriptional activator, acts on GCC-box–containing genes and influences resistance to the rice blast fungus P. oryzae [40]. The GCC-box defines a core element of JA/ET-driven immune transcription, linking pathogen perception to downstream defense gene activation in plants.

3. Core disease-responsive genes and their functions

3.1 Pathogenesis-related (PR) gene families

Pathogenesis-related (PR) proteins are among the earliest-discovered plant defense proteins, playing a crucial role in the plant defense mechanism against pathogenic invasion. Recently, PR proteins have been grouped into nineteen families (PR-1 to PR-19) based on their characteristics and functions [7, 9]. Depending on the plant-pathogen interactions, various PR proteins are typically involved in SAR defense mechanism, which leads to modifications of the cell wall and phytoalexin production.

Several PR proteins exhibit enzymatic activities that are directly involved in the plant defense mechanism. For instance, β-1,3-glucanases and chitinases degrade structural polysaccharides in pathogen cell walls, peroxidases help generate ROS activity, and ribonucleases may participate in phytohormone-dependent signaling [9]. By contrast, some PR proteins function as non-enzymatic antimicrobials, most notably thionins and defensins, which exhibit toxicity toward invading pathogens [104]. PR-1, PR-2, and PR-5 are SA-responsive and associate with biotrophic pathogens, whereas PR-3, PR-4, and PR-5 are involved in JA and ET signaling pathways and contribute to resistance against necrotrophs [7]. In this chapter, we discuss common PR proteins induced by pathogens in model plants and Hevea.

$\beta$ -1,3-glucanases, members of the PR-2 protein family, are endonuclease enzymes (E.C.3.2.1.39) found in bacteria, fungi, invertebrates, and plants. β-1,3-glucanases play multiple roles in plant physiological and developmental processes, including cell division and seed germination. These enzymes also act as defenses against pathogens [105, 106, 107]. In the context of plant-pathogen interaction, tobacco class I β-1,3-glucanases inhibit Fusarium solani hyphal germination, resulting in lysis because of hydrolysis of the fungal cell walls [108]. Similarly, in wheat kernels, β-1,3-glucanase plays differential inhibitory effects on the hyphal growth of Fusarium graminearum, spore formation of Penicillium sp., and mycelial morphology of Alternaria spp. [109]. Moreover, the interaction between rice and P. oryzae demonstrated the antifungal function of Gns6, a β-1,3-glucanase, which can inhibit the germination of germ tubes and appressoria of P. oryzae, a pathogen that causes blast disease in rice [110].

Chitinases are hydrolytic enzymes (E.C. 3.2.1.14) that catalyze the hydrolysis of chitin, a polymer of N-acetyl-D-glucosamine. Chitinases in plants function in the degradation of chitin in fungal cell walls. These enzymes hydrolyze pathogen elicitors, transforming them into eliciting oligosaccharides [9]. Researchers have conducted functional studies on PR-3 proteins and their corresponding genes. Filyushin et al. [111] revealed that chitinase genes in garlic (AsCHI2, AsCHI3, and AsCHI7) were induced during Fusarium proliferatum infection and were linked to the SAR pathway, as evidenced by the presence of SA-responsive elements in the promoters of AsCHI2, AsCHI3, and AsCHI7. In addition, He et al. [112] reported that overexpressing strawberry FvChi-14 in Arabidopsis modulated in SA and JA signaling pathways, thereby conferring resistance to C. gloeosporioides. Moreover, chitinase activity from bean expressed in transgenic tobacco delayed disease development following infection with Rhizoctonia solani [113].

In Arabidopsis thaliana, At3g49120 (AtPCb) and At3g49110 (AtPCa) encode class III peroxidases that are involved in H₂O₂ production in response to Fusarium oxysporum infection [114]. Similarly, the tomato LePrx09 gene is transcriptionally induced by diverse stressors, including wounding, oxidative stress (H₂O₂ exposure), and infection with Alternaria solani [115]. Collectively, these findings highlight the importance role of peroxidase in plants during pathogen infection, specifically the modulation of H₂O₂ homeostasis and signaling [8]. Pathogen-responsive genes in plants are summarized in Table 2.

Table 2: Pathogen-responsive genes involved in plant responses to biotic stress

Protein/gene	Plant	Pathogen	Function	Reference
β-1,3-glucanase	Tobacco	Fusarium solani	Involved in the inhibition of fungal hyphal germination via hydrolysis of fungal cell walls.	[108]
β-1,3-glucanase	Wheat	Fusarium graminearum Penicillium sp., Alternaria spp.	Inhibition of hyphal growth.	[109]
β-1,3-glucanase	Rice	P. oryzae	Inhibits the germination of germ tubes and appressoria.	[110]
Chitinase AsCHI2, AsCH13, AsCHI7	Garlic	Fusarium proliferatum	Involve in SAR through SA-mediated pathway.	[111]
Chitinase FvChi-14 (overexpression)	Arabidopsis	Colletotrichum gloeosporioides	Linked to SA and JA signaling pathway.	[112]
Peroxidase LePrx09 (overexpression)	Tomato	Alternaria solani	LePrx09 participate in the H2O2 signaling pathway.	[115]

In recent years, numerous studies have examined the roles of PR genes in Hevea during pathogen infection. PR-1, PR-2 (β-1,3-glucanase), PR-3 chitinase, and PR-10 genes are induced upon pathogen infection by Microcyclus ulei, Corynespora cassiicola, Phytophthora palmivora, Phytophthora meadii and Rigidoporus microporus [10, 12, 116, 117, 118, 119, 120, 121]. Hurtado Páez et al. [10] reported that M. ulei suppressed ET/JA-associated pathway by downregulating AP2/ERF genes, while inducing SA accumulation and cell-wall reinforcement. This phenomenon is consistent with classical SA-ET/JA crosstalk in plant immunity. During necrotrophic infection by Corynespora cassiicola, both tolerant and susceptible Hevea clones activate defense response, including production of PR protein, and secondary metabolism. In the tolerant clone, transcriptional reprogramming occurs earlier, whereas in the susceptible clone, the transcriptional response is delayed but exhibits a much stronger HR-like burst of gene expression [120]. The summary of pathogen-responsive genes in Hevea is presented in Table 3.

Table 3: Pathogen-responsive genes in Hevea responses to biotic stress

Pathogen/Stress/treatment	Analysis/method	Finding	Gene	Reference
Microcyclus ulei (SALB) Biotroph	RNA-Seq (Resistance clone FX 3864)	Induction of PR/chitinase, phenylpropanoid, cell-wall reinforcement, SA-related genes. Suppression of ET/JA-associated pathway via down-regulation of AP2/ERF genes.	PR1/PR5, chitinase, β-1,3-glucanase, PAL/4CL	[10]
Corynespora cassiicola Cassicolin Cas1 toxin Necrotroph (toxin-mediated)	RNA-seq (time course transcriptome analysis of a tolerant and a susceptible clone)	Both clones activate defense genes and secondary metabolisms. The transcriptional response in the susceptible clone is delayed but exhibits a much stronger HR-like burst of gene expression.	AP2/ERF TFs, chitinase, defensin-like, kinases	[120]
Phytophthora palmivora (hemibiotroph oomycetes)	PTI/priming by elicitor and ABA treatment	ABA activated with PRs and cell-wall reinforcement.	HbPR1, HbASI, HbCAT	[117]
Rigidoporus microporus (white root disease; necrotroph)	qRT-PCR analysis	Differential expression of defense-related genes among clones.	Defense-related genes with clones specific HbPR1, HbPR3, HbPAL (high in tolerance clone)	[119]
Phytophthora meadii	RNA-seq; qRT-PCR	Early induction of WRKY and MYB TFs and a robust hormonal signaling response during mid-phase of pathogen response in the tolerant rubber clone.	HbPR genes; R genes, ROS-related genes	[116, 121]

3.2 Reactive oxygen species (ROS) biosynthesis and detoxification genes

ROS are produced naturally from redox reaction during aerobic respiration and photosynthesis. ROS production is required for SAR and its production peaks during PTI have been extensively reviewed in [122]. To mitigate the potentially damaging effect of ROS and to preserve redox homeostasis, plant cells coordinate networks of enzymatic and non-enzymatic scavenging systems. During stress responses, plants synthesize ROS, known as oxidative burst. Microbial elicitors and pathogen attacks trigger a cascade of host gene expressions, some of which play important roles in the biosynthesis and detoxification of ROS. Here, we review the functions and transcription of genes involved in ROS biosynthesis and detoxification as affected by biotic assaults; however discussion of ROS signaling pathways in response to stress is beyond the scope of our review and has been addressed elsewhere (see [122, 123, 124, 125]).

Superoxide (O₂^-) production is catalyzed by respiratory burst oxidase homologs (Rbohs), a NADPH oxidase (NOX) homolog in plant. Arabidopsis Atrboh transcripts are modulated by environmental cues, where AtrbohC to F are activated by a variety of biotic stresses [126, 127]. AtrbohD and AtrbohF function in ROS production but have distinctive functions in hypersensitive resistance regulation during interactions with avirulent P. syringae and Hyaloperonospora arabidopsis [127]. Enhanced resistance to necrotrophic fungus A. brassicola is conferred in mutants of atrbohD [128]. Repression of Rboh activity altered redox-related metabolism and induced multiple pleiotropic developmental effects, in addition to impairing systemic wound responses [126, 129]. In tomato, silencing of SlRbohB, a homolog of Arabidopsis AtRbohD, reduced resistance to B. cinerea, accompanied by diminished pathogen-induced ROS accumulation and attenuated activation of defense-related genes [130]. Together, these findings highlight Rboh proteins as key enzymatic hubs integrating environmental cues with ROS-mediated defense signaling and developmental regulation.

ROS production is an integral component of phytohormone-mediated signaling pathways. SA is synthesized via the isochorismate and phenylalanine ammonia-lyase pathways [131], processes that are promoted by ROS accumulation [132]. ROS generated by Rboh act in several hormonal signaling pathways [126] and plant immunity responses during pathogen-host interactions [133, 134]. Pogány et al. [128] revealed that SA reinforces ROS signaling by transcriptionally activating ROS-producing genes, thereby promoting localized cell death in infected tissues. Mechanistically, ROS and SA engage in a positive feedback loop in which ROS promotes SA biosynthesis, while SA enhances ROS accumulation through coordinated transcriptional regulation.

Bacterial, fungal, viral, and herbivore infections alter the transcripts of ROS-related genes. A comprehensive computational analysis of transcriptomic datasets by Bilgin et al. [135] revealed coordinated changes in the expression of both ROS biosynthesis and detoxification genes in response to diverse biotic stressors. Notably, among genes encoding ROS-detoxifying enzymes, 30 were upregulated while 35 were downregulated [135], highlighting the dynamic and context-dependent modulation of redox homeostasis during plant-pathogen interactions.

In addition to the genome-wide transcriptomic profiling, specific regulatory mechanisms linking ROS homeostasis to immune signaling have been identified. Zhang et al. [136] reported that the transcriptional repressor MAPK Alfin-like 7 (MAPK-AL7) interacts with nucleotide-binding leucine-rich repeat (NLR) proteins to suppress the expression of ROS-scavenging genes. This suppression promotes NLR-mediated immunity during ETI, leading to enhanced ROS accumulation and increased disease resistance. Transcriptional activation of ROS-scavenging genes has been reported in a study on soybean. Hydrogen peroxide (H₂O₂) from the oxidative burst triggered by the elicitor Phytophthora sojae induces glutathione S-transferase (GST) and glutathione peroxidase (GPX) transcripts in soybean cells [137].

Genome-wide analyses of redox-related gene families in Hevea have revealed that 30 gene families are involved in ROS production and scavenging, including superoxidase dismutases (SODs), glutathione (GSH)-associated enzymes, class III peroxidases, thioredoxins, and other antioxidant systems. Many of these genes are associated with physiological stress called tapping panel dryness (TPD) [138, 139], and subsets of ROS-scavenging components have also been implicated in pathogen defense. For example, Koop et al. [11] demonstrated that a rubber genotype resistance to Pseudocercospora ulei exhibits strong induction of ROS-related genes, including RBOHs, peroxidases, superoxide dismutase (SOD), catalase (CAT), and ascorbate peroxidase (APX), directly linking resistance to NADPH oxidase-dependent ROS production. These findings suggest that pathogen infection triggers an early oxidative burst mediated by RBOHs and peroxidases, followed by coordinated upregulation of ROS-scavenging enzymes to maintain a balance between defense signaling and oxidative damage. In addition, Wang et al. [140] reported that HbRbohD, a homolog of AtRbohD, is localized to the plasma membrane and is involved in biotic stress responses by modulating SA signaling pathways. Despite limited mechanistic understanding of transcription factor-ROS gene regulation in Hevea, accumulating evidence from RNA-seq and gene expression studies [10, 116, 117, 119, 120, 121] supports the notion that transcriptional control of ROS production and scavenging plays a pivotal role in Hevea immune responses to biotic stress.

4. Comparative overview: Model plants vs Hevea brasiliensis

In classical plant immunity, pathogen perception by PRRs or NLRs activates downstream signaling cascades, including MAPK pathways. These signaling events are mediated by conserved families of transcription factors, such as WRKY, NAC, MYB, and AP2/ERF, which bind to cis-regulatory elements in the promoters of target genes, thereby activating defense-related transcriptional programs. Notably, some TFs function as dual regulators, acting as transcriptional activators or repressors of downstream defense genes depending on pathogen identity, infection stage, and cellular context.

Transcriptional regulation in Hevea shows considerable evolutionary conservation with model plants in core signaling mechanisms, particularly involving the WRKY, AP2/ERF, NAC, and MYB TF families. In Arabidopsis, these TF families are well-characterized and are established as central modulators of immune signaling through specific interactions with cis-regulatory elements, including the W-box, GCC-box, and NAC/MYB-binding elements in promoter regions, thereby promoting immune responses [96, 141].

This conserved transcriptional regulation is evidenced in Hevea by the identification of HbERF-IX genes, one of which is an ortholog of AtERF1 and has been shown to transactivate the GCC-box [44], as well as by the recent characterization of HbRbohD [140]. RbohD is a plasma membrane-localized respiratory burst oxidase that translates regulatory signals into a physical ROS burst. Experimental validation demonstrated that HbRbohD is up-regulated by biotic stimuli and SA, and that HbRbohD overexpression enhances plant resistance to fungal pathogens [140]. Together, these findings suggest that key immune control mechanisms governing ROS burst and defense gene activation are structurally conserved across species, with conserved HbWRKY40 homologs initiating SA-mediated resistance [25].

Despite these conserved elements, distinct functional divergence characterizes the Hevea immune systems, driven in part by the metabolic complexity of its laticifer network as a woody perennial. Unlike Arabidopsis, for which detailed functional information is available on the dual regulatory role of AtWRKY40 [21, 141], Hevea transcription factors exhibit specialized, tissue-specific expression within laticifers, enabling the integration of targeted immune responses that protect latex yield under biotic stress. This notion is further supported by the identification of the HbNAC family VIII, a unique lineage that likely evolved in this particular woody plant physiology [52]. Similarly, the HbMYB TF family has diverged to primarily regulate secondary metabolism, wood formation, and lignification [67, 69], suggesting that Hevea must continuously regulate laticifer tissues and produce wood-forming compounds that are not prioritized in model plants. In addition, although genomic studies in Hevea have identified numerous differentially expressed genes (DEGs) during pathogen infection [12, 116, 120], these studies largely lack functional validation using knockout mutants in model system.

The expansion of these TF families in the rubber genome suggests the presence of specialized regulatory networks that adapt conserved hormonal signaling pathways to the unique physiology of laticifers, while ensuring effective pathogen defense. Finally, by integrating the conserved ability of HbERF-IX proteins to bind the GCC-box with tissue-specific regulatory patterns, Hevea maintains a balance between pathogen defense and the preservation of natural rubber biosynthesis [44, 138]. A schematic representation of hormone and ROS signaling in plant biotic stress responses is shown in Figure 1.

Figure 1: Schematic representation of hormone and ROS signaling in plant biotic stress response. Salicylic acid (SA) is involved in systemic acquired resistance (SAR) in plants through the inhibition of catalase (CAT) and ascorbate peroxidase (APX) activities, thereby enhancing the accumulation of H₂O₂ [142, 143]. CAT and APX function by maintaining ROS homeostasis in cells [144], however, the resulting H₂O₂ induces the expression of defense-related genes associated with SAR [142, 143]. SA-mediated inhibition of antioxidant enzymes elevates ROS levels, thereby activating a positive feedback loop that amplifies SA biosynthesis and the activation of downstream defense genes [145]. This establishes that ROS signaling functions both upstream and downstream of SA signaling. Respiratory burst oxidase homolog (RBOH) proteins are required for ROS production following successful pathogen recognition [125]. SA and ethylene (ET) can promote the spread of cell death [128, 146]. Mutation of RBOHD alters the transcript levels of defense-related genes during necrotrophic fungal pathogen attack. RBOHD does not appear to function as a direct inducer of defense gene expression but instead modulates SA and ET hormone levels to regulate plant cell death [128]. At the transcriptional level, immune signaling converges on conserved transcription factor families, including WRKY, AP2/ERF, NAC, and MYB. WRKY and ERF factors regulate canonical defense genes and hormone-responsive pathways, while NAC and MYB transcription factors integrate stress responses with development, secondary metabolism, and cell wall modification. SA exhibits antagonistic effects on JA/ET-mediated transcriptional responses [147]. Specifically, SA suppresses the expression of a subset of JA/ET-induced genes through repression of ORA59, which encodes a master AP2/ERF transcription factor [148,149].

5. Conclusion and future perspectives

Although gene expression studies in Hevea remain at an early stage compared to model systems, emerging transcriptomic and proteomic evidence already points to the conservation of core plant immune mechanisms. Continued advances in RNA-seq profiling, cis-regulatory analysis, and functional genomics will be essential to deepen our understanding of transcriptional regulation in Hevea and will accelerate the development of disease-resistant rubber cultivars through molecular breeding and targeted genetic improvement.

CRediT authorship contribution statement

Afdholiatus Syafaah: Writing–original draft, Writing–review & editing, Visualization, Conceptualization. Okechukwu S. Ezeh: Writing–original draft, Writing–review & editing, Visualization. Yoshiharu Y. Yamamoto: Writing–review & editing, Conceptualization, Supervision.

Funding

This work was in part supported by the Science and Technology Research Partnership for Sustainable Development (SATREPS).

Conflict of Interest

The authors declare no conflict of interest.

Data availability statement

No new data were generated or analyzed in this study.

References

• [1] Zipfel C (2009) Early molecular events in PAMP-triggered immunity. Curr. Opin. Plant Biol., 12: 414–420. https://doi.org/10.1016/j.pbi.2009.06.003
• [2] Zipfel C (2014) Plant pattern-recognition receptors. Trends Immunol, 35: 345–351. https://doi.org/10.1016/j.it.2014.05.004
• [3] Yu X, Niu H, Liu C, Wang H, Yin W and Xia X (2024) PTI‐ETI synergistic signal mechanisms in plant immunity. Plant Biotechnol J., 22: 2113–2128. https://doi.org/10.1111/pbi.14332
• [4] Grant M and Lamb C (2006) Systemic immunity. Curr. Opin. Plant Biol., 9: 414–420. https://doi.org/10.1016/j.pbi.2006.05.013
• [5] Katiyar A, Smita S, Lenka SK, Rajwanshi R, Chinnusamy V and Bansal KC (2012) Genome-wide classification and expression analysis of MYB transcription factor families in rice and Arabidopsis. BMC Genomics, 13: 544. https://doi.org/10.1186/1471-2164-13-544
• [6] Zhang H (2015) Arabidopsis AtERF15 positively regulates immunity against Pseudomonas syringae pv. tomato DC3000 and Botrytis cinerea. Front. Plant Sci., Sec. Plant Pathogen Interactions: 6. https://doi.org/10.3389/fpls.2015.00686
• [7] Islam MM, El-Sappah AH, Ali HM, Zandi P, Huang Q, Soaud SA et al. (2023) Pathogenesis-related proteins (PRs) countering environmental stress in plants: A review. South Afr. J. Bot., 160: 414–427. https://doi.org/10.1016/j.sajb.2023.07.003
• [8] Li S, Zheng H, Sui N and Zhang F (2024) Class III peroxidase: An essential enzyme for enhancing plant physiological and developmental process by maintaining the ROS level: A review. Int. J. Biol. Macromol., 283: 137331. https://doi.org/10.1016/j.ijbiomac.2024.137331
• [9] Santos C d and Franco OL (2023) Pathogenesis-related proteins (PRs) with enzyme activity activating plant defense responses. Plants, 12: 2226. https://doi.org/10.3390/plants12112226
• [10] Hurtado Páez UA, García Romero IA, Restrepo Restrepo S, Aristizábal Gutiérrez FA and Montoya Castaño D (2015) Assembly and analysis of differential transcriptome responses of Hevea brasiliensis on interaction with Microcyclus ulei. PLOS ONE, 10: e0134837. https://doi.org/10.1371/journal.pone.0134837
• [11] Koop DM, Rio M, Sabau X, Almeida Cardoso SE, Cazevieille C, Leclercq J et al. (2016) Expression analysis of ROS producing and scavenging enzyme-encoding genes in rubber tree infected by Pseudocercospora ulei. Plant Physiol. Biochem., 104: 188–199. https://doi.org/10.1016/j.plaphy.2016.03.022
• [12] Roy CB, Liu H, Rajamani A and Saha T (2019) Transcriptome profiling reveals genetic basis of disease resistance against Corynespora cassiicola in rubber tree (Hevea brasiliensis). Curr. Plant Biol., 17: 2–16. https://doi.org/10.1016/j.cpb.2019.02.002
• [13] Chen W, Provart NJ, Glazebrook J, Katagiri F, Chang H-S, Eulgem T et al. (2002) Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell, 14: 559–574. https://doi.org/10.1105/tpc.010410
• [14] Dong B, Liu Y, Huang G, Song A, Chen S, Jiang J et al. (2024) Plant NAC transcription factors in the battle against pathogens. BMC Plant Biol., 24: 958. https://doi.org/10.1186/s12870-024-05636-x
• [15] Ng DW-K, Abeysinghe JK and Kamali M (2018) Regulating the regulators: The control of transcription factors in plant defense signaling. Int. J. Mol. Sci., 19: 3737. https://doi.org/10.3390/ijms19123737
• [16] Yuan X, Wang H, Cai J, Li D and Song F (2019) NAC transcription factors in plant immunity. Phytopathol. Res., 1: 3. https://doi.org/10.1186/s42483-018-0008-0.
• [17] Llorca CM, Potschin M and Zentgraf U (2014) bZIPs and WRKYs: two large transcription factor families executing two different functional strategies. Front. Plant Sci., 5: 169. https://doi.org/10.3389/fpls.2014.00169
• [18] Eulgem T, Rushton PJ, Robatzek S and Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci., 5: 199–206. https://doi.org/10.1016/S1360-1385(00)01600-9
• [19] Bai Y, Sunarti S, Kissoudis C, Visser RGF and C. Gerard van der Linden (2018) The role of tomato WRKY genes in plant responses to combined abiotic and biotic stresses. Front. Plant Sci., 9: 801. https://doi.org/10.3389/fpls.2018.00801
• [20] Rushton PJ, Somssich IE, Ringler P and Shen QJ (2010) WRKY transcription factors. Trends Plant Sci., 15: 247–258. https://doi.org/10.1016/j.tplants.2010.02.006
• [21] Xu X, Chen C, Fan B and Chen Z (2006) Physical and functional interactions between pathogen-induced Arabidopsis WRKY18, WRKY40, and WRKY60 transcription factors. Plant Cell, 18: 1310–1326. https://doi.org/10.1105/tpc.105.037523
• [22] Birkenbihl RP, Diezel C and Somssich IE (2012) Arabidopsis WRKY33 is a key transcriptional regulator of hormonal and metabolic responses toward Botrytis cinerea infection. Plant Physiol., 159: 266–285. https://doi.org/10.1104/pp.111.192641
• [23] Zheng Z, Qamar SA, Chen Z and Mengiste T (2006) Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. Plant J., 48: 592–605. https://doi.org/10.1111/j.1365-313X.2006.02901.x
• [24] Wang Y, Li W, Qu J, Li F, Du W and Weng J (2023) Genome-wide characterization of the maize (Zea mays L.) WRKY transcription factor family and their responses to Ustilago maydis. Int. J. Mol. Sci., 24(19): 14916. https://doi.org/10.3390/ijms241914916
• [25] Yang J, Wang Q, Luo H, He C and An B (2020) HbWRKY40 plays an important role in the regulation of pathogen resistance in Hevea brasiliensis. Plant Cell Rep., 39: 1095–1107. https://doi.org/10.1007/s00299-020-02551-x
• [26] Kang G, Yan D, Chen X, Li Y, Yang L and Zeng R (2020) Molecular characterization and functional analysis of a novel WRKY transcription factor HbWRKY83 possibly involved in rubber production of Hevea brasiliensis. Plant Physiol. Biochem., 155: 483–493. https://doi.org/10.1016/j.plaphy.2020.08.013
• [27] Qu L, Li H-L, Guo D, Wang Y, Zhu J-H, Yin L-Y et al. (2020) HbWRKY27, a group IIe WRKY transcription factor, positively regulates HbFPS1 expression in Hevea brasiliensis. Sci. Rep., 10: 20639. https://doi.org/10.1038/s41598-020-77805-5
• [28] Zhang Q, Zhu J, Ni Y, Cai Y and Zhang Z (2012) Expression profiling of HbWRKY1, an ethephon-induced WRKY gene in latex from Hevea brasiliensis in responding to wounding and drought. Trees, 26: 587–595. https://doi.org/10.1007/s00468-011-0623-1
• [29] Duan C, Argout X, Gébelin V, Summo M, Dufayard J-F, Leclercq J et al. (2013) Identification of the Hevea brasiliensis AP2/ERF superfamily by RNA sequencing. BMC Genomics, 14: 30. https://doi.org/10.1186/1471-2164-14-30
• [30] Huang L, Zhang J, Zeng L, Yu P, Lu M and Li N (2002) The AP2/ERF transcription factor ORA59 regulates ethylene‐induced phytoalexin synthesis through modulation of an acyltransferase gene expression. J. Cell. Physiol., 239 (3): 539–551. https://doi.org/10.1002/jcp.30935
• [31] Phukan UJ, Jeena GS, Tripathi V and Shukla RK (2017) Regulation of apetala2/ethylene response factors in plants. Front. Plant Sci., 8: 150. https://doi.org/10.3389/fpls.2017.00150
• [32] Abiri R, Shaharuddin NA, Maziah M, Yusof ZNB, Atabaki N, Sahebi M et al. (2017) Role of ethylene and the APETALA 2/ethylene response factor superfamily in rice under various abiotic and biotic stress conditions. Environ. Exp. Bot., 134: 33–44. https://doi.org/10.1016/j.envexpbot.2016.10.015
• [33] Ma N, Sun P, Li Z, Zhang F, Wang X, You C et al. (2024) Plant disease resistance outputs regulated by AP2/ERF transcription factor family. Stress Biol., 4: 140. https://doi.org/10.1007/s44154-023-00140-y
• [34] Saxesena RR, Yadav OP and Gaur LB (2024) AP2/ERF transcription factors in crop plants’ disease resistance response. Asian J. Adv. Agric. Res., 24: 65–74. https://doi.org/10.9734/ajaar/2024/v24i12573
• [35] Xie Z, Nolan TM, Jiang H and Yin Y (2019) AP2/ERF transcription factor regulatory networks in hormone and abiotic stress responses in Arabidopsis. Front. Plant Sci., 10: 228. https://doi.org/10.3389/fpls.2019.00228
• [36] Zhang H, Hong Y, Huang L, Li D and Song F (2016) Arabidopsis AtERF014 acts as a dual regulator that differentially modulates immunity against Pseudomonas syringae pv. tomato and Botrytis cinerea. Sci. Rep., 6: 30251. https://doi.org/10.1038/srep30251
• [37] Jisha V, Dampanaboina L, Vadassery J, Mithöfer A, Kappara S and Ramanan R (2015) Overexpression of an AP2/ERF type transcription factor OsEREBP1 confers biotic and abiotic stress tolerance in rice. PLOS ONE, 10 (5): e0127831. https://doi.org/10.1371/journal.pone.0127831
• [38] Hong Y, Wang H, Gao Y, Bi Y, Xiong X, Yan Y et al. (2022) ERF transcription factor Osbierf3 positively contributes to immunity against fungal and bacterial diseases but negatively regulates cold tolerance in rice. Int. J. Mol. Sci., 23 (2): 606. https://doi.org/10.3390/ijms23020606
• [39] Tezuka D, Kawamata A, Kato H, Saburi W, Mori H and Imai R (2019) The rice ethylene response factor OsERF83 positively regulates disease resistance to Magnaporthe oryzae. Plant Physiol. Biochem., 135: 263–271. https://doi.org/10.1016/j.plaphy.2018.12.017
• [40] Liu D, Chen X, Liu J, Ye J and Guo Z (2012) The rice ERF transcription factor OsERF922 negatively regulates resistance to Magnaporthe oryzae and salt tolerance. J. Exp. Bot., 63 (10): 3899–3911. https://doi.org/10.1093/jxb/ers079
• [41] Loh SC, Othman AS and Veera Singham G (2019) Identification and characterization of jasmonic acid- and linolenic acid-mediated transcriptional regulation of secondary laticifer differentiation in Hevea brasiliensis. Sci. Rep., 9: 14296. https://doi.org/10.1038/s41598-019-50800-1
• [42] Putranto RA and Montoro P (2016) The Hevea brasiliensis AP2/ERF superfamily: from ethylene signalling to latex harvesting and physiological disease response. E-J. Menara Perkeb., 84: 201. https://doi.org/10.22302/iribb.jur.mp.v84i1.201
• [43] Yue YC, Li Feng W, Shu Guang Y and Wei Min T (2013) Molecular characterization of HbEREBP2, a jasmonate-responsive transcription factor from Hevea brasiliensis Muell. Arg. Afr. J. Biotechnol., 10 (45): 9751–9759. https://doi.org/10.5897/AJB11.541
• [44] Putranto R-A, Duan C, Kuswanhadi, Chaidamsari T, Rio M, Piyatrakul P et al. (2015) Ethylene response factors are controlled by multiple harvesting stresses in Hevea brasiliensis. PLoS ONE, 10 (4): e0123618. https://doi.org/10.1371/journal.pone.0123618
• [45] Fang Y, You J, Xie K, Xie W and Xiong L (2008) Systematic sequence analysis and identification of tissue-specific or stress-responsive genes of NAC transcription factor family in rice. Mol. Genet. Genomics, 280: 547–563. https://doi.org/10.1007/s00438-008-0386-6
• [46] Ooka H (2003) Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Res., 10 (6): 239–247. https://doi.org/10.1093/dnares/10.6.239
• [47] Fan K, Wang M, Miao Y, Ni M, Bibi N, Yuan S et al. (2014) Molecular evolution and expansion analysis of the NAC transcription factor in Zea mays. PLoS ONE, 9 (11): e111837. https://doi.org/10.1371/journal.pone.0111837
• [48] Lu M, Sun Q-P, Zhang D, Wang T-Y and Pan J (2015) Identification of 7 stress-related NAC transcription factor members in maize (Zea mays L.) and characterization of the expression pattern of these genes. Biochem. Biophys. Res. Commun., 462: 144–150. https://doi.org/10.1016/j.bbrc.2015.04.113
• [49] Vranić M, Perochon A and Doohan FM (2023) Transcriptional profiling reveals the wheat defences against Fusarium head blight disease regulated by a NAC transcription factor. Plants, 12(14): 2708. https://doi.org/10.3390/plants12142708
• [50] Wang X, Goregaoker SP and Culver JN (2009) Interaction of the Tobacco mosaic virus replicase protein with a NAC domain transcription factor is associated with the suppression of systemic host defenses. J. Virol., 83 (19): 9720–9730. https://doi.org/10.1128/JVI.00941-09
• [51] Du M, Zhai Q, Deng L, Li S, Li H, Yan L et al. (2014) Closely related NAC transcription factors of tomato differentially regulate stomatal closure and reopening during pathogen attack. Plant Cell, 26: 3167–3184. https://doi.org/10.1105/tpc.114.128272
• [52] Yang B, Zhang C, Yang J, An Z and Liang M (2024) Genome-wide investigation of NAC transcription factors and their response to cold stress in rubber tree (Hevea brasiliensis). J. Plant Growth Regul., 43: 4085–4098. https://doi.org/10.1007/s00344-024-11372-1
• [53] Luke LP, Sathik MBM, Thomas M, Kuruvilla L and Sumesh KV (2017) Expression of NAC transcription factor is altered under intermittent drought stress and re-watered conditions in Hevea brasiliensis. J. Plant Biotechnol., 44 (2): 142–148. https://doi.org/10.5010/JPB.2017.44.2.142
• [54] Mohamed Sathik MB, Luke LP, Rajamani A, Kuruvilla L, Sumesh KV and Thomas M (2018) De novo transcriptome analysis of abiotic stress-responsive transcripts of Hevea brasiliensis. Mol. Breed., 38: 32. https://doi.org/10.1007/s11032-018-0782-5
• [55] Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C and Lepiniec L (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci., 15 (10): 573–581. https://doi.org/10.1016/j.tplants.2010.06.005
• [56] Biswas D, Gain H and Mandal A (2023) MYB transcription factor: A new weapon for biotic stress tolerance in plants. Plant Stress, 10: 100252. https://doi.org/10.1016/j.stress.2023.100252
• [57] Yu Y, Zhang S, Yu Y, Cui N, Yu G, Zhao H et al. (2023) The pivotal role of MYB transcription factors in plant disease resistance. Planta, 258: 16. https://doi.org/10.1007/s00425-023-04180-6
• [58] Ambawat S, Sharma P, Yadav NR and Yadav RC (2013) MYB transcription factor genes as regulators for plant responses: an overview. Physiol. Mol. Biol. Plants, 19 (3): 307–321. https://doi.org/10.1007/s12298-013-0179-1
• [59] Mengiste T, Chen X, Salmeron J and Dietrich R (2003) The BOTRYTIS SUSCEPTIBLE1 gene encodes an r2r3myb transcription factor protein that is required for biotic and abiotic stress responses in Arabidopsis. Plant Cell, 15: 2551–2565. https://doi.org/10.1105/tpc.014167
• [60] Mabuchi K, Maki H, Itaya T, Suzuki T, Nomoto M, Sakaoka S et al. (2018) MYB30 links ROS signaling, root cell elongation, and plant immune responses. Proc. Natl. Acad. Sci., 115(26): 6867–6872. https://doi.org/10.1073/pnas.1804233115
• [61] Raffaele S, Vailleau F, Léger A, Joubès J, Miersch O, Huard C et al. (2008) A MYB transcription factor regulates very-long-chain fatty acid biosynthesis for activation of the hypersensitive cell death response in Arabidopsis. Plant Cell, 20: 752–767. https://doi.org/10.1105/tpc.107.054858
• [62] Chezem WR, Memon A, Li F-S, Weng J-K and Clay NK (2017) SG2-Type R2R3-MYB transcription factor MYB15 controls defense-induced lignification and basal immunity in Arabidopsis. Plant Cell, 29: 1907–1926. https://doi.org/10.1105/tpc.16.00954
• [63] Kim SH, Lam PY, Lee M-H, Jeon HS, Tobimatsu Y and Park OK (2020) The Arabidopsis R2R3 MYB transcription factor MYB15 is a key regulator of lignin biosynthesis in effector-triggered immunity. Front. Plant Sci., 11: 583153. https://doi.org/10.3389/fpls.2020.583153
• [64] Vannini C, Iriti M, Bracale M, Locatelli F, Faoro F, Croce P et al. (2006) The ectopic expression of the rice Osmyb4 gene in Arabidopsis increases tolerance to abiotic, environmental and biotic stresses. Physiol. Mol. Plant Pathol., 69: 26–42. https://doi.org/10.1016/j.pmpp.2006.12.005
• [65] Kishi-Kaboshi M, Seo S, Takahashi A and Hirochika H (2018) The MAMP-responsive MYB transcription factors MYB30, MYB55 and MYB110 activate the HCAA synthesis pathway and enhance immunity in rice. Plant Cell Physiol., 59 (5): 903–915. https://doi.org/10.1093/pcp/pcy062
• [66] Li W, Wang K, Chern M, Liu Y, Zhu Z, Liu J et al. (2020) Sclerenchyma cell thickening through enhanced lignification induced by OsMYB30 prevents fungal penetration of rice leaves. New Phytol., 226 (6): 1850–1863. https://doi.org/10.1111/nph.16505
• [67] Wang Y, Zhan D-F, Li H-L, Guo D, Zhu J-H, and Peng S-Q (2017) Transcriptome-wide identification and characterization of MYB transcription factor genes in the laticifer cells of Hevea brasiliensis. Front. Plant Sci., 8: 1974. https://doi.org/10.3389/fpls.2017.01974
• [68] Peng S-Q, Wu K-X, Huang G-X, and Chen S-C (2011) HbMyb1, a Myb transcription factor from Hevea brasiliensis, suppresses stress induced cell death in transgenic tobacco. Plant Physiol. Biochem., 49 (12): 1429–1435. https://doi.org/10.1016/j.plaphy.2011.09.007
• [69] Meng X, Wang Y, Li J, Jiao N, Zhang X, Zhang Y et al. (2021) RNA sequencing reveals phenylpropanoid biosynthesis genes and transcription factors for Hevea brasiliensis reaction wood formation. Front. Genet., 12: 763841. https://doi.org/10.3389/fgene.2021.763841
• [70] Dodds PN and Rathjen JP (2010) Plant immunity: towards an integrated view of plant–pathogen interactions. Nat. Rev. Genet., 11 (7): 539–548. https://doi.org/10.1038/nrg2812
• [71] Tsuda K and Somssich IE (2015) Transcriptional networks in plant immunity. New Phytol., 206 (4): 932–947. https://doi.org/10.1111/nph.13286
• [72] Bigeard J, Colcombet J and Hirt H (2015) Signaling mechanisms in pattern-triggered immunity (PTI). Mol. Plant, 8 (4): 521–539. https://doi.org/10.1016/j.molp.2014.12.022
• [73] Pieterse CMJ, Van Der Does D, Zamioudis C, Leon-Reyes A, and Van Wees SCM (2012) Hormonal modulation of plant immunity. Annu. Rev. Cell. Dev. Biol., 28: 489–521. https://doi.org/10.1146/annurev-cellbio-092910-154055
• [74] Walley JW, Coughlan S, Hudson ME, Covington MF, Kaspi R, Banu G et al. (2007) Mechanical stress induces biotic and abiotic stress responses via a novel cis-element. PLoS Genet., 3 (10): e172. https://doi.org/10.1371/journal.pgen.0030172
• [75] Alves M, Dadalto S, Gonçalves A, De Souza G, Barros V and Fietto L (2013) Plant bZIP transcription factors responsive to pathogens: A Review. Int. J. Mol. Sci., 14 (4): 7815–7828. https://doi.org/10.3390/ijms14047815
• [76] Rushton PJ, Somssich IE, Ringler P and Shen QJ (2010) WRKY transcription factors. Trends Plant Sci., 15 (5): 247–258. https://doi.org/10.1016/j.tplants.2010.02.006
• [77] Eulgem T (1999) Early nuclear events in plant defence signalling: rapid gene activation by WRKY transcription factors. EMBO J., 18 (17): 4689–4699. https://doi.org/10.1093/emboj/18.17.4689
• [78] Pandey SP and Somssich IE (2009) The role of wrky transcription factors in plant immunity. Plant Physiol., 150 (4): 1648–1655. https://doi.org/10.1104/pp.109.138990
• [79] Asai T, Tena G, Plotnikova J, Willmann MR, Chiu W-L, Gomez-Gomez L et al. (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature, 415: 977–983. https://doi.org/10.1038/415977a
• [80] Navarro L, Zipfel C, Rowland O, Keller I, Robatzek S, Boller T et al. (2004) The transcriptional innate immune response to flg22. interplay and overlap with avr gene-dependent defense responses and bacterial pathogenesis. Plant Physiol., 135: 1113–1128. https://doi.org/10.1104/pp.103.036749
• [81] Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JDG, Felix G et al. (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature, 428: 764–767. https://doi.org/10.1038/nature02485
• [82] Birkenbihl RP, Kracher B, Roccaro M and Somssich IE (2017) Induced genome-wide binding of three arabidopsis WRKY transcription factors during early MAMP-triggered immunity. Plant Cell, 29: 20–38. https://doi.org/10.1105/tpc.16.00681
• [83] Kong W, Ding L, Cheng J and Wang B (2018) Identification and expression analysis of genes with pathogen-inducible cis-regulatory elements in the promoter regions in Oryza sativa. Rice, 11 (1): 52. https://doi.org/10.1186/s12284-018-0243-0
• [84] Lebel E, Heifetz P, Thorne L, Uknes S, Ryals J and Ward E (1998) Functional analysis of regulatory sequences controlling PR-1 gene expression in Arabidopsis. Plant J., 16 (2): 223–233. https://doi.org/10.1046/j.1365-313x.1998.00288.x
• [85] Yu D, Chen C and Chen Z (2001) Evidence for an important role of WRKY DNA binding proteins in the regulation of NPR1 gene expression. Plant Cell, 13 (7): 1527–1540. https://doi.org/10.1105/TPC.010115
• [86] Du L and Chen Z (2000) Identification of genes encoding receptor-like protein kinases as possible targets of pathogen- and salicylic acid-induced WRKY DNA-binding proteins in Arabidopsis. Plant J., 24 (6): 837–847. https://doi.org/10.1111/j.1365-313X.2000.00923.x
• [87] Lippok B, Birkenbihl RP, Rivory G, Brümmer J, Schmelzer E, Logemann E et al. (2007) Expression of AtWRKY33 encoding a pathogen- or PAMP-responsive WRKY transcription factor is regulated by a composite DNA motif containing W box elements. Mol. Plant-Microbe Interact., 20: 420–429. https://doi.org/10.1094/MPMI-20-4-0420
• [88] Mohr TJ, Mammarella ND, Hoff T, Woffenden BJ, Jelesko JG and McDowell JM (2010) The Arabidopsis downy mildew resistance gene RPP8 is induced by pathogens and salicylic acid and is regulated by W Box cis elements. Mol. Plant-Microbe Interact., 23 (10): 1303–1315. https://doi.org/10.1094/MPMI-01-10-0022
• [89] Cai M, Qiu D, Yuan T, Ding X, Li H, Duan L et al. (2008) Identification of novel pathogen-responsive cis-elements and their binding proteins in the promoter of OsWRKY13, a gene regulating rice disease resistance. Plant Cell Environ., 31 (1): 86–96. https://doi.org/10.1111/j.1365-3040.2007.01739.x
• [90] Rushton PJ, Reinstädler A, Lipka V, Lippok B and Somssich IE (2002) Synthetic plant promoters containing defined regulatory elements provide novel insights into pathogen- and wound-induced signaling. Plant Cell, 14:749–62. https://doi.org/10.1105/tpc.010412
• [91] Eulgem T and Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr. Opin. Plant Biol., 10 (4): 366–371. https://doi.org/10.1016/j.pbi.2007.04.020
• [92] Jimmy JL and Babu S (2015) Role of OsWRKY transcription factors in rice disease resistance. Trop. Plant Pathol., 40: 355–361. https://doi.org/10.1007/s40858-015-0058-0
• [93] Koo SC, Moon BC, Kim JK, Kim CY, Sung SJ, Kim MC et al. (2009) OsBWMK1 mediates SA-dependent defense responses by activating the transcription factor OsWRKY33. Biochem. Biophys. Res. Commun., 387: 365–370. https://doi.org/10.1016/j.bbrc.2009.07.026
• [94] Dong J, Chen C and Chen Z (2003) Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant Mol. Biol., 51: 21–37. https://doi.org/10.1023/A:1020780022549
• [95] Catinot J, Huang J, Huang P, Tseng M, Chen Y, Gu S et al. (2015) Ethylene response factor 96 positively regulates Arabidopsis resistance to necrotrophic pathogens by direct binding to GCC elements of jasmonate- and ethylene‐responsive defence genes. Plant Cell Environ., 38: 2721–2734. https://doi.org/10.1111/pce.12583
• [96] Fujimoto SY, Ohta M, Usui A, Shinshi H, and Ohme-Takagi M (2000) Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC Box–mediated gene expression. Plant cell, 12: 393–404. https://doi.org/10.1105/tpc.12.3.393
• [97] Maruyama Y, Yamoto N, Suzuki Y, Chiba Y, Yamazaki K, Sato T et al. (2013) The Arabidopsis transcriptional repressor ERF9 participates in resistance against necrotrophic fungi. Plant Sci., 213: 79–87. https://doi.org/10.1016/j.plantsci.2013.08.008
• [98] Ohme-Takagi M and Shinshi H (1995) Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell, 7: 173–182. https://doi.org/10.1105/tpc.7.2.173
• [99] Ohme-Takagi M, Suzuki K and Shinshi H (2000) Regulation of Ethylene-Induced Transcription of Defense Genes. Plant Cell Physiol., 41: 1187–1192. https://doi.org/10.1093/pcp/pcd057
• [100] Brown RL, Kazan K, McGrath KC, Maclean DJ and Manners JM (2003) A role for the GCC–Box in jasmonate-mediated activation of the PDF1.2 gene of Arabidopsis. Plant Physiol.,132: 1020–1032. https://doi.org/10.1104/pp.102.017814
• [101] Manners JM, Penninckx IAMA, Vermaere K, Kazan K, Brown RL, Morgan A et al. (1998) The promoter of the plant defensin gene PDF1.2 from Arabidopsis is systemically activated by fungal pathogens and responds to methyl jasmonate but not to salicylic acid. Plant Mol. Biol., 38 (6): 1071–1080. https://doi.org/10.1023/A:1006070413843
• [102] Zhang H, Xie B, Lu X, Yang Y and Huang R (2004) GCC box in Arabidopsis PDF1.2 promoter is an essential and sufficient cis-acting element in response to MeJA treatment. Chin. Sci. Bull., 49 (23): 2476–2480. https://doi.org/10.1007/BF03183717
• [103] Zarei A, Körbes AP, Younessi P, Montiel G, Champion A and Memelink J (2011) Two GCC boxes and AP2/ERF-domain transcription factor ORA59 in jasmonate/ethylene-mediated activation of the PDF1.2 promoter in Arabidopsis. Plant Mol. Biol., 75: 321–331. https://doi.org/10.1007/s11103-010-9728-y
• [104] Sudhisa J, Sharathchandra RG, Amruthesh KN, Kumar A and Shetty HS (2012) Pathogenesis-related proteins in plant defense response. In: Plant Defence: Biological Control (Merillon JM and Ramawat KG, eds.), pp.379–403, Springer. Dordrecht.
• [105] Beffa R and Meins F (1996) Pathogenesis-related functions of plant β-1,3-glucanases investigated by antisense transformation — a review. Gene, 179 (1-2): 97–103. https://doi.org/10.1016/S0378-1119(96)00421-0
• [106] Côté F (1991) Pathogenesis-related acidic β-1,3–glucanase genes of tobacco are regulated by both stress and developmental signals. Mol. Plant Microbe Interact., 4: 173. https://doi.org/10.1094/MPMI-4-173
• [107] Perrot T, Pauly M and Ramírez V (2022) Emerging roles of β-glucanases in plant development and adaptative responses. Plants, 11(9): 1119. https://doi.org/10.3390/plants11091119
• [108] Sela-Buurlage MB, Ponstein AS, Bres-Vloemans SA, Melchers LS, Van Den Elzen PJM and Cornelissen BJC (1993) Only specific tobacco (Nicotiana tabacum) chitinases and β-1,3-glucanases exhibit antifungal activity. Plant Physiol., 101: 857–863. https://doi.org/10.1104/pp.101.3.857
• [109] Zhang SB, Zhang WJ, Zhai HC, Lv YY, Cai JP, Jia F et al. (2019) Expression of a wheat β-1,3-glucanase in Pichia pastoris and its inhibitory effect on fungi commonly associated with wheat kernel. Protein Expr. Purif., 154: 134–139. https://doi.org/10.1016/j.pep.2018.10.011
• [110] Wang Y, Liu M, Wang X, Zhong L, Shi G, Xu Y et al. (2021) A novel β-1,3-glucanase Gns6 from rice possesses antifungal activity against Magnaporthe oryzae. J. Plant Physiol., 265:153493. https://doi.org/10.1016/j.jplph.2021.153493
• [111] Filyushin MA, Anisimova OK, Kochieva EZ and Shchennikova AV (2021) Genome-wide identification and expression of chitinase class I genes in garlic (Allium sativum L.) cultivars resistant and susceptible to Fusarium proliferatum. Plants, 10: 720. https://doi.org/10.3390/plants10040720
• [112] He T, Fan J, Jiao G, Liu Y, Zhang Q, Luo N et al. (2023) Bioinformatics and expression analysis of the chitinase genes in strawberry (Fragaria vesca) and functional study of FvChi-14. Plants, 12 (7): 1543. https://doi.org/10.3390/plants12071543
• [113] Brogue K, Chet I, Holliday M, Cressman R, Biddle P, Knowlton S et al. (1991) Transgenic plants with enhanced resistance to the fungal pathogen Rhizoctonia solani. Science, 254: 1194–1197. https://doi.org/10.1126/science.254.5035.1194
• [114] Bindschedler LV, Dewdney J, Blee KA, Stone JM, Asai T, Plotnikov J et al. (2006) Peroxidase‐dependent apoplastic oxidative burst in Arabidopsis required for pathogen resistance. Plant J., 47: 851–863. https://doi.org/10.1111/j.1365-313X.2006.02837.x
• [115] Wang CJ, Chan YL, Shien CH and Yeh KW (2015) Molecular characterization of fruit-specific class III peroxidase genes in tomato (Solanum lycopersicum). J. Plant Physiol., 177: 83–92. https://doi.org/10.1016/j.jplph.2015.01.011
• [116] Aswathy CS, Roy CB, Shahina K, Vinod MP and Biji CL (2024) Comparative transcriptomic analysis of rubber (Hevea brasiliensis) clones differing in disease tolerance provides novel insights into the disease response associated with abnormal leaf fall disease caused by Phytophthora meadii. South Afr. J. Bot., 168: 130–150. https://doi.org/10.1016/j.sajb.2024.03.009
• [117] Kuyyogsuy A, Deenamo N, Khompatara K, Ekchaweng K and Churngchow N (2018) Chitosan enhances resistance in rubber tree (Hevea brasiliensis), through the induction of abscisic acid (ABA). Physiol. Mol. Plant Pathol., 102: 67–78. https://doi.org/10.1016/j.pmpp.2017.12.001
• [118] Longsaward R, Pengnoo A, Kongsawadworakul P and Viboonjun U (2023) A novel rubber tree PR-10 protein involved in host-defense response against the white root rot fungus Rigidoporus microporus. BMC Plant Biol., 23: 157. https://doi.org/10.1186/s12870-023-04149-3
• [119] Oghenekaro AO, Omorusi VI and Asiegbu FO (2016) Defence-related gene expression of Hevea brasiliensis clones in response to the white rot pathogen, Rigidoporus microporus. For. Pathol., 46 (4): 318–326. https://doi.org/10.1111/efp.12260
• [120] Ribeiro S, Label P, Garcia D, Montoro P and Pujade-Renaud V (2021) Transcriptome profiling in susceptible and tolerant rubber tree clones in response to cassiicolin Cas1, a necrotrophic effector from Corynespora cassiicola. PLoS ONE, 16. https://doi.org/10.1371/journal.pone.0254541
• [121] Thanseem I, Joseph A and Thulaseedharan A (2005) Induction and differential expression of -1,3-glucanase mRNAs in tolerant and susceptible Hevea clones in response to infection by Phytophthora meadii. Tree Physiol., 25: 1361–1368. https://doi.org/10.1093/treephys/25.11.1361
• [122] Castro B, Citterico M, Kimura S, Stevens DM, Wrzaczek M and Coaker G (2021) Stress-induced reactive oxygen species compartmentalization, perception and signalling. Nat. Plants, 7: 403–412. https://doi.org/10.1038/s41477-021-00887-0
• [123] Sahu PK, Jayalakshmi K, Tilgam J, Gupta A, Nagaraju Y, Kumar A et al. (2022) ROS generated from biotic stress: Effects on plants and alleviation by endophytic microbes. Front. Plant. Sci.,13: 1042936. https://doi.org/10.3389/fpls.2022.1042936
• [124] Waszczak C, Carmody M and Kangasjärvi J (2018) Reactive Oxygen Species in Plant Signaling. Annu. Rev. Plant Biol., 69: 209–236. https://doi.org/10.1146/annurev-arplant-042817-040322
• [125] Torres MA, Jones JDG and Dangl JL (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiol., 141: 373–378. https://doi.org/10.1104/pp.106.079467
• [126] Sagi M and Fluhr R (2006) Production of reactive oxygen Species by plant NADPH oxidases. Plant Physiol., 141: 336–340. https://doi.org/10.1104/pp.106.078089
• [127] Torres MA, Dangl JL and Jones JDG (2002) Arabidopsis gp91^phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc. Natl. Acad. Sci., 99: 517–522. https://doi.org/10.1073/pnas.012452499
• [128] Pogány M, Von Rad U, Grün S, Dongó A, Pintye A, Simoneau P et al. (2009) Dual roles of reactive oxygen species and NADPH oxidase RBOHD in an Arabidopsis-Alternaria Pathosystem. Plant Physiol., 151: 1459–1475. https://doi.org/10.1104/pp.109.141994
• [129] Sagi M, Davydov O, Orazova S, Yesbergenova Z, Ophir R, Stratmann JW et al. (2004) Plant respiratory burst oxidase homologs impinge on wound responsiveness and development in Lycopersicon esculentum. Plant Cell, 16: 616–628. https://doi.org/10.1105/tpc.019398
• [130] Li X, Zhang H, Tian L, Huang L, Liu S, Li D et al. (2015) Tomato SlRbohB, a member of the NADPH oxidase family, is required for disease resistance against Botrytis cinerea and tolerance to drought stress. Front. Plant Sci., 6: 463. https://doi.org/10.3389/fpls.2015.00463
• [131] Ullah C, Chen YH, Ortega MA and Tsai CJ (2023) The diversity of salicylic acid biosynthesis and defense signaling in plants: Knowledge gaps and future opportunities. Curr. Opin. Plant Biol., 72: 102349. https://doi.org/10.1016/j.pbi.2023.102349
• [132] Roychowdhury R, Mishra S, Anand G, Dalal D, Gupta R, Kumar A et al. (2024) Decoding the molecular mechanism underlying salicylic acid (SA)‐mediated plant immunity: an integrated overview from its biosynthesis to the mode of action. Physiol. Plant, 176: e14399. https://doi.org/10.1111/ppl.14399
• [133] Rivas FJM, Fernie AR and Aarabi F (2023) Roles and regulation of the RBOHD enzyme in initiating ROS-mediated systemic signaling during biotic and abiotic stress. Plant Stress, 11: 100327. https://doi.org/10.1016/j.stress.2023.100327
• [134] Wu B, Qi F and Liang Y (2023) Fuels for ROS signaling in plant immunity. Trends Plant Sci., 28: 1124–1131. https://doi.org/10.1016/j.tplants.2023.04.007
• [135] Bilgin DD, Zavala JA, Zhu J, Clough SJ, Ort DR and DeLUCIA EH (2010) Biotic stress globally downregulates photosynthesis genes. Plant Cell Environ., 3: 1597–1613. https://doi.org/10.1111/j.1365-3040.2010.02167.x
• [136] Zhang D, Gao Z, Zhang H, Yang Y, Yang X, Zhao X et al. (2023) The MAPK-Alfin-like 7 module negatively regulates ROS scavenging genes to promote NLR-mediated immunity. Proc. Natl. Acad. Sci., 120: e2214750120. https://doi.org/10.1073/pnas.2214750120
• [137] Levine A, Tenhaken R, Dixon R and Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell., 79: 583–593. https://doi.org/10.1016/0092-8674(94)90544-4
• [138] Zhang Y, Leclercq J, Wu S, Ortega-Abboud E, Pointet S, Tang C et al. (2019) Genome-wide analysis in Hevea brasiliensis laticifers revealed species-specific post-transcriptional regulations of several redox-related genes. Sci. Rep., 9: 5701. https://doi.org/10.1038/s41598-019-42197-8
• [139] Zhang Y, Leclercq J and Montoro P (2017) Reactive oxygen species in Hevea brasiliensis latex and relevance to tapping panel dryness. Tree Physiol., 37: 261–269. https://doi.org/10.1093/treephys/tpw106
• [140] Wang M, Song Y, An B, Wang Q, Chen J, He C et al. (2025) Rubber tree respiratory burst oxidases homolog D contributed to plant biotic and abiotic resistance. Trop. Plants, 4: e037. https://doi.org/10.48130/tp-0025-0029
• [141] Pandey SP, Roccaro M, Schön M, Logemann E and Somssich IE (2010) Transcriptional reprogramming regulated by WRKY18 and WRKY40 facilitates powdery mildew infection of Arabidopsis: WRKY18/40 in powdery mildew susceptibility. Plant J., 64: 912–923. https://doi.org/10.1111/j.1365-313X.2010.04387.x
• [142] Chen Z, Silva H and Klessig DF (1993) Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science, 262: 1883–1886. https://doi.org/10.1126/science.8266079
• [143] Durner J and Klessig DF (1995) Inhibition of ascorbate peroxidase by salicylic acid and 2,6-dichloroisonicotinic acid, two inducers of plant defense responses. Proc. Natl. Acad. Sci., 92: 11312–11316. https://doi.org/10.1073/pnas.92.24.11312
• [144] Mittler R, Vanderauwera S, Gollery M and Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci., 9: 490–498. https://doi.org/10.1016/j.tplants.2004.08.009
• [145] Slaymaker DH, Navarre DA, Clark D, Del Pozo O, Martin GB and Klessig DF (2002) The tobacco salicylic acid-binding protein 3 (SABP3) is the chloroplast carbonic anhydrase, which exhibits antioxidant activity and plays a role in the hypersensitive defense response. Proc. Natl. Acad. Sci., 99: 11640–11645. https://doi.org/10.1073/pnas.182427699
• [146] Torres MA, Jones JDG and Dangl JL (2005) Pathogen-induced, NADPH oxidase–derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nat. Genet., 37: 1130–1134. https://doi.org/10.1038/ng1639
• [147] Pieterse CMJ, Leon-Reyes A, Van Der Ent S and Van Wees SCM (2009) Networking by small-molecule hormones in plant immunity. Nat. Chem. Biol., 5: 308–316. https://doi.org/10.1038/nchembio.164
• [148] Zander M, La Camera S, Lamotte O, Métraux J-P and Gatz C (2009) Arabidopsis thaliana class-II TGA transcription factors are essential activators of jasmonic acid/ethylene-induced defense responses: Class-II TGA factors activate JA/ET-induced responses. Plant J., 61: 200–210. https://doi.org/10.1111/j.1365-313X.2009.04044.x
• [149] Van Der Does D, Leon-Reyes A, Koornneef A, Van Verk MC, Rodenburg N, Pauwels L et al (2013) Salicylic acid suppresses jasmonic acid signaling downstream of SCFCOI1-JAZ by targeting GCC promoter motifs via transcription factor ORA59. Plant Cell, 25: 744–761. https://doi.org/10.1105/tpc.112.108548