Xylem is a plant vascular tissue that transports water and dissolved minerals from the roots to the rest of the plant. It consists of specialized water-conducting tracheary elements, supporting fibre cells and storage parenchyma cells. Certain plant pathogenic fungi, oomycetes and bacteria have evolved strategies to invade xylem vessels and cause highly destructive vascular wilt diseases that affect the crop production and forest ecosystems worldwide. In this chapter, we consider the molecular mechanisms of root-specific defence responses against vascular wilt pathogens, with an emphasis on the most important and well-studied fungal (Verticillium spp. and Fusarium oxysporum) and bacterial (Xanthomonas spp. and Ralstonia solanacearum) pathogens. In particular, we present the current understanding of plant immune responses, from invasion perception to signal transduction and termination. Furthermore, we address the role of specific transcription factors involved in plant immunity and their regulatory network. We also highlight the crucial roles of phytohormones as signalling molecules in local and systemic defence responses. Finally, we summarize the current knowledge of plant defence responses to xylem-invading pathogens to devise new strategies and methods for controlling these destructive plant pathogens.
- Vascular wilt pathogens
- plant innate immunity
- signal transduction
- biotic stress
The disease triangle concept, introduced in the 1960s by George McNew to predict plant disease outcomes, shows the complex interactions among the environment, the host and the infectious (or abiotic) agent . Plants, continuously challenged by numerous abiotic stresses, potential pests and pathogens, have evolved efficient strategies to perceive and respond to such threats. Plants lack specialized immune cells and their survival relies upon a highly sophisticated innate immune system, in which each plant cell responds autonomously [2–5]. The first line of defence is a basal resistance response called pattern-triggered immunity (PTI). It is induced by recognition of exogenous microbe or pathogen-associated molecular patterns (MAMPs or PAMPs) or endogenous molecules released on pathogen perception or pathogen-induced cell damage (damage-associated molecular patterns, DAMPs) via pattern-recognition receptors (PRRs) in the plasma membrane . Successful pathogens overcome PTI by secreting effectors, hydrolytic enzymes or toxins, which suppress or interfere with host defence molecules . In an evolutionary arms race, plants have evolved a robust defence response network termed effector-triggered immunity (ETI) to intercept pathogen effectors through intracellular receptors, such as nucleotide-binding site/leucine-rich repeat (NLR) proteins [5,7,8]. An intricate network of signalling pathways transduces these incoming signals into a diverse array of immune responses activating reactive oxygen species (ROS) generation, MAP kinases, Ca2+ signalling, the production of phytohormones and extensive transcriptional reprogramming .
In the past, comprehensive research has been dedicated to understanding plant physiological and molecular responses to individual abiotic and biotic stresses under controlled laboratory conditions. Recent studies of plant responses to concurrent abiotic and biotic stress conditions [10–16] have demonstrated that plants perceive and respond to combined stresses in a specific and unique manner. Moreover, the underlying signalling pathways are carefully modulated [14,17,18] and coordinated to ensure that plant growth and fitness are not significantly retarded .
Vascular wilt pathogens are soil-borne bacteria, fungi and oomycetes that employ various infection strategies to invade plant roots at different infection sites . They subsequently advance inter- or intracellularly through the root cortex and enter the xylem vessels, where they proliferate and spread passively with xylem sap to aerial plant parts . The characteristic wilt symptoms develop as a consequence of obstructed transportation of water and minerals, either due to the physical blockage of vessels by the pathogen or indirectly due to the activation of plant physical defence responses (e.g. formation of tyloses, accumulation of pectin-rich gels and gums) that confine the further spread of the pathogen . In addition to wilting, other disease symptoms include vein clearing, leaf epinasty, chlorosis, vascular browning, stunting, necrosis and eventually plant death [21–24].
Primarily due to the specific lifestyle of vascular wilt pathogens, relatively little is known about their interactions with host plants and root-specific defence responses on molecular and biochemical levels compared to foliar pathogens. This chapter, therefore, summarizes the currently available molecular, cellular and systems biology data gathered from studies of signalling networks in model plants and crops challenged by bacterial or fungal pathogens and applies this general knowledge to advance understanding of vascular wilt pathogenesis and implement all these findings into the design of new strategies for the protection of crops and forest ecosystems.
2. Plant immune signalling initiation
Several factors contribute to the complex regulatory mechanisms in the initiation of plant immune signalling: (i) as sessile organisms, plants need to respond promptly to danger signals, (ii) each plant cell reacts autonomously to different stimuli, but the response needs to be integrated at a higher organizational level to ensure the plant’s survival and (iii) immune reactions are energy- and resource-demanding processes requiring the proper timing and amplitude of response . Typically, immune responses occur on recognition of conserved microbe-, pathogen- or damage-associated molecular patterns or after perception of effector molecules that are species-, race-, or strain-specific and contribute to pathogen virulence . However, not all microbial elicitors conform to the common distinction between PAMPs and effectors, and so Thomma et al.  proposed that plant immunity should be considered as a continuum, instead of a two-branched system composed of PAMP-triggered immunity (PTI) and effector-triggered immunity (ETI). An alternative perspective of plant innate immunity as a system that evolves to detect invasion has recently been extended into a so-called invasion model . In this model, invasion patterns (IPs), externally encoded or modified-self ligands that signify invasion, are perceived by plant invasion pattern receptors (IPRs) and induce IP-triggered responses that do not result in immunity by default.
2.1. Plant PRRs convey danger signals to the intracellular immune signalling pathways
Recently emerging structural biology data on plant–pathogen interactions,  together with data obtained primarily from genetic and biochemical studies on the leaves of model plants and crops, have revealed that fine-tuning and coordination of immune responses are achieved within large protein complexes at the plasma membrane, where plant PRRs reside . Plant PRRs are either receptor-like kinases (RLKs) or receptor-like proteins (RLPs) [4,6,25,29]. RLKs are modular proteins comprised of an extracellular domain involved in recognition of MAMPs/DAMPs, a single-pass transmembrane domain and a cytosolic serine/threonine kinase domain that transmits a signal to downstream signalling components. RLPs have a similar architecture, but their short cytoplasmic tail lacks kinase activity. RLPs, therefore, probably form heteromeric complexes with RLKs or other cytosolic kinases to relay downstream signalling. Extracellular domains of PRRs contain various motifs involved in recognition and binding of ligands. Leucine-rich repeat (LRR) motifs are widespread and serve as a scaffold for protein- or peptide–protein interactions . Well-characterized examples of LRR–RLKs are
2.1.1. Perception of chitin
The chitin-responsive PRR system has been thoroughly investigated in both dicots and monocots. The perception of chitin in monocot plants is best described in rice (
The model dicot plant
2.1.2. Perception of flagellin
Extensive research of the model plant
2.1.3. Perception of peptidoglycan
Peptidoglycan (PGN), a polymer of N-acetylglucosamine and N-acetylmuramic acid branched with a short peptide, is an essential component of a bacterial cell wall and is another well-studied MAMP. In
2.1.4. Perception of DAMPs
Some PRRs respond to damage-associated molecular patterns (DAMPs), endogenous molecules such as cell wall fragments or peptides released on pathogen attack or various abiotic stresses [25,56]. Partial degradation of pectic polysaccharide homogalacturonan (HGA) by pathogen or plant polygalacturonases produces oligogalacturonides (OGs), oligomers of α-1,4–linked galacturonic acid [57,58]. In
The best studied peptides acting as DAMPs belong to the plant elicitor peptides (Peps) family. They are processed from precursor PROPEPs [61,62]. AtPep1, a 23 amino acid peptide released from the C-terminal of PROPEP1, was the first peptide elicitor isolated from
2.2. Intracellular immune receptors NLRs detect pathogen effectors
In addition to PRRs, plants have evolved a second class of immune receptors that intercept effectors in different parts of the cell . These intracellular receptors, so called NLRs, are characterized as multi-domain proteins that have a conserved central nucleotide-binding (NB) domain and variable C-terminal leucine-rich repeats (LRR) domain . In terms of their distinct N-terminal domains, NLRs are broadly divided into two groups: TNLs that harbour a Toll–interleukin 1 receptor (TIR) domain and CNLs that contain a coiled-coil (CC) domain [69–71]. NLRs belong to signal transduction ATPases with numerous domains (STAND) that operate as molecular switches cycling between an inactive closed ADP-bound state and active open state with bound GTP [72–74]. In the resting state, N-terminal TIR or CC and C-terminal LRR domains sterically inhibit the NB domain from ADP–ATP exchange. On pathogen recognition, a series of conformational changes occur that expose the NB domain, promote ADP–ATP exchange and initiate signal transduction . Effector recognition by NLRs often, but not always, leads to a form of programmed cell death termed as a hypersensitive response . NLRs are, therefore, under precise control by accessory proteins. NLRs interact with conserved Hsp90-Sgt1-RAR1 protein complexes for proper folding, accumulation and regulation [76,77]. Moreover, Sgt1 interacts with the suppressor of
Various strategies of effector recognition by NLRs exist and are represented in different models. In the gene-for-gene model, originally described by Flor in 1971, NLRs can recognize effectors directly (e.g.
Activated NLRs trigger a variety of immune responses, from the generation of ROS, elevation of intracellular Ca2+, activation of MAPK cascades, transcriptional reprogramming to production of phytohormones . Although effector-triggered responses are qualitatively similar to immune responses elicited by MAMPs/DAMPs, there are quantitative differences in the strength and duration of pathways, which result in different resistance responses and signalling networks .
2.3. Signal transduction cascades
Perception of MAMPs/DAMPs by their cognate receptors triggers an array of immune responses, comprising changes in intracellular calcium levels [Ca2+]i, membrane potential depolarization, extracellular alkalinization, production of ROS, NO and phosphatidic acid, activation of kinases (mitogen-activated protein kinases (MAPKs) or Ca2+-dependent protein kinases (CDPKs)), transcriptional reprogramming and changes in plant hormone concentrations (e.g. ethylene, salicylic and jasmonic acid) [88,89].
2.3.1. Calcium and ROS signalling interconnection
Ca2+ is a ubiquitous second messenger released in response to various stresses and developmental processes. In
Rapid production of reactive oxygen species (ROS) in response to MAMPs/DAMPs depends primarily on respiratory burst oxidase homologues (RBOHs) [92,93]. These NADPH oxidases are integral membrane proteins that generate superoxide anions (O2−), which are rapidly converted into hydrogen peroxide (H2O2). RBOHs have cytosolic FAD- and NADPH-binding domains in the C-terminal region, six membrane-spanning domains and a cytosolic N-terminal extension that harbours two EF-hand motifs and multiple phosphorylation sites . Recent studies in
2.3.2. MAPK signalling
Plant mitogen-activated protein kinase (MAPK) cascades generally comprise MAPKK kinases (or MEKKs), which receive signals from receptors/sensors and phosphorylate downstream MAPK kinases (or MKKs) and which subsequently activate MAPKs (or MPKs) that control the activities and synthesis of a plethora of transcription factors (TFs), enzymes, hormones, peptides and antimicrobial chemicals [101,102]. In
2.4. Transcriptional reprogramming converges with complex phytohormone signalling networks
Transcription factors (TFs) involved in plant immunity reside in transcriptional complexes and, together with co-regulatory proteins, directly or indirectly recruit RNA polymerase II to the target promoters or release it from them . TFs vital for plant immunity comprise members of the AP2/ERF, bHLH, bZIP, MYB, NAC and WRKY TF families and perform diverse roles . For instance, certain members of apetala2/ethylene-response element binding factor (AP2/ERF) participate in the regulation of genes related to the jasmonic acid (JA) and ethylene hormone signalling pathways .
TF expression and activities are regulated in multiple ways. Certain nucleotide-binding site/leucine-rich repeat (NLR) proteins directly regulate transcription by physically interacting with TFs [120–123]. Several TFs are controlled by phosphorylation as downstream targets of activated MAPK cascades [109,124–127]. Another mechanism of TFs activation is carried out by Ca2+sensors such as CaMs and CDPKs [128–133]. Additional factors (e.g. components of mediator complex [134,135], chromatin modifications [136–138]) and levels of regulation (e.g. ubiquitination , sumoylation , alternative mRNA splicing ) also contribute to the complexity of transcriptional networks and fine-tuning of immune responses.
Coordination of diverse stress responses and growth is resolved within complex phytohormone signalling networks, in which salicylic acid (SA), jasmonic acid (JA) and ethylene (ET) perform central roles, while other hormones merely modulate their responses . SA is synthesized in chloroplasts from chorismate by isochorismate synthase  and exported to the cytosol . In response to pathogens and various abiotic stresses, SA mediates expression of pathogenesis-related (PR) genes and the synthesis of antimicrobial compounds to provide basal defence and systemic acquired resistance (SAR) . SA activates these defence responses through transcription cofactor nonexpresser of PR genes 1 (NPR1)  and transcription factors TGA2, TGA5 and TGA6 . In the absence of SA, NPR1 is sequestered in the cytosol and forms oligomeric complexes stabilized by intermolecular disulphide bonds . In response to activation of SA pathway, thioredoxins reduce these disulphide bonds, causing the release of NPR1 in monomeric form, which can translocate to the nucleus via a nuclear translocation signal (NLS) . In addition, NPR1 protein levels oscillate through CUL3NPR3- and CUL3NPR4-mediated degradation in the nucleus, which is required for fine-tuning of immune responses [147,149,150].
Jasmonates (JAs) are plant hormones with essential roles in plant defence and development . JAs are derived from
Ethylene (ET) is a gaseous hormone that often works synergistically with JA . Important steps in ET biosynthesis are the conversion of
Plant hormonal crosstalk is extensive and occurs in several combinations . The molecular mechanism underlying SA-mediated reprogramming of the JA transcriptional network points to immune signalling antagonism and the involvement of transcriptional regulators NPR1, TGA, WRKY and ORA59 as signal integrators . Phytohormones JA and ET synergistically regulate plant defence responses to necrotrophic fungi via JA-induced EIN3 and EIL1 activation and ET-induced EIN3 and EIL1 stabilization. In addition, antagonistic effects observed in JA and ET signalling are mediated by the interaction of JA-activated MYC2 TF and ET-stabilized TF EIN3 .
2.5. Inactivation of immune signalling pathways
Various negative regulation mechanisms ensure immune signalling activation is switched off when there is no danger. In the absence of ligand, several phosphatases interact with PRRs and their associated kinases to keep immune complexes inactive through dephosphorylation. For instance, Ser/Thr phosphatase type 2A (PP2A) constitutively associates with BRI1-associated kinase1 (BAK1) and negatively controls BAK1 activation in PRR immune receptor complexes . Negative regulation exerted by downstream phosphatases is illustrated by
Ubiquitination and proteasomal degradation are other mechanisms by which plant immune responses are attenuated. For example, two U-box E3 ubiquitin ligases, PUB12 and PUB13, are recruited to flagellin-induced FLS2/BAK1 receptor complex and phosphorylated by BAK1 to polyubiquitinate FLS2 and promote its degradation . Downregulation of immune signalling can also be achieved by ligand-induced endocytosis and degradation . This has been reported in localization studies of flg22-induced FLS2 receptors in
3. Plant defence responses to xylem-invading pathogens
3.1. General perception of MAMPs in roots
Despite the fact that roots are subjected to a rich microbial community, the perception of MAMPs and immune responses in roots are poorly understood. Millet et al.  studied immune responses in
3.2. Perception of vascular wilt pathogens
At early stages of infection, vascular wilt pathogens are faced with preformed physical and chemical root defences and MAMP-induced immune responses that hinder their invasion . Once they breach the rigid secondary xylem walls and enter the xylem vessels, vascular wilt pathogens are presumably recognized by specific extracellular receptors in the parenchyma cells surrounding the xylem vessels .
3.2.1. Perception of Verticillium spp.
In tomato, extracellular LRR RLP Ve1 [24,175,176] plays a role in xylem defence and provides resistance against race 1 strains of
Ve1 forms heterodimers with a tomato orthologue of the
3.2.2. Perception of Fusarium oxysporum f. sp. lycopersici
Three I (immunity) genes have been identified in tomato  in a resistance response to
3.2.3. Perception of Xanthomonas oryzae pv. oryzae
The rice LRR RLK Xa21 that provides resistance to
3.2.4. Perception of Ralstonia solanacearum
A pair of
3.3. Induced defence responses to vascular wilt pathogens
Recognition of vascular wilt pathogens by plant immune receptor complexes activates defence responses in the xylem vessels. Physical defence responses that confine pathogens from further spread comprise the formation of tyloses, accumulation of pectin-rich gels and gums, vascular coating and callose and secondary cell wall deposition [20,21]. An interesting adaptation to vascular wilt infection is vein clearing, a tissue-specific developmental programme leading to the formation of new xylem elements . Furthermore, significant metabolic changes have been reported in response to xylem infection and involve the induction of pathogenesis-related (PR) proteins, peroxidases, proteases as well as the production of antimicrobial secondary metabolites such as phytoalexins, sulphur-containing compounds and phenolic compounds [20,21].
Studies of defence signalling in response to root pathogens have so far mainly focused on the leaves and have provided evidence that defence mechanisms involve similar signalling pathways (Ca2+-signalling, induction of ROS and MAPK cascades, modulation of phytohormone signalling) . Moreover, plant microarray and RNASeq studies have revealed that the interaction between vascular wilt pathogens and host plants involves transcriptional reprogramming of hundreds of genes [208–211]. Interestingly, in an incompatible interaction, only modest changes in gene and protein expression have been reported [210,212–214] and most of the differentially expressed genes have been repressed in roots rather than in leaves . Moreover, genes implicated in photorespiration, hypoxia, glycoxylate metabolism and auxin signalling show inverse regulation on infection with the foliar pathogen
Genome-wide analyses on transcriptional and proteomic levels, together with functional characterization of individual genes, have revealed a convergence of signalling pathways in response to individual pathogens, in mostly controlled conditions. In the field, plants are simultaneously challenged by multiple stress factors, both biotic and abiotic. Even though signalling components of plant regulatory networks are partly shared in both and point to general stress response mechanisms, there is evidence of specific responses to combined stresses that are controlled by different signalling pathways and such studies may provide additional candidates for crop protection breeding [14–16,18].
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