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Review

An Overview of the Molecular Genetics of Plant Resistance to the Verticillium Wilt Pathogen Verticillium dahliae

by
Ranran Song
,
Junpeng Li
,
Chenjian Xie
*,
Wei Jian
and
Xingyong Yang
*
Chongqing Engineering Research Center of Specialty Crop Resources and The College of Life Science, Chongqing Normal University, Chongqing 401331, China
*
Authors to whom correspondence should be addressed.
Int. J. Mol. Sci. 2020, 21(3), 1120; https://doi.org/10.3390/ijms21031120
Submission received: 13 December 2019 / Revised: 9 January 2020 / Accepted: 28 January 2020 / Published: 7 February 2020
(This article belongs to the Special Issue Plant Disease Resistance)
Browse Figure
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Abstract

:
Verticillium dahliae is a soil-borne hemibiotrophic fungus that can lead to plant vascular disease and significant economic loss worldwide. Its hosts include over 400 dicotyledon plant species, such as annual herbs, perennials, and woody plants. The average yield loss of cotton crop caused by Verticillium wilt is approximately 10–35%. As the control of this disease is an urgent task for many countries, further understanding of the interaction between plants and V. dahliae is essential. Fungi can promote or inhibit plant growth, which is important; however, the most important relationship between plants and fungi is the host–pathogen relationship. Plants can become resistant to V. dahliae through diverse mechanisms such as cell wall modifications, extracellular enzymes, pattern recognition receptors, transcription factors, and salicylic acid (SA)/jasmonic acid (JA)/ethylene (ET)-related signal transduction pathways. Over the last decade, several studies on the physiological and molecular mechanisms of plant resistance to V. dahliae have been undertaken. In this review, many resistance-related genes are summarised to provide a theoretical basis for better understanding of the molecular genetic mechanisms of plant resistance to V. dahliae. Moreover, it is intended to serve as a resource for research focused on the development of genetic resistance mechanisms to combat Verticillium wilt.

1. Introduction

The soil-borne hemibiotrophic phytopathogenic fungus Verticillium dahliae can cause refractory vascular Verticillium wilt in a wide range of crops worldwide due to its highly aggressive pathogenicity and production of melanised dormant structures called microsclerotia, which can survive for several years in the soil [1]. It produces cell wall-degrading enzymes and phytotoxins, which cause signs of the disease. The fungus infects more than 200 dicotyledon plant species, such as annual herbs, perennials, and woody plants. The average yield loss of cotton crop caused by Verticillium wilt is approximately 10–35% in many countries. It generally causes plant dysplasia, leaf wilt, and yellowing and browning of vascular bundles, eventually leading to early death in some plants. At present, there are no fungicides available to control the infected plants [2], and thus Verticillium wilt results in extensive economic losses [3].
V. dahliae can infect a variety of dicotyledonous species including cotton, tobacco, tomatoes, Arabidopsis, and others. It usually invades and colonises the roots of plants, and then spreads throughout the plant [4]. V. dahliae begins to infect the roots of the plant through the soil, and hyphae penetrate the surface of the plant roots to colonise the vascular bundles, leading to plant death [5,6].
The main mechanism of its pathogenesis is xylem vessel blockage and toxin production. When the fungus invades the plant body, the mycelium blocks the xylem vessel, affecting the transport of water and nutrients in the plant [1,7]. However, transpiration and respiration of the aerial part are strong, causing water imbalance in the plant and signs such as leaf wilting and yellowing, which eventually leads to plant death [8]. However, catheter blockage is not the primary cause of plant wilting [7,9]. In the toxin theory, histological evidence indicates that leaf necrosis is caused by the action of mycotoxins [10]. The toxin produced by V. dahliae is an acidic protein–lipopolysaccharide complex [11]. It can seriously damage the metabolism of the plant body, fix carbon dioxide, decompose H3PO4, and eventually lead to plant death [12]. Current research indicates that toxin production is the main cause of plant wilting [2,13].
Plants have evolved numerous defence mechanisms to protect themselves from invading pathogens [14], and plant extracellular enzymes and the cell wall are the first defence barriers. Subsequently, plants induce pathogen-associated molecular pattern (PAMP)-triggered immunity by recognizing pathogens using cell-surface pattern recognition receptors (PRRs). In turn, pathogens have evolved mechanisms such as effectors to overcome these PAMP-induced defence mechanisms. The effector is recognised by plants to activate effector-triggered immunity (Figure 1). The plant immune defences have been described as a ‘zigzag’ model, in which many genes are involved in this ‘zigzag’ procedure [15].
Functional analysis of the key genes involved in growth and pathogenicity is the molecular genetic basis of revealing plant resistance to V. dahliae. Currently, several studies focusing on plant resistance to V. dahliae have been reported. In this review, some key findings and resistance-related genes are summarised to provide a theoretical basis to further understand the molecular genetic mechanisms of plant resistance to V. dahliae.

2. Defence-Related Proteins

In plants, defence-related proteins play a significant role in plant resistance to fungal pathogens. Polygalacturonase, which digests pectin in plant cell walls, contributes to fungal pathogenicity and plays a considerable role in the pathogenicity of V. dahliae [23]. A class of plant defence proteins, polygalacturonase-inhibiting proteins (PGIPs), can specifically inhibit endo-polygalacturonases. Further, the overexpression of CkPGIP1 from Cynanchum komarovii and GhPGIP1 from Gossypium hirsutum in cotton can improve cotton resistance to V. dahliae, which is associated with the upregulated expression of pathogenesis-related proteins (PRs), enhanced disease susceptibility 1 (EDS1), phytoalexin-deficient 4 (PAD4), and isochorismate synthase 1 (ICS1) genes that enhance xylem lignification [24,25].
NaD1, a plant defensin from Nicotiana alata with strong antifungal activity against many filamentous fungi, is associated with significant resistance to V. dahliae after transgenic expression in cotton plants [26]. GbNRX1 gene codes an apoplastic thioredoxin protein from Verticillium wilt-resistant island cotton (G. hirsutum cv Hai 7124), which is associated with an increase in abundance in response to V. dahliae infection. The observed increase in apoplastic reactive oxygen species (ROS) accumulation and reduced V. dahliae resistance in GbNRX1-silenced plants suggest that GbNRX1 can scavenge apoplastic ROS and is pivotal for the apoplastic immune response [27]. Hydroxyproline-rich proteins (HyPRPs) comprise a plant cell wall glycoprotein subfamily enriched in proline. The GbHyPRP1 protein from Gossypium barbadense contains proline-rich repetitive and Pollen Ole e I domains and negatively regulates the resistance of cotton plants to V. dahliae. GbHyPRP1 silencing was shown to markedly enhance cotton plant resistance to V. dahliae via cell wall thickening and ROS accumulation [28].
Non-expressor of pathogenesis-related protein 1 (NPR1) is a key regulator of systemic acquired resistance (SAR) in plants. When plants lack functional NPR1, their ability to express the PR gene is impaired and they show a near-total lack of an SAR response to pathogen infection [29]. Constitutive expression of the Arabidopsis NPR1 (AtNPR1) gene in cotton significantly increases the resistance of transgenic plants to non-defoliating V. dahliae [30]. StoNPR1, a Solanum torvum NPR1 gene, was previously expressed in V. dahliae-sensitive potato, which increased the resistance of transgenic plants to V. dahliae. Further, ICS1 and PR1a expression was also evidently enhanced in the StoNPR1 overexpression lines and was significantly induced by V. dahliae infection [31]. GhMLP28, a defence-related major latex protein (MLP) from G. hirsutum, is induced by V. dahliae, jasmonic acid (JA), salicylic acid (SA), and ethylene (ET). GhMLP28 silencing enhances the susceptibility of cotton plants to V. dahliae infection, whereas GhMLP28 ectopic overexpression in tobacco increases disease resistance. A further assay demonstrated that GhMLP28 activates the transcription factor activity of ET response factor 6 (GhERF6), which augmented the expression of some GCC-box (AGCCGCC element) genes, contributing to defence against V. dahliae [32].
Sulphur plays a considerable role in tomato disease resistance against V. dahliae. The expression of genes related to sulphur uptake and assimilation, sulphur-containing defence compounds, and high-affinity sulphate transporter genes are increased in V. dahliae-infected tomatoes during companion cropping [33]. The haumatin-like protein (TLP) gene is related to plant biotic and abiotic stress regulation. Transgenic plants with higher expression of the cotton TLP gene (GbTLP1) show enhanced resistance to different stress factors including V. dahliae infection [34]. A synthetic non-cyclic 0200-defensin derivative, BTD-S, shows robust antimicrobial activity to V. dahliae in vitro [35]. Further, the expression of BTD-S in Arabidopsis thaliana increases resistance to V. dahliae [36].
StoCYP77A2 is a wild eggplant cytochrome P450 gene and is induced by V. dahliae. Constitutive expression of StoCYP77A2 in tobacco enhances plant resistance to V. dahliae infection. Protein extraction from StoCYP77A2-transgenic tobacco indicated strong antifungal activity, which implies that StoCYP77A2 should participate in the synthesis of some antifungal compounds [37]. GhDIR1 encodes a putative dirigent protein and its overexpression leads to increases in lignin content in transgenic cotton plants, which display enhanced tolerance to V. dahliae infection [38]. GhUMC1, an umecyanin-like gene in cotton, is involved in the resistance of cotton plants to V. dahliae through regulation of the JA signalling pathway and lignin metabolism [39].

3. Enzymes

In plants, extracellular enzymes are often the first line of defence against fungal pathogens. Increasing evidence shows that chitinase is a key hydrolytic enzyme, which degrades the fungal cell wall [40], and its expression can be initiated in response to biotic and abiotic stress [41]. Chi28 belongs to the class IV chitinase subfamily, and Chi28 silencing significantly impairs cotton plant resistance to V. dahliae. VdSSEP1, a secretory serine protease, was shown to hydrolyse Chi28; however, cotton apoplastic protein CRR1 protects Chi28 from VdSSEP1-induced cleavage [42].
Pectins as the main element of the primary plant cell wall play a key role in defence mechanisms against plant pathogens. Pectin methylesterases (PMEs) catalyse dimethyl esterification of the homogalacturonan domains of pectin in the plant cell wall. GhPMEI3 silencing in cotton leads to enhanced susceptibility to V. dahliae. Moreover, GhPMEI3 and GhPMEs might participate in protein–protein interactions and are important for plant evolution to resist fungal pathogens [43].
Lignification in the plant cell wall is a plant innate immune defence response and the lignification of lignin in resistant cotton stems contributes to the resistance of cotton to disease [44]. GhLAC15, a laccase gene, was demonstrated to be strongly induced by pathogens. Moreover, its overexpression increases Verticillium wilt resistance via increased defence-induced lignification and arabinose and xylose accumulation in the upland cotton cell wall [45].
The expression of GbSBT1 in G. babardense, which encodes a subtilase that is mainly localised to the cell membrane, is induced by V. dahliae, JA, and ET, as it translocates to the cytoplasm following JA and ET treatment. GbSBT1 gene silencing reduces the tolerance of Pima-90 (resistant genotype) to V. dahliae infection. Moreover, the overexpression of GbSBT1 activates the expression of defence-related genes and increases Arabidopsis resistance to Fusarium oxysporum and V. dahliae [46].
Enoyl-CoA reductase (ECR) plays a crucial role in very-long-chain fatty acid formation. GhECR-silenced cotton plants are susceptible to V. dahliae infection, indicating that the GhECR gene is related to cotton resistance to different V. dahliae strains [47]. Cotton GbANS contributes to anthocyanin biosynthesis, and GbANS silencing significantly reduces anthocyanin production and cotton plant resistance to V. dahliae [48]. A U-box E3 ubiquitin ligase, GhPUB17, which can interact with and is inhibited by the antifungal protein GhCyP3, negatively regulates cotton resistance to Verticillium wilt pathogen [49]. The production of gossypol is sufficient to influence the resistance of cotton plants to V. dahliae. As such, silencing GbCAD1, encoding a key enzyme involved in gossypol biosynthesis, compromises cotton plant resistance to V. dahliae [50].

4. Receptor-Like Proteins

Lysin motif (LysM)-containing proteins are important PRRs in plants, which function in chitin recognition and the activation of defence responses against fungal pathogen attacks [51,52,53]. GhLYK1 and GhLYK2, two LysM-containing proteins, are induced after V. dahliae infection. However, GhLYK1 and GhLYK2 silencing compromises cotton plant resistance to V. dahliae. GhLYK2, but not GhLYK1, can induce ROS bursts in plants. Therefore, GhLYK2 and GhLYK1 might be distinctively dedicated to cotton defence [54]. In addition, in cotton, three important PRRs (Lyp1, Lyk7, and LysMe3) play an important role in activating downstream defence processes and inducing the defence response to V. dahliae via the recognition of chitin signals. The three PRR proteins are induced in response to V. dahliae, and their silencing greatly impairs SA, JA, and ROS generation, as well as resistance to V. dahliae [53].
In tomato (Solanum lycopersicum), Ve encodes receptor-like proteins containing extracellular leucine-rich repeats, and the Ve R-gene locus contributes to Verticillium resistance [25]. Ve1 is involved in the race-specific resistance to Verticillium wilt pathogen infection [55]. The Ve locus includes two closely-linked inverted genes, Ve1 and Ve2, encoding the extracellular leucine-rich repeat receptor-like protein (eLRR-RLP) and cell surface receptors [16]. Furthermore, it was shown that Ve genes encode a class of cell-surface glycoproteins with leucine zipper and receptor-mediated endocytosis-like signals [56]. Antagonistic relationships exist between Ve1 and Ve2 proteins, in which Ve1 modulates the induction of defence/stress proteins by Ve2 [25]. However, Ve1 transgene introduction does not alter the endogenous Ve2 expression [57].
Ve1 mediates plant resistance by monitoring the presence of the Ave1 effector in V. dahliae [58]. Some results suggested that H2O2, peroxidase, lignins, phenylalanine-ammonia lyase (PAL) gene expression, and JA are required for Ve1-mediated resistance to V. dahliae [59,60]. Ve1-transgenic Arabidopsis is only resistant to race 1, but not to race 2, strains of V. dahliae, V. albo-atrum, and V. longisporum. Importantly, the critical elements for resistance signalling are conserved, and the signalling components ACIF, MEK2, SERK3/BAK1, and SERK1 play a role in Ve1-positive regulation [61]. The defence signalling cascade downstream of Ve1 is required by ACIF, EDS1, NRC1, NDR1, MEK2, and SERK3/BAK1. Ve1-mediated plant defence requires the basal defence signalling elements EDS1, NRC1, and NDR1 [61,62]. The constitutive expression of tomato Ve1 in Arabidopsis, cotton, and tobacco plants results in increased resistance to Verticillium wilt [63]. As a consequence of Ve1/Ave1-induced immune signalling, the immune receptor Ve1 recognises the V. dahliae effector protein Ave1 and then triggers a hypersensitive response in tobacco and tomato [64], but it is not entirely required for Verticillium resistance [65].
Phylogenetic analysis also indicates that Ve1 homologues are extensively scattered in land plants, and that Ve1 homologues in hop (Humulus lupulus), potato (S. tuberosum), tobacco (Nicotiana glutinosa), and wild eggplant (S. torvum) have been cloned and characterised [66]. Gbve1, a tomato Ve homolog, was cloned from an island cotton cultivar with resistance to Verticillium wilt and it can be induced by V. dahliae infection via SA, JA, and ET. Gbve1 silencing in resistant cotton decreases the resistance to V. dahliae. Conversely, the overexpression of Gbve1 in Arabidopsis and upland cotton plants enhances resistance to V. dahliae [67].
Ve homologous genes, Gbvdr3 and Gbvdr6, encode plasma membrane receptor-like protein in the Verticillium wilt-resistant cotton cultivar G. barbadense Hai7124 [68,69]. Silencing and overexpression experiments suggested their involvement in cotton resistance against V. dahliae and that they can enhance transgenic cotton or Arabidopsis resistance to V. dahliae. Their expression is activated by SA, methyl jasmonate, abscisic acid, and ET, and is induced by V. dahliae. In transgenic Arabidopsis, the overexpression of Gbvdr3 and Gbvdr6 enhances the expression of JA/ET signalling pathway-related genes ethylene-responsive factor 1 (ERF1), PR3, and PDF 1.2; SA-related genes PR1 and PR2; the ET-regulated gene GST2; and ROS and callose accumulation in the early stage after V. dahliae infection [68,69,70].
A Ve1 homologous gene, VvVe, was identified in Vitis vinifera, and its overexpression in tobacco significantly increased resistance to V. dahliae and upregulated defence-related gene expression, including the SA-regulated pathogenesis-related protein gene (PR1), ET- and JA-regulated genes (ERF1), and lipoxygenase (LOX), and enhanced the accumulation of ROS, callose, and PAL [71]. StoVe1 is a Ve1 homolog from S. torvum, and StoVe1-overexpressing potato lines show increased resistance to V. dahliae [72]. StVe, a potential Verticillium wilt disease resistance gene, from S. torvum and SlVe1 from S. lycopersicoides are homologous to Ve1 and Ve2, respectively, and StVe and SlVe1 encode cell surface-like receptor proteins [73,74].
Micro-RNAs (miRNAs) are indispensable regulators of plant responses to biotic and abiotic stresses [75]. RNA silencing has an important role in plant defence against fungal pathogens and exerts specific defence functions against V. dahliae [76]. Upland cotton KV-1 displays multi-level resistance against Verticillium wilt, and some novel small RNAs have been identified after infection by V. dahliae strains with different virulence, V991 and D07038 [77]. Variants 3444a-5p and miR5562 showed the highest expression level in virulent conditions, whereas miR1423a-5p showed low-level expression [78]. Members of the potato miR482 superfamily and their variants were shown to target a class of disease-resistance proteins with nucleotide-binding sites and leucine-rich repeat (LRR) motifs, and miR482e-overexpressing transgenic potato plants show hypersensitivity to V. dahliae infection [79]. GhlncNAT-ANX2 and GhlncNAT-RLP7 are two species-conserved long noncoding RNAs, and their silencing in cotton significantly increases resistance to V. dahliae, which is possibly related to the upregulated expression of lipoxygenase 1 and lipoxygenase 2 [80]. Expression of GbRLK, a receptor-like kinase gene from the disease-resistant cotton G. barbadense Hai7124, is induced by V. dahliae. Moreover, transgenic cotton and the overexpression of GbRLK in Arabidopsis plants result in resistance against V. dahliae infection [17].

5. Transcription Factors

The MYB family of proteins is both large and diverse, with many members functioning as transcription factors. Increasing evidence shows that plant MYB transcription factors partake in defence against pathogen infection. Infection by V. dahliae stimulates Ca2+ influx into the cytosol and enhances GhMYB108 expression in cotton root cells. GhMYB108 was demonstrated as interacting with the calmodulin-like protein GhCML11 in a calcium-dependent manner; thus, GhCML11 and GhMYB108 silencing enhances cotton susceptibility to V. dahliae [81]. A stress-responsive HD-ZIP I transcription factor in cotton, GhHB12, negatively regulates the resistance of cotton plants by suppressing JA response genes [82]. CBP60g and SARD1 are two related plant-specific transcription factors involved in SA signalling. The secretory protein VdSCP41 in V. dahliae directly targets CBP60g to inhibit plant immunity, and mutations in Arabidopsis CBP60g and SARD1 compromise resistance to V. dahliae [83]. A homeodomain transcription factor gene (HDTF1) was isolated from cotton, and silencing HDTF1 was found to significantly enhance cotton plant resistance to V. dahliae and Botrytis cinerea, resulting in activation of JA-mediated signalling and JA accumulation [84]. Further, a basic helix-loop-helix (bHLH) transcription factor, GbbHLH171, interacts with and is phosphorylated by a defence-related receptor-like kinase in G. barbadense, namely, GbSOBIR1, in vitro and in vivo, and has a positive effect on cotton resistance to V. dahliae [85].

6. Signal Transduction

The ribosomal protein L18 (GaRPL18) gene from G.arboreum mediates plant resistance to V. dahliae via an SA-related signalling pathway. Silencing GaRPL18 impairs cotton plants resistance to V. dahliae, whereas GaRPL18 overexpression enhances Arabidopsis resistance to V. dahliae [86]. The phi-class glutathione (GSH) S-transferase gene (GaGSTF9) in Gossypium arboreum was found to be induced by V. dahliae via SA-related signalling pathway. GaGSTF9 silencing in cotton enhances its susceptibility. Conversely, the overexpression of GaGSTF9 increases Arabidopsis resistance to V. dahliae and the accumulation of endogenous SA and GST, indicating that GST might adjust ROS content via catalytic reduction of the tripeptide GSH, which in turn affects SA content [87].
Spermine (Spm) signalling is correlated with plant resistance to abiotic and biotic stresses. Two key rate-limiting enzymes in Spm biosynthesis are Spm synthase (GhSPMS) and S-adenosylmethionine decarboxylase (GhSAMDC), and GhSAMDC and GhSPMS silencing in cotton impairs plant resistance to V. dahliae infection. Enhanced resistance and the higher accumulation of Spm, SA, and leucine in transgenic A. thaliana overexpressing GhSAMDC suggest that GhSAMDC mediates Spm biosynthesis and contributes to plant resistance to V. dahliae via SA- and leucine-related signalling pathways [88]. The overexpression of cotton GhACL5 in Arabidopsis increases both plant height and T-Spm levels. Moreover, GhACL5 silencing in cotton results in a dwarf phenotype and also reduces resistance to V. dahliae. These results suggest that GhACL5 expression is related to in planta levels of T-Spm and contributes to stem elongation and defence responses to V. dahliae [89]. A polyamine oxidase gene (PAO), which can catalyse the conversion of Spm to spermidine (Spd), is induced early and strongly via plant hormone application and inoculation with V. dahliae. The constitutive expression of GhPAO in A. thaliana enhances resistance against V. dahliae and results in the accumulation of high levels of hydrogen peroxide, SA, and camalexin (a phytoalexin). These results suggest that GhPAO contributes to plant resistance to V. dahliae by activating Spm and camalexin signalling pathways [90].
Cotton cyclin-dependent kinase E (GhCDKE) is induced in cotton via V. dahliae infection and MeJA treatment. GhCDKE increases plant resistance to V. dahliae, which is mediated by the JA response pathway. GhCDKE silencing in cotton enhances susceptibility to Verticillium wilt pathogen, whereas GhCDKE overexpression in A. thaliana increases resistance to the pathogen [91]. GbWRKY1, a negative regulator of the JA-mediated defence pathway, contributes to plant resistance against B. cinerea and V. dahliae. During plant infection by V. dahliae, GbWRKY1 is also a key regulator that mediates the plant defence-to-development transition by activating JAZ1 expression [92]. GhCPK33 from G. hirsutum negatively regulates cotton resistance to V. dahliae by directly controlling JA biosynthesis. GhCPK33 silencing was shown to constitutively activate JA biosynthesis and JA mediated-defence responses and enhance resistance to V. dahliae infection [93]. GbSSI2 is an important regulator of the crosstalk between SA and JA signalling pathways. Moreover, the exogenous application of brassinolide can activate brassinosteroids and JA and enhance the resistance of cotton plants to V. dahliae [50].
Further, one study found that ET signalling in cotton roots infected with V. dahliae is significantly activated, which resulted in the high expression of ET biosynthesis and signal components [94]. The etr1-1 (ET receptor mutant) Arabidopsis strain shows enhanced resistance to V. dahliae, as well as enhanced activation and increased accumulation of CHI-1, CHI-2, GSTF12, GSTU16, Myb75, PR-1, PR-2, and PR-5 [95]. Ethylene-responsive factors (ERFs) commonly play an important role in pathogen defence responses. GbERFb, a new AP2/ERF transcription factor, can improve plant disease resistance [96]. GbERF1-like, ET response-related factor derived from G. barbadense, contributes to plant resistance against V. dahliae by positively regulating lignin synthesis. This resistance depends on the activation of GhHCT1 and AtPAL3 promoters by GbERF1-like proteins [97]. GbABR1 is an ERF subfamily B4 member and a new member of the AP2 family from G. barbadense. GbABR1-silenced plants show a higher disease index, indicating that this gene positively regulates resistance to Verticillium wilt [98].
Nucleotide-binding site leucine-rich repeat (NBS-LRR) proteins play a key role in plant defence against pathogens. A genome-wide association study indicated that CG02-containing TIR-NBS-LRR domains are the most likely candidate underlying cotton resistance to V. dahliae [99]. The island cotton NBS-LRR gene GbaNA1 can be induced by the pathogen V. dahliae and by the phytohormones ET, JA, and SA, contributing to island cotton resistance to V. dahliae isolate Vd991 [100]. The overexpression of GbaNA1 in A. thaliana enhances ROS content and the expression of genes related to the ethylene signalling pathway [101].
Serine/threonine-protein kinase (STK) is involved in responses to pathogen infection and oxidative stress via phosphorylation. The overexpression of G. barbadense GbSTK in Arabidopsis enhances resistance to V. dahliae and elevates PR-4, PR-5, and EREBP expression [102]. Moreover, the mitogen-activated protein kinase (MAPK) cascade plays key roles in plant defence against pathogen attack. MKK members in MAPK signalling cascades play dual roles in subtly regulating the resistance of cotton plants to Verticillium wilt; GhMKK4, GhMKK6, and GhMKK9 positively regulate, whereas GhMKK10 negatively regulates, cotton resistance [103]. As such, GhMKK2 and GhNDR1 silencing compromises the resistance of cotton plants to V. dahliae infection [104].

7. Concluding Remarks

Currently, numerous genes related to V. dahliae resistance have been identified in plants (Table 1). However, Verticillium wilt is still an enormous threat to agricultural production. Due to the presence of microsclerotia in V. dahliae, it can survive in the soil for many years, and it rapidly spreads; thus, it is difficult to control once infection occurs. Moreover, there is no fungicide available for plants, further limiting efficient control. Currently, the most effective control measures are genetic resistance. Therefore, it is necessary to further explore the genes related to V. dahliae resistance in plants. Resistance-related genes can be explored from various perspectives such as extracellular enzymes, the cell wall, PRRs, transcription factors, and SA/JA/ET-related signal transduction pathways. The further development of new technology such as host-induced gene silencing can aid in plant protection. At present, many genes remain unidentified, and there are few known genes related to resistance. Therefore, the technology available for genetic research is also extremely limited. In this paper, we summarised the genes related to V. dahliae resistance in plants on the basis of extracellular enzymes, cell walls, PRRs, transcription factors, and SA/JA/ET-related signal transduction pathways. This report provides a good theoretical resource for researchers and could aid in the discovery of additional genes related to resistance by providing a theoretical basis to further understand the molecular genetic mechanisms of plant resistance to V. dahliae. With the development of molecular biology technology and the application of multi-omics integrative analyses to the study plant disease resistance mechanisms, it is possible to study interactions between plants and Verticillium wilt, which will contribute to the discovery of plant disease resistance genes. At the same time, with the in-depth analysis of the molecular mechanisms underlying plant resistance to Verticillium wilt, it will be possible to obtain crops varieties that are resistant to Verticillium wilt through genetic engineering and breeding technology.

Funding

This research was funded by [the Basic Research and Frontier Exploration Foundation of Chongqing] grant number [cstc2018jcyjAX0707, cstc2017jcyjA0573] and [the National Natural Science Foundation of China] grant number [31701734].

Conflicts of Interest

The authors declare that they have no conflict of interest.

References

  1. Klosterman, S.J.; Atallah, Z.K.; Vallad, G.E.; Subbarao, K.V. Diversity, pathogenicity; and management of Verticillium Species. Annu. Rev. Phytopathol. 2009, 47, 39–62. [Google Scholar] [CrossRef] [Green Version]
  2. Fradin, E.F.; Thomma, B.P. Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. albo-atrum. Mol. Plant Pathol. 2006, 7, 71–86. [Google Scholar] [CrossRef] [PubMed]
  3. Wang, X.K.; Wang, C.Y.; Xie, C.J.; Yang, X.Y. Advances in molecular mechanisms of Verticillium pathogenicity and plant resistance to Verticillium wilt. J. Henan. Agr. Sci. 2014, 43, 1–6. [Google Scholar]
  4. Zhang, J.; Fang, H.; Zhou, H.; Sanogo, S.; Ma, Z. Genetics; breeding; and marker-assisted selection for Verticillium wilt resistance in cotton. Crop Sci. 2014, 54, 1289–1303. [Google Scholar] [CrossRef]
  5. Prieto, P.; Navarroraya, C.; Valverdecorredor, A.; Amyotte, S.G.; Dobinson, K.F.; Mercadoblanco, J.; Segura, A.; Preston, G.; Wit, P.D. Colonization process of olive tissues by Verticillium dahliae and its in planta interaction with the biocontrol root endophyte Pseudomonas fluorescens PICF7. Microb. Biotechnol. 2010, 2, 499–511. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  6. Zhao, P.; Zhao, Y.L.; Jin, Y.; Zhang, T.; Guo, H.S. Colonization process of Arabidopsis thaliana roots by a green fluorescent protein-tagged isolate of Verticillium dahliae. Protein Cell 2014, 5, 94–98. [Google Scholar]
  7. Shaban, M.; Miao, Y.; Ullah, A.; Khan, A.H.; Ahmed, M.M.; Tabassum, M.A.; Zhu, L. Physiological and molecular mechanism of defense in cotton against Verticillium dahliae. Plant Physiol. Biochem. 2018, 125, 193–204. [Google Scholar] [CrossRef]
  8. Temple, S.H.; DeVay, J.; Forrester, L.L. Temperature effects upon development and pathogenicity of defoliating and nondefoliating pathotypes of Verticillium dahliae in leaves of cotton plants. Phytopathology 1973, 63, 953–958. [Google Scholar] [CrossRef]
  9. Daayf, F. Verticillium wilts in crop plants: Pathogen invasion and host defence responses. Can. J. Plant Pathol. 2015, 37, 8–20. [Google Scholar] [CrossRef]
  10. Talboys, P.W. Association of tylosis and hyperplasia of the xylem with vascular invasion of the hop by Verticillium albo-atrum. Trans. Brit. Mycol. Soc. 1958, 41, 249–260. [Google Scholar] [CrossRef]
  11. Meyer, R.; Slater, V.; Dubery, I.A. A phytotoxic protein-lipopolysaccharide complex produced by Verticillium dahliae. Phytochemistry 1994, 35, 1449–1453. [Google Scholar] [CrossRef]
  12. Porter, C.; Green, R. Production of exotoxin in the genus Verticillium. Phytopathology 1952, 42, 472. [Google Scholar]
  13. Luo, X.; Xie, C.; Dong, J.; Yang, X.; Sui, A. Interactions between Verticillium dahliae and its host: Vegetative growth, pathogenicity, plant immunity. Appl. Microbiol. Biotechnol. 2014, 98, 6921–6932. [Google Scholar] [CrossRef] [PubMed]
  14. Belien, T.; Van, C.S.J.; Volckaert, G. Microbial endoxylanases, effective weapons to breach the plant cell-wall barrier or, rather, triggers of plant defense systems? Mol. Plant-Microbe Interact. 2006, 19, 1072–1081. [Google Scholar] [CrossRef] [PubMed]
  15. Jones, J.D.; Dangl, J.L. The plant immune system. Nature 2006, 444, 323–329. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  16. Fradin, E.F.; Zhang, Z.; Rovenich, H.; Song, Y.; Liebrand, T.W.; Masini, L.; van den Berg, G.C.; Joosten, M.H.; Thomma, B.P. Functional analysis of the tomato immune receptor Ve1 through domain swaps with its non-functional homolog Ve2. PLoS ONE 2014, 9, e88208. [Google Scholar] [CrossRef] [Green Version]
  17. Zhao, J.; Zhang, Z.; Gao, Y.; Zhou, L.; Fang, L.; Chen, X.; Ning, Z.; Chen, T.; Guo, W.; Zhang, T. Overexpression of GbRLK, a putative receptor-like kinase gene, improved cotton tolerance to Verticillium wilt. Sci. Rep. 2015, 5, 15048. [Google Scholar]
  18. Bu, B.; Qiu, D.; Zeng, H.; Guo, L.; Yuan, J.; Yang, X. A fungal protein elicitor PevD1 induces Verticillium wilt resistance in cotton. Plant Cell Rep. 2014, 33, 461–470. [Google Scholar] [CrossRef]
  19. Liang, Y.; Cui, S.; Tang, X.; Zhang, Y.; Qiu, D.; Zeng, H.; Guo, L.; Yuan, J.; Yang, X. An asparagine-rich protein Nbnrp1 modulate Verticillium dahliae protein PevD1-induced cell death and disease resistance in Nicotiana benthamiana. Front. Plant Sci. 2018, 9, 303. [Google Scholar] [CrossRef] [Green Version]
  20. Liu, M.; Khan, N.U.; Wang, N.; Yang, X.; Qiu, D. The protein elicitor PevD1 enhances resistance to pathogens and promotes growth in Arabidopsis. Int. J. Biol. Sci. 2016, 12, 931–943. [Google Scholar] [CrossRef] [Green Version]
  21. Zhang, Y.; Gao, Y.; Liang, Y.; Dong, Y.; Yang, X.; Qiu, D. Verticillium dahliae PevD1, an Alt a 1-like protein, targets cotton PR5-like protein and promotes fungal infection. J. Exp. Bot. 2019, 70, 613–626. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  22. Zhou, R.; Zhu, T.; Han, L.; Liu, M.; Xu, M.; Liu, Y.; Han, D.; Qiu, D.; Gong, Q.; Liu, X. The asparagine-rich protein NRP interacts with the Verticillium effector PevD1 and regulates the subcellular localization of cryptochrome 2. J. Exp. Bot. 2017, 68, 3427–3440. [Google Scholar] [CrossRef] [PubMed]
  23. Liu, N.; Ma, X.; Yun, S.; Zhang, X.; Li, F.; Hou, Y. Necrotizing activity of Verticillium dahliae and Fusarium oxysporum f. sp. vasinfectum endopolygalacturonases in cotton. Plant Dis. 2017, 101, 1128–1138. [Google Scholar] [PubMed]
  24. Liu, N.; Zhang, X.; Sun, Y.; Wang, P.; Li, X.; Pei, Y.; Li, F.; Hou, Y. Molecular evidence for the involvement of a polygalacturonase-inhibiting protein, GhPGIP1, in enhanced resistance to Verticillium and Fusarium wilts in cotton. Sci. Rep. 2017, 7, 39840. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Nazar, R.N.; Xu, X.; Kurosky, A.; Robb, J. Antagonistic function of the Ve R-genes in tomato. Plant Mol. Biol. 2018, 98, 67–79. [Google Scholar] [CrossRef] [PubMed]
  26. Gaspar, Y.M.; McKenna, J.A.; McGinness, B.S.; Hinch, J.; Poon, S.; Connelly, A.A.; Anderson, M.A.; Heath, R.L. Field resistance to Fusarium oxysporum and Verticillium dahliae in transgenic cotton expressing the plant defensin NaD1. J. Exp. Bot. 2014, 65, 1541–1550. [Google Scholar] [CrossRef]
  27. Li, Y.B.; Han, L.B.; Wang, H.Y.; Zhang, J.; Sun, S.T.; Feng, D.Q.; Yang, C.L.; Sun, Y.D.; Zhong, N.Q.; Xia, G.X. The thioredoxin GbNRX1 plays a crucial role in homeostasis of apoplastic reactive oxygen species in response to Verticillium dahliae infection in cotton. Plant Physiol. 2016, 170, 2392–2406. [Google Scholar] [CrossRef] [Green Version]
  28. Yang, J.; Zhang, Y.; Wang, X.; Wang, W.; Li, Z.; Wu, J.; Wang, G.; Wu, L.; Zhang, G.; Ma, Z. HyPRP1 performs a role in negatively regulating cotton resistance to Verticillium dahliae via the thickening of cell walls and ROS accumulation. BMC Plant Boil. 2018, 18, 339. [Google Scholar]
  29. Pajerowska-Mukhtar, K.M.; Emerine, D.K.; Mukhtar, M.S. Tell me more: Roles of NPRs in plant immunity. Trends Plant Sci. 2013, 8, 402–411. [Google Scholar] [CrossRef]
  30. Parkhi, V.; Kumar, V.; Campbell, L.A.M.; Bell, A.A.; Rathore, K.S. Expression of Arabidopsis NPR1 in transgenic cotton confers resistance to non-defoliating isolates of Verticillium dahliae but not the defoliating isolates. J. Phytopathol. 2010, 158, 822–825. [Google Scholar] [CrossRef]
  31. Jue, D.; Liu, Y.; Shi, C.; Min, C.; Yang, Q. Cloning and characterization of a Solanum torvum NPR1 gene involved in regulating plant resistance to Verticillium dahliae. Acta Physiol. Plant. 2014, 36, 2999–3011. [Google Scholar]
  32. Yang, C.L.; Liang, S.; Wang, H.Y.; Han, L.B.; Wang, F.X.; Cheng, H.Q.; Wu, X.M.; Qu, Z.L.; Wu, J.H.; Xia, G.X. Cotton major latex protein 28 functions as a positive regulator of the ethylene responsive factor 6 in defense against Verticillium dahliae. Mol. Plant. 2015, 8, 399–411. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  33. Fu, X.; Li, C.; Zhou, X.; Liu, S.; Wu, F. Physiological response and sulfur metabolism of the V. dahliae-infected tomato plants in tomato/potato onion companion cropping. Sci. Rep. 2016, 6, 36445. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  34. Munis, M.F.; Tu, L.; Deng, F.; Tan, J.; Xu, L.; Xu, S.; Long, L.; Zhang, X. A thaumatin-like protein gene involved in cotton fiber secondary cell wall development enhances resistance against Verticillium dahliae and other stresses in transgenic tobacco. Biochem. Biophys. Res. Commun. 2010, 393, 38–44. [Google Scholar] [CrossRef]
  35. Li, F.; Shen, H.; Wang, M.; Fan, K.; Bibi, N.; Ni, M.; Yuan, S.; Wang, X. A synthetic antimicrobial peptide BTD-S expressed in Arabidopsis thaliana confers enhanced resistance to Verticillium dahliae. Mol. Genet. Genom. 2016, 291, 1647–1661. [Google Scholar] [CrossRef]
  36. Ni, M.; Zhao, Y.; Bibi, N.; Shao, M.; Yuan, S.; Fan, K.; Zhang, G.; Li, F.; Wang, X. A non-cyclic baboon θ-defensin derivative exhibiting antimicrobial activity against the phytopathogen Verticillium dahliae. Appl. Microbiol. Bio. 2013, 97, 2043–2052. [Google Scholar] [CrossRef]
  37. Liu, Y.; Shi, C.; Mu, X.; Chao, L.; Ke, S.; Zhu, W.; Yang, Q. Cloning and expression of a wild eggplant cytochrome P450 gene, StoCYP77A2, involved in plant resistance to Verticillium dahliae. Plant Biotech. Rep. 2015, 9, 167–177. [Google Scholar]
  38. Shi, H.; Liu, Z.; Zhu, L.; Zhang, C.; Chen, Y.; Zhou, Y.; Li, F.; Li, X. Overexpression of cotton (Gossypium hirsutum) dirigent1 gene enhances lignification that blocks the spread of Verticillium dahliae. Acta Biochim. Biophys. Sin. 2012, 44, 555–564. [Google Scholar] [CrossRef] [Green Version]
  39. Zhu, W.; Gao, E.; Shaban, M.; Wang, Y.; Wang, H.; Nie, X.; Zhu, L. GhUMC1, a blue copper-binding protein; regulates lignin synthesis and cotton immune response. Biochem. Bioph. Res. Commun. 2018, 504, 75–81. [Google Scholar] [CrossRef]
  40. Xu, J.; Xu, X.; Tian, L.; Wang, G.; Zhang, X.; Wang, X.; Guo, W. Discovery and identification of candidate genes from the chitinase gene family for Verticillium dahliae resistance in cotton. Sci. Rep. 2016, 6, 29022. [Google Scholar] [CrossRef]
  41. Cheng, X.X.; Zhao, L.H.; Klosterman, S.J.; Feng, H.J.; Feng, Z.L.; Feng, W.; Shi, Y.Q.; Li, Z.F.; Zhu, H.Q. The endochitinase VDECH from Verticillium dahliae inhibits spore germination and activates plant defense responses. Plant Sci. 2017, 259, 12. [Google Scholar] [CrossRef]
  42. Han, L.B.; Li, Y.B.; Wang, F.X.; Wang, W.Y.; Liu, J.; Wu, J.H.; Zhong, N.Q.; Wu, S.J.; Jiao, G.L.; Wang, H.Y.; et al. The cotton apoplastic protein CRR1 stabilizes chitinase 28 to facilitate defense against the fungal pathogen Verticillium dahliae. Plant Cell 2019, 31, 520–536. [Google Scholar] [CrossRef] [PubMed]
  43. Liu, N.; Sun, Y.; Pei, Y.; Zhang, X.; Wang, P.; Li, X.; Li, F.; Hou, Y. A pectin methylesterase inhibitor enhances resistance to Verticillium wilt. Plant Physiol. 2018, 176, 2202–2220. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  44. Xu, L.; Zhu, L.; Tu, L.; Liu, L.; Yuan, D.; Jin, L.; Long, L.; Zhang, X. Lignin metabolism has a central role in the resistance of cotton to the wilt fungus Verticillium dahliae as revealed by RNA-Seq-dependent transcriptional analysis and histochemistry. J. Exp. Bot. 2011, 62, 5607–5621. [Google Scholar] [CrossRef] [Green Version]
  45. Zhang, Y.; Wu, L.; Chen, B.; Zhao, J.; Cui, J.; Li, Z.; Yang, J.; Wu, L.; Zhang, G.; Ma, Z. The cotton laccase gene GHLAC15 enhances Verticillium wilt via an increase in defence-induced lignification and lignin components in the cell walls of plants. Mol. Plant Pathol. 2018, 20, 309–322. [Google Scholar] [CrossRef] [Green Version]
  46. Duan, X.; Zhang, Z.; Wang, J.; Zuo, K. Characterization of a novel cotton subtilase gene GbSBT1 in response to extracellular stimulations and its role in Verticillium resistance. PLoS ONE 2016, 11, e0153988. [Google Scholar] [CrossRef] [Green Version]
  47. Mustafa, R.; Hamza, M.; Kamal, H.; Mansoor, S.; Scheffler, J.; Amin, I. tobacco rattle virus-based silencing of enoyl-CoA reductase gene and its role in resistance against cotton wilt disease. Mol. Biotechnol. 2017, 59, 241–250. [Google Scholar] [CrossRef]
  48. Long, L.; Zhao, J.R.; Xu, F.C.; Yang, W.W.; Liao, P.; Gao, Y.; Gao, W.; Song, C.P. Silencing of GbANS reduces cotton resistance to Verticillium dahliae through decreased ROS scavenging during the pathogen invasion process. Plant Cell Tiss. Org. 2018, 135, 213–221. [Google Scholar] [CrossRef]
  49. Qin, T.; Liu, S.; Zhang, Z.; Sun, L.; He, X.; Lindsey, K.; Zhu, L.; Zhang, X. GhCyP3 improves the resistance of cotton to Verticillium dahliae by inhibiting the E3 ubiquitin ligase activity of GhPUB17. Plant Mol. Biol. 2019, 99, 379–393. [Google Scholar] [CrossRef]
  50. Gao, W.; Long, L.; Zhu, L.F.; Xu, L.; Gao, W.H.; Sun, L.Q.; Liu, L.L.; Zhang, X.L. Proteomic and virus-induced gene silencing (VIGS) analyses reveal that gossypol, brassinosteroids, and jasmonic acid contribute to the resistance of cotton to Verticillium dahliae. Mol. Cell Proteomics 2013, 12, 3690–3703. [Google Scholar] [CrossRef] [Green Version]
  51. Tanaka, K.; Nguyen, C.T.; Liang, Y.; Cao, Y.; Stacey, G. Role of LysM receptors in chitin-triggered plant innate immunity. Plant Signal Behav. 2013, 8, e22598. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  52. Wan, J.; Tanaka, K.; Zhang, X.C.; Son, G.H.; Brechenmacher, L.; Nguyen, T.H.; Stacey, G. LYK4, a lysin motif receptor-like kinase, is important for chitin signaling and plant innate immunity in Arabidopsis. Plant Physiol. 2012, 160, 396–406. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  53. Xu, J.; Wang, G.; Wang, J.; Li, Y.; Tian, L.; Wang, X.; Guo, W. The lysin motif-containing proteins, Lyp1, Lyk7 and LysMe3, play important roles in chitin perception and defense against Verticillium dahliae in cotton. BMC Plant Biol. 2017, 17, 148. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  54. Gu, Z.; Liu, T.; Ding, B.; Li, F.; Wang, Q.; Qian, S.; Ye, F.; Chen, T.; Yang, Y.; Wang, J.; et al. Two Lysin-motif receptor kinases; Gh-LYK1 and Gh-LYK2; contribute to resistance against Verticillium wilt in upland cotton. Front. Plant Sci. 2017, 8, 2133. [Google Scholar] [CrossRef] [Green Version]
  55. Nazar, R.N.; Castroverde, C.D.M.; Xu, X.; Kurosky, A.; Robb, J. Wounding induces tomato Ve1 R-gene expression. Planta 2019, 249, 1779–1797. [Google Scholar] [CrossRef]
  56. Kawchuk, L.M.; Hachey, J.; Lynch, D.R.; Kulcsar, F.; van Rooijen, G.; Waterer, D.R.; Robertson, A.; Kokko, E.; Byers, R.; Howard, R.J.; et al. Tomato Ve disease resistance genes encode cell surface-like receptors. Proc. Natl. Acad. Sci. USA 2001, 98, 6511–6515. [Google Scholar] [CrossRef] [Green Version]
  57. Castroverde, C.D.; Xu, X.; Blaya, F.J.; Nazar, R.N.; Robb, J. Epistatic influence in tomato Ve1-mediated resistance. Plant Biol. 2017, 19, 843–847. [Google Scholar] [CrossRef]
  58. De Jonge, R.; van Esse, H.P.; Maruthachalam, K.; Bolton, M.D.; Santhanam, P.; Saber, M.K.; Zhang, Z.; Usami, T.; Lievens, B.; Subbarao, K.V.; et al. Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proc. Natl. Acad. Sci. USA 2012, 109, 5110–5115. [Google Scholar] [CrossRef] [Green Version]
  59. Castroverde, C.D.; Xu, X.; Nazar, R.N.; Robb, J. Biotic factors that induce the tomato Ve1 R-gene. Plant Sci. 2017, 265, 61–69. [Google Scholar] [CrossRef]
  60. Gayoso, C.; Pomar, F.; Novo-Uzal, E.; Merino, F.; de Ilarduya, O.M. The Ve-mediated resistance response of the tomato to Verticillium dahliae involves H2O2, peroxidase and lignins and drives PAL gene expression. BMC Plant Biol. 2010, 10, 232. [Google Scholar] [CrossRef] [Green Version]
  61. Fradin, E.F.; Abd-El-Haliem, A.; Masini, L.; van den Berg, G.C.; Joosten, M.H.; Thomma, B.P. Interfamily transfer of tomato Ve1 mediates Verticillium resistance in Arabidopsis. Plant Physiol. 2011, 156, 2255–2265. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  62. Fradin, E.F.; Zhang, Z.; Juarez-Ayala, J.C.; Castroverde, C.D.; Nazar, R.N.; Robb, J.; Liu, C.M.; Thomma, B.P. Genetic dissection of Verticillium wilt resistance mediated by tomato Ve1. Plant Physiol. 2009, 150, 320–332. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  63. Song, Y.; Liu, L.; Wang, Y.; Valkenburg, D.J.; Zhang, X.; Zhu, L.; Thomma, B. Transfer of tomato immune receptor Ve1 confers Ave1-dependent Verticillium resistance in tobacco and cotton. Plant Biotechnol. J. 2018, 16, 638–648. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  64. Zhang, Z.; Fradin, E.; de Jonge, R.; van Esse, H.P.; Smit, P.; Liu, C.M.; Thomma, B.P. Optimized agroinfiltration and virus-induced gene silencing to study Ve1-mediated Verticillium resistance in tobacco. Mol. Plant Microbe. Interact. 2013, 26, 182–190. [Google Scholar] [CrossRef] [Green Version]
  65. Zhang, Z.; van Esse, H.P.; van Damme, M.; Fradin, E.F.; Liu, C.M.; Thomma, B.P. Ve1-mediated resistance against Verticillium does not involve a hypersensitive response in Arabidopsis. Mol. Plant Pathol. 2013, 14, 719–727. [Google Scholar] [CrossRef]
  66. Song, Y.; Zhang, Z.; Seidl, M.F.; Majer, A.; Jakse, J.; Javornik, B.; Thomma, B.P. Broad taxonomic characterization of Verticillium wilt resistance genes reveals an ancient origin of the tomato Ve1 immune receptor. Mol. Plant Pathol. 2017, 18, 195–209. [Google Scholar] [CrossRef]
  67. Zhang, B.; Yang, Y.; Chen, T.; Yu, W.; Liu, T.; Li, H.; Fan, X.; Ren, Y.; Shen, D.; Liu, L. Island cotton Gbve1 gene encoding a receptor-like protein confers resistance to both defoliating and non-defoliating isolates of Verticillium dahliae. PLoS ONE 2012, 7, e51091. [Google Scholar] [CrossRef] [Green Version]
  68. Yang, Y.; Chen, T.; Ling, X.; Ma, Z. Gbvdr6, a gene encoding a receptor-like protein of cotton (Gossypium barbadense), confers resistance to Verticillium wilt in Arabidopsis and upland cotton. Front. Plant Sci. 2017, 8, 2272. [Google Scholar] [CrossRef] [Green Version]
  69. Zhang, B.J.; Zhang, H.P.; Chen, Q.Z.; Tang, N.; Wang, L.K.; Wang, R.F.; Zhang, B.L. Molecular cloning and analysis of a receptor-like promoter of Gbvdr3 gene in sea island cotton. Genet. Mol. Res. 2016, 15, gmr.15028636. [Google Scholar] [CrossRef]
  70. Chen, T.; Kan, J.; Yang, Y.; Ling, X.; Chang, Y.; Zhang, B. A Ve homologous gene from Gossypium barbadense, Gbvdr3, enhances the defense response against Verticillium dahliae. Plant Physiol. Biochem. 2006, 98, 101–111. [Google Scholar] [CrossRef]
  71. Tang, J.; Lin, J.; Yang, Y.; Chen, T.; Ling, X.; Zhang, B.; Chang, Y. Ectopic expression of a Ve homolog VvVe gene from Vitis vinifera enhances defense response to Verticillium dahliae infection in tobacco. Gene 2016, 576, 492–498. [Google Scholar] [CrossRef] [PubMed]
  72. Liu, S.; Zhu, Y.; Xie, C.; Jue, D.; Hong, Y.; Chen, M.; Hubdar, A.K.; Yang, Q. Transgenic potato plants expressing StoVe1 exhibit enhanced resistance to Verticillium dahliae. Plant Mol. Biol. Rep. 2012, 30, 1032–1039. [Google Scholar] [CrossRef]
  73. Chai, Y.; Zhao, L.; Liao, Z.; Sun, X.; Zuo, K.; Zhang, L.; Wang, S.; Tang, K. Molecular cloning of a potential Verticillium dahliae resistance gene SlVe1 with multi-site polyadenylation from Solanum licopersicoides. DNA Seq. 2003, 14, 375–384. [Google Scholar] [CrossRef] [PubMed]
  74. Fei, J.; Chai, Y.; Wang, J.; Lin, J.; Sun, X.; Sun, C.; Zuo, K.; Tang, K. cDNA cloning and characterization of the Ve homologue gene StVe from Solanum torvum Swartz. DNA Seq. 2004, 15, 88–95. [Google Scholar] [CrossRef]
  75. Jones-Rhoades, M.W.; Bartel, D.P. Computational identification of plant microRNAs and their targets; including a stress-induced miRNA. Mol. Cell 2004, 14, 787–799. [Google Scholar] [CrossRef]
  76. Ellendorff, U.; Fradin, E.F.; Thomma, B.P.; De Jonge, R. RNA silencing is required for Arabidopsis defence against Verticillium wilt disease. J. Exp. Bot. 2008, 60, 591–602. [Google Scholar] [CrossRef] [Green Version]
  77. He, X.; Sun, Q.; Jiang, H.; Zhu, X.; Mo, J.; Long, L.; Xiang, L.; Xie, Y.; Shi, Y.; Yuan, Y. Identification of novel microRNAs in the Verticillium wilt-resistant upland cotton variety KV-1 by high-throughput sequencing. SpringerPlus 2014, 3, 564. [Google Scholar] [CrossRef] [Green Version]
  78. He, X.H.; Shi, M.; Sun, Q.; Cai, Y.F. Expression profile analysis and target gene prediction of three conserved MicroRNAs in resistant Gossypium hirsutum cv. KV-1 responding to Verticillium dahlia. In Advanced Materials Research; Trans Tech Publications: Zurich, Switzerland, 2014; pp. 441–445. [Google Scholar]
  79. Yang, L.; Mu, X.; Liu, C.; Cai, J.; Shi, K.; Zhu, W.; Yang, Q. Overexpression of potato miR482e enhanced plant sensitivity to Verticillium dahliae infection. J. Integ. Plant. Boil. 2015, 57, 1078–1088. [Google Scholar] [CrossRef]
  80. Zhang, L.; Wang, M.; Li, N.; Wang, H.; Qiu, P.; Pei, L.; Xu, Z.; Wang, T.; Gao, E.; Liu, J. Long noncoding RNA s involve in resistance to Verticillium dahliae; a fungal disease in cotton. Plant Biotechnol. J. 2018, 16, 1172–1185. [Google Scholar] [CrossRef] [Green Version]
  81. Cheng, H.Q.; Han, L.B.; Yang, C.L.; Wu, X.M.; Zhong, N.Q.; Wu, J.H.; Wang, F.X.; Wang, H.Y.; Xia, G.X. The cotton MYB108 forms a positive feedback regulation loop with CML11 and participates in the defense response against Verticillium dahliae infection. J. Exp. Bot. 2016, 67, erw016. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  82. He, X.; Wang, T.; Zhu, W.; Wang, Y.; Zhu, L. GhHB12, a HD-ZIP I transcription factor, negatively regulates the cotton resistance to Verticillium dahliae. Int. J. Mol. Sci. 2018, 19, 3997. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  83. Qin, J.; Wang, K.; Sun, L.; Xing, H.; Wang, S.; Li, L.; Chen, S.; Guo, H.S.; Zhang, J. The plant-specific transcription factors CBP60g and SARD1 are targeted by a Verticillium secretory protein VdSCP41 to modulate immunity. eLife 2018, 7, e34902. [Google Scholar] [CrossRef]
  84. Gao, W.; Long, L.; Xu, L.; Lindsey, K.; Zhang, X.; Zhu, L. Suppression of the homeobox gene HDTF1 enhances resistance to Verticillium dahliae and Botrytis cinerea in cotton. J. Integr. Plant Biol. 2016, 58, 503–513. [Google Scholar] [CrossRef] [Green Version]
  85. Zhou, Y.; Sun, L.; Wassan, G.M.; He, X.; Shaban, M.; Zhang, L.; Zhu, L.; Zhang, X. GbSOBIR1 confers Verticillium wilt resistance by phosphorylating the transcriptional factor GbbHLH171 in Gossypium barbadense. Plant Biotechnol. J. 2019, 17, 152–163. [Google Scholar] [CrossRef] [Green Version]
  86. Gong, Q.; Yang, Z.; Wang, X.; Butt, H.I.; Chen, E.; He, S.; Zhang, C.; Zhang, X.; Li, F. Salicylic acid-related cotton (Gossypium arboreum) ribosomal protein GaRPL18 contributes to resistance to Verticillium dahliae. BMC Plant Biol. 2017, 17, 59. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  87. Gong, Q.; Yang, Z.; Chen, E.; Sun, G.; He, S.; Butt, H.I.; Zhang, C.; Zhang, X.; Yang, Z.; Du, X.; et al. A Phi-class glutathione S-transferase gene for Verticillium wilt resistance in Gossypium arboreum identified in a genome-wide association study. Plant Cell Physiol. 2018, 59, 275–289. [Google Scholar] [CrossRef]
  88. Mo, H.J.; Sun, Y.X.; Zhu, X.L.; Wang, X.F.; Zhang, Y.; Yang, J.; Yan, G.J.; Ma, Z.Y. Cotton S-adenosylmethionine decarboxylase-mediated spermine biosynthesis is required for salicylic acid- and leucine-correlated signaling in the defense response to Verticillium dahliae. Planta 2016, 243, 1023–1039. [Google Scholar] [CrossRef]
  89. Mo, H.; Wang, X.; Zhang, Y.; Yang, J.; Ma, Z. Cotton ACAULIS5 is involved in stem elongation and the plant defense response to Verticillium dahliae through thermospermine alteration. Plant Cell Rep. 2015, 34, 1975–1985. [Google Scholar] [CrossRef]
  90. Mo, H.; Wang, X.; Zhang, Y.; Zhang, G.; Zhang, J.; Ma, Z. Cotton polyamine oxidase is required for spermine and camalexin signalling in the defence response to Verticillium dahliae. Plant J. 2015, 83, 962–975. [Google Scholar] [CrossRef] [Green Version]
  91. Li, X.; Pei, Y.; Sun, Y.; Liu, N.; Wang, P.; Liu, D.; Ge, X.; Li, F.; Hou, Y. A cotton cyclin-dependent kinase E confers resistance to Verticillium dahliae mediated by jasmonate-responsive pathway. Front. Plant Sci. 2018, 9, 642. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  92. Li, C.; He, X.; Luo, X.; Xu, L.; Liu, L.; Min, L.; Jin, L.; Zhu, L.; Zhang, X. Cotton WRKY1 mediates the plant defense-to-development transition during infection of cotton by Verticillium dahliae by activating JASMONATE ZIM-DOMAIN1 expression. Plant Physiol. 2014, 166, 2179–2194. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  93. Hu, Q.; Zhu, L.; Zhang, X.; Guan, Q.; Xiao, S.; Min, L.; Zhang, X. GhCPK33 negatively regulates defense against Verticillium dahliae by phosphorylating GhOPR3. Plant Physiol. 2018, 178, 876–889. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  94. Wang, F.X.; Ma, Y.P.; Yang, C.L.; Zhao, P.M.; Yao, Y.; Jian, G.L.; Luo, Y.M.; Xia, G.X. Proteomic analysis of the sea-island cotton roots infected by wilt pathogen Verticillium dahliae. Proteomics 2011, 11, 4296–4309. [Google Scholar] [CrossRef]
  95. Pantelides, I.S.; Tjamos, S.E.; Paplomatas, E.J. Ethylene perception via ETR1 is required in Arabidopsis infection by Verticillium dahliae. Mol. Plant Pathol. 2010, 11, 191–202. [Google Scholar] [CrossRef]
  96. Liu, J.; Wang, Y.; Zhao, G.; Zhao, J.; Du, H.; He, X.; Zhang, H. A novel Gossypium barbadense ERF transcription factor, GbERFb, regulation host response and resistance to Verticillium dahliae in tobacco. Physiol. Mol. Biol. Plant. 2017, 23, 1–10. [Google Scholar] [CrossRef] [Green Version]
  97. Guo, W.; Jin, L.; Miao, Y.; He, X.; Hu, Q.; Guo, K.; Zhu, L.; Zhang, X. An ethylene response-related factor; GbERF1-like; from Gossypium barbadense improves resistance to Verticillium dahliae via activating lignin synthesis. Plant Mol. Biol. 2016, 91, 305–318. [Google Scholar] [CrossRef]
  98. Liu, Y.; Xin, L.; Lu, L.; Wang, W.; Quan, S.; Bo, L.; Wang, C.; Cheng, J.; Zhang, Y.; Xie, Y. GbABR1 is associated with Verticillium wilt resistance in cotton. Biologia. 2018, 73, 449–457. [Google Scholar] [CrossRef]
  99. Li, T.; Ma, X.; Li, N.; Zhou, L.; Liu, Z.; Han, H.; Gui, Y.; Bao, Y.; Chen, J.; Dai, X. Genome-wide association study discovered candidate genes of Verticillium wilt resistance in upland cotton (Gossypium hirsutum L). Plant Biotechnol. J. 2017, 15, 1520–1532. [Google Scholar] [CrossRef] [Green Version]
  100. Li, N.Y.; Ma, X.F.; Short, D.P.G.; Li, T.G.; Zhou, L.; Gui, Y.J.; Kong, Z.Q.; Zhang, D.D.; Zhang, W.Q.; Li, J.J.; et al. The island cotton NBS-LRR gene GbaNA1 confers resistance to the non-race 1 Verticillium dahliae isolate Vd991. Mol. Plant Pathol. 2018, 19, 1466–1479. [Google Scholar] [CrossRef] [Green Version]
  101. Li, N.Y.; Zhou, L.; Zhang, D.D.; Klosterman, S.J.; Li, T.G.; Gui, Y.J.; Kong, Z.Q.; Ma, X.F.; Short, D.P.G.; Zhang, W.Q.; et al. Heterologous expression of the cotton NBS-LRR gene GbaNA1 enhances Verticillium wilt resistance in Arabidopsis. Front. Plant Sci. 2018, 9, 119. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  102. Zhang, Y.; Wang, X.; Li, Y.; Wu, L.; Zhou, H.; Zhang, G.; Ma, Z. Ectopic expression of a novel Ser/Thr protein kinase from cotton (Gossypium barbadense), enhances resistance to Verticillium dahliae infection and oxidative stress in Arabidopsis. Plant Cell Rep. 2013, 32, 1703–1713. [Google Scholar] [CrossRef] [PubMed]
  103. Meng, J.; Gao, H.; Zhai, W.; Shi, J.; Zhang, M.; Zhang, W.; Jian, G.; Zhang, M.; Qi, F. Subtle regulation of cotton resistance to Verticillium wilt mediated by MAPKK family members. Plant Sci. 2018, 272, 235–242. [Google Scholar] [CrossRef] [PubMed]
  104. Gao, X.; Wheeler, T.; Li, Z.; Kenerley, C.M.; He, P.; Shan, L. Silencing GhNDR1 and GhMKK2 compromises cotton resistance to Verticillium wilt. Plant J. 2011, 66, 293–305. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Ijms 21 01120 g001 550
Figure 1. Regulation of intracellular signalling-related genes and signal transduction-related genes in response to Verticillium dahliae in plants. Plants have developed a sophisticated immune system to defend against V. dahliae. Plant cells immediately trigger signal transduction, leading to a rapid defence response including large-scale transcription reprogramming, while they recognise microbial-related molecular patterns or internal effectors from V. dahliae. Ijms 21 01120 i001, phosphorylation; CRY2, cryptochrome 2; ET, ethylene; GCC-box, ethylene-responsive element binding factor associated amphiphilic repression domain; GSH, phi-class glutathione; HDTF1: homeodomain transcription factor gene 1; JA, jasmonic acid; JAZ1, Jasmonate Zim-domain1; NBS-LRR, nucleotide-binding site leucine-rich repeat; PevD1, an elicitor from V. dahliae; SARD1, the Arabidopsis master immune regulator; SA: salicylic acid; Spd, spermidine; Spm, spermine; ROS, reactive oxygen species; SA, salicylic acid; VdSCP41, a secretory protein from V. dahliae [7,16,17,18,19,20,21,22]. Red lines represent negative regulation and green lines represent positive regulation.
Figure 1. Regulation of intracellular signalling-related genes and signal transduction-related genes in response to Verticillium dahliae in plants. Plants have developed a sophisticated immune system to defend against V. dahliae. Plant cells immediately trigger signal transduction, leading to a rapid defence response including large-scale transcription reprogramming, while they recognise microbial-related molecular patterns or internal effectors from V. dahliae. Ijms 21 01120 i001, phosphorylation; CRY2, cryptochrome 2; ET, ethylene; GCC-box, ethylene-responsive element binding factor associated amphiphilic repression domain; GSH, phi-class glutathione; HDTF1: homeodomain transcription factor gene 1; JA, jasmonic acid; JAZ1, Jasmonate Zim-domain1; NBS-LRR, nucleotide-binding site leucine-rich repeat; PevD1, an elicitor from V. dahliae; SARD1, the Arabidopsis master immune regulator; SA: salicylic acid; Spd, spermidine; Spm, spermine; ROS, reactive oxygen species; SA, salicylic acid; VdSCP41, a secretory protein from V. dahliae [7,16,17,18,19,20,21,22]. Red lines represent negative regulation and green lines represent positive regulation.
Ijms 21 01120 g001
Table
Table 1. Genes related to plant resistance to V. dahlia and their regulatory mechanisms.
Table 1. Genes related to plant resistance to V. dahlia and their regulatory mechanisms.
ClassificationProtein (Gene) NameAnnotationHostResistance MechanismReferences
Defence-related proteinsPGIPplant defence proteinCk, Ghinhibit fungal polygalacturonase activity[24]
NaD1plant defensinNaantifungal activity[26]
GbNRX1apoplastic thioredoxin proteinGbapoplastic immune response and scavenge ROS[27]
GbHyPRP1proline-rich proteinGbthickening cell walls and ROS accumulation[28]
AtNPR1non-expressor of Pr1Atupregulating expression of ICS1 and PR1a[30]
GhMLP28defence-related major latex proteinStenhance GhERF6 activity[32]
GbTLP1thaumatin-like proteinGbsecondary cell wall development[34]
BTD-Ssynthetic defensin derivativeSyntheticantifungal activity[35,36]
StoCYP77A2cytochrome P450Ntsynthesis of antimicrobial compounds[37]
EnzymesChi28class IV chitinase subfamilyGh, Gbdegrade the fungal cell wall[42]
GhPMEI3pectin methylesterasesGhdegrade the fungal cell wall[43]
GhLAC15laccaseGhlignification of the cell wall[45]
GbSBT1a subtilase geneGbactivating defence-related genes expressionn[46]
GhECRenoyl-CoA reductaseGhproduction of very long chain fatty acids[47]
GbANSanthocyanidin synthaseGbregulating biosynthesis of anthocyanins[48]
GhPUB17U-box E3 ubiquitin ligaseGhnegatively regulating immunity[49]
Receptor-like proteinsGhDIR1putative dirigent proteinGhlignification of the cell wall[38]
GhUMC1umecyanin-like proteinGh[39]
Lyp1, Lyk7,LysMe3lysin-motif receptor kinasesGbrecognize chitin, receptor-mediated endocytosis-like signals and leucine zipper, enhance the expression of the JA/ET signalling pathway-related genes, increase the expressions of defence-related genes[53]
Gh-LYK1,Gh-LYK2Gh[54]
Ve1 and Ve2cell-surface glycoproteinsSl[16,25]
GbSOBIR1defence-related receptor-like kinasesGb[85]
Gbvdr3, Gbvdr6
Gbve1, VvVe, StVe
StoVe1,SlVe1, GbRLK		Ve1 homologuesGb, Vv
St, Sl		[17,64,68,69,70,71,72,73,74]
miR482emiR482 superfamilySttarget disease-resistance proteins with NBS and LRR motifs[79]
Transcription factorsGhHB12HD-ZIP I transcription factorGhsuppressing JA-response genes[82]
GhMYB108plant MYB transcription factorsGhenhance defence signalling molecules[81]
CBP60g and SARD1plant-specific transcription factorsAtregulating SA signalling[83]
Signal transductionGaRPL18ribosomal protein L18Gamediate resistance by SA-signalling[86]
GaGSTF9phi-class glutathione S-transferaseGaregulating ROS via catalytic reduction of glutathione[87]
GhSAMDC,GhSPMSS-adenosylmethionine decarboxylaseGhregulating Spm biosynthesis by SA-signalling[88]
GhPAOpolyamine oxidaseGhregulating Spm and camalexin signalling[90]
GhCDKEcyclin-dependent kinaseGhenhance plant resistance by JA pathway[91]
HDTF1homeodomain transcription factorGhactivation of JA-mediated signalling[84]
GbWRKY1regulator mediatingGbactivating JAZ1 expression[92]
GbSSI2,GbCAD1regulating signal pathwaysGbactivating JA-mediated signalling[50]
GbaNA1NBS-LRR proteinGbregulating ROS and ET signalling pathway[100,101]
ETR1ET receptorAtactivation and increased accumulation of defence proteins[95]
GbERF1-likeET response-related factorGbpositive regulator in lignin synthesis[97]
Notes: At, Arabidopsis thaliana; Ck, Cynanchum komarovii; ET, ethylene; Ga, Gossypium arboreum; Gb, Gossypium barbadense; Gh, Gossypium hirsutum; ICS, isochorismate synthase; JA, jasmonic acid; LncRNAs, long noncoding RNAs; Na, Nicotiana alata; Nt, Nicotiana tabacum; Pr, pathogenesis-related protein; ROS, reactive oxygen species; SA, salicylic acid; Spm, spermine; Sl, Solanum lycopersicum; St, Solanum torvum; T, threonine; Vv, Vitis vinifera.

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Song, R.; Li, J.; Xie, C.; Jian, W.; Yang, X. An Overview of the Molecular Genetics of Plant Resistance to the Verticillium Wilt Pathogen Verticillium dahliae. Int. J. Mol. Sci. 2020, 21, 1120. https://doi.org/10.3390/ijms21031120

AMA Style

Song R, Li J, Xie C, Jian W, Yang X. An Overview of the Molecular Genetics of Plant Resistance to the Verticillium Wilt Pathogen Verticillium dahliae. International Journal of Molecular Sciences. 2020; 21(3):1120. https://doi.org/10.3390/ijms21031120

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Song, Ranran, Junpeng Li, Chenjian Xie, Wei Jian, and Xingyong Yang. 2020. "An Overview of the Molecular Genetics of Plant Resistance to the Verticillium Wilt Pathogen Verticillium dahliae" International Journal of Molecular Sciences 21, no. 3: 1120. https://doi.org/10.3390/ijms21031120

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