A comprehensive review on elucidating the host disease resistance mechanism from the perspective of the interaction between cotton and Verticillium dahliae

Abstract

Verticillium wilt, caused by the infamous pathogen Verticillium dahliae, presents a primary constraint on cotton cultivation worldwide. The complexity of disease resistance in cotton and the largely unexplored interaction dynamics between the cotton plant host and V. dahliae pathogen pose a crucial predicament for effectively managing cotton Verticillium wilt. Nevertheless, the most cost-effective approach to controlling this disease involves breeding and cultivating resistant cotton varieties, demanding a meticulous analysis of the mechanisms underlying cotton’s resistance to Verticillium wilt and the identification of pivotal genes. These aspects constitute focal points in disease-resistance breeding programs. In this review, we comprehensively discuss genetic inheritance associated with Verticillium wilt resistance in cotton, the advancements in molecular markers for disease resistance, the functional investigation of resistance genes in cotton, the analysis of pathogenicity genes in V. dahliae, as well as the intricate interplay between cotton and this fungus. Moreover, we delve into the future prospects of cutting-edge research on cotton Verticillium wilt, aiming to proffer valuable insights for the effective management of this devastating fungus.

Background

Cotton, a vital natural fiber material and cash crop, plays an indispensable role in the national economy in China (Zhang et al. 2022a). With the rise in labor costs and a growing need for mechanization in China, the cultivation practices of cotton have been optimized and adjusted. Xinjiang Uygur Autonomous Region has grown as the primary hub of cotton production in China. According to the announcement made by National Bureau of Statistics of China in 2023, Xinjiang accounts for an impressive 84.98% of the national total cotton planting area, with its yield contributing to an astounding 90.99%. In recent years, the incidence of cotton Verticillium wilt (CVW) in Xinjiang cotton fields has reached alarming levels, affecting an overwhelming 50%–70% of them, posing a significant hindrance to the green and healthy development of cotton in China (Liu et al. 2015a; Palanga et al. 2021). Similarly, CVW stands as a formidable threat to cotton production on a global scale, inflicting average yield losses of 15%–30% and surpassing 50% in severe instances (Zhu et al. 2017). Its notorious pathogenic fungus, Verticillium dahliae, is a soil-borne plant pathogen that infests the xylem tissue and instigates Verticillium wilt diseases across a spectrum of over 200 plant species worldwide (Zhang et al. 2022a). Under favorable temperature and humidity conditions, the V. dahliae spores germinate and give rise to hyphae that intricately entangle themselves around the delicate root tips of cotton plants and then form the hyphopodium at the infection site, which develops into penetration pegs piercing the root epidermis, leading to penetrating the gaps between the root epidermis layers (Zhao et al. 2016). In particular, penetration peg serves as a crucial tool for V. dahliae during host root penetration (Zhang et al. 2022b). The penetration peg subsequently matures into the hyphal neck, establishing a distinct fungal-host interface that elegantly facilitates the transmission and secretion of small secreted proteins in an efficient manner (Zhao et al. 2016; Zhou et al. 2017). Eventually, these structures elongate into the vascular tissues, causing obstruction of the vascular bundle and release of toxins that inflict harm upon host plant cells. Consequently, cotton leaves wither, turn yellow, and ultimately succumb to death (Klosterman et al. 2009) (Fig. 1).

Fig. 1

A concise schematic diagram illustrating the infection and reproduction cycles of V. dahliae in cotton

The infection cycle of V. dahliae primarily encompasses the germination of microsclerotia within the soil, the subsequent germination of hyphae that infiltrate the cotton plant from the root tip, the colonization of cotton’s vascular bundles, and the infection of the foliage, resulting in wilting and chlorosis, followed by the re-isolation of pathogenic fungus from affected leaves. The reproductive cycle of V. dahliae chiefly involves mycelial expansion, the formation of branched conidiophores, the production of conidia, and the subsequent enlargement and darkening of the mycelium, resulting in the development of microsclerotia.

Due to the lack of robust disease resistance genes in upland cotton (Gossypium hirsutum), understanding the intricate molecular mechanisms underlying cotton’s resistance to Verticillium wilt proves to be an arduous task (Chen et al. 2005; Shaban et al. 2018). Furthermore, the substantial variability exhibited by these pathogens and their co-evolution with plants have obscured the interaction mechanism between plants and pathogens, presenting a critical challenge to the effective prevention and control of this disease (Bai et al. 2022a; Yang et al. 2023). Cultivating and planting disease-resistant varieties have been proved as the most economically viable approach for preventing and managing CVW (Li et al. 2019). In particular, delving deeper into the mechanisms underlying cotton’s resistance to Verticillium wilt and unraveling key genes involved are pivotal aspects of disease-resistant breeding program. Furthermore, in-depth research on future prospects of cutting-edge studies on cotton Verticillium wilt can provide valuable insights for effective management of this destructive fungus disease.

Genetic inheritance of cotton resistance to Verticillium wilt

Owning to the dynamic and coevolutionary nature of V. dahliae in cotton, significant variations exist in resistance levels across different cotton varieties. Furthermore, the use of various disease grading indicators and statistical methods, along with variations in disease conditions and stages, has led to different research findings. This has resulted in a lack of consensus on this matter (Li et al. 2022). To date, the primary point of contention lies in whether cotton resistance is governed by a singular or major gene, or if it is controlled by multiple micro-genes (Zhao et al. 2021). Additionally, the debate also explores whether disease resistance exhibits dominance or recessiveness in terms of susceptibility (Zhang et al. 2013). Inoculating a single CVW strain under controlled greenhouse or growth chamber conditions minimizes environmental impact and predominantly support the conclusion that resistance to Verticillium wilt is primarily determined by a single gene. Conversely, under field disease conditions, where V. dahliae strains are more complex and greatly influenced by the environment, resistance to Verticillium wilt demonstrates polygenic inheritance (Ma et al. 2000). It appears evident that the resistance of island cotton (Gossypium barbadense) to Verticillium wilt is mainly determined by a single gene, while demonstrating genetic inheritance associated with quality traits (Zhang et al. 2017). However, for upland cotton, resistance inheritance is more intricate. Typically, conducted inoculations using a single strain of V. dahliae in greenhouses tend to result in qualitative trait inheritance (Ma et al. 2000). On the other hand, when identifying resistance within field disease nurseries, quantitative trait inheritance prevails with additive effects being predominant approach utilized (Wang et al. 2012). Based on the aforementioned research reports, it is believed that the inheritance of resistance in upland cotton is significantly influenced by factors such as parental material selection, pathogen type, variations in identification conditions, and standardized disease grading criteria.

Development of molecular markers for cotton Verticillium wilt resistance

In recent years, the advancement of molecular marker technology has greatly facilitated the exploration of the genetic basis and resistance breeding of cotton against Verticillium wilt. Currently, an assortment of molecular markers including simple sequence repeat (SSR), random amplification polymorphism DNA (RAPD), sequence-related amplified polymorphism (SRAP), and amplified fragment length polymorphism (AFLP) are extensively employed in constructing of cotton genetic linkage maps (Zhu et al. 2017; Yuan et al. 2018). The establishment of molecular marker-linked genetic maps serves as a cornerstone for gene localization, cloning, and genomic research. Currently, numerous genetic linkage maps have been developed employing molecular marker technology in the study of cotton (Jiang et al. 2009; Zhao et al. 2021). Researchers have utilized a combination of major gene + polygene inheritance model and multi-generation joint analysis to investigate the genetic characteristics of cotton Verticillium wilt leaves ratio. These findings reveal that disease resistance is governed by two pairs of additive-dominant-epistatic major genes, with the primary genetic effect relying on major effect genes in each segregating generation (Wang et al. 2008). Through quantitative trait locus (QTL) mapping analysis, distinct clusters of disease-resistant QTLs have been identified on chromosomes D7 and D9 (Jiang et al. 2009). In upland cotton, 15 QTLs for Fusarium wilt resistance and 13 QTLs for Verticillium wilt resistance have also been unveiled (Abdelraheem et al. 2020). Institute of Cotton Research of Chinese Academy of Agricultural Sciences has employed segregating populations and natural populations to screen multiple QTLs associated with Verticillium wilt resistance via QTL mapping and association analysis (Zhao et al. 2017). The selection effects of these QTLs can be reliably inherited across different generations. Notably, a predominant QTL cluster linked to Verticillium wilt resistance in cotton was primarily located on chromosome 16 (Zhao et al. 2014, 2021). Furthermore, genome wide association study (GWAS) has identified three loci associated with Verticillium wilt resistance in cotton. Particularly noteworthy, Gh_D06G0687, encoding an NB-ARC protein domain, exhibited a significant association with Verticillium wilt resistance (Fang et al. 2017a). Another GWAS result revealed that loci on chromosomes A02, A03, A05, A06, A08, A12, D05, D07, D10, D11, and D12 were found to be linked to Verticillium wilt resistance in cotton. Among them, chromosome D11 harbored the candidate gene cluster of receptor kinases containing L-type lectins (GhLecRKs-V.9), which was of particular interest (Zhang et al. 2021). Furthermore, a TIR-NBS-LRR protein was identified as a potential candidate target for disease resistance through GWAS analysis; genome-edited plants showed reduced resistance against V. dahliae (Li et al. 2017). To sequence the genomes of a population consisting of 299 upland cotton germplasm resources effectively and accurately assessing their association with disease index of Verticillium wilt, the specific locus amplified fragment sequencing (SLAF-seq) method was employed. Through the association analysis between approximately 85 000 SNPs and disease index of Verticillium wilt, 17 significantly associated loci were detected (Li et al. 2013).

Although numerous of QTLs associated with pivotal traits in upland cotton have been unveiled, the exploration of genomic interactions remains deficient (Li et al. 2014; Ma et al. 2018). The question of whether intricate epistatic relationships exist among QTLs responsible for disease resistance remains unresolved, and deciphering the functional implications of epistatic QTLs presents formidable challenges (Ma et al. 2018). Furthermore, solely QTLs with major effects have been discovered thus far, while minor effect QTLs largely remain enigmatic (Ma et al. 2021b; Zhao et al. 2023). Consequently, it becomes imperative to establish artificial populations, such as nested association mapping (NAM) and multiparent advanced generation inter-cross (MAGIC) populations, for uncovering minor effect loci and investigating cumulative effects between loci, thereby delving into exceptional disease-resistant genes.

Functional interpretation of resistance genes in cotton

Upon invasion by V. dahliae, cotton undergoes a cascade of physiological and biochemical changes that contribute to the development of resistance in tissue structure. These changes include the thickening of cell walls, accumulation of suberin and lignin, burst of reactive oxygen species (ROS), and increased production of plant antimicrobial compounds, which partially impede the invasion and spread of V. dahliae within cotton plants (Chen et al. 2021b; Zhang et al. 2022b, 2022c). However, the pathogen can overcome cotton’s physical defenses and cause infection (Liu et al. 2014; Ding et al. 2018). Cotton has evolved intricate mechanisms for disease resistance, primarily involving immune responses regulated by disease-resistant related proteins, extracellular enzymes, membrane receptor proteins, transcription factors, and signaling pathways (Jones et al. 2006; Song et al. 2020; Yang et al. 2020). In recent years, genomics, transcriptomics, and proteomics have provided valuable platforms for dissecting pivotal factors involved in regulating Verticillium wilt resistance in cotton as well as exploring candidate genes (Zhang et al. 2019a; Mo et al. 2021). These key disease-resistance genes are the main players against V. dahliae, and their roles are well-established (Table 1).

Table 1 Genes for Verticillium wilt resistance in cotton

To date, researchers employed V. dahliae to infect various resistant cotton varieties and observed significant disparities in the root phosphoproteome between resistant and susceptible cultivars, with involvement in multiple defense-related metabolic pathways such as lignin biosynthesis, reactive oxygen species generation, and signaling hormones regulation (Mo et al. 2015; Zhang et al. 2016b, 2019b). Subsequent analysis revealed that succinate dehydrogenase GhSDH1-1 and ribosomal protein RPS6 positively regulated cotton’s resistance to Verticillium wilt through the salicylic acid (SA) pathway (Zhu et al. 2021). Furthermore, GhWAKL was found to interact with DnaJ protein to activate SA biosynthesis, but mutationed at the Ser 628 site could disrupt this interaction, resulting in weakening cotton’s resistance (Feng et al. 2021). These findings provide potential molecular targets and pathways for controlling Verticillium wilt and inducing resistance in cotton. As a hemibiotrophic pathogen, V. dahliae exhibits biotrophic tendencies during the early stage of infection, transitioning into a necrotrophic lifestyle as the infection progresses. Thus, the SA signaling pathway was required to confer resistance against V. dahliae (Dhar et al. 2020). Numerous plant hormones orchestrate the formation of vascular bundle cell walls to combat pathogen invasion and spread. Among these hormones, ethylene (ET) participates in lignin and suberin biosynthesis, while abscisic acid (ABA) coordinated suberin deposition, jasmonic acid (JA) aided in lignin biosynthesis, with SA counteracting JA’s inducing effect on lignin production (Mo et al. 2016; Wang et al. 2020). Moreover, GhWRKY41 positively regulated the cotton resistance to V. dahliae by enhancing the accumulation of flavonoids (Xiao et al. 2023). Besides, the miR530-GhSAP6 module in cotton leaves responded remotely to V. dahliae infection from roots via systemic acquired resistance, and then enlarged SA signaling at locations farther from the injection sites, leading to enhanced resistance of cotton plants to V. dahliae (Hu et al. 2023). By analyzing the transcriptome of G. barbadense after inoculation with V. dahliae, genes involved in the “SA→NPR1→TGA→PR-1→disease resistance” signaling pathway were elucidated, leading to the discovery of numerous defense gene sequences against Verticillium wilt in cotton (Zhang et al. 2013). Through proteomics and virus-induced gene silencing (VIGS) technology, it was revealed that gossypol, brassinosteroids (BR), and JA play a pivotal role in cotton’s resistance to Verticillium wilt (Gao et al. 2013). Furthermore, GbERF1-like genes could induce upregulation of resistance-related genes, regulate lignin accumulation, and enhance cotton’s resistance to Verticillium wilt (Guo et al. 2016). Overexpression of the pathogenesis-related protein gene GbPR10.5D1 in cotton enhanced the resistance to V. dahliae, accompanied by the activation of genes involved in suberin biosynthesis (Guo et al. 2022). Moreover, the analysis of the diploid cotton A2 and D5 subgenomes, along with the tetraploid upland cotton A2D5 genome, has unveiled the crucial role of the cotton NBS-LRR gene family in Verticillium wilt resistance (Li et al. 2015). Most of the apoplastic proteins secreted by the root in cotton were involved in ROS metabolism and defense response. In a study conducted the silencing and overexpression of the GbNRX1 gene demonstrated its regulator role in maintaining ROS balance and enhancing cotton’s resistance to this disease (Li et al. 2016). Through the utilization of VIGS and transgenic Arabidopsis, Gong et al. (2017) revealed that the pivotal role of ribosomal protein GaRPL18 in regulating cotton’s resistance to Verticillium wilt through the SA signaling pathway, thereby bolstering its disease resistance; the carotenoid cleavage dioxygenases GbCCD7 and GbCCD8b positively regulated the accumulation of strigolactone, and consequently activated the JA and ABA signaling. This interplay establishes a positive feedback loop involving ABA and a negative feedback loop associated with JA, which collaboratively regulate the homeostasis of strigolactone. Such intricate hormonal balance enhances the resilience of cotton against V. dahliae (Yi et al. 2023). Additionally, several genes with negative regulatory effects on plant resistance to Verticillium wilt have been identified. For instance, Song et al. (2021) discovered that GhBIN2 interacted with JAZ proteins to exert a negative regulation on plant resistance. Furthermore, a series of transcription factors including HDTF1, GhHB12, and GhBLH7-D06 were found to exhibit negative regulatory effects as well (Gao et al. 2016; He et al. 2018; Ma et al. 2020). A recent study revealed that GhnsLTPsA10 coordinated plant resistance against this fungus and pests by redirecting the metabolic flux in flavonoid biosynthesis and lignin biosynthesis pathways through the regulation of phenylpropane metabolism (Chen et al. 2021a). This elucidation of functional genes related to resistance serves as the foundation for comprehending the molecular mechanisms underlying cotton resistance and provides an array of high-quality candidate genes for transgenic disease-resistant breeding programs.

Functional annotation of pathogenic genes in V. dahliae

The molecular pathogenic mechanism of V. dahliae is highly intricate and meticulously connected to a myriad of genes associated with pathogenicity (Cai et al. 2018; Bui et al. 2019). Recently, scholars have extensively investigated the pathogenic-related genes of V. dahliae from various perspectives such as genomics, transcriptomics, proteomics, and T-DNA mutant libraries, yielding substantial advancements (Liu et al. 2015b; Qi et al. 2015; Rehman et al. 2016; Wu et al. 2019). Functional analysis of pivotal genes implicated in fungal growth and pathogenicity provides the molecular genetic foundation for comprehending the pathogenic mechanism of V. dahliae (Li et al. 2015; Zhang et al. 2016b). Although genes related to growth and development are not inevitably entwined with pathogenicity, those associated with pathogenicity exhibit some degree of correlation with nutritional growth (Luo et al. 2014; Zhang et al. 2015). The remarkable ability of this fungus to finely adapt to the oligotrophic conditions within vascular bundles has captivated the scientific community (Fang et al. 2017b, 2019; Lv et al. 2022). Comparative genomics investigations have uncovered that unlike other non-vascular bundle pathogenic fungi, the genome of V. dahliae has undergone intricate modifications to evolve a sophisticated network for degrading plant cell walls, encoding a staggering total of 504 carbohydrate-degrading enzymes. Among these, the members of the pectinase family (including PL1, PL3, and PL9 families) have experienced substantial expansion compared with other plant pathogenic fungi. This expansion directly correlated with the functional prerequisites for degrading host cells rich in pectin during the infection and colonization processes, facilitating entry into vascular bundles and reproduction within them (Klimes et al. 2008, 2015; Chen et al. 2016). Consequently, the expansion of gene family encoding cell wall degradation enzymes and their extracellular secretion by V. dahliae represent a significant adaptive strategy for thriving in the oligotrophic environment of vascular bundles (Eynck et al. 2007; El Hadrami et al. 2015). This capacity is further underscored through the involvement of numerous cell wall-degrading enzymes in the infection and colonization processes of V. dahliae, thereby exerting a profound influence on the pathogenicity of this pathogen. For instance, VdSSP1, a glycoside hydrolase, contributed to the pathogenicity of V. dahliae by breaking down plant cell wall components (Liu et al. 2013); VdEg-1 cellulase played a critical role in early colonization of host wood (Maruthachalam et al. 2011); GH12 (glycoside hydrolase) family proteins such as VdEG1 and VdEG3 acted as pathogenic factors in cotton by actively participating in cellulose degradation (Gui et al. 2017); and the xylanase member VdXyn4 has been definitively implicated in the breakdown of xylan, pectin, and cellulose while instigating collapse of vascular bundle tissue (Cheng et al. 2017; Wang et al. 2021a). Furthermore, multiple signaling factors involved in the regulating cell wall-degrading enzymes also partake in the degradation and utilization of plant cell wall components by V. dahliae during infection and colonization processes within vascular bundles. These factors encompass the sucrose non-fermenting protein kinase VdSNF1, transcription factor VdFTF1, and the target of rapamycin protein VdTOR (Tzima et al. 2011; Zhang et al. 2018; Li et al. 2019). The absorption and utilization of nitrogen sources by V. dahliae in the oligotrophic environment of vascular bundles played a pivotal role in its infection and colonization processes. Transcriptome analysis has unveiled distinct regulatory mechanisms employed by V. dahliae to discriminate between nitrogen and nitrate utilization, with transcription factors such as the MADS-box transcription factor VdMcm1 and the basic leucine zipper (bZIP) transcription factor VdHapX intricately involved in this intricate process (Xiong et al. 2016; Wang et al. 2018). Furthermore, another bZIP transcription factor VdAtf1 has been discovered to be implicated in response to active nitrogen and regulation of metabolic equilibrium of nitrate and ammonium within V. dahliae (Tang et al. 2020). Additionally, V. dahliae commonly activates its own pathway for amino acid synthesis in response to the environmental stress caused by nitrogen source deficiency within vascular conduits. This functional mechanism has been validated in the closely related species Verticillium longisporum, wherein the transcription factor VlCPC1 played a role in amino acid synthesis, removal of which substantially impeded growth under an amino acid-depleted environment (Timpner et al. 2013). Similarly, these functional genes contribute to vital biological processes that facilitate V. dahliae’s adaptation to the nutritionally impoverished milieu within vascular conduits, thereby dictating its colonization and proliferation capabilities within such conduit systems. Consequently, the deletion of those genes led to a marked decrease in the pathogenicity of V. dahliae, which was evidenced by varying degrees of pathogenic loss (Zhang et al. 2022a; Wen et al. 2023).

In summary, V. dahliae employs a series of signal perception and transduction events to generate specialized structures, such as hyphopodia and infection pegs, facilitating its infiltration into the host and subsequent exploration of vascular bundles (Tran et al. 2014; Zhao et al. 2016; Harting et al. 2020). Simultaneously, it secretes an abundant array of effector proteins and enzymes that degrade the cell wall, thereby carrying out its pathogenic functions (Qi et al. 2016; Qin et al. 2020). Moreover, it engages diverse strategies to adapt to environmental adversity and nutritional scarcities within vascular bundles, thus promoting its growth and propagation (Xiong et al. 2015; Bui et al. 2019; Yang et al. 2020). Collectively, these functional genes constitute the molecular basis for the successful establishment and acclimatization of V. dahliae within vascular bundles (Table 2).

Table 2 Genes related to pathogenicity in V. dahliae

The interplay between cotton and V. dahliae

Jones et al. (2006) proposed the ‘zigzag’ model, which presents a systematic interpretation of the dynamic balance between plants and pathogens in the ongoing arms race involving disease resistance and pathogenesis. Plants defend against pathogen invasion by recognizing pathogen-associated molecular patterns (PAMPs) via receptor proteins, thereby triggering PAMPs-triggered immunity (PTI) (Zhou et al. 2017; Gao et al. 2019). Furthermore, plants engaged more intricate immune responses, known as effector-triggered immunity (ETI), by specifically identifying effector proteins secreted by pathogenic fungi using NBS-LRR class proteins (Yang et al. 2010; Leach et al. 2017; Hua et al. 2018). In order to elude or suppress immune responses, pathogens have undergone evolutionary adaptations resulting in a diverse array of effector proteins to successfully infiltrate plants (Gao et al. 2020; Zhu et al. 2023).

Fortunately, cotton has gradually developed its own innate defense system through the protracted coexistence, competition, and coevolution with the fungi pathogen (Yang et al. 2017). The intricate molecular mechanism underlying cotton’s resistance to Verticillium wilt is not solely reliant on the functionality of cotton disease resistance genes, but also hinges on the interplay between plant and pathogen (Huang et al. 2021; Zhang et al. 2022a) (Fig. 2). Plant ubiquitin ligases PUBs (PUB25 and PUB26) exerted a negative regulatory control over plant disease resistance. These PUBs not only interacted with VDAL (Asp f 2-like protein) in V. dahliae, but also engaged with the plant transcription factor MYB6. As an effector protein, VDAL competed with PUBs to shield MYB6 from ubiquitination degradation, thereby accumulating MYB6 to orchestrate plant resistance against V. dahliae effectively (Ma et al. 2021a). Plant calcium-binding protein CBP60g possessed a calcium-binding domain and positively modulated plant resistance to Verticillium wilt while relinquishing its transcriptional activity upon interaction with VdSCP41 protein secreted by V. dahliae. Arabidopsis mutants lacking CBP60g displayed diminished resistance to this pathogen (Qin et al. 2018). The secreted endopolygalacturonase VdEPG1 positively governed the pathogen’s virulence by intricately modulating its growth and development, and effectively suppressed the host immune response elicited by NLP1/INF1. During V. dahliae infection process in host, GhOPR9, a plant oxophytodienoate reductase involved in the JA synthesis pathway, interfaced with VdEPG1 on the cell membrane to induce a robust plant immune response that hindered V. dahliae infection (Liu et al. 2020, 2023; Chang et al. 2023). The recent study has divulged that GhCML41 through phosphoproteomics analysis, which is a calcium-like protein, positively regulated plant resistance against Verticillium wilt; suppression of the GhCML41 gene led to diminished lignin synthesis, reduced suberin deposition, lower SA content in cotton leaves, but elevated JA content; the introduction of GhCML41 into Arabidopsis augmented resistance against V. dahliae (Zhao 2019). Additionally, the interaction between V. dahliae VdM35-1, VdASPF2, and cotton GhCML41 through the Yeast two-hybrid system and further analysis revealed that the two genes belong to the metalloproteases M35 family of pathogenic fungi; VdM35-1 and VdASPF2 have been identified as secreted proteins of V. dahliae; deletion of those genes resulted in diminished spore production, stunted hyphal branch growth, abnormal spores, and impaired carbon source utilization, significantly attenuating the pathogenicity of this pathogen to host cotton (Lv et al. 2022). Moreover, glutathione-s-transferse (GST) pull-down and luciferase complementation imaging (LCI) technologies have confirmed the interaction between GhCML41 and the V. dahliae metalloproteases VdM35-1 and VdASPF2. These investigations provide novel insights into the mechanisms underpinning plant disease resistance while fortifying our theoretical understanding of molecular interactions between plants and pathogens.

Fig. 2

Strategy diagram of cotton and V. dahliae in the arms race between host and pathogen. The diagram presents the ancient Chinese symbol of Taiji, indicating that the attack of V. dahliae and the defense of cotton are systematic and complex, with a synergistic evolutionary relationship. V. dahliae has evolved a sophisticated pathogenicity mechanism to infect cotton, a cascade of reaction involving microsclerotia development, effector proteins, transcription factors, etc.; on the contrary, cotton has taken a series of defensive measures, including plant basic resistance, PTI/ETI, hormone signaling, etc.

Problem and prospect

Cotton, as a tetraploid crop, possesses an intricate genome structure and gene regulatory network (Wang et al. 2021b). With advancements in the field of life sciences, molecular biology, and technologies in cell biology such as in situ Hi-C, chromatin conformation capture sequencing, and three-dimensional genome features, a wealth of functional information is now available for a molecular-based disease-resistant breeding program (Pei et al. 2022). Therefore, elucidating the functional roles of non-coding genomic sequences, such as cis-regulatory elements, enhancers, and transcribed RNA elements, alongside protein-coding genes, will furnish crucial resources for the development of genomic-assisted breeding programs.

Verticillium wilt, an archetypal soil-borne vascular systemic disease, poses a formidable challenge in terms of field control. Breeding resistant varieties stands out as the most economically viable countermeasure against this disease (Bai et al. 2022b). Significant progress has been made in molecular markers, signal transduction pathways, tissue structural resistance, and transgenic breeding for improving cotton Verticillium wilt resistance (Parkhi et al. 2010). Nevertheless, progress in breeding disease-resistant cotton varieties has been slow due to the lack of highly resistant upland cotton germplasm, unclear genetic basis and resistance mechanism, and their linkage with undesirable agronomic traits. As a result, the majority of developed varieties display weak disease resistance (Zhang et al. 2016a). Moreover, the resistance of certain tolerant varieties rapidly wanes after introduction into production due to frequent pathogen variation (Ma et al. 2000). Molecular designed breeding is expected to emerge as the pivotal avenue for future cotton breeding endeavors. The ongoing completion of the diploid A2 and D5 subgenomes of cotton, as well as sketches of the tetraploid upland cotton A2D5 genome, is expected to expedite the selection process for high-quality disease-resistant varieties (Li et al. 2015).

Furthermore, a synergistic coevolution between plants and pathogens exists in nature. Consequently, the elucidation of plant defense mechanisms depends not only on the acquiring of plant resistance genes and deciphering of signaling pathways but also on the understanding pathogen virulence and variation mechanisms (Yang et al. 2020; Zhu et al. 2023). Therefore, studying the interaction between cotton and V. dahliae is of paramount importance. Timely communication between these two aspects is essential to unravel the mechanisms behind cotton’s resistance to Verticillium wilt and to achieve sustainable, effective control over its incidence in cotton production.