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2023 Volume 3
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REVIEW   Open Access    

Advancements in unraveling and enhancing bacterial wilt resistance in Solanaceous crops

  • # These authors contributed equally: Juan Du, Bingsen Wang

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  • Ralstonia solanacearum significantly threatens Solanaceous crops, necessitating efficient genetic control strategies. With advancements in genomics, untapped resources for disease resistance are expected to be identified soon. Intensified research in remote hybridization and somatic cell fusion is crucial to enhance resistance to bacterial wilt. The application of effectors could enable high-throughput methodologies for bacterial wilt resistance identification and promote screening in wild species. For difficult-to-identify receptors, resistant varieties could be developed by incorporating resistance genes from Arabidopsis thaliana and other Solanaceous plants. The use of genome-editing techniques and the completion of whole-genome sequencing for key Solanaceous crops should expedite resistance gene cloning. Methods such as Resistance gene enrichment sequencing (RenSeq) could expedite receptor identification, promising a future where R. solanacearum-resistant crop development is within reach.
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  • Supplemental Table S1 General genome information of 325 Ralstonia solanacearum strains in the NCBI database.
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  • Cite this article

    Du J, Wang B, Huang M, Chen X, Nie L, et al. 2023. Advancements in unraveling and enhancing bacterial wilt resistance in Solanaceous crops. Vegetable Research 3:29 doi: 10.48130/VR-2023-0029
    Du J, Wang B, Huang M, Chen X, Nie L, et al. 2023. Advancements in unraveling and enhancing bacterial wilt resistance in Solanaceous crops. Vegetable Research 3:29 doi: 10.48130/VR-2023-0029

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Advancements in unraveling and enhancing bacterial wilt resistance in Solanaceous crops

Vegetable Research  3 Article number: 29  (2023)  |  Cite this article

Abstract: Ralstonia solanacearum significantly threatens Solanaceous crops, necessitating efficient genetic control strategies. With advancements in genomics, untapped resources for disease resistance are expected to be identified soon. Intensified research in remote hybridization and somatic cell fusion is crucial to enhance resistance to bacterial wilt. The application of effectors could enable high-throughput methodologies for bacterial wilt resistance identification and promote screening in wild species. For difficult-to-identify receptors, resistant varieties could be developed by incorporating resistance genes from Arabidopsis thaliana and other Solanaceous plants. The use of genome-editing techniques and the completion of whole-genome sequencing for key Solanaceous crops should expedite resistance gene cloning. Methods such as Resistance gene enrichment sequencing (RenSeq) could expedite receptor identification, promising a future where R. solanacearum-resistant crop development is within reach.

    • Ralstonia solanacearum, a soil-borne pathogen, is responsible for bacterial wilt (BW) disease affecting 200 plant species in over 50 families, including crucial Solanaceous crops like potato, tomato, pepper, eggplant, and tobacco, as well as model plants, such as Arabidopsis thaliana and Medicago truncatula[1]. As such, it is ranked as the world's second most impactful plant pathogenic bacteria in terms of scientific and economic significance[1]. After infecting the host, R. solanacearum enters the plant's vascular system, resulting in wilting and, ultimately, death, thus preparing it for the next transmission cycle[1]. Water is a vital condition for its survival, particularly in agricultural irrigation environments[2]. Remarkably, under sterile water conditions in labs, R. solanacearum can survive without a decrease in pathogenicity for over four years[2], indicating its robust survival capabilities and partly explaining its global dissemination.

      The extensive genetic diversity within R. solanacearum, stemming from factors such as geographical distribution, host range, and pathogenicity, led to the application of the term 'species complex' for this organism. This 'R. solanacearum species complex' (RSSC) consists of four phylotypes, each predominantly originating from different global regions[3]. Phylotype I largely originates from Asia, phylotype II from America, phylotype III from Africa and surrounding islands in the Indian Ocean, and phylotype IV from Indonesia, Japan, and Australia[3]. Recent studies have redefined these phylotypes into separate species, including R. solanacearum (phylotype II), R. pseudosolanacearum (phylotypes I and III), and an array of R. syzygii (phylotype IV)[4,5]. Furthermore, a new sub-clade, referred to as phylotype IIC, has been identified within phylotype II[6]. The phylotypes of RSSC are not related to the host preference, reflecting the genetic diversity and difficulty of prevention and control of bacterial wilt[7].

      The advent of high-throughput sequencing technology has accelerated our understanding of R. solanacearum's genetics. The first complete genome sequence of this pathogen was published in 2002[8]. Currently, the NCBI database archives a total of 325 R. solanacearum genomes, although the hosts for 58 of these strains remain unidentified (Supplemental Table S1). Significantly, the predominant hosts among the identified strains are Solanum lycopersicum (tomato), Solanum tuberosum (potato), and Capsicum annuum (pepper) (Supplemental Table S1). These plants have given rise to 70, 69, and 23 strains respectively, indicating their key role as hosts for R. solanacearum. This substantial genomic repository has streamlined the process of identifying genes related to pathogenicity and comprehending their pathogenic mechanisms. This wealth of information forms an essential foundation for the development of disease-resistant Solanaceous varieties.

    • Various Solanaceous crops and their closely related species present a diverse set of plant accessions with varied degrees of disease resistance against R. solanacearum strains. For example, accessions of tomato (S. lycopersicum Hawaii 7996, TML46, CLN1463 and R3034), eggplant (Solanum melongena Ceylan SM 164, SM6, Surya, and AG91-25), pepper (C. annuum CA8 and MC4), potato (S. chacoense and S. sparsipilum), and tobacco (Nicotiana tabacum, N. benthamiana, and N. glutinosa) are resistant to BW[911]. The utilization of somatic hybridization has significantly enhanced BW resistance, especially in eggplant and potato cultivars (Table 1). Resistant somatic hybrids, generated through the fusion of different Solanum species, exhibit improved BW resistance, showcasing somatic hybridization's potential in enhancing resistance traits.

      Table 1.  Production of somatic hybrids through protoplast fusion for bacterial wilt resistance in Solanaceous crops.

      CropParentsReference
      EggplantS. melongena × S. aethiopicum[12]
      S. melongena × S. aethiopicum[13]
      S. integrifolium × S. violaceum[14]
      S. melongena × S. torvum[15]
      S. integrifolium × S. sanitwongsei[16]
      PotatoS. tuberosum × S. commersonii[18]
      S. tuberosum × S. phureja[22]
      S. tuberosum × S. commersonnii[19]
      S. tuberosum × S. stenotomum[23]
      S. tuberosum × S. chacoense[24]
      Eggplant to potatoS. melongena × S. tuberosum[26]

      Resistant somatic hybrids in eggplants were successfully created via electrical fusion between S. melongena and S. aethiopicum[12]. Furthermore, their hybrids exhibited enhanced resistance to BW and displayed superior fertility compared to conventional eggplant varieties[13]. In another notable development, a somatic hybrid line (27-14) was produced through protoplast fusion involving Solanum integrifolium, a commonly used rootstock in eggplant cultivation, and Solanum violaceum, a wild species exhibiting BW tolerance. This hybrid exhibited increased resistance to BW[14]. Similarly, hybrids derived from S. melongena and Solanum torvum demonstrated commendable resistance to BW[15]. In an innovative approach, hybrids originating from UV-irradiated cotyledonary protoplasts of S. integrifolium and iodoacetamide-treated protoplasts of S. sanitwongsei were not only vigorous and capable of bearing viable seeds but also exhibited a morphology intermediate to the parent species. This suggests their potential as eggplant rootstock candidates[16].

      In the pursuit of enhancing BW resistance in potatoes, breeders have identified and integrated resistance traits from various tuber-bearing Solanums into breeding programs. Despite the endosperm balance number incompatibility system restricting a direct cross between S. commersonii and S. tuberosum[17], innovative approaches such as somatic hybridization have enabled successful circumvention of this barrier. For instance, somatic hybrids between S. tuberosum and S. commersonii have overcome sexual incompatibilities, yielding disease-resistant lines compatible with S. tuberosum[18]. Moreover, resistant lines from their hybrids have been successfully bred with S. tuberosum varieties for amplified BW resistance[19]. Subsequent studies have undertaken an in-depth analysis of the behavior of S. commersonii chromosomes and the colonization patterns of R. solanacearum in the introgression lines[20,21]. In a similar vein, resistance traits from other Solanum species have been introduced into S. tuberosum through somatic hybridization. Notably, dihaploid potato and Solanum phureja hybrids have demonstrated increased BW resistance[22]. Remarkably, S. tuberosum and S. stenotomum hybrids have retained their parent's resistance level even after five years of in vitro maintenance[23]. Further, somatic hybrids originating from the protoplast fusion between S. tuberosum and S. chacoense exhibited enhanced BW resistance, marked by the presence of three specific S. chacoense simple sequence repeat (SSR) alleles linked to resistance[24,25]. An impressive achievement was the successful transfer of BW resistance from S. melongena cv. 508.3 to potato AC142-01 via interspecific symmetric protoplast fusion, resulting in resistant somatic hybrids dominant in potato parent nuclear genomes[26]. In the same lab, researchers also carried out asymmetric protoplast fusion and fused UV-treated protoplasts of the same resistant eggplant variety 508.3 with protoplasts of another susceptible potato variety to obtain 32 somatic hybrids, revealing the introgression of alien chromosome fragments and suggesting potential markers, emk03O04, emi04P17, and emd13E02a, associated with bacterial wilt resistance[27]. Later, researchers in the same lab successfully identified a gene, smPGH1, and seven BW-linked SSRs in somatic hybrids of potato and eggplant, providing valuable genetic resources for improving bacterial wilt resistance in cultivated potato through genome composition and transcriptome analysis[28].

      In conclusion, developing additional resistant germplasm is essential to meet the co-evolutionary challenges posed by the pathogen and the diverse demands for improved agronomic traits. Broadening the scope of BW resistance through hybrid creation between resistant and susceptible varieties offers a promising approach to safeguard Solanaceous crops. Furthermore, ploidy manipulation through sexual hybridization could present viable alternatives to surpass sexual barriers, as exemplified by S. commersonii. By doubling its chromosome number, a 4x line of S. commersonii was crossed with 2x genotypes, generating triploid progeny. These triploids, producing 2n eggs, were crossed with S. tuberosum in 3x × 4x configurations, yielding offspring with a near-pentaploid chromosome number[29]. Significantly, seven out of 26 near-pentaploid sexual hybrids between S. commersonii and cultivated S. tuberosum displayed S. commersonii-like resistance to BW, with notable inhibition of bacterial growth in the plant's aerial part[30]. Subsequent research efforts by various groups have also accomplished the successful transfer of resistance from S. commersonii to S. tuberosum[31,32]. The ongoing advancement of such resistant germplasm is indispensable for effectively combating the evolving challenges from pathogens and meeting the diverse demands for improved agronomic traits.

    • Plants employ sophisticated systems, including pattern-recognition receptors (PRRs) and nucleotide-binding leucine-rich repeat domains (NLRs), to perceive and defend against diverse microbial molecules. Positioned on the plasma membrane, PRRs operate as extracellular receptors that discern pathogen-associated molecular patterns (PAMPs). Conversely, NLRs, which reside within the cell, act as intracellular receptors to sense proteins that pathogens directly inject into plant cells[33]. These mechanisms, broadly considered as invasion patterns, initiate a sequence of immune responses, strengthening the plant's defenses[34].

      In A. thaliana, various PRRs involved in bacterial recognition have been identified, including FLS2, EFR, XPS1, RLP1, RLP32, LYM1/3, and LORE[33]. However, recognition of the elongation factor Tu (EF-Tu) by the Receptor-Like Kinase (RLK) EFR is limited to the Brassicaceae family[35,36]. Intriguingly, Solanaceous plants, lacking EFR, are incapable of recognizing EF-Tu from R. solanacearum. Yet, transgenic introduction of Arabidopsis EFR in tomato and potato enhances disease resistance to R. solanacearum infection, demonstrating that interfamily transfer of PRRs can extend recognition of bacterial PAMPs, potentially providing durable disease resistance[31,35,3739]. Moreover, the recent discovery of an R. solanacearum csp22 peptide (csp22Rsol) has been found to initiate immune responses in N. benthamiana and tomato, but not in A. thaliana[40]. Remarkably, csp22Rsol treatment boosted resistance to BW in tomato. Even more, transgenic A. thaliana plants expressing the tomato csp22 receptor (SlCORE) acquired the ability to respond to csp22Rsol and developed greater resistance to R. solanacearum infection[40].

      The main virulence determinant of RSSC bacteria is the type III secretion system (T3SS), a 'molecular syringe' that allows the translocation of several type III effector proteins (T3Es) directly into the host cell[41]. Termed Ralstonia Injected Proteins (Rips), these T3Es can be detected by Nucleotide-binding Leucine-rich Repeat proteins (NLRs) as avirulence effectors, thereby triggering resistance to BW. In A. thaliana, extensive molecular studies have identified the major resistance gene RRS1, encoding a Toll/Interleukin-1 Receptor-Nucleotide Binding Site-Leucine-Rich Repeat (TIR-NBS-LRR) resistance protein that interacts directly with the avirulence effector PopP2[4244]. In addition, RRS1 requires the RD19 gene-encoded Cys protease to mediate resistance to the phylotype I strain GMI1000[45]. Moreover, the RRS1 gene collaborates with the RPS4 gene to enhance resistance to strains of both Pseudomonas and RSSC carrying AvrRps4 and PopP2 effectors, respectively[46,47].

      Within Solanaceous crops, the identification of intracellular receptors remains relatively limited. The major gene ERs1 has been discovered in eggplant via a map-based cloning method[48]. Utilizing a candidate gene approach, RE-bw, an intracellular receptor encompassing both NB-ACR and WRKY domains, was located within eggplant and proven to confer resistance against BW[49]. Using a multiplexed NbNLR-VIGS library, the RRS-Y (RESISTANCE TO RALSTONIA SOLANACEARUM RIPY) was identified in N. benthamiana[50]. Further, specific Rips have been detected as avirulence factors in Solanaceous plants, which can be recognized by known NLR proteins against other pathogens. As an example, RipB, a homolog of Xanthomonas XopQ, is recognized by the N. benthamiana NLR protein Roq1, signifying it as an avirulence factor in N. benthamiana[51]. Both RipE1 and RipBN can be recognized by Ptr1, thereby conferring resistance to BW in N. benthamiana and S. lycopersicoides, respectively[5254]. Additional effectors, including RipA5, RipH2, RipP1, RipP2, RipX, RipAA, RipAT, RipAV, RipAX2, and RipBI, have been observed to trigger cell death in Solanaceous plants[55]. Moreover, a comparative genomic analysis of R. solanacearum strains HA4-1 and HZAU091 led to the identification of four candidate avirulence effectors in HA4-1 that trigger immunity in wild potatoes[56,57]. As research advances, the discovery of further intracellular receptors can be optimistically anticipated.

    • As a model pathogen for root and vascular diseases, R. solanacearum contains a great quantity of functionally characterized T3Es. The T3Es have evolved sufficiently to adapt to the plant immune system over a long period of natural evolution, making them indispensable molecular probes in plant immunity studies. A pan-effectome of 140 R. solanacearum strains has been created, comprising 102 known T3Es and 16 putative ones[58]. Recently, the novel T3E RS_T3E_Hyp9 was identified and renamed as RipBT, shown to promote R. solanacearum infection in potatoes[59]. Roughly half of these effectors have been characterized to varying degrees, with nine having identified host targets (Table 2[58]). For instance, RipAB targets TGA transcription factors to disrupt SA signaling and suppress plant immunity[60]. RipAC inhibits MAPK-mediated SGT1 phosphorylation and targets the plant E3 ubiquitin ligase PUB4 to repress immunity[61,62]. RipAC also targets a quantitative susceptibility factor BWS1 to regulate the SGT1-dependent immune response[63]. RipAK can inhibit host catalases and the oligomerization and enzymatic activity of pyruvate decarboxylases to promote disease[64,65]. RipAS diminishes the nucleolar accumulation of StTOPP6, contributing to virulence in potato[66]. RipAY degrades glutathione, inhibits the RipE1-triggered immune responses, and thus suppresses the immune response[6769]. RipD targets VAMP721/722 to promote disease[50]. RipI is a multifunctional effector that modulates plant metabolism and immunity. RipI enhances gamma-aminobutyric acid (GABA) accumulation by promoting calmodulin binding to glutamate decarboxylases (GADs), which contribute to virulence in tomato and Arabidopsis[70]. However, RipI also interacts with the transcription factor bHLH93, triggering a defense response in N. benthamiana[71]. RipTAL targets a 17-bp sequence upstream of arginine decarboxylase (ADC) genes, inhibiting the growth of R. solanacearum niche competitors in tomato[72,73]. Lastly, RipX suppresses the expression of mitochondrial atpA, inducing a defense response in N. benthamiana[74]. These identified host targets represent a wealth of genetic resources for breeding resistance to BW.

      Table 2.  Rips with identified host targets in Solanaceous crops.

      RipsAnonationTarget genesTarget plantsReferences
      RipAB(PopB), harboring proteinTGA transcription factorsSolanum tuberosum; Solanum lycopersicum; Arabidopsis thaliana.[60]
      RipAC(PopC), LRR domainSGT1; PUB4; BWS1Arabidopsis thaliana; Solanum lycopersicum; Nicotiana benthamiana[6163]
      RipAKCATs; PDCsNicotiana tabacum; Arabidopsis thaliana; Solanum lycopersicum.[64,65]
      RipASTOPP6Solanum tuberosum[66]
      RipAYTRX-hArabidopsis thaliana; Nicotiana benthamiana.[6769]
      RipBInosine-uridine nucleoside
      N-ribohydrolase
      Roq1Nicotiana benthamiana
      RipBNcysteine protease, AvrRPt2 familyPtr1Solanum lycopersicoides[52,53]
      RipDVAMP721/722Arabidopsis thaliana[66]
      RipE1Ptr1Nicotiana benthamiana[54]
      RipIbHLH93 transcription factor; plant calmodulin and GADsSolanum lycopersicum; Arabidopsis thaliana[70,71]
      RipP2AcetyltransferasebHLH94 transcription factorArabidopsis thaliana[44]
      RipTALTranscription Activator-Like proteinbHLH95 transcription factorSolanum lycopersicoides[72,73]
      RipX(PopA), HarpinbHLH96 transcription factorNicotiana benthamiana[74]
      RipYAnkyrin RepeatsbHLH97 transcription factorNicotiana benthamiana[50]
    • Assisting in resistance breeding to R. solanacearum, marker-assisted selection (MAS) significantly improves breeding efficiency for oligogenic or polygenic resistance within Solanaceous crops. Notably, the Solanaceae family's genetic diversity offers multiple sources of BW resistance, extensively studied in tomatoes (Table 3). A case in point is the Hawaii 7996 tomato cultivar, which has demonstrated exceptional resistance against BW, achieving an impressive 97% survival rate across 12 field trials conducted in 11 countries spanning Asia, America, Australia, and the Indian Ocean region[75]. This resilience makes Hawaii 7996 a stable source of resistance and an ideal resistant parent for the creation of the interspecific population Hawaii7996 × Wva700, designed for resistance mapping studies. Pioneering research discovered a genetic locus on chromosome 12 exhibiting robust resistance against a certain R. solanacearum strain, which alongside another locus on chromosome 6, contributed significantly to the control of resistance[76]. The marker TG564 on chromosome 12 emerged as the primary association with resistance, accounting for a substantial proportion of the genetic variation[76]. Subsequent research pinpointed four quantitative trait loci (QTLs)-Bwr-3, Bwr-4, Bwr-6, and Bwr-8-that accounted for 3.2 to 29.8% of the phenotypic variation, with Bwr-6 and Bwr-3 persistently detected in both cool and hot seasons, while Bwr-4 and Bwr-8 were only detected during the hot season, implicating environmental factors in resistance manifestation[77]. The study underscored the importance of Bwr-6 and Bwr-3 in resistance to R. solanacearum race 3-phylotype II and suggested a potential overlap with resistance QTLs against other strains[77]. Further studies conducted on recombinant inbred lines identified Bwr-12 and Bwr-6 as principal contributors to resistance, wherein Bwr-12 controlling 17.9%−56.1% of total resistance variation, and Bwr-6 accounting for 11.5%−22.2% of phenotypic variation, with lines containing resistance alleles from both loci exhibiting the least disease incidence[78]. Thus, these findings reinforce the polygenic nature of tomato resistance to BW and the significance of Bwr-6 and Bwr-12 in conferring resistance.

      Table 3.  Quantitative trait loci (QTLs) and molecular markers linked to the resistance loci to bacterial wilt in Solanaceous crops.

      CropLocusChromosomeMarker IDMarker typeReference
      Tomato12TG564RFLP[76]
      Bwr-3, Bwr-4, Bwr-6 and Bwr-8RFLP[77]
      TSCARAAT/CGA,
      TSCARAAG/CAT
      SCAR[83]
      Bwr-6, Bwr-126, 12SSR[78]
      SCU176-534SCAR[79]
      Bwr-1212KHU-1SNP[80]
      Bwr-66SNP[80]
      SCU176-534SCAR[79]
      Bwr-6, near Bwr-126, 12RsR6-5, RsR12-1CAPS[81]
      Bwr-6.1, Bwr-6.3 and Bwr-126, 12SNP[82]
      Bwr-3Bwr3.2dCAPSSNP[84]
      EggplantERs19AFLP, SSR, and SRAP[48]
      EBWR9(ERs1), EBWR14, EBWR29, 5, 2SNP[86]
      3, 6SNP[87]
      emh21J12, emf01K16SSR[88]
      emb01D10, emh11I06,
      emh02E08, SSR–46
      SSR[89]
      PotatoqBWR-1, qBWR-2, qBWR-3,
      qBWR-4, and qBWR-5
      1, 3, 7, 10 and 11SNP[90]
      PBWR-6b6SNP[91]
      PBWR-6b6Rbw6-1allele-specific[92]
      PepperBw11CAMS451SSR[93]
      qRRs-10.110SNP[93]
      Bwr6w-7.2, Bwr6w-8.1, Bwr6w-9.1, Bwr6w-9.2, and Bwr6w-10.1, Bwr6w-5.1, Bwr6w-6.1,
      and Bwr6w-7.1
      5, 6, 7, 8, 9, 10C07_224926788-HRM, C08_134064617-HRM, C09_3486004-HRM, C10_232244800-HRM, C05_224016474-HRM, and C07_115436147-HRMHRM[95]
      TobaccoqBWR3a, qBWR-3b, qBWR-5a
      and qBWR-5b
      PT20275 and PT30229SSR[97]
      qBWR17aSSR[98]

      Beyond the aforementioned loci, the development of supplementary molecular markers has led to significant advancements. For instance, the SCAR marker (SCU176-534) was associated with BW resistance in the Hawaii 7996 line, as identified through bulked segregant analysis (BSA) and rapid amplified polymorphic DNA (RAPD) techniques[79]. This marker showed promise for accelerating the selection of resistant lines in breeding efforts involving Hawaii 7996. Separate investigations revealed 5,259 non-synonymous single nucleotide polymorphisms (SNPs) between seven BW-resistant tomato varieties and two susceptible counterparts, mainly located on chromosomes 6 and 12. Notably, the SNP marker KHU-1, located in gene Solyc12g009690.1, encoding a putative leucine-rich repeat (LRR) receptor-like protein and potentially linked to the Bwr-12 QTL, effectively differentiated resistant from susceptible tomato varieties[80]. Further developments include the creation of two CAPS markers, RsR6-5 and RsR12-1 on chromosomes 6 and 12, respectively. These markers proved effective in distinguishing between resistant and susceptible tomato varieties to BW[81]. A comprehensive study mapped a genetic chart using 1604 SNP markers, locating seven QTLs linked to BW resistance on chromosomes 6 and 12 within the 'Hawaii 7996' tomato line[82]. By phenotyping 80 BC3F3 near-isogenic lines (NILs), this study verified the specific effects of Bwr-6.1, Bwr-6.3, and Bwr-12 on disease severity after exposure to two different BW strains across two seasons[82]. In another study involving a cross between the resistant cultivar T51A and the susceptible cultivar T9230, a BSA applied to an F2 population identified two markers, TSCARAAT/CGA and TSCARAAG/CAT, using PCR-based amplified fragment length polymorphism (AFLP) techniques. These markers, converted into co-dominant SCAR markers, were found on the opposite side of TRSR-1[83]. Moreover, an analysis of resistance segregation in two populations and whole-genome sequence data from six BW-resistant and nine BW-susceptible tomato lines suggested possible roles of loci other than Bwr-6 and Bwr-12 in conferring resistance[84]. This investigation revealed 27,046 unique SNPs and 5,975 indels in the resistant lines, implicating 385 genes. Among these, a significant variant on chromosome 3, marked by Bwr3.2dCAPS in the Asc gene, was strongly associated with resistance[84].

      Eggplant, exhibiting potential resistance to all phylotypes of R. solanacearum (RSSC), serves as an intriguing subject for studying BW resistance. Recent research on the resistant breeding line AG91-25, derived from S. melongena and S. aethiopicum, yielded promising results[85]. In this context, a recombinant inbred lines (RILs) population, derived from a cross between AG91-25 and a susceptible parent (line MM738), was phenotyped with phylotype I strains[48]. Utilizing AFLP, SSR, and SRAP markers, researchers generated an intraspecific map with 119 molecular markers across 18 linkage groups. This led to the identification of a unique monogenic resistance locus, ERs1, in crop RSSC resistance[48]. When exposed to four additional RSSC strains representing phylotypes I, IIA, IIB, and III, this population showed one major phylotype-specific QTL, EBWR9 (which coincided with the previously identified ERs1), and two broad-spectrum QTLs, EBWR14 and EBWR2[86]. Notably, EBWR14 and EBWR2, located on chromosomes 2 and 5, offered partial resistance to strains of phylotypes I, IIA, III and strains of phylotypes IIA and III, respectively[86]. Additional studies on 123 doubled haploid lines, bred from a susceptible eggplant line (MM738) and a resistant counterpart (EG203), resulted in the mapping of 10 and three resistance QTLs for phylotypes I and III, respectively[87]. Interestingly, the most reliable QTLs were found on chromosomes 3 and 6, with the one on chromosome 6 resonating with the broad-spectrum resistance QTL Bwr-6 observed in tomatoes[87]. Screening of six elite eggplant genotypes in a field setting identified three—CARI-1, IIHR-7, and IIHR-500A—as resistant to BW. This led to the identification of two SSR markers, emh21J12 and emf01K16, associated with this resistance[88]. Subsequently, BSA was performed in two F2 populations exhibiting BW resistance, derived from crosses between resistant lines (CARI-1 and IIHR -7) and susceptible lines (Rampur Local and Arka Kushmakar IIHR-108). The SSR markers emb01D10, emh11I06, emh02E08, and SSR-46 co-segregated with resistant and susceptible genotypes of the two F2 populations and were linked to BW resistance loci[89].

      In the realm of potato research, a crossbreeding effort was undertaken between a resistant diploid line, 10-03-30, and a susceptible diploid line, F1-1. This yielded a diploid F1 population of 94 genotypes, a kind of two-way pseudo-testcross[90]. From this population, five QTLs (qBWR-1 to -5) were identified through QTL analysis. These QTLs were located on potato chromosomes 1, 3, 7, 10, and 11, accounting for 9.3%−18.4% of the phenotypic variance. Of particular note was that the alleles for qBWR-2 to -4 were resistant, whereas those for qBWR-1 and qBWR-5 were susceptible[90]. Subsequent investigation uncovered 10 resistance QTLs in an F1 population, which was derived from a cross between a resistant haploid line from Saikai 35 and a susceptible diploid line[91]. Among these, QTL PBWR-6b was the most effective, originating from the resistant parent and located on potato chromosome 6. In a later study, a resistance allele was identified and an allele-specific molecular marker (Rbw6-1) for PBWR-6b was developed[92]. This discovery marked a significant advance in our understanding of potato resistance to BW.

      In the domain of pepper research, Mimura et al. employed a double haploid mapping population derived from 'California Wonder' (susceptible) and 'LS2341' (resistant) to probe pepper's resistance to BW. This study successfully generated a linkage map encompassing 15 groups through the application of SSRs and AFLP. A significant QTL, Bw1, was discovered on pepper chromosome 1 (P1), accounting for 33% of the resistance attributed to 'LS2341'. This QTL was mapped using the SSR marker CAMS451[93]. More recently, Du et al. shed light on the dynamics of bioluminescent R. solanacearum colonization through an examination using reciprocal grafts of a resistant line (BVRC 1) and a susceptible line (BVRC 25). They pinpointed a key QTL (qRRs-10.1) on chromosome 10, hosting several resistance and defense-related genes, which plays a significant role in BW resistance[94]. Additionally, Lee et al. identified five QTLs (Bwr6w-7.2, Bwr6w-8.1, Bwr6w-9.1, Bwr6w-9.2, and Bwr6w-10.1) conferring resistance to a moderately pathogenic 'HS' isolate. In contrast, three QTLs (Bwr6w-5.1, Bwr6w-6.1, and Bwr6w-7.1) were found to resist a highly pathogenic 'HWA' isolate of R. solanacearum in two F2 populations derived from the highly resistant pepper cultivar 'Konesian hot'. Within the same study, six high-resolution melting (HRM) markers linked to these QTLs were also developed[95].

      In the realm of tobacco research, four QTL mapping studies have been conducted for tobacco bacterial wilt (TBW) resistance across bi-parental and diverse genetic populations, utilizing SSR and AFLP markers. An AFLP analysis identified a significant QTL linked with 15 markers, accounting for over 30% of the resistance variance, within the resistant variety W6 and susceptible variety Michinoku 1, thus yielding 117 useful DNA markers[96]. In an examination of the F2:3 and F2:4 progeny resulting from crosses between wilt-resistant breeding lines (Enshu and Yanyan97) and a susceptible line (TI448A), Qian et al. uncovered four QTLs (qBWR3a, qBWR-3b, qBWR-5a, and qBWR-5b) in linkage groups 3 and 5[97]. The closely linked markers PT20275 and PT30229, detected in both crosses, offer a valuable tool for the selection of resistant plants[97]. In another significant study, a major QTL (qBWR17a) was identified that accounted for 30% of the phenotypic variation, providing a noteworthy advantage for MAS in TBW resistance breeding[98]. A distinct investigation into 'K346' tobacco's resistance to BW associated three QTLs with resistance, explaining 50.3% of the observed variation[99]. Furthermore, a pioneering study identified 142 quantitative trait nucleotides (QTNs) that account for a substantial portion of the phenotypic variance for TBW resistance, with 38 of these QTNs being stable across varied environments and methodologies[100]. This research, marking the first identification of QTNs and superior alleles for the breeding of TBW-resistant tobacco varieties, also suggested the five most effective cross combinations for resistance and highlighted 52 potential candidate genes. These insights are invaluable for future studies in genetic architecture, marker-assisted selection, and functional genomics of TBW resistance, aiming to increase crop productivity. As a result, these discoveries offer instrumental tools for MAS in the breeding program to enhance resistance to BW in Solanaceous crops.

    • R. solanacearum presents a considerable threat to Solanaceous crops, and the development of effective genetic control strategies remains a pressing priority. Emerging advancements in genomics, relating to both pathogens and host plants, offer the exciting potential to discover previously unrecognized resources for disease resistance in the near future. As such, intensifying our research efforts in remote hybridization and somatic cell fusion is critical, aiming to increase success rates and create a collection of Solanaceous germplasm with strong resistance to BW. The application of effectors could play a key role in implementing high-throughput methodologies for identifying BW resistance[101]. This strategy may also stimulate resistance screening in wild species, thereby enhancing the selection of disease-resistant materials and receptor identification. When identifying receptors in certain Solanaceous plants proves challenging, we could consider the development of resistant varieties by integrating resistance genes from A. thaliana and other Solanaceous plants. Moreover, genome-editing technologies present promising avenues for manipulating host target genes. The successful completion of whole-genome sequencing for key Solanaceous crops, including potato, tomato, eggplant, pepper, and tobacco (referenced at https://solgenomics.net), is set to expedite the cloning process for resistance genes against BW. Furthermore, the adoption of recent methodological advancements, such as Resistance gene enrichment sequencing (RenSeq)[102], could facilitate quicker receptor identification within Solanaceous crops. These combined efforts give rise to the promising future of R. solanacearum-resistant crop development, transforming it from a distant goal into an imminent reality.

    • The authors confirm contribution to the paper as follows: study conception and design: study conception and design: Du J, Wang B, Chen H, Song B; data collection: Du J, Wang B, Huang M, Chen X, Nie L, Wang T; draft manuscript preparation: Du J, Wang B, Huang M, Chen X, Chen H, Song B. All authors reviewed the results and approved the final version of the manuscript.

    • All data supporting the findings of this research are available within the paper and within its supplementary data.

      • The work was partially supported by the National Natural Science Foundation of China (32201789) and the China Agriculture Research System of MOF and MARA (CARS-09).

      • The authors declare that they have no conflict of interest.

      • # These authors contributed equally: Juan Du, Bingsen Wang

      • Supplemental Table S1 General genome information of 325 Ralstonia solanacearum strains in the NCBI database.
      • Copyright: © 2023 by the author(s). Published by Maximum Academic Press, Fayetteville, GA. This article is an open access article distributed under Creative Commons Attribution License (CC BY 4.0), visit https://creativecommons.org/licenses/by/4.0/.
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    Du J, Wang B, Huang M, Chen X, Nie L, et al. 2023. Advancements in unraveling and enhancing bacterial wilt resistance in Solanaceous crops. Vegetable Research 3:29 doi: 10.48130/VR-2023-0029
    Du J, Wang B, Huang M, Chen X, Nie L, et al. 2023. Advancements in unraveling and enhancing bacterial wilt resistance in Solanaceous crops. Vegetable Research 3:29 doi: 10.48130/VR-2023-0029

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