Duoduo Wang, Palash Mandal, Md Sazan Rahman, Lirong Yang
{"title":"Engineering tomato disease resistance by manipulating susceptibility genes.","authors":"Duoduo Wang, Palash Mandal, Md Sazan Rahman, Lirong Yang","doi":"10.3389/fgeed.2025.1537148","DOIUrl":null,"url":null,"abstract":"<p><p>Various pathogens severely threaten tomato yield and quality. Advances in understanding plant-pathogen interactions have revealed the intricate roles of resistance (R) and susceptibility (S) genes in determining plant immunity. While R genes provide targeted pathogen resistance, they are often vulnerable to pathogen evolution. Conversely, S genes offer a promising avenue for developing broad-spectrum and durable resistance through targeted gene editing. Recent breakthroughs in CRISPR/Cas-based technologies have revolutionized the manipulation of plant genomes, enabling precise modification of S genes to enhance disease resistance in tomato without compromising growth or quality. However, the utilization of the full potential of this technique is challenging due to the complex plant-pathogen interactions and current technological limitations. This review highlights key advances in using gene editing tools to dissect and engineer tomato S genes for improved immunity. We discuss how S genes influence pathogen entry, immune suppression, and nutrient acquisition, and how their targeted editing has conferred resistance to bacterial, fungal, and viral pathogens. Furthermore, we address the challenges associated with growth-defense trade-offs and propose strategies, such as hormonal pathway modulation and precise regulatory edits, to overcome these limitations. This review underscores the potential of CRISPR-based approaches to transform tomato breeding, paving the way for sustainable production of disease-resistant cultivars amidst escalating global food security challenges.</p>","PeriodicalId":73086,"journal":{"name":"Frontiers in genome editing","volume":"7 ","pages":"1537148"},"PeriodicalIF":4.9000,"publicationDate":"2025-02-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11847883/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Frontiers in genome editing","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.3389/fgeed.2025.1537148","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2025/1/1 0:00:00","PubModel":"eCollection","JCR":"Q1","JCRName":"BIOTECHNOLOGY & APPLIED MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Various pathogens severely threaten tomato yield and quality. Advances in understanding plant-pathogen interactions have revealed the intricate roles of resistance (R) and susceptibility (S) genes in determining plant immunity. While R genes provide targeted pathogen resistance, they are often vulnerable to pathogen evolution. Conversely, S genes offer a promising avenue for developing broad-spectrum and durable resistance through targeted gene editing. Recent breakthroughs in CRISPR/Cas-based technologies have revolutionized the manipulation of plant genomes, enabling precise modification of S genes to enhance disease resistance in tomato without compromising growth or quality. However, the utilization of the full potential of this technique is challenging due to the complex plant-pathogen interactions and current technological limitations. This review highlights key advances in using gene editing tools to dissect and engineer tomato S genes for improved immunity. We discuss how S genes influence pathogen entry, immune suppression, and nutrient acquisition, and how their targeted editing has conferred resistance to bacterial, fungal, and viral pathogens. Furthermore, we address the challenges associated with growth-defense trade-offs and propose strategies, such as hormonal pathway modulation and precise regulatory edits, to overcome these limitations. This review underscores the potential of CRISPR-based approaches to transform tomato breeding, paving the way for sustainable production of disease-resistant cultivars amidst escalating global food security challenges.
各种病原体严重威胁着番茄的产量和质量。随着对植物与病原体相互作用认识的不断深入,抗性(R)基因和易感性(S)基因在决定植物免疫力方面发挥着错综复杂的作用。虽然 R 基因能有针对性地抵抗病原体,但它们往往容易受到病原体进化的影响。相反,S 基因为通过靶向基因编辑开发广谱、持久的抗性提供了一条大有可为的途径。基于 CRISPR/Cas 技术的最新突破彻底改变了对植物基因组的操作,使 S 基因的精确改造成为可能,从而在不影响番茄生长或品质的情况下增强其抗病性。然而,由于植物与病原体之间复杂的相互作用以及当前技术的局限性,要充分发挥这一技术的潜力仍面临挑战。本综述重点介绍了利用基因编辑工具剖析和改造番茄 S 基因以提高免疫力的主要进展。我们讨论了 S 基因如何影响病原体进入、免疫抑制和营养获取,以及对其进行定向编辑如何赋予其对细菌、真菌和病毒病原体的抗性。此外,我们还探讨了与生长-防御权衡相关的挑战,并提出了一些策略,如激素途径调节和精确调控编辑,以克服这些限制。这篇综述强调了基于 CRISPR 的方法在改变番茄育种方面的潜力,为在全球粮食安全挑战不断升级的情况下可持续地生产抗病栽培品种铺平了道路。