Characterizing the Mode of Resistance Conferred Against Asian Soybean Rust by CcRpp1, a Novel R Gene from Cajanus cajan (L.) Millsap.

IF 3.1 2区 农林科学 Q2 PLANT SCIENCES
Mark A Chamberlin, Annaliese Cramer, Ashley Saunders, Ebony T Johnson, Mary A Rupe, Hongyu Wang, Sai Guna Ranjan Gurazada, Shawn R Thatcher, John L Van Hemert, Jan P Hazebroek, Aline Sartor Chicowski, Jeffrey E Habben, Karen E Broglie
{"title":"Characterizing the Mode of Resistance Conferred Against Asian Soybean Rust by <i>CcRpp1</i>, a Novel <i>R</i> Gene from <i>Cajanus cajan</i> (L.) Millsap.","authors":"Mark A Chamberlin, Annaliese Cramer, Ashley Saunders, Ebony T Johnson, Mary A Rupe, Hongyu Wang, Sai Guna Ranjan Gurazada, Shawn R Thatcher, John L Van Hemert, Jan P Hazebroek, Aline Sartor Chicowski, Jeffrey E Habben, Karen E Broglie","doi":"10.1094/PHYTO-02-25-0048-R","DOIUrl":null,"url":null,"abstract":"<p><p>Asian soybean rust (ASR), caused by <i>Phakopsora pachyrhizi</i>, poses a significant threat to soybean production, especially in South America. The <i>CcRpp1</i> gene (<i>Cajanus cajan</i> Resistance against <i>P. pachyrhizi</i> 1) has demonstrated robust resistance to ASR when introduced into soybean. This study explores the underlying mechanisms of <i>CcRpp1</i>-mediated resistance through integrated cytological, transcriptomic, and metabolomic analyses. Cytological observations revealed that <i>CcRpp1</i>-expressing plants rapidly halt fungal infection within 24-36 hours post-inoculation (hpi) by inhibiting hyphal growth and differentiation, as well as sequestering fungal feeding structures inside host cells. Transcriptomic profiling at 36 hpi showed upregulation of genes involved in photosynthesis, primary metabolism, and carbon utilization, while genes associated with protein synthesis were downregulated. This pattern suggests a metabolic shift that prioritizes energy production and defense over growth. Metabolomic analyses further indicated that <i>CcRpp1</i>-mediated resistance is marked by a swift and substantial depletion of amino acids and nitrogen-containing metabolites following infection. This rapid metabolic reprogramming likely restricts nutrient availability to the pathogen, contributing to the observed resistance and highlighting a potential mode-of-action. Overall, these findings provide new insights into the molecular and metabolic basis of <i>CcRpp1</i>-mediated ASR resistance and lays the groundwork for additional in-depth studies that will lead to the development of sustainable and effective strategies for deployment of durable resistance against ASR.</p>","PeriodicalId":20410,"journal":{"name":"Phytopathology","volume":" ","pages":""},"PeriodicalIF":3.1000,"publicationDate":"2025-07-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Phytopathology","FirstCategoryId":"97","ListUrlMain":"https://doi.org/10.1094/PHYTO-02-25-0048-R","RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"PLANT SCIENCES","Score":null,"Total":0}
引用次数: 0

Abstract

Asian soybean rust (ASR), caused by Phakopsora pachyrhizi, poses a significant threat to soybean production, especially in South America. The CcRpp1 gene (Cajanus cajan Resistance against P. pachyrhizi 1) has demonstrated robust resistance to ASR when introduced into soybean. This study explores the underlying mechanisms of CcRpp1-mediated resistance through integrated cytological, transcriptomic, and metabolomic analyses. Cytological observations revealed that CcRpp1-expressing plants rapidly halt fungal infection within 24-36 hours post-inoculation (hpi) by inhibiting hyphal growth and differentiation, as well as sequestering fungal feeding structures inside host cells. Transcriptomic profiling at 36 hpi showed upregulation of genes involved in photosynthesis, primary metabolism, and carbon utilization, while genes associated with protein synthesis were downregulated. This pattern suggests a metabolic shift that prioritizes energy production and defense over growth. Metabolomic analyses further indicated that CcRpp1-mediated resistance is marked by a swift and substantial depletion of amino acids and nitrogen-containing metabolites following infection. This rapid metabolic reprogramming likely restricts nutrient availability to the pathogen, contributing to the observed resistance and highlighting a potential mode-of-action. Overall, these findings provide new insights into the molecular and metabolic basis of CcRpp1-mediated ASR resistance and lays the groundwork for additional in-depth studies that will lead to the development of sustainable and effective strategies for deployment of durable resistance against ASR.

Cajanus cajan (L.)新R基因CcRpp1对亚洲大豆锈病抗性模式的研究米尔萨普。
亚洲大豆锈病(ASR)是由肿根Phakopsora pachyrhizi引起的,对大豆生产构成重大威胁,特别是在南美洲。CcRpp1基因(Cajanus cajan Resistance against P. pachyrhizi 1)被引入大豆后显示出对ASR的强大抗性。本研究通过综合细胞学、转录组学和代谢组学分析探讨了ccrpp1介导的耐药性的潜在机制。细胞学观察表明,表达ccrpp1的植物在接种后24-36小时内通过抑制菌丝生长和分化,以及在宿主细胞内隔离真菌摄食结构,迅速停止真菌感染。转录组学分析显示,在36 hpi时,参与光合作用、初级代谢和碳利用的基因上调,而与蛋白质合成相关的基因下调。这种模式表明,新陈代谢的转变优先考虑能源生产和防御,而不是增长。代谢组学分析进一步表明,ccrpp1介导的抗性以感染后氨基酸和含氮代谢物的迅速和大量消耗为特征。这种快速的代谢重编程可能限制了病原体的营养可用性,有助于观察到的耐药性,并突出了潜在的作用模式。总的来说,这些发现为ccrpp1介导的ASR耐药的分子和代谢基础提供了新的见解,并为进一步的深入研究奠定了基础,这些研究将导致开发可持续和有效的策略来部署对ASR的持久抗性。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
Phytopathology
Phytopathology 生物-植物科学
CiteScore
5.90
自引率
9.40%
发文量
505
审稿时长
4-8 weeks
期刊介绍: Phytopathology publishes articles on fundamental research that advances understanding of the nature of plant diseases, the agents that cause them, their spread, the losses they cause, and measures that can be used to control them. Phytopathology considers manuscripts covering all aspects of plant diseases including bacteriology, host-parasite biochemistry and cell biology, biological control, disease control and pest management, description of new pathogen species description of new pathogen species, ecology and population biology, epidemiology, disease etiology, host genetics and resistance, mycology, nematology, plant stress and abiotic disorders, postharvest pathology and mycotoxins, and virology. Papers dealing mainly with taxonomy, such as descriptions of new plant pathogen taxa are acceptable if they include plant disease research results such as pathogenicity, host range, etc. Taxonomic papers that focus on classification, identification, and nomenclature below the subspecies level may also be submitted to Phytopathology.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:604180095
Book学术官方微信