Multi-site fungicides suppress banana Panama disease, caused by Fusarium oxysporum f. sp. cubense Tropical Race 4.
Multi-site fungicides suppress banana Panama disease, caused by Fusarium oxysporum f. sp. cubense Tropical Race 4.
复制标题
DOI：
10.1371/journal.ppat.1010860
复制
发表时间：
2022-10
期刊：
影响因子：
6.7
通讯作者：
Steinberg, Gero
中科院分区：
文献类型：
--
作者：
Cannon, Stuart;Kay, William;Kilaru, Sreedhar;Schuster, Martin;Gurr, Sarah Jane;Steinberg, Gero
全球香蕉生产目前受到由尖孢镰刀菌专化型引起的巴拿马病的挑战。 cubense 热带种族 4 (FocTR4)。没有有效的基于杀菌剂的策略来控制这种土传病原体。这可能是由于病原体对杀菌剂和/或土壤施用本身不敏感。在这里，我们测试了 12 种单位点杀菌剂和 9 种多位点杀菌剂对 FocTR4 和 Foc Race1 (FocR1) 的定量菌落生长效果，以及纯化的 FocTR4 大分生孢子、小分生孢子和厚垣孢子的细胞存活测定。我们证明这些 FocTR4 形态型都会导致香蕉巴拿马病。这些实验揭示了 FocTR4 对所有单位点杀菌剂的先天抗性，唑类、琥珀酸脱氢酶抑制剂 (SDHI)、嗜球果伞素或苯并咪唑均不能杀死这些孢子形式。我们在经杀菌剂处理的菌丝中发现，这种先天抗性发生在“持久”细胞亚群中，并且不是遗传性的。 FocTR4 持续细胞对 3 μg ml-1 唑类或 1000 μg ml-1 嗜球果伞素或 SDHI 做出反应，通过强烈上调编码靶酶的基因（高达 660 倍）、推定的外排泵和转运蛋白基因（高达 230 倍）和外源解毒酶（高达 200 倍）。对在相同条件下生长的 FocTR4 和小麦发酵壳孢 (Zymoseptoria tritici) 中的基因表达进行比较表明，这种反应仅在 FocTR4 中观察到。相比之下，FocTR4 对大多数多位点杀菌剂几乎没有表现出先天抗性。然而，土壤种植香蕉的定量毒力测定表明，只有克菌丹 (20 μg ml-1) 和所有亲脂性阳离子 (200 μg ml-1) 能有效抑制巴拿马病。这些杀菌剂可以帮助保护香蕉免受 FocTR4 造成的未来产量损失。香蕉是世界各地最受欢迎的水果之一，但其生产受到真菌尖镰孢的严重挑战。 sp。 cubense，热带种族 4 (FocTR4)。迄今为止，尚未描述控制这种毁灭性疾病的有效策略。事实上，即使是通常被认为是我们对抗植物病原真菌的“前线武器”的杀菌剂，也被认为对FocTR4无效。在此，我们分析了 12 种单位点杀菌剂和 9 种多位点杀菌剂针对 FocTR4 和 FocR1（古巴尖镰刀菌专化型，第 1 种）的使用情况，并将这些结果与小麦病原体 Zymoseptoria tritici 获得的数据进行比较。我们使用 FocTR4 菌丝和 3 种孢子类型（大分生孢子、小分生孢子、厚垣孢子）进行定量生长和细胞存活测定。我们发现所有 FocTR4 形态类型对最广泛使用的单位点杀菌剂（唑类、琥珀酸脱氢酶抑制剂、嗜球果伞素）具有高度耐受性。对幸存的“持久性”菌丝的基因表达分析表明，它们通过多种机制应对单靶点杀菌剂。这包括增加杀菌剂目标酶、外排蛋白和解毒酶的产量。只有多位点杀菌剂能够通过多种方式影响病原体细胞，被证明可以有效杀死 FocTR4。然而，对经杀菌剂处理的香蕉的疾病症状发展的定量评估表明，只有克菌丹和三种亲脂性阳离子具有控制巴拿马病的潜力。
Global banana production is currently challenged by Panama disease, caused by Fusarium oxysporum f.sp. cubense Tropical Race 4 (FocTR4). There are no effective fungicide-based strategies to control this soil-borne pathogen. This could be due to insensitivity of the pathogen to fungicides and/or soil application per se. Here, we test the effect of 12 single-site and 9 multi-site fungicides against FocTR4 and Foc Race1 (FocR1) in quantitative colony growth, and cell survival assays in purified FocTR4 macroconidia, microconidia and chlamydospores. We demonstrate that these FocTR4 morphotypes all cause Panama disease in bananas. These experiments reveal innate resistance of FocTR4 to all single-site fungicides, with neither azoles, nor succinate dehydrogenase inhibitors (SDHIs), strobilurins or benzimidazoles killing these spore forms. We show in fungicide-treated hyphae that this innate resistance occurs in a subpopulation of "persister" cells and is not genetically inherited. FocTR4 persisters respond to 3 μg ml-1 azoles or 1000 μg ml-1 strobilurins or SDHIs by strong up-regulation of genes encoding target enzymes (up to 660-fold), genes for putative efflux pumps and transporters (up to 230-fold) and xenobiotic detoxification enzymes (up to 200-fold). Comparison of gene expression in FocTR4 and Zymoseptoria tritici, grown under identical conditions, reveals that this response is only observed in FocTR4. In contrast, FocTR4 shows little innate resistance to most multi-site fungicides. However, quantitative virulence assays, in soil-grown bananas, reveals that only captan (20 μg ml-1) and all lipophilic cations (200 μg ml-1) suppress Panama disease effectively. These fungicides could help protect bananas from future yield losses by FocTR4. Bananas are amongst the most popular fruits eaten world-wide, yet their production is seriously challenged by the fungus Fusarium oxysporum f. sp. cubense, Tropical Race 4 (FocTR4). Hitherto, no effective strategy to control this devastating disease has been described. Indeed, even fungicides, which are generally considered to be our "front-line weapon" against plant pathogenic fungi, are deemed ineffective against FocTR4. Here, we analyse the use of 12 single-site and 9 multiple-site fungicides against FocTR4 and FocR1 (Fusarium oxysporum f. sp. cubense, Race 1) and compare these findings with data raised from the wheat pathogen Zymoseptoria tritici. We perform quantitative growth and cell survival assays, using FocTR4 hyphae and the 3 spore types (macroconidia, microconidia, chlamydospores). We show that all FocTR4 morphotypes are highly tolerant of the most widely-used single-site fungicides (azoles, succinate dehydrogenase inhibitors, strobilurins). Analysis of gene expression in surviving "persister" hyphae suggests that they cope with single-target fungicides by multiple mechanisms. This includes increased production of fungicide target enzymes, efflux proteins and detoxification enzymes. Only multi-site fungicides, which have multiple ways to affect the pathogen cell, proved to be effective in killing FocTR4. However, quantitative assessment of disease symptom development in fungicide-treated bananas revealed that only captan and three lipophilic cations have the potential to control Panama disease.
登录
查看更多内容
影响因子：
4.9
作者：
De Backer, MD;Ilyina, T;Vanden Bossche, H
通讯作者：
Vanden Bossche, H
影响因子：
4.8
作者：
Hargrove, Tatiana Y.;Friggeri, Laura;Lepesheva, Galina I.
通讯作者：
Lepesheva, Galina I.
影响因子：
5.6
作者：
Dita M;Barquero M;Heck D;Mizubuti ESG;Staver CP
通讯作者：
Staver CP
影响因子：
3.7
作者：
Guo L;Han L;Yang L;Zeng H;Fan D;Zhu Y;Feng Y;Wang G;Peng C;Jiang X;Zhou D;Ni P;Liang C;Liu L;Wang J;Mao C;Fang X;Peng M;Huang J
通讯作者：
Huang J
影响因子：
5.2
作者：
Golubeva, Polina;Ryo, Masahiro;Rillig, Matthias C.
通讯作者：
Rillig, Matthias C.