評估高溫對水稻與徒長病菌交互作用之影響

Abstract

全球暖化對作物及其病原菌皆造成深遠影響，嚴重危害農業生產及糧食安全。 Fusarium fujikuroi 引起之水稻徒長病過去被視為次要病害，近年來卻已成為限制生產的重要因子之一，其是否受暖化影響仍待釐清。本研究探討高溫下臺灣徒長病菌株的生理反應及徒長病病程變化，並分析高溫對水稻抗性與病原菌毒力在轉錄層級的影響。結果顯示，高溫同時抑制徒長病菌毒力與水稻防禦，從而改變病程發展。高溫下徒長病菌菌絲生長、孢子萌發及吉貝素 (GA3) 合成均受到抑制；水稻防禦反應亦減弱，尤以植物賀爾蒙訊號傳遞與轉錄因子調控最為明顯。在徒長病菌與水稻雙雙弱化下，徒長病發生情形減輕，導致病害嚴重度、植體內徒長病菌菌量、GA3及鐮孢菌酸 (fusaric acid) 訊號降低。結合溫度 (日/夜30/25℃與35/30℃)、水稻品種 [臺農67號 (TNG67) 與Zerawchanica Karatals (ZK)] 以及接種處理 (徒長病菌接種組與健康對照組) 作為變因進行轉錄體分析。主成分分析與差異表達基因 (differentially expressed gene, DEG) 分析顯示高溫對基因表現的影響較徒長病菌侵染更為顯著，且TNG67中所鑑定出的DEGs數量也多於 ZK。熱逆境下光合作用、氧化還原穩態、碳水化合物代謝、膜完整性與RNA修飾相關的基因本體詞彙 (Gene Ontology term, GO term) 顯著富集，其中的DEGs在TNG67中普遍受到下調、在ZK中則以上調居多，顯示TNG67與ZK具有不同的熱適應策略。感染徒長病時，防禦相關 之GO terms (如：植物賀爾蒙訊息傳遞) 顯著富集，且其中的DEGs在兩個品種中皆呈上調。無論是在健康或是接種徒長病菌的植株中，茉莉酸 (jasmonic acid, JA) 與水楊酸 (salicylic acid, SA) 訊息傳遞在高溫下皆遭抑制，使得整體防禦反應削弱。乙烯 (ethylene, ET) 訊息傳遞則在高溫與徒長病菌侵染逆境下皆上調，可能是其中的整合性角色。多個廣泛參與抗性調控的轉錄因子家族 (如：WRKY、NAC、MYB) 在徒長病菌侵染下上調，但在高溫下受到抑制，顯示熱逆境干擾水稻的防禦調控網絡。有趣的是，少數基因在兩種逆境下均上調，彰顯其做為氣候韌性與徒長病抗性改良標的之價值。此外，多數防禦相關基因在高溫下被抑制，支持植物在面對非生物與生物逆境間存在調控權衡 (trade-off) 的觀點。在徒長病菌方面，富集分析指出病原菌在面對熱逆境與感病寄主時，下調其壓力反應和蛋白質摺疊相關途徑，並上調代謝、轉譯與細胞壁分解功能，反映其調控模式可能由維持細胞功能轉向代償機制或致病功能。此外，比卡菌素 (bikaverin) 與GA生合成基因分別在應對熱逆境與感病寄主時活化，突顯徒長病菌次級代謝物在環境適應與致病力中的角色。綜合而言，本研究揭示高溫如何透過轉錄調控網絡影響水稻–徒長病菌交互作用，對氣候變遷下水稻徒長病潛在的發生生態變化提供機制面的理解。雖然全球暖化可能降低徒長病嚴重度，但在水稻抗性降低的情況下，應重視耐熱菌株演化帶來的潛在風險，突顯持續監測與目標性抗病育種策略的重要性。

Global warming has exerted profound impacts on both crops and their associated pathogens, posing serious threats to agricultural productivity and food security. Bakanae disease, caused by Fusarium fujikuroi, was historically considered a minor issue in rice cultivation but has recently re-emerged as a major constraint on production. However, it remains unclear whether this phenomenon has been influenced by climate change. This study aimed to investigate the physiological responses of F. fujikuroi isolates in Taiwan to high temperature and to assess disease progression under elevated temperature. Additionally, we analyzed how heat affects rice defense responses and pathogen virulence mechanisms at the transcriptomic level. Our results demonstrate that high temperature simultaneously suppresses both F. fujikuroi virulence and rice immune responses, thereby reshaping disease progression. Under elevated temperature, the pathogen exhibited reduced hyphal growth, spore germination, and gibberellin A3 (GA3) production. Concurrently, rice defense responses were weakened, particularly in phytohormone signaling and transcription factor regulation. The combined attenuation of host and pathogen activity led to lower disease severity index, reduced fungal biomass, and decreased in planta levels of GA3 and fusaric acid. Transcriptome analysis was conducted by integrating temperature (30/25℃ vs. 35/30℃), rice cultivars [Tainung 67 (TNG67) vs. Zerawchanica Karatals (ZK)], and inoculation treatment (Ff266-inoculated vs. mock-treated) as experimental variables. Principle component analysis and differentially expressed gene (DEG) analysis revealed that heat exerted a more profound influence on gene expression than fungal infection. Furthermore, a greater number of DEGs were identified in TNG67 compared with ZK. Gene Ontology (GO) terms related to photosynthesis, redox homeostasis, carbohydrate metabolism, membrane integrity, and RNA modification were significantly enriched under heat stress. The majority of DEGs were downregulated in TNG67 but upregulated in ZK, indicating that the two cultivars employed distinct transcriptomic strategies in response to heat stress. During F. fujikuroi infection, defense-related GO terms, such as those involved in phytohormone signaling, were significantly enriched. The associated DEGs were consistently upregulated in both cultivars. In both healthy and infected seedlings, jasmonic acid (JA) and salicylic acid (SA) signaling—key components of plant defense—were suppressed by heat, reflecting compromised immune function. Conversely, ethylene (ET) signaling was consistently upregulated under both heat stress and fungal infection, suggesting a potential integrative role in dual stress responses. Several transcription factor families commonly involved in defense regulation (e.g., WRKY, NAC, MYB) were induced by infection but suppressed by heat, indicating that elevated temperature disrupted immune regulatory networks in rice. Interestingly, a small subset of genes was consistently upregulated under both stress conditions, highlighting their potential as targets for breeding climate-resilient and disease-resistant rice varieties. Meanwhile, the broader downregulation of defense genes supported the concept of a regulatory trade-off between abiotic and biotic stress responses. On the pathogen side, enrichment analysis revealed that F. fujikuroi downregulated pathways associated with stress responses and protein homeostasis in response to heat stress and the susceptible host, while upregulating those related to metabolism, translation, and cell wall degradation. These transcriptional changes suggested a regulatory shift from cellular maintenance toward compensatory mechanisms or infection functions. Furthermore, the activation of bikaverin and GA biosynthetic genes in response to heat stress and susceptible hosts, respectively, underscored the role of secondary metabolites in adaptation and virulence. Collectively, this study demonstrated how high temperature modulates rice–F. fujikuroi interactions via transcriptomic regulatory networks, providing mechanistic insights into how climate change may influence bakanae disease dynamics. Although disease severity may appear reduced under warming scenarios, the observed suppression of host immunity raises concerns about the emergence of heat-tolerant F. fujikuroi isolates. These findings underscore the importance of ongoing field surveillance and targeted resistance breeding strategies.