近日，华中农业大学植物科学技术学院、湖北洪山实验室、园艺植物生物学教育部重点试验室徐文兴教授课题组在国际上首次报道了从真菌内发现的一类类病毒类似的新非细胞生物，命名为“真菌类病毒”（“mycoviroid”），并证明真菌类病毒具有基因调控功能，是一类新的表观信息调控携带因子，是目前报道的唯一一类能够自然侵染真菌并在真菌内复制的小单链环状RNA分子生物，为采用亚病毒开展作物真菌病害生物防治打开了一扇新的窗口。相关研究成果以题为“Novel Viroid-Like RNAs Naturally Infect a Filamentous Fungus”在线发表于国际期刊在Advanced Science。华中农业大学植物科学技术学院博士研究生董凯莉为论文第一作者，徐文兴教授为论文通讯作者。

     类病毒（viroid）是一类侵染植物具有自我复制功能的单链环状RNA分子，大小为246～401个核苷酸，可引起一些作物严重损失，是世界上已知的最小生物。目前，植物为类病毒的唯一自然寄主，在其它细胞生物内是否存在类病毒或其它单链环状RNA分子生物尚不清楚。本研究前期从植物病原真菌-葡萄座腔菌（Botryosphaeria dothidea）中分离得到了一类小的RNA条带，经鉴定为外源单链环状RNA分子，大小为157～450个核苷酸，我们将其命名为葡萄座腔菌环状RNA（Botryosphaeria dothidea cirRNA, BdcRNA）1～3，其二级结构呈多分枝状，能够经菌丝水平传播和经孢子垂直传播。通过Northern blot 及荧光原位杂交发现，BdcRNA1～3在真菌细胞核中以对称滚环方式复制，但具有不同的自催化能力。

    其中，BdcRNA2具有一种新型的核酶结构（不同于类病毒的锤头核酶），可以进行RNA自剪切，而BdcRNA1和3不具有核酶活性。构建BdcRNA1～3二聚体RNA转染真菌原生质体，表明三种环状RNA因种类不同调节寄主真菌的形态、生长速度、致病力和渗透压和氧化应激能力等生物学性状发生不同程度的变化，特别是BdcRNA1转染后可以使真菌生长更加“健壮”，但致病性丧失，显示了良好的生防应用潜能。进一步采用转录组和荧光定量RT-PCR分析，显示BdcRNA引起寄主生物学性状变化与其改变寄主的相关代谢通路相关。

    本研究在国际上首次报道了一类感染真菌的小单链环状RNA分子生物，代表一类新的基因组成上处于生命边缘的生物，具有基因调控功能，是一类新的表观信息调控携带因子，是目前报道的唯一一类能够自然侵染真菌并在真菌内复制的单链环状RNA分子生物，也是目前报道的唯一一类能够自然侵染植物以外生物的类病毒类似（或外源小环状RNA）的分子生物，命名为“真菌类病毒”（“mycoviroid”）（一类感染真菌的类病毒类似单链环状RNA分子。注：区别于已有的“能够感染健康真菌的类病毒”定义）。此外，本研究还首次实验显示了一种环状RNA分子在真菌内的亚细胞定位、复制、分布和移动证据。“真菌类病毒”的发现为全面理解真菌的变异及采用亚病毒开展作物病害生物防治打开了一扇新的窗口。

 参考文献： Novel Viroid-like RNAs Naturally Infect a Filamentous Fungus

Kaili Dong, Chuan Xu, Ioly Kotta-Loizou, Jingjing Jiang, Ruiying Lv, Linghong Kong, Shifang Li, Ni Hong, Guoping Wang, Robert H. A. Coutts, Wenxing Xu* 

Advanced Science https://doi.org/10.1002/advs.202204308 

 Abstract  To date, viroids have been found to naturally infect only plants, resulting in substantial losses for some crops. Whether viroids or viroid-like RNAs naturally infect non-plant hosts remains unknown. Here the existence of a set of exogenous, single-stranded circular RNAs, ranging in size from 157 to 450 nucleotides, isolated from the fungus Botryosphaeria dothidea and nominated B. dothidea RNAs (BdcRNAs) is reported. BdcRNAs replicate autonomously in the nucleus via a rolling-circle mechanism following a symmetric pathway. BdcRNA infection induces symptoms, because BdcRNAs can apparently modulate, to different degrees, specific biological traits (e.g., alter morphology, decrease growth rate, attenuate virulence, and increase or decrease tolerance to osmotic and oxidative stress) of the host fungus. Overall, BdcRNAs have genome characteristics similar to those of viroids and exhibit pathogenic effects on fungal hosts. It is proposed that these novel fungus infecting RNAs should be termed mycoviroids. BdcRNA(s) may be considered additional inhabitants at the frontier of life in terms of genomic complexity, and represent a new class of acellular entities endowed with regulatory functions, and novel epigenomic carriers of biological information.
Full text:  https://onlinelibrary.wiley.com/doi/10.1002/advs.202204308  

述评：Novel Viroid-Like RNAs Naturally Infect a Filamentous Fungus (Adv. Sci. 3/2023)

Viroid-Like RNAs

In article number 2204308, Wenxing Xu, Kaili Dong, and co-workers characterize a novel class of viroid-like RNAs naturally infecting a filamentous fungus Botryosphaeria dothidea isolated from apple and termed as mycoviroids. These mycoviroids replicate autonomously in the nucleus via a rolling-circle mechanism following a symmetric pathway, can apparently modulate specific biological traits of the host fungus, and represent a new class of acellular entities endowed with regulatory functions, and novel epigenomic carriers of biological information. This is the first report of infectious viroid-like RNAs (or exogenous small circular RNAs) in a life kingdom (fungi) other than plants.

https://doi.org/10.1002/advs.202370014