Non-native plant viruses prevalent in remnant natural plant communities harm native perennial hosts

IF 3.3 3区 生物学 Q2 MICROBIOLOGY Phytobiomes Journal Pub Date : 2023-10-09 DOI:10.1094/pbiomes-05-23-0033-r
Tessa M. Shates, Marco Gebiola, Penglin Sun, Amani Helo, Oaksoe Aung, Jaimie Kenney, Carolyn Malmstrom, Kerry E. Mauck
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Abstract

Plant viruses are ubiquitous throughout plant communities, but research on viral impacts largely focuses on crops. Little is known about how viruses influence wild plants in their native habitats. To address this gap, we examined virus interactions with wild drought-tolerant perennials in California desert natural areas encroached upon by agriculture. We used metagenomics, targeted diagnostics, and phylogenetics to assess virus diversity and clade relationships, and experiments to investigate viral influence on hosts. We focused on three herbaceous perennials (Cucurbita foetidissima, Cucurbita palmata, and Datura wrightii) and tested the hypothesis that these wild species accumulate virus infections typically found in crops and transmitted by polyphagous insects. We predicted that such infections might be retained across seasons and potentially impair plant performance. Virome profiling revealed a rich community of previously-characterized virus species (12 total), with virus community structure varying by site and host species. The dominant viruses in the wild hosts were non-native crop pathogens, including cucurbit aphid-borne yellows virus (CABYV) and cucurbit yellow stunting disorder virus (CYSDV). Targeted testing revealed that CABYV infected as many as 88% of sampled wild Cucurbita individuals, with dual CABYV-CYSDV infections common in natural areas adjacent to desert agriculture. CABYV infections reduced shoot and root production in greenhouse experiments with the two wild Cucurbita species. Phylogenetic analyses suggest that CABYV was introduced to California multiple times from other continents. Our findings provide concerning evidence of ways in which human activities can alter virus pressure on wild plants and potentially contribute to plant decline.
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在自然植物残群中普遍存在的非本地植物病毒对本地多年生寄主造成危害
植物病毒在植物群落中无处不在,但对病毒影响的研究主要集中在作物上。人们对病毒如何影响野生植物的原生栖息地知之甚少。为了解决这一差距,我们研究了病毒与加州沙漠自然地区被农业侵占的野生耐旱多年生植物的相互作用。我们使用宏基因组学、靶向诊断和系统遗传学来评估病毒多样性和进化支关系,并通过实验来研究病毒对宿主的影响。我们以三种多年生草本植物为研究对象(葫芦巴、棕榈葫芦巴和西葫芦),并验证了这些野生物种积累病毒感染的假设,这些病毒感染通常在作物中发现,并由多食昆虫传播。我们预测这种感染可能会在整个季节中保留,并可能损害植物的性能。病毒组分析揭示了一个丰富的病毒群落(共12种),病毒群落结构因地点和宿主物种而异。野生寄主的优势病毒为非本地作物病原菌,包括葫芦蚜传黄病毒(CABYV)和葫芦黄发育障碍病毒(CYSDV)。有针对性的检测显示,多达88%的野生葫芦个体被CABYV感染,CABYV- cysdv双重感染在毗邻沙漠农业的自然地区很常见。在温室试验中,CABYV感染降低了两种野生葫芦的茎和根产量。系统发育分析表明,CABYV曾多次从其他大陆引入加州。我们的发现提供了有关的证据,证明人类活动可以改变野生植物的病毒压力,并可能导致植物衰退。
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来源期刊
CiteScore
7.40
自引率
6.80%
发文量
42
审稿时长
4 weeks
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