Citrus exocortis viroid causes ribosomal stress in tomato plants

• Published in: Nucleic acids research Vol. 47; no. 16; pp. 8649 - 8661
• Main Authors: Cottilli, Patrick, Belda-Palazón, Borja, Adkar-Purushothama, Charith Raj, Perreault, Jean-Pierre, Schleiff, Enrico, Rodrigo, Ismael, Ferrando, Alejandro, Lisón, Purificación
• Format: Journal Article
• Language: English
• Published: England Oxford University Press 19-09-2019
• Subjects: Citrus - virology; Host-Pathogen Interactions - genetics; Lycopersicon esculentum - genetics; Lycopersicon esculentum - metabolism; Lycopersicon esculentum - virology; Molecular Biology; Organelle Biogenesis; Plant Diseases - genetics; Plant Diseases - virology; Plant Leaves - genetics; Plant Leaves - metabolism; Plant Leaves - virology; Protein Biosynthesis; Ribosomal Proteins - genetics; Ribosomal Proteins - metabolism; Ribosomes - genetics; Ribosomes - metabolism; RNA Interference; RNA, Plant - antagonists & inhibitors; RNA, Plant - genetics; RNA, Plant - metabolism; RNA, Ribosomal, 18S - antagonists & inhibitors; RNA, Ribosomal, 18S - genetics; RNA, Ribosomal, 18S - metabolism; RNA, Viral - genetics; RNA, Viral - metabolism; Stress, Physiological - genetics; Viroids - genetics; Viroids - metabolism; Viroids - pathogenicity
• ISSN: 0305-1048; 1362-4962
• DOI: 10.1093/nar/gkz679

Viroids are naked RNAs that do not code for any known protein and yet are able to infect plants causing severe diseases. Because of their RNA nature, many studies have focused on the involvement of viroids in RNA-mediated gene silencing as being their pathogenesis mechanism. Here, the alterations caused by the Citrus exocortis viroid (CEVd) on the tomato translation machinery were studied as a new aspect of viroid pathogenesis. The presence of viroids in the ribosomal fractions of infected tomato plants was detected. More precisely, CEVd and its derived viroid small RNAs were found to co-sediment with tomato ribosomes in vivo, and to provoke changes in the global polysome profiles, particularly in the 40S ribosomal subunit accumulation. Additionally, the viroid caused alterations in ribosome biogenesis in the infected tomato plants, affecting the 18S rRNA maturation process. A higher expression level of the ribosomal stress mediator NAC082 was also detected in the CEVd-infected tomato leaves. Both the alterations in the rRNA processing and the induction of NAC082 correlate with the degree of viroid symptomatology. Taken together, these results suggest that CEVd is responsible for defective ribosome biogenesis in tomato, thereby interfering with the translation machinery and, therefore, causing ribosomal stress.