Phytoplasma-Responsive microRNAs Modulate Hormonal, Nutritional, and Stress Signalling Pathways in Mexican Lime Trees

Farveh Ehya,Laleh Karimi Farsad,Ehsan Mohseni Fard,Mojtaba Khayam Nekouei,Ghasem Hosseini Salekdeh,Aboozar Monavarfeshani,Mohsen Mardi,Gustavo Bonaventure

doi:10.1371/journal.pone.0066372

Abstract

BackgroundWitches’ broom disease of Mexican lime (Citrus aurantifolia L.), which is associated to the phytoplasma ‘Candidatus Phytoplasma aurantifolia’, is a devastating disease that results in significant economic losses. Plants adapt to biotic stresses by regulating gene expression at the transcriptional and post-transcriptional levels. MicroRNAs (miRNAs) are a recently identified family of molecules that regulate plant responses to environmental stresses through post-transcriptional gene silencing.MethodsUsing a high-throughput approach to sequence small RNAs, we compared the expression profiles of miRNAs in healthy Mexican lime trees and in plants infected with ‘Ca. P. aurantifolia’.ResultsOur results demonstrated the involvement of different miRNAs in the response of Mexican lime trees to infection by ‘Ca. P. aurantifolia’. We identified miRNA families that are expressed differentially upon infection with phytoplasmas. Most of the miRNAs had variants with small sequence variations (isomiRs), which are expressed differentially in response to pathogen infection.ConclusionsIt is likely that the miRNAs that are expressed differentially in healthy and phytoplasma-infected Mexican lime trees are involved in coordinating the regulation of hormonal, nutritional, and stress signalling pathways, and the complex interactions between them. Future research to elucidate the roles of these miRNAs should improve our understanding of the level of diversity of specific plant responses to phytoplasmas.

Highlights

Witches’ broom disease of Mexican lime (Citrus aurantifolia L.) is a devastating disease that results in significant economic losses [1]
The raw small RNA data were submitted to Gene Expression Omnibus (GEO) under accession no
Identification of Known miRNAs To identify known miRNAs, all the sequences obtained after the data-cleaning procedure from both healthy and infected plants were used to interrogate the in-house C. aurantifolia EST sequences and citrus ESTs in the NCBI databases to identify orthologous and paralogous miRNA sequences with an identity of at least 18 nt, and no more than 3 mismatched nt

Summary

Introduction

Witches’ broom disease of Mexican lime (Citrus aurantifolia L.) is a devastating disease that results in significant economic losses [1]. It is associated to ‘Candidatus Phytoplasma aurantifolia’, an obligate biotrophic plant pathogen Since it was first reported in the northern coastal plain of the Sultanate of Oman in the 1980s, witches’ broom disease has spread throughout the region and has affected Mexican lime trees in southern Iran [2,3]. The symptoms of witches’ broom disease include the development of many thin secondary shoots, each with shortened internodes, which develop from axillary buds that normally stay dormant Many of these shoots, the so-called ‘witches’ brooms’, appear during the advanced stages of the disease. Witches’ broom disease of Mexican lime (Citrus aurantifolia L.), which is associated to the phytoplasma ‘Candidatus Phytoplasma aurantifolia’, is a devastating disease that results in significant economic losses. MicroRNAs (miRNAs) are a recently identified family of molecules that regulate plant responses to environmental stresses through post-transcriptional gene silencing

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