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Global alteration of microRNAs and transposon-derived small RNAs in cotton (Gossypium hirsutum) during Cotton leafroll dwarf polerovirus (CLRDV) infection

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Abstract

Small RNAs (sRNAs) are a class of non-coding RNAs ranging from 20- to 40-nucleotides (nts) that are present in most eukaryotic organisms. In plants, sRNAs are involved in the regulation of development, the maintenance of genome stability and the antiviral response. Viruses, however, can interfere with and exploit the silencing-based regulatory networks, causing the deregulation of sRNAs, including small interfering RNAs (siRNAs) and microRNAs (miRNAs). To understand the impact of viral infection on the plant sRNA pathway, we deep sequenced the sRNAs in cotton leaves infected with Cotton leafroll dwarf virus (CLRDV), which is a member of the economically important virus family Luteoviridae. A total of 60 putative conserved cotton miRNAs were identified, including 19 new miRNA families that had not been previously described in cotton. Some of these miRNAs were clearly misregulated during viral infection, and their possible role in symptom development and disease progression is discussed. Furthermore, we found that the 24-nt heterochromatin-associated siRNAs were quantitatively and qualitatively altered in the infected plant, leading to the reactivation of at least one cotton transposable element. This is the first study to explore the global alterations of sRNAs in virus-infected cotton plants. Our results indicate that some CLRDV-induced symptoms may be correlated with the deregulation of miRNA and/or epigenetic networks.

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Acknowledgments

We thank the Brazilian sponsoring agency CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico, 150639/2010-4-PDJ) for financial support to CEGS and a postdoctoral fellowship to ER, FAPERJ (Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro) for financial support to MFSV through APQ1 E26/110.264/2010 and Pensa Rio E-26/110.324/2010, and CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) for the studentship to TFS. This work is part of the PhD thesis written by TFS for the Programa de Biotecnologia Vegetal from Universidade Federal do Rio de Janeiro, Brazil. We also thank Magne Osteras, Cécile Deluen, Christelle Barras, Elisabeth Dieterle and Patricia O. Hernandez from Fasteris Co. for technical assistance with deep sequencing and Tereza Galvão Carvalho from UFRJ for helping with plant care and RNA extractions. We thank Dr. Rogério Margis from UFRGS for exciting and helpful discussions and Dr. Marie-Anne and her students at USP for stimulating discussions and help with the bioinformatics programs used to study TEs.

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Authors and Affiliations

  1. Departamento de Genética, Instituto de Biologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

    Elisson Romanel, Régis L. Corrêa & Carlos E. G. Schrago

  2. Departamento de Virologia, Instituto de Microbiologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

    Tatiane F. Silva & Maite F. S. Vaslin

  3. Fasteris SA, Plan-les-Ouates, Switzerland

    Laurent Farinelli

  4. Department of Biology, West Virginia University, Morgantown, WV, 26506, USA

    Jennifer S. Hawkins

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  3. Régis L. Corrêa
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Corresponding author

Correspondence to Maite F. S. Vaslin.

Additional information

Elisson Romanel and Tatiane F. Silva contributed equally to the production of the paper.

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11103_2012_9959_MOESM1_ESM.ppt

Figure S1: The percentage of 5′ nt identities of Gossypium hirsutum small RNA (sRNA) in uninfected (UIL) and infected (IL) libraries. The percentage of 5’ nt identities among the 18-26 nt sRNA classes from the unique (A and B) and redundant (C and D) data are shown. sRNAs sequences (reads) beginning with A (red), C (orange), G (yellow), and U (green) are indicated for each size class. A and C – The data from the uninfected library. B and D – The data from the infected library. (PPT 162 kb)

11103_2012_9959_MOESM2_ESM.ppt

Figure S2: Predicted stem-loop hairpin secondary structures of four new miRNAs identified in conserved cotton miRNAs families. Stem-loop structures of the novel conserved miRNAs Ghr-miR172f (A) and Ghr-miR319a (B) deduced from the Gossypium raimondii genome. Stem-loop structures of the novel conserved miRNAs Ghr-miR393c (C) and Ghr-miR3476a (D) deduced from G. hirsutum ESTs. The red lines indicate the position of the mature miRNA sequences. The pre-miRNA sequences used for Ghr-miR172, Ghr-miR319, Ghr-miR393 and Ghr-miR3476 were gnl|ti|2101390498 FITC127369.g1, gnl|ti|2102160818 FONU88474.g1, TA29056_3635 and DW497660, respectively. (PPT 223 kb)

11103_2012_9959_MOESM3_ESM.ppt

Figure S3: Effects of CLRDV infection on cotton 20, 22 and 24-nt miRNA expression. Comparative analysis of the cotton 20, 22 and 24-nt miRNAs families identified in the uninfected (UIL) and CLRDV-infected (IL) deep-sequencing libraries. Histograms represent the percentage of miRNA families. Only miRNA families with more than four reads in at least one library and containing reads in both libraries were analyzed. (PPT 276 kb)

11103_2012_9959_MOESM4_ESM.ppt

Figure S4: Determining specificity of RT-qPCR TE-specific primers. Melting curves of the retrotransposons from Gossypium hirsutum Gypsy 2, Copia 1 and Copia 2 showing the amplification of a single product and Gypsy 1 showing multiple products after RT-qPCR analysis using SYBRGreen. (PPT 1080 kb)

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Romanel, E., Silva, T.F., Corrêa, R.L. et al. Global alteration of microRNAs and transposon-derived small RNAs in cotton (Gossypium hirsutum) during Cotton leafroll dwarf polerovirus (CLRDV) infection. Plant Mol Biol 80, 443–460 (2012). https://doi.org/10.1007/s11103-012-9959-1

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