Post-transcriptional regulation of several biological processes involved in latex production in Hevea brasiliensis

Julie Leclercq; Shuangyang Wu; Benoît Farinas; Stéphanie Pointet; Bénédicte Favreau; Hélène Vignes; Kuswanhadi Kuswanhadi; Enrique Ortega-Abboud; Jean-François Dufayard; Shenghan Gao; Gaëtan Droc; Songnian Hu; Chaorong Tang; Pascal Montoro

doi:10.7717/peerj.8932

Post-transcriptional regulation of several biological processes involved in latex production in Hevea brasiliensis

PeerJ. 2020 Apr 29:8:e8932. doi: 10.7717/peerj.8932. eCollection 2020.

Authors

Julie Leclercq^#^{1

2}, Shuangyang Wu^#³, Benoît Farinas^{1

2}, Stéphanie Pointet^{1

2}, Bénédicte Favreau^{1

2}, Hélène Vignes^{1

2}, Kuswanhadi Kuswanhadi⁴, Enrique Ortega-Abboud^{1

2}, Jean-François Dufayard^{1

2}, Shenghan Gao³, Gaëtan Droc^{1

2}, Songnian Hu³, Chaorong Tang⁵, Pascal Montoro^{1

2}

Affiliations

¹ CIRAD, UMR AGAP, Montpellier, France.
² AGAP, University of Montpellier, CIRAD, INRAE, Institut Agro, Montpellier, France.
³ University of Chinese Academy of Sciences, CAS Key Laboratory of Genome Sciences and Information, Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, China.
⁴ Sembawa Research Centre, Indonesian Rubber Research Institute, Palembang, Indonesia.
⁵ Hainan University, College of Tropical Crops, Haikou, China.

^# Contributed equally.

Abstract

Background: Small RNAs modulate plant gene expression at both the transcriptional and post-transcriptional level, mostly through the induction of either targeted DNA methylation or transcript cleavage, respectively. Small RNA networks are involved in specific plant developmental processes, in signaling pathways triggered by various abiotic stresses and in interactions between the plant and viral and non-viral pathogens. They are also involved in silencing maintenance of transposable elements and endogenous viral elements. Alteration in small RNA production in response to various environmental stresses can affect all the above-mentioned processes. In rubber trees, changes observed in small RNA populations in response to trees affected by tapping panel dryness, in comparison to healthy ones, suggest a shift from a transcriptional to a post-transcriptional regulatory pathway. This is the first attempt to characterise small RNAs involved in post-transcriptional silencing and their target transcripts in Hevea.

Methods: Genes producing microRNAs (MIR genes) and loci producing trans-activated small interfering RNA (ta-siRNA) were identified in the clone PB 260 re-sequenced genome. Degradome libraries were constructed with a pool of total RNA from six different Hevea tissues in stressed and non-stressed plants. The analysis of cleaved RNA data, associated with genomics and transcriptomics data, led to the identification of transcripts that are affected by 20-22 nt small RNA-mediated post-transcriptional regulation. A detailed analysis was carried out on gene families related to latex production and in response to growth regulators.

Results: Compared to other tissues, latex cells had a higher proportion of transcript cleavage activity mediated by miRNAs and ta-siRNAs. Post-transcriptional regulation was also observed at each step of the natural rubber biosynthesis pathway. Among the genes involved in the miRNA biogenesis pathway, our analyses showed that all of them are expressed in latex. Using phylogenetic analyses, we show that both the Argonaute and Dicer-like gene families recently underwent expansion. Overall, our study underlines the fact that important biological pathways, including hormonal signalling and rubber biosynthesis, are subject to post-transcriptional silencing in laticifers.

Keywords: Abiotic stress; Crop epigenomics; Degradome; Latex; Rubber tree; Small RNA; miRNA.

Associated data

figshare/10.6084/m9.figshare.10264979.v1

Grants and funding

Shuangyang Wu benefited a scholarship from the UCAS Joint PhD Training Program. Julie Leclercq and Shuangyang Wu benefited a mobility program in 2018 from Campus France (Xu Guangqi Program no 41241QJ). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.