High-throughput deep sequencing reveals that microRNAs play important roles in salt tolerance of euhalophyte Salicornia europaea

Abstract

BackgroundmicroRNAs (miRNAs) are implicated in plant development processes and play pivotal roles in plant adaptation to environmental stresses. Salicornia europaea, a salt mash euhalophyte, is a suitable model plant to study salt adaptation mechanisms. S. europaea is also a vegetable, forage, and oilseed that can be used for saline land reclamation and biofuel precursor production on marginal lands. Despite its importance, no miRNA has been identified from S. europaea thus far.ResultsDeep sequencing was performed to investigate small RNA transcriptome of S. europaea. Two hundred and ten conserved miRNAs comprising 51 families and 31 novel miRNAs (including seven miRNA star sequences) belonging to 30 families were identified. About half (13 out of 31) of the novel miRNAs were only detected in salt-treated samples. The expression of 43 conserved and 13 novel miRNAs significantly changed in response to salinity. In addition, 53 conserved and 13 novel miRNAs were differentially expressed between the shoots and roots. Furthermore, 306 and 195 S. europaea unigenes were predicted to be targets of 41 conserved and 29 novel miRNA families, respectively. These targets encoded a wide range of proteins, and genes involved in transcription regulation constituted the largest category. Four of these genes encoding laccase, F-box family protein, SAC3/GANP family protein, and NADPH cytochrome P-450 reductase were validated using 5′-RACE.ConclusionsOur results indicate that specific miRNAs are tightly regulated by salinity in the shoots and/or roots of S. europaea, which may play important roles in salt tolerance of this euhalophyte. The S. europaea salt-responsive miRNAs and miRNAs that target transcription factors, nucleotide binding site-leucine-rich repeat proteins and enzymes involved in lignin biosynthesis as well as carbon and nitrogen metabolism may be applied in genetic engineering of crops with high stress tolerance, and genetic modification of biofuel crops with high biomass and regulatable lignin biosynthesis.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-015-0451-3) contains supplementary material, which is available to authorized users.

Solanum lycopersicum microRNA1916 targets multiple target genes and negatively regulates the immune response in tomato

“…Transcripts of UGT , MYB12 , and R1B‐16 with different lengths were obtained (Figure a), but all seemed to be either shorter or longer than the length of the cleaved transcripts predicted from the location of the canonical cleavage sites and showed the graphic display of 21‐nt siRNA arrays after the canonical cleavage site by sly‐miR1916 (Figure b). These cleavage sites could be due to other siRNA‐mediated cleavage, or DCL4 cleavage of the RDR6 product (Feng et al, ; Ronemus, Vaughn, & Martienssen, ). To further investigate whether overexpression and silencing of miR1916 can be affected by those putative miR1916 target genes, the transcript levels in the transgenic and wild‐type plants were analysed.…”

Genome‐wide identification and characterization of Eutrema salsugineummicroRNAs for salt tolerance

“…For example, miR167, miR171, miR319 and miR396 were previously shown to be upregulated in response to salt stress in Arabidopsi s using a microarray analysis (Liu et al ); bju‐miR160_1, bju‐miR390_1 and bju‐miR172_2 were downregulated under salt stresses in Brassica juncea , as determined using high‐throughput sequencing and TaqMan qRT‐PCR assays (Bhardwaj et al ). In addition, seu‐miR160a, seu‐miR164a‐5p, seu‐miR164b, seu‐miR164d, seu‐miR167e, seu‐miR172d, seu‐miR319a‐3p and seu‐miR396i were suppressed in salt‐treated euhalophyte Salicornia europaea shoots or roots, as determined using high‐throughput sequencing technology; whereas seu‐miR171b, seu‐miR396b and seu‐miR396c were upregulated (Feng et al ). Finally, hcmiR171b‐3p, hcmiR160a‐3p and hcmiR172e‐3p were downregulated by salinity stress, and hcmiR160 was upregulated in halophyte Halostachys caspica (Yang et al ).…”

“…Similar results have been reported in other studies. In S. europaea , miR319a‐3p was downregulated in root that was salt‐treated for 12 and 7 d, whereas the expression of miR319b was induced in the shoots and suppressed in the roots (Feng et al ). miR167 was induced in response to salt stress in poplar plantlets ( P. tremula ), while miR167h was suppressed (Jia et al ).…”

Computational prediction and experimental validation of a novel miRNA in Suaeda maritima, a halophyte

“…Ubiquitinprotein ligase serves as a unit of the ubiquitin/26S proteasome system, which is involved in polyubiquitination-mediated degradation of soluble proteins and influences their activity and abundance and thus affecting a variety of cellular functions. Suppression of the miRNA (seu-miR396h/I) that targets ubiquitin-specific protease, which is involved in protein degradation, has also been reported in the euhalophyte S. europaea during long-term salt treatment (Feng et al, 2015). The biological role of the ubiquitin/26S proteasome system has been investigated in relation to abiotic stress tolerance in plants, which can be positively or negatively regulated (Stone, 2014).…”

“…Sunkar and Zhu (2004) showed, for the first time, that upregulation of miR393, miR402, miR397b, and miR319c occurred in response to at least one of the following stresses; drought, cold, and salt. However, with regard to salt-responsiveness, research has mostly been carried out on test species that are either sensitive or naturally not tolerant to salt (Ding et al, 2009;De Paola et al, 2012), with the exclusion of studies by Khraiwesh et al (2013) and Feng et al (2015).…”