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Transcriptionally and Post-Transcriptionally Regulated Micrornas in Heat Stress Response in Barley

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Transcriptionally and Post-Transcriptionally Regulated Micrornas in Heat Stress Response in Barley Journal of Experimental Botany, Vol. 65, No. 20, pp. 6123–6135, 2014 doi:10.1093/jxb/eru353 Advance Access publication 2 September, 2014 This paper is available online free of all access charges (see http://jxb.oxfordjournals.org/open_access.html for further details) v RESEArCH PApEr Transcriptionally and post-transcriptionally regulated microRNAs in heat stress response in barley Katarzyna Kruszka1,*, Andrzej Pacak1,*, Aleksandra Swida-Barteczka1,*, Przemyslaw Nuc1, Sylwia Alaba2, Zuzanna Wroblewska1, Wojciech Karlowski2, Artur Jarmolowski1 and Zofia Szweykowska-Kulinska1,2,† Downloaded from https://academic.oup.com/jxb/article/65/20/6123/2485545 by guest on 30 September 2021 1 Department of Gene Expression, Institute of Molecular Biology and Biotechnology, Faculty of Biology, Adam Mickiewicz University in Poznan, Umultowska 89, 61-614 Poznan, Poland 2 Bioinformatics Laboratory, Institute of Molecular Biology and Biotechnology, Faculty of Biology, Adam Mickiewicz University in Poznan, Umultowska 89, 61-614 Poznan, Poland * These authors contributed equally to this work. † To whom correspondence should be addressed. E-mail: [email protected] Received 16 April 2014; Revised 28 July 2014; Accepted 29 July 2014 Abstract Heat stress is one of the major abiotic factors that can induce severe plant damage, leading to a decrease in crop plant productivity. Despite barley being a cereal of great economic importance, few data are available concerning its thermotolerance mechanisms. In this work microRNAs (miRNAs) involved in heat stress response in barley were investigated. The level of selected barley mature miRNAs was examined by hybridization. Quantitative real-time PCR (RT-qPCR) was used to monitor the changes in the expression profiles of primary miRNA (pri-miRNA) precursors, as well as novel and conserved target genes during heat stress. The miRNA-mediated cleavage sites in the target tran- scripts were confirmed by degradome analysis and the 5’ RACE (rapid amplification of cDNA ends) approach. Four barley miRNAs (miR160a, 166a, 167h, and 5175a) were found which are heat stress up-regulated at the level of both mature miRNAs and precursor pri-miRNAs. Moreover, the splicing of introns hosting miR160a and miR5175a is also heat induced. The results demonstrate transcriptional and post-transcriptional regulation of heat-responsive miRNAs in barley. The observed induction of miRNA expression is correlated with the down-regulation of the expression level of their experimentally identified new and conservative target genes. Key words: Barley, heat stress, microRNA, pri-miRNA, splicing, target gene. Introduction Plants as sessile organisms have developed exceptional abili- elegans (Lee et al., 1993), miRNAs have been detected in all ties to cope with multiple environmental stimuli. The expo- multicellular eukaryotic organisms (Reinhart et al., 2002; sure to various stressful environmental conditions requires Lagos-Quintana et al., 2003). the induction of proper molecular responses operating at MiRNAs are short 20–22 nucleotide (nt) long small RNAs the transcriptional, post-transcriptional, translational, and that play a regulatory role in response to environmental post-translational levels (Banival et al., 2004; Sunkar, 2010). stimuli, plant development, or signal transduction (Lu and The importance of microRNAs (miRNAs) as key regulators Huang, 2008; Kruszka et al., 2012; Nozawa et al., 2012). of gene expression at the post-transcriptional level has been Plant miRNAs are produced from primary (pri-miRNA) widely documented (Mallory and Vaucheret, 2006; Sunkar, precursors that contain a characteristic hairpin structure 2010; Bielewicz et al., 2013). First identified inCaenorhabditis with the miRNA/miRNA* duplex located within the hairpin © The Author 2014. Published by Oxford University Press on behalf of the Society for Experimental Biology. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. 6124 | Kruszka et al. stem (Reinhart et al., 2002). The miRNA/miRNA* duplex is Barley (Hordeum vulgare) grain production ranks fourth diced out from the precursor by a DCL1 enzyme (Kurihara in global cereal production (FAO, http://www.fao.org), indi- and Watanabe, 2004), which, accompanied mainly by a cating the economic importance of this monocotyledonous SERRATE (SE) and a HYPONASTIC LEAVES 1 (HYL1), crop plant. For spring barley, an air temperature ~20–25 ºC is forms a microprocessing complex (Kurihara et al., 2006; considered to be optimum for growth and development. An Yang et al., 2006) that ensures efficiency and accuracy of increase in temperature above these values often results in the precursor processing to mature miRNA (Dong et al., 2008). reduction of agricultural productivity (Acevedo et al., 2002; Subsequently, the miRNA/miRNA* duplex is exported to Hossain et al., 2012). Hence the importance of determin- the cytoplasm in a HASTY (HST)-dependent manner (Park ing and understanding the biological factors and processes et al., 2005), where the miRNA guide strand is selectively involved in heat response in plants. loaded into an ARGONAUTE1 (AGO1)-containing RNA- It was considered to be of interest to find out whether induced silencing complex (RISC) (Vaucheret et al., 2004; barley miRNAs might function in response to high tem- Baumberger and Baulcombe, 2005). MiRNAs regulate gene perature and what might be the mechanisms regulating the expression in a sequence-specific manner (Baulcombe, 2004; miRNA biogenesis upon heat stress. Here it is shown that Voinnet, 2009) by targeting mRNAs for cleavage or trans- four mature miRNAs—miR160a, 166a, 167h, and 5175a— Downloaded from https://academic.oup.com/jxb/article/65/20/6123/2485545 by guest on 30 September 2021 lational repression (Bartel, 2004; Brodersen et al., 2008; are up-regulated under heat stress in barley. The studies also Beauclair et al., 2010). revealed that the level of their pri-miRNAs was affected in MiRNAs have two major physiological roles in plants: (i) the heat stress conditions. Surprisingly, the splicing of the inducing cell differentiation in response to an endogenous intron-containing precursors pri-miR160a and pri-miR5175a stimulus during development and (ii) activation of an adap- was induced by heat and correlated with the accumulation tive response to a particular exogenous stress. A number of of mature miRNAs, suggesting the post-trancriptional regu- miRNAs have been demonstrated to function in biotic and lation of miRNA precursor processing. Furthermore, con- abiotic stress responses in plants (Sunkar and Zhu, 2004; served (HD-Zip transcription factors and auxin response Khraiwesh et al., 2012; Kruszka et al., 2012; Bielewicz et al., factors) as well as novel target genes (HOX9, ACC oxidase, 2013). The role of miRNAs in plants infected by pathogenic and Nek5-like kinase) of the heat-responsive barley miRNAs bacteria, viruses, nematodes, and fungi has been widely were experimentally identified using the ′5 rapid amplification reported (Ruiz-Ferrer and Voinnet, 2009; Katiyar-Agarwal of cDNA ends (RACE) approach and the degradome data. and Jin, 2010). Plant miRNAs have also been reported to The level of target genes is regulated through a slicing mecha- play an important role in response to cold (Sunkar and Zhu, nism, and it was experimentally confirmed that the level of 2004; Zhang et al., 2009; Lv et al., 2010), drought (Bartels the putative target mRNAs was down-regulated in heat stress and Sunkar, 2005; Liu et al., 2008; Jian et al., 2010; Pieczynski conditions. A miRNA–target gene network in response to et al., 2013), salt (Liu et al., 2008; Zhao et al., 2009), or oxida- heat stress in barley is discussed. The results of the present tive stresses induced by heavy metals, salinity, and nutrient study shed new light on the regulation of miRNA precursors deficiency (Sunkar et al., 2006; Jagadeeswaran et al., 2009). and mature miRNA biogenesis, and indicate the important Heat stress is one of the major abiotic stresses that can role of miRNAs in response to heat stress in barley. induce severe plant damage (Baniwal et al., 2004; Wahid et al., 2007). Given the increasing amount of evidence for worldwide climate change, the possible consequences of a Materials and methods temperature increase are a concern not only for climatolo- gists but also for farmers and crop breeders. Heat stress is Plant material and stress conditions very often accompanied by drought, and these two com- Spring barley plants, cultivar Rolap (Devaux et al., 1992), were bined stressful conditions are the major limitations to food grown in a Conviron environmental chamber (Conviron, Winnipeg, Manitoba, Canada) with a 16 h day/8 h night photoperiod, and production worldwide, especially in areas that use rainfed 800 μmol light conditions. Plants were grown at 22 ºC day/15 ºC agriculture. Observed in recent decades, global warm- night temperature in 250 ml pots containing field soil, and were ing is predicted to have a general negative effect on plant watered to maintain optimal growth conditions of 70% SWC (soil growth, development, and reproduction mostly due to the water content). Two-week-old plants at the three-leaf stage (code destructive effect of high temperature (Bita and Gerats, 13 of Zadoks system; Zadoks et al., 1974) were subjected to heat treatment at 35.5 ºC.
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