Comparative transcriptome profiling of Pyropia yezoensis (Ueda) M.S. Hwang & H.G. Choi in response to temperature stresses

Sun et al. BMC Genomics (2015) 16:463 DOI 10.1186/s12864-015-1586-1 RESEARCH ARTICLE Open Access Comparative transcriptome profiling of Pyropia yezoensis (Ueda) M.S. Hwang & H.G. Choi in response to temperature stresses Peipei Sun1, Yunxiang Mao1*, Guiyang Li2, Min Cao1, Fanna Kong1, Li Wang3 and Guiqi Bi1 Abstract Background: Pyropia yezoensis is a model organism often used to investigate the mechanisms underlying stress tolerance in intertidal zones. The digital gene expression (DGE) approach was used to characterize a genome-wide comparative analysis of differentially expressed genes (DEGs) that influence the physiological, developmental or biochemical processes in samples subjected to 4 treatments: high-temperature stress (HT), chilling stress (CS), freezing stress (FS) and normal temperature (NT). Results: Equal amounts of total RNAs collected from 8 samples (two biological replicates per treatment) were sequenced using the Illumina/Solexa platform. Compared with NT, a total of 2202, 1334 and 592 differentially expressed unigenes were detected in HT, CS and FS respectively. Clustering analysis suggested P. yezoensis acclimates to low and high-temperature stress condition using different mechanisms: In heat stress, the unigenes related to replication and repair of DNA and protein processing in endoplasmic reticulum were active; however at low temperature stresses, unigenes related to carbohydrate metabolism and energy metabolism were active. Analysis of gene differential expression showed that four categories of DEGs functioning as temperature sensors were found, including heat shock proteins, H2A, histone deacetylase complex and transcription factors. Heat stress caused chloroplast genes down-regulated and unigenes encoding metacaspases up-regulated, which is an important regulator of PCD. Cold stress caused an increase in the expression of FAD to improve the proportion of polyunsaturated fatty acids. An up-regulated unigene encoding farnesyl pyrophosphate synthase was found in cold stress, indicating that the plant hormone ABA also played an important role in responding to temperature stress in P. yezoensis. Conclusion: The variation of amount of unigenes and different gene expression pattern under different temperature stresses indicated the complicated and diverse regulation mechanism in response to temperature stress in P. yezoensis. Several common metabolism pathways were found both in P. yezoensis and in higher plants, such as FAD in low-temperature stress and HSP in heat stress. Meanwhile, many chloroplast genes and unigene related to the synthesis of abscisic acid were detected, revealing its unique temperature-regulation mechanism in this intertidal species. This sequencing dataset and analysis may serve as a valuable resource to study the mechanisms involved in abiotic stress tolerance in intertidal seaweeds. Keywords: Pyropia yezoensis, RNA-seq, High temperature stress, Chilling stress, Freezing stress, DGE, Transcriptome Background Because plants lack the ability of locomotion, they are exposed to various environmental stresses. Temperature stress is the most common type of stress to which plants are subjected. Temperature-related stress can occur at * Correspondence: 1 Key Laboratory of Marine Genetics and Breeding (MOE), College of Marine Life Sciences, Ocean University of China, Qingdao 266003, China Full list of author information is available at the end of the article (a) temperatures below freezing, (b) low temperatures above freezing, and (c) high temperatures [1]. Stressful temperature conditions can damage the enzymes needed for photosynthesis, respiration, and protein synthesis and so affect the growth and development of plants [2]. Consequently, plants have evolved mechanisms to monitor their environments and to respond with cellular, physiological, and developmental changes to optimize growth and reproductive success. © 2015 Sun et al. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http:// creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Sun et al. BMC Genomics (2015) 16:463 Intertidal seaweeds inhabit an inherently stressful environment with rapidly changing physical conditions. Seaweed in this zone undergoes extreme environmental changes that include desiccation, osmotic shock, exposure to intense sunlight, and high and freezing temperatures. A better understanding of the mechanisms involved in abiotic stress tolerance in seaweeds could help elucidate their successful survival, reproduction, and distribution in the intertidal region. Transcriptome analysis is an efficient way of achieving this goal. A transcriptome is a complete set of the transcripts in a cell that becomes active at a specific developmental stage or under certain physiological conditions. Transcriptomes provide information that can be used to identify the functional elements of the genome and the molecular constituents of cells and tissues [3]. Digital gene expression (DGE), which is based on the sequencing of genome-wide expression profiles, is an efficient method that can be used to analyze transcriptome data and so identify, quantify, and annotate expressed genes at the genome level even without prior sequence knowledge. This allows for higher confidence in target discovery and pathway studies. Currently, this technique is widely used in higher plant research. In the Chinese bayberry (Myrica rubra), it has been used to examine gene expression in developing bayberry fruit. Results showed energy-related metabolism to be enhanced and all genes involved in anthocyanin biosynthesis to be up-regulated during the fruit ripening processes [4]. In Lycoris sprengeri, DGE was performed to evaluate differential gene expression between bulbs and bulblets and determine the biological and molecular mechanisms underlying bulb development [5]. In Vitis vinifera, it was used to describe how plant transcriptomes change during three developmental stages, post setting, veraison, and ripening [6]. Pyropia yezoensis (Ueda), M.S. Hwang & H.G. Choi, one of the most economically important marine crops, is widely cultivated in China, Japan, and Korea, with an annual harvest of more than 1 million tons (fresh weight) and a value of over U.S. $1.5 billion per year (http://www.fao.org/fishery/statistics/en). P. yezoensis is naturally distributed in the intertidal zone of the temperate region in the northern hemisphere. In this region, the temperature may change dramatically between seawater and air, especially in the changeover seasons between autumn and winter as well as winter and spring. The thallus of P. yezoensis is totally submerged (...truncated)