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Transcriptome and Degradome Sequencing Reveals Dormancy Mechanisms of Cunninghamia Lanceolata Seeds1

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Transcriptome and Degradome Sequencing Reveals Dormancy Mechanisms of Cunninghamia Lanceolata Seeds1 Transcriptome and Degradome Sequencing Reveals Dormancy Mechanisms of Cunninghamia lanceolata Seeds1 Dechang Cao2,HuiminXu2, Yuanyuan Zhao, Xin Deng, Yongxiu Liu, Wim J.J. Soppe, and Jinxing Lin* Key Laboratory for Genetics and Breeding of Forest Trees and Ornamental Plants of Ministry of Education, College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing 100083, China (D.C., H.X., Y.Z., J.L.); Key Laboratory of Plant Resources, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China (X.D., Y.L., J.L.); Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, Jena 07745, Germany (D.C.); and Department of Plant Breeding and Genetics, Max Planck Institute for Plant Breeding Research, Cologne 50829, Germany (W.J.J.S.) ORCID IDs: 0000-0002-0397-4316 (D.C.); 0000-0002-9955-2467 (Y.Z.); 0000-0002-6075-2429 (X.D.). Seeds with physiological dormancy usually experience primary and secondary dormancy in the nature; however, little is known about the differential regulation of primary and secondary dormancy. We combined multiple approaches to investigate cytological changes, hormonal levels, and gene expression dynamics in Cunninghamia lanceolata seeds during primary dormancy release and secondary dormancy induction. Light microscopy and transmission electron microscopy revealed that protein bodies in the embryo cells coalesced during primary dormancy release and then separated during secondary dormancy induction. Transcriptomic profiling demonstrated that expression of genes negatively regulating gibberellic acid (GA) sensitivity reduced specifically during primary dormancy release, whereas the expression of genes positively regulating abscisic acid (ABA) biosynthesis increased during secondary dormancy induction. Parallel analysis of RNA ends revealed uncapped transcripts for ;55% of all unigenes. A negative correlation between fold changes in expression levels of uncapped versus capped mRNAs was observed during primary dormancy release. However, this correlation was loose during secondary dormancy induction. Our analyses suggest that the reversible changes in cytology and gene expression during dormancy release and induction are related to ABA/GA balance. Moreover, mRNA degradation functions as a critical posttranscriptional regulator during primary dormancy release. These findings provide a mechanistic framework for understanding physiological dormancy in seeds. Seed dormancy mediates the crucial interaction be- various classes of dormancy to regulate the timing of tween the environment and the plant life cycle transi- seed germination, help seedlings emerge under favor- tion from durable seeds to vulnerable seedlings (Willis able conditions, and maximize the growing season et al., 2014). Different plant species have adopted (Baskin and Baskin, 2004; Donohue et al., 2010). Phys- iological dormancy, the most widely occurring type, is caused by inadequate growth potential of the embryo, 1 This work was supported by the National Natural Science Foun- which prevents it from overcoming the resistance of its dation of China (31370212 and 31270224), by the Beijing Advanced surrounding tissues (Baskin and Baskin, 2014). Seeds Innovation Center for Tree Breeding by Molecular Design, by the with physiological dormancy can change their degree Programme of Introducing Talents of Discipline to Universities of dormancy, a process known as dormancy cycling: (111 Project, B13007), by the Programme for Changjiang Scholars and Innovative Research Team in University (IRT13047), and by the Primary dormant seeds enter nondormancy during China Postdoctoral Science Foundation (2013M530536 and seasons favorable for germination, and nondormant 2015M570943). seeds may reenter dormancy (secondary dormancy) 2 These authors contributed equally to the article. under unfavorable conditions if they have not germi- * Address correspondence to [email protected]. nated (Footitt et al., 2011; Cao et al., 2014). Due to the The author responsible for distribution of materials integral to the importance of seed dormancy in the plant life cycle, findings presented in this article in accordance with the policy de- particularly in agriculture and vegetative restoration, scribed in the Instructions for Authors (www.plantphysiol.org) is: many studies have focused on the regulatory mecha- Jinxing Lin ([email protected]). nisms underlying seed dormancy. D.C. and J.L. conceived the project idea and designed the experi- Genetic studies have revealed some genes that reg- ments; D.C. and H.X. performed the experiments; D.C. performed the data analysis and prepared the figures and tables; W.J.J.S., X.D., Y.L., ulate seed dormancy and germination, especially genes and Y.Z. advised on the analysis and interpretation of the results; involved in abscisic acid (ABA) and gibberellic acid D.C. and H.X. did most of the writing of the manuscript in consulta- (GA) pathways (Shu et al., 2013; Vaistij et al., 2013; tion with all others; all authors approved the final manuscript. Wang et al., 2013). Also exogenous application of these www.plantphysiol.org/cgi/doi/10.1104/pp.16.00384 phytohormones modifies seed germination (Ogawa Ò Plant Physiology , December 2016, Vol. 172, pp. 2347–2362, www.plantphysiol.org Ó 2016 American Society of Plant Biologists. All Rights Reserved. 2347 Downloaded from on January 31, 2020 - Published by www.plantphysiol.org Copyright © 2016 American Society of Plant Biologists. All rights reserved. Cao et al. et al., 2003; Oh et al., 2007), suggesting that they play a volume of 734 million m3; State Forest Administration central role in the physiological dormancy of seeds. P.R. China, 2014). Due to the rapid growth and com- Recently, emerging “-omics” technologies have in- mercial importance, much effort has focused on exploring creased our understanding of the regulation of physi- the regulatory mechanisms underlying wood production ological dormancy at the whole-genome level. Indeed, and reproduction of this species, and high-throughput species of stored mRNAs account for more than half of sequencing technologies have been used extensively in the genome mRNAs in dry Arabidopsis (Arabidopsis recent years to identify functional genes in this species thaliana) seeds (Nakabayashi et al., 2005), and numer- (Shi et al., 2010; Wan et al., 2012; Qiu et al., 2013). ous genes with various functions show differential ex- To increase our understanding of the regulatory pression during dormancy release, indicating that a mechanisms underlying seed dormancy in trees, we highly complex network regulates seed dormancy, in applied light microscopy and transmission electron mi- addition to the crucial roles of ABA and GA (Cadman croscopy to investigate the cellular and subcellular et al., 2006; Carrera et al., 2008). changes that occur during dormancy release and in- Despite the distinct gene expression programs between duction in C. lanceolata seeds. We also profiled global dormant and nondormant seeds (Cadman et al., 2006; mRNA expression in C. lanceolata seeds with various Carrera et al., 2008), little is known about the regulation of dormancy statuses (primary dormancy, secondary dor- gene expression during dormancy release. mRNA deg- mancy, and nondormancy) to explore the regulatory radation is involved in rapid changes and precise ad- network of seed dormancy. Furthermore, we used PARE justments in gene expression in eukaryotic cells (Goeres to investigate the role of mRNA degradation in gene et al., 2007; Belasco, 2010; Haimovich et al., 2013), expression of C. lanceolata seeds. The long-term objective and mRNA decapping mediated by decapping en- of our research is to provide reference maps of the reg- zymes (DCPs) represents a crucial step in bulk mRNA ulatory mechanisms underlying seed dormancy, with an degradation (Coller and Parker, 2004; Franks and Lykke- emphasis on the regulation of orchestrated gene ex- Andersen, 2008), after which decapped mRNA interme- pression during dormancy release and induction. diates are digested by the 59-39 exonuclease XRN1 or degraded in 39-59 orientation by the exosome complex (Houseley and Tollervey, 2009; Haimovich et al., 2013). RESULTS Alternatively, mRNA degradation can be initiated by in- ternal cleavage by endonucleases or small RNAs, in- Obtaining C. lanceolata Seeds with Various cluding microRNAs (miRNAs) and small interfering Dormancy Statuses RNAs (Houseley and Tollervey, 2009; Belasco, 2010). Both To obtain seeds with various dormancy statuses, we the activity of decapping enzymes and internal cleavage first tested the germination percentages of seeds that had by endonucleases and small RNAs produce uncapped 9 been subjected to different environmental conditions (Fig. mRNAs, which are characterized by a 5 monophosphate 1A). C. lanceolata seeds maintained relatively high germi- and a shortened poly(A) tail (Jiao et al., 2008). In addition, nation percentages at 30°C throughout the experiment (Fig. nonsense-mediated mRNA decay also produces uncap- 1, B and C). The freshly matured seeds germinated to ped mRNAs (Schoenberg and Maquat, 2012). Parallel 6 fi 48.7% 3.0% at 20°C, and germination gradually in- analysis of RNA ends (PARE), which was rst developed creased in response to cold stratification, increasing sig- to identify miRNA cleavage on target mRNAs (German fi , 6 fi ni cantly (P 0.05) to 70.8% 3.2% after 12 d of cold et al., 2008), has been proven a powerful tool for pro ling stratification (Fig. 1B). After eight additional days of cold uncapped mRNAs in eukaryotic
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