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Transcriptomic Analysis of Soil-Grown Arabidopsis Thaliana Roots and Shoots in Response to a Drought Stress

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Transcriptomic Analysis of Soil-Grown Arabidopsis Thaliana Roots and Shoots in Response to a Drought Stress ORIGINAL RESEARCH published: 23 February 2016 doi: 10.3389/fpls.2016.00180 Transcriptomic Analysis of Soil-Grown Arabidopsis thaliana Roots and Shoots in Response to a Drought Stress Sultana Rasheed 1, 2, Khurram Bashir 1, Akihiro Matsui 1, Maho Tanaka 1 and Motoaki Seki 1, 2, 3* 1 Plant Genomic Network Research Team, RIKEN Center for Sustainable Resource Sciences, Yokohama, Japan, 2 Kihara Institute for Biological Research, Yokohama City University, Yokohama, Japan, 3 CREST, Japan Science and Technology Agency, Saitama, Japan Drought stress has a negative impact on crop yield. Thus, understanding the molecular mechanisms responsible for plant drought stress tolerance is essential for improving this beneficial trait in crops. In the current study, a transcriptional analysis was conducted of gene regulatory networks in roots of soil-grown Arabidopsis plants in response to a drought stress treatment. A microarray analysis of drought-stressed roots and shoots was performed at 0, 1, 3, 5, 7, and 9 days. Results indicated that the expression of many drought stress-responsive genes and abscisic acid biosynthesis-related genes Edited by: was differentially regulated in roots and shoots from days 3 to 9. The expression of Mohammad Anwar Hossain, cellular and metabolic process-related genes was up-regulated at an earlier time-point Bangladesh Agricultural University, Bangladesh in roots than in shoots. In this regard, the expression of genes involved in oxidative Reviewed by: signaling, chromatin structure, and cell wall modification also increased significantly in Biswapriya Biswavas Misra, roots compared to shoots. Moreover, the increased expression of genes involved in University of Florida, USA Byeong-ha Lee, the transport of amino acids and other solutes; including malate, iron, and sulfur, was Sogang University, South Korea observed in roots during the early time points following the initiation of the drought *Correspondence: stress. These data suggest that plants may utilize these signaling channels and metabolic Motoaki Seki adjustments as adaptive responses in the early stages of a drought stress. Collectively, [email protected] the results of the present study increases our understanding of the differences pertaining Specialty section: to the molecular mechanisms occurring in roots vs. shoots in response to a drought This article was submitted to stress. Furthermore, these findings also aid in the selection of novel genes and promoters Plant Biotechnology, a section of the journal that can be used to potentially produce crop plants with increased drought tolerance. Frontiers in Plant Science Keywords: abiotic stresses, abscisic acid, Arabidopsis thaliana, drought, microarray, transcription factors Received: 24 December 2015 Accepted: 02 February 2016 Published: 23 February 2016 INTRODUCTION Citation: Rasheed S, Bashir K, Matsui A, Adverse environmental factors, such as drought stress, severely limit agricultural production and Tanaka M and Seki M (2016) reduce the yield and quality of crop plants. Water scarcity is predicted to increase as an outcome Transcriptomic Analysis of Soil-Grown Arabidopsis thaliana Roots and of climate change, and thus poses a serious challenge to agricultural production worldwide. Shoots in Response to a Drought Understanding the molecular response of plants to a drought stress and utilizing this knowledge Stress. Front. Plant Sci. 7:180. for developing different molecular approaches to ameliorate the harmful effects of water deficit has doi: 10.3389/fpls.2016.00180 always been an important objective for molecular breeders (Xiong et al., 2002; Umezawa et al., 2006; Frontiers in Plant Science | www.frontiersin.org 1 February 2016 | Volume 7 | Article 180 Rasheed et al. Drought-Regulated Transcriptomic Changes in Roots Yamaguchi-Shinozaki and Shinozaki, 2006; Seki et al., 2007; in plants (Osakabe et al., 2014). The ABA independent pathway Shinozaki and Yamaguchi-Shinozaki, 2007; Hirayama and is mainly regulated by dehydration-responsive element/C- Shinozaki, 2010). repeat (DRE/CRT) and DRE-/CRT-binding protein 2 (DREB2) Plants sense changes in the environment and modify cellular transcription factors (Yamaguchi-Shinozaki and Shinozaki, physiology in a complex, integrated manner by upregulating the 2006). expression of various combinations of regulatory and functional As previously mentioned, the root system is the first to genes. Despite a comprehensive knowledge of mechanisms perceive drought stress signals. Therefore, root development is governing cellular responses, our understanding of the early significantly affected by water availability in the soil. Most studies events in the perception of stress signals is relatively poor (Urao in Arabidopsis, however, have explored transcriptomic changes in et al., 1999; Wohlbach et al., 2008). Drought stress triggers whole plants by only investigating shoots on soil-grown plants significant molecular and physiological changes in plants, such as or air-dried roots. Therefore, at the present time, the drought adjustments of metabolism and osmotic potential, and reducing response of roots in soil-grown plants remains largely unknown. leaf turgor pressure, which lead to a reduction or cessation of To fill this gap, changes in the expression of genes in roots and growth (Tardieu et al., 2014). Although water deficiency inhibits shoots of soil-grown plants in response to a progressive drought plant growth at whole plant level, roots can grow under low stress were characterized and compared by sampling plants at water potentials that completely inhibit stem and leaf growth 0, 1, 3, 5, 7, and 9 days of a drought stress. This provided the (Spollen and Sharp, 1991; Spollen et al., 1993; Chazen and opportunity to dissect the molecular response of shoots vs. roots Neumann, 1994; Wu and Cosgrove, 2000; Sharp et al., 2004). to a drought stress. The objective of the study was to obtain Since increasing root surface area facilitates water absorption, information that could be used to develop new strategies for it is plausible that differences between roots and shoots may developing drought tolerant plants. have evolved in response to water scarcity as an adaptation strategy to dry conditions (Wu and Cosgrove, 2000; Sharp et al., MATERIALS AND METHODS 2004). Cellular and molecular responses underlying adaptation to environmental stresses have been extensively studied and are Plant Material and Growth Conditions governed by changes in gene expression (Matsui et al., 2008; Liu Seeds of Arabidopsis thaliana (Col-0 ecotype) were grown on et al., 2014). Changes in the expression of a large number of genes MS medium at 22◦C under 16-h-light/8-h-dark (40–80 µmol belonging to diverse functional groups, such as transcription photons m−2 s−1) for 9 days. Plantlets were then transferred factors, protein kinases, and phosphatases, all contribute to the to ceramics granular soil (size 2.5L, Sakatanotane, Japan) and signal transduction that occurs in plants in response to and grown for 8 days at 22◦C (16h light/8h dark cycle, 60 µmol adaptation to a drought stress (Kreps et al., 2002; Seki et al., 2002, m−2 s−1 photon flux density). The drought treatment was then 2007; Xiong et al., 2002; Shinozaki et al., 2003; Matsui et al., 2008; commenced by removing excess water from the trays and ceasing Hirayama and Shinozaki, 2010). any subsequent watering. Roots and shoots were harvested Drought stress response has been extensively studied separately at 0, 1, 3, 5, 7, and 9 days after the onset of drought in Arabidopsis and the subject has been comprehensively treatment. Plants were removed from soil and roots and shoots reviewed (Iuchi et al., 2001; Xiong et al., 2002; Seki et al., of 12 plants were harvested from 3 pots for each biological 2007; Shinozaki and Yamaguchi-Shinozaki, 2007; Matsui replication. All samples were collected at noon. After harvesting, et al., 2008; Harb et al., 2010; Osakabe et al., 2014). Stress- samples were immediately placed in liquid nitrogen and stored responsive genes are comprised of enzymes regulating osmotic at −80◦C until RNA extraction. pressure, aquaporins, detoxifying enzymes, late embryogenesis abundant proteins, reactive oxygen species scavengers and Microarray Analysis chaperones that protect the integrity of cell membranes and RNA was extracted from all biological replicates with the ensure ion transport/balances. Additionally, functionally mirVana™ miRNA Isolation Kit (Ambion, USA) according diverse transcription factors and protein kinases, that regulate to the manufacturer’s instructions. The microarray analyses gene expression and signal transduction, are also an integral were carried out as previously described (Nguyen et al., 2015). component of the drought stress response (Wei et al., 2009). Briefly, fluorescent-labeled (Cy3) cRNAs were prepared from The molecular response of plants to drought stress has been 400 ng total RNA from each sample using a Quick Amp categorized into abscisic acid (ABA) dependent and ABA labeling kit (Agilent Technologies) and subsequently hybridized independent pathways (Yamaguchi-Shinozaki and Shinozaki, to an Agilent Arabidopsis custom microarray (GPL19830). Three 2006). ABA biosynthesis, transport and accumulation all increase biological replicates were processed for each treatment, with in response to a water deficit. The increased ABA content in the exception of roots 7 and 9 days as well as shoot 1 and 3 leaves triggers stomata closure, ultimately decreasing the days, where four biological replications were processed,
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