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The Temporal Foliar Transcriptome of the Perennial C3 Desert Plant

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The Temporal Foliar Transcriptome of the Perennial C3 Desert Plant Yates et al. BMC Plant Biology 2014, 14:2 http://www.biomedcentral.com/1471-2229/14/2 RESEARCH ARTICLE Open Access The temporal foliar transcriptome of the perennial C3 desert plant Rhazya stricta in its natural environment Steven A Yates1,IgorChernukhin1, Ruben Alvarez-Fernandez1, Ulrike Bechtold1, Mohammed Baeshen2,NabihBaeshen2, Mohammad Z Mutwakil2,JamalSabir2,TracyLawson1 and Philip M Mullineaux1* Abstract Background: The perennial species Rhazya stricta (R. stricta) grows in arid zones and carries out typical C3 photosynthesis under daily extremes of heat, light intensity and low humidity. In order to identify processes attributable to its adaptation to this harsh environment, we profiled the foliar transcriptome of apical and mature leaves harvested from the field at three time periods of the same day. Results: Next generation sequencing was used to reconstruct the transcriptome and quantify gene expression. 28018 full length transcript sequences were recovered and 45.4% were differentially expressed (DE) throughout the day. We compared our dataset with microarray experiments in Arabidopsis thaliana (Arabidopsis) and other desert species to identify trends in circadian and stress response profiles between species. 34% of the DE genes were homologous to Arabidopsis circadian-regulated genes. Independent of circadian control, significant overlaps with Arabidopsis genes were observed only with heat and salinity/high light stress-responsive genes. Also, groups of DE genes common to other desert plants species were identified. We identified protein families specific to R. stricta which were found to have diverged from their homologs in other species and which were over -expressed at midday. Conclusions: This study shows that temporal profiling is essential to assess the significance of genes apparently responsive to abiotic stress. This revealed that in R. stricta, the circadian clock is a major regulator of DE genes, even of those annotated as stress-responsive in other species. This may be an important feature of the adaptation of R. stricta to its extreme but predictable environment. However, the majority of DE genes were not circadian-regulated. Of these, some were common to other desert species and others were distinct to R. stricta, suggesting that they are important for the adaptation of such plants to arid environments. Keywords: Next generation sequencing, Transcriptomics, Circadian clock, Rhazya stricta, Perennial desert plants, Heat stress, Salinity stress, C3 photosynthesis Background daily flooding with seawater [3,4]. Such zones have a low The greater than 250,000 extant angiosperm species are a diversity of plant species as a consequence of the extensive consequence of diversification that has driven adaptation adaptations required for successful growth and reproduction to virtually all terrestrial ecosystems [1,2]. These include in such environments [5–8]. In these conditions, speciation many with a wide range of challenging climatic zones is driven more by climate and other abiotic factors than compared with those in which we grow our major crop by competition with other plant species [6,9,10]. species. Challenging environments include those that have Arid zones (60-250 mm of annual rainfall [11]), have a extremes of temperature, low and erratic precipitation and range of climatic and meteorological features which impact on the vegetation [12]. This ranges from rocky plateaux that permit the growth of only shallow rooted annuals * Correspondence: [email protected] 1School of Biological Sciences, University of Essex, Colchester CO4 3SQ, UK and mesophyte ephemerals to dry river bed wadis that Full list of author information is available at the end of the article © 2014 Yates et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. 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. Yates et al. BMC Plant Biology 2014, 14:2 Page 2 of 22 http://www.biomedcentral.com/1471-2229/14/2 can support deep rooted perennials [12–14]. The study of R. stricta in its arid environment and may be worthy of perennial plants adapted to function for extended periods future study and transfer to C3 crop species. This paper in arid environments could provide rewarding insights to reports our initial survey and interpretation of changes in help develop novel traits and genes for crop improvement the patterns of global gene expression at three periods in the face of abiotic factors such as heat, high light inten- of the day and a comparison of these responses with sities, salinity and low nutrient and water availability [12]. published studies on transcriptome responses to stress Studies of such plants in their natural extreme environment in a range of plant species. are a contrast to the many laboratory-based experiments that focus on a single stress [3]. Results The advent of massively parallel DNA sequencing Physiology technologies and allied developments in bioinformatics Figure 1a-d illustrates the diurnal changes in photosynthesis has brought genome-scale studies of orphan plant species assimilation rate (A), stomatal conductance (Gs), internal within the range of many laboratories [15]. Several plant CO2 concentration (Ci) and transpiration rate (E) at three species adapted to extreme environments have been sub- measurement periods: morning, midday and dusk. Also jected to such investigations. For example, genome sequen- shown (Figure 1e-f) is the leaf temperature and vapour cing of Thellungiella parvula, a species adapted to a saline pressure deficit (VPD). Gs was greatest in the morning, and resource poor environment [16]; transcriptome analysis and showed a midday depression which was maintained of the resurrection plant, Craterostigma plantagineum, throughout the rest of the day (Figure 1a). A followed for dessication tolerance [17]; a comparative survey of the diurnal pattern of irradiance (Figure 1b), with the the transcriptome of two mangrove species, Rhizophora highest values obtained at midday (despite reduced Gs). mangle and Heritiera littoralis [4] for multiple abiotic Ci was greatly reduced during this period of high assimi- stresses and Populus euphratica a desert tree adapted to lation and low Gs suggesting that stomatal control of drought and salinity [18]. A feature of many of these species CO2 uptake limited A. It is noteworthy that E did not is that their adaptations are extensive, such as recovery mirror GS (Figure1eandd).Thiswasmostlikelydue from desiccation in resurrection plants and the mor- to the 18°C increase in leaf temperature and VPD in- phological and biochemical developments associated with crease to 6 kPa observed between morning and midday crassulacean acid metabolism (CAM) photosynthesis (Figure 1e). [17–19]. While such features are intrinsically worthy of study, such adaptations do not lend themselves readily De novo transcriptome reconstruction and annotation to transfer to crop plants because the control of the The de novo transcriptome assembly produced 28018 underlying genes that determine these processes remain unique transcript sequences with a mean length of 1643 bp unknown. and N50 2199 bp (Figure 2b). 27617 sequences were In this study, we report an initial survey of the transcrip- uploaded to transcriptome shotgun assembly (TSA) Ac- tome of the perennial desert plant species Rhazya stricta cession GAMW01000000, according to TSA criteria; the Decne growing in its natural environment. R. stricta is a full list is available upon request. We were able to assign a glabrous erect perennial evergreen shrub approximately functional description and gene ontology to 71.2% (19950) 90 cm high with dense semi-erect branches [20] (see also and 68.0% (19046) of the contigs, respectively (Figure 2c). Additional file 1). It is native to South Asia and the Middle The annotations are provided in Additional file 2 and the East and belongs to the family Apocynacae (Asterid clade), mean count per million (CPM) per leaf at each time in which includes species of medicinal value [21,22]. R. stricta Additional file 3, and FDR significance results for 23037 is common in arid zones at elevations of 100-700 m above quantifiable genes. sea level [14] and has been found to have improved growth in wadis [21], suggesting a deep root system, like other arid RNA-seq zone perennial species [12]. It is able to tolerate a wide To calculate expression, all reads were mapped against the range of soil mineral salt compositions by accumulating de novo reconstructed transcriptome. To estimate the Na+,K+,Ca2+ and Cl- in its leaves [21]. variation both between and within plants the biological Our reason for studying the transcriptome of R. stricta coefficient of variation (BCV) was calculated (Table 1). is that it has a typical C3 photosynthetic physiology, which The results show the BCV within plants was low (between is able to function well under typical desert conditions of 14-22%), but the BCV between plants was relatively very high light intensities, temperatures and vapor pressure greater. The latter is likely due to the inclusion of four deficits [23,24]. The analysis of gene expression patterns plants, sampled over a four hour time frame. The next may reveal mechanisms associated with stress tolerance step was to use multivariate analysis to determine how and protection of the photosynthetic apparatus. This would well the gene expression profiles distinguished between identify adaptations that contribute to the success of thesamplingtimepointsandfactors.Thiswasdone Yates et al. BMC Plant Biology 2014, 14:2 Page 3 of 22 http://www.biomedcentral.com/1471-2229/14/2 ) abc) ) -1 -1 -1 s s s -2 -2 -2 A (µmolm Ci (µmolm Gs (mmolm Morning Midday Dusk Morning Midday Dusk Morning Midday Dusk ) de f -1 s -2 Temp ( C) VPD (kPa) E (mmolm Morning Midday Dusk Morning Midday Dusk Morning Midday Dusk Figure 1 Gas exchange measurements.
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