Comparative Transcriptome Analysis Reveals Unique Genetic Adaptations Conferring Salt Tolerance in a Xerohalophyte

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Comparative Transcriptome Analysis Reveals Unique Genetic Adaptations Conferring Salt Tolerance in a Xerohalophyte CSIRO PUBLISHING Functional Plant Biology https://doi.org/10.1071/FP18295 Comparative transcriptome analysis reveals unique genetic adaptations conferring salt tolerance in a xerohalophyte Wei-Wei Chai A, Wen-Ying Wang A, Qing MaA, Hong-Ju Yin A, Shelley R. Hepworth A,B and Suo-Min Wang A,C AState Key Laboratory of Grassland Agro-ecosystems; Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs; College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou, 730020, PR China. BDepartment of Biology, Institute of Biochemistry, Carleton University, Ottawa, ON, Canada. CCorresponding author. Email: [email protected] Abstract. Most studies on salt tolerance in plants have been conducted using glycophytes like Arabidopsis thaliana (L.) Heynh., with limited resistance to salinity. The xerohalophyte Zygophyllum xanthoxylum (Bunge) Engl. is a salt- accumulating desert plant that efficiently transports Na+ into vacuoles to manage salt and exhibits increased growth under salinity conditions, suggesting a unique transcriptional response compared with glycophytes. We used transcriptome profiling by RNA-seq to compare gene expression in roots of Z. xanthoxylum and A. thaliana under 50 mM NaCl treatments. Gene Ontology (GO) functional annotation and Kyoto Encyclopedia of Genes and Genomes (KEGG) metabolic pathway analysis suggested that 50 mM NaCl was perceived as a stimulus for Z. xanthoxylum whereas a stress for A. thaliana. Exposure to 50 mM NaCl caused metabolic shifts towards gluconeogenesis to stimulate growth of Z. xanthoxylum, but triggered defensive systems in A. thaliana. Compared with A. thaliana, a vast array of ion transporter genes was induced in Z. xanthoxylum, revealing an active strategy to uptake Na+ and nutrients from the environment. An ascorbate-glutathione scavenging system for reactive oxygen species was also crucial in Z. xanthoxylum, based on high expression of key enzyme genes. Finally, key regulatory genes for the biosynthesis pathways of abscisic acid and gibberellin showed distinct expression patterns between the two species and auxin response genes were more active in Z. xanthoxylum compared with A. thaliana. Our results provide an important framework for understanding unique patterns of gene expression conferring salt resistance in Z. xanthoxylum. Additional keywords: glycophyte, RNA-seq, salt response, stimulus, xerohalophyte, Zygophyllum xanthoxylum. Received 9 November 2018, accepted 11 March 2019, published online 8 May 2019 Introduction ions, often coupled with specialised morphologies, such as Soil salinity is a major abiotic stress that severely constrains plant succulent leaves for storing excess salt ion. growth and productivity (Zhu 2001; Munns and Tester 2008). Zygophyllum xanthoxylum (Bunge) Engl. is a succulent A high level of Na+ is toxic to plants because it disturbs xerohalophyte, native to desert areas of China and Mongolia. cytoplasmic Na+/K+ homeostasis and leads to secondary This species has the great capacity to absorb Na+ into succulent osmotic and oxidative stresses (Taji et al. 2004). Fortunately, leaves for osmotic adjustment, exhibiting improved growth and plants have evolved various mechanisms to combat salinity, excellent photosynthetic capacity in salty soils (Ma et al. 2012; including the regulation of ion homeostasis (Zhu 2003), Yue et al. 2012). Additionally, Na+ ions promote the uptake of reactive oxygen species (ROS) scavenging systems (Das and important nutrients in Z. xanthoxylum, such as N, P, Fe, Si, Ca2+ Roychoudhury 2014) and hormone responses (Bari and Jones and Mg2+, thereby stimulating growth (Wang et al. 2019). Salt 2009). To date, much effort has aimed at deciphering molecular exposure also increases enzyme activities important for ROS mechanisms of plant salt tolerance and identifying the relevant scavenging in Z. xanthoxylum (Cai et al. 2011). Further, several genes. However, most of these studies have focussed on studies have been performed to elucidate the molecular glycophytes like Arabidopsis thaliana (L.) Heynh. with limited mechanism of salt tolerance in Z. xanthoxylum. Key tolerance to salinity. In recent years, it is experimentally proven functional genes involved in Na+ and K+ homeostasis that halophytes are more appropriate models for studying salt have been explored, such as tonoplast Na+/H+ antiporter tolerance (Shabala 2013; Flowers et al. 2015; Song and Wang ZxNHX (Wu et al. 2011; Yuan et al. 2015), plasma 2015). Halophytes have evolved unique strategies, such as membrane Na+/H+ antiporter ZxSOS1 (Ma et al. 2014), stelar efficient control of uptake and compartmentalisation of salt K+ outward rectifying channel ZxSKOR (Hu et al. 2016), Journal compilation Ó CSIRO 2019 www.publish.csiro.au/journals/fpb B Functional Plant Biology W. W. Chai et al. inward-rectifying K+ channel ZxAKT1 (Ma et al. 2017). For hydroculture, 3-week-old seedlings grown on 1/2 MS In contrast to A. thaliana, Z. xanthoxylum has superior media plates were transferred to containers containing mechanisms for thriving in salty soils. modified Hoagland nutrient solution (same as Z. xanthoxylum). Collective studies suggest that quantitative changes in gene The opaque vinyl chloride containers (175 Â 95 Â 35 mm) were expression are mainly responsible for salt tolerance or sensitivity covered with an opaque vinyl chloride board (1 mm) that had 36 (Bartels and Dinakar 2013; Volkov 2015; Mishra and Tanna holes (3 mm) at regular intervals to diameter 30-mm shield the 2017). Thus, comparative analysis of gene expression in root zone from sunlight (to make sure roots got plenty of air, Z. xanthoxylum and A. thaliana, is a promising strategy for we chose nine holes to fix seedlings, one seedling per hole). The revealing key differences responsible for salt tolerance. RNA nutritional solution was replaced with fresh solution every 3 days. sequencing (RNA-seq) is an effective tool because it provides Plants were grown in a greenhouse at 22C under long detailed information about a broad spectrum of genes (Halimaa days (200 mmol m–2Ás–1 photon flux density). Five-week-old et al. 2014). A. thaliana seedlings were used for the same treatments as Roots are the primary tissue exposed to soil salinity (Ouyang Z. xanthoxylum. The roots of A. thaliana seedlings were et al. 2007). This pivotal organ has key functions in absorbing collected after 6 and 24 h treatment respectively. water and nutrients, secreting enzymes and organic acids, as well as producing hormones (Zhai et al. 2013). Root growth of Data acquisition glycophytes is typically inhibited by salinity (Zolla et al. Eight samples in total were marked as follows: ZxC6R, ZxC24R, 2010,Huet al. 2015). By contrast, the roots of halophytes can ZxS6R, ZxS24R, AtC6R, AtC24R, AtS6R, AtS24R where Zx maintain normal growth or even improved growth under salinity denotes Z. xanthophyllum and At denotes A. thaliana, conditions (Hu et al. 2012). Therefore, it is attractive to examine respectively; ‘C’ and ‘S’ denote control and salt treatments contrasting gene regulation strategies in roots of halophytes with 50 mM NaCl, respectively, 6 and 24 denote 6 and 24 h versus glycophytes. Here, we compared patterns of transcript of treatment, respectively, and R denotes roots. Transcriptome abundance between salt-treated Z. xanothxylum and A. thaliana, data of Z. xanthoxylum were preliminarily published by Ma et al. fi fi and identi ed genes with a unique transcription pro le in (2016). RNA isolation and first-strand cDNA synthesis for Z. xanthoxylum. A. thaliana were performed as described previously for Z. xanthoxylum (Ma et al. 2016). Materials and methods Cultivation of plants and salt exposure Differentially expressed genes (DEGs) analysis Zygophyllum xanthoxylum (Bunge) Engl. plants were cultivated Complementary DNA libraries were constructed in parallel as previously described by Ma et al.(2016). Briefly, seeds of using a tag-based digital gene expression (DGE) system (Xue Z. xanthoxylum were collected from wild plants in the Alxa et al. 2010). Genes were determined to be differentially Desert of the Inner Mongolia Autonomous Region, China. Seeds expressed using a false discovery rate (FDR) adjusted value < > were sterilised for 3 min with 5% (v/v) sodium hypochlorite, of P 0.001 and an absolute value of log2 ratio 1 as the rinsed five times with distilled water, then soaked in distilled threshold. water at 4C for 1 day, and then germinated at 25C in the dark on filter paper wetted with distilled water. Upon sprouting, uniform Re-annotation, functional categorisation of DEGs seedlings weretransplanted intoplugged holes in5 Â5cm square To obtain orthologous gene pairs, unigenes from the plastic containers (two seedlings per container) filled with sand transcriptome library of Z. xanthoxylum (Ma et al. 2016) were and irrigated with modified Hoagland nutrient solution aligned to the Arabidopsis genome assembly TAIR10 (www. containing 2 mM KNO3, 0.5 mM KH2PO4, 0.5 mM arabidopsis.org/, accessed 2 January 2019) using blastn MgSO4*7H2O, 0.5 mM Ca(NO3)2*4H2O, 60 mM Fe-citrate, 50 with stringent parameters ‘blastn.exe -task blastn -query All- mMH3BO3,10mM MnCl2*4H2O, 1.6 mM ZnSO4*7H2O, 0.6 mM Unigene.fa -db TAIR10.fasta -outfmt 7 -max_target_seqs CuSO4*5H2O and 0.05 mMNa2MoO4*2H2O. Seedlings were 1 -evalue 1e-5 -out raw_result. fasta’ to obtain the closest grown under long days (16 h light/8 h dark; photon flux density A. thaliana homologues. The unigene of Z. xanthoxylum with 800 mmol m–2Ás–1) in a greenhouse
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