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Next-Generation Sequencing (NGS) Transcriptomes Reveal Association Of Planta DOI 10.1007/s00425-015-2304-6 ORIGINAL ARTICLE Next-generation sequencing (NGS) transcriptomes reveal association of multiple genes and pathways contributing to secondary metabolites accumulation in tuberous roots of Aconitum heterophyllum Wall. 1 1 1 1 Tarun Pal • Nikhil Malhotra • Sree Krishna Chanumolu • Rajinder Singh Chauhan Received: 13 February 2015 / Accepted: 10 April 2015 Ó Springer-Verlag Berlin Heidelberg 2015 Abstract transcriptomes, respectively. In silico expression profiling of Main conclusion The transcriptomes of Aconitum the mevalonate/2-C-methyl-D-erythritol 4-phosphate (non- heterophyllum were assembled and characterized for mevalonate) pathway genes for aconites biosynthesis re- the first time to decipher molecular components con- vealed 4 genes HMGR (3-hydroxy-3-methylglutaryl-CoA tributing to biosynthesis and accumulation of metabo- reductase), MVK (mevalonate kinase), MVDD (mevalonate lites in tuberous roots. diphosphate decarboxylase) and HDS (1-hydroxy-2-methyl- 2-(E)-butenyl 4-diphosphate synthase) with higher expres- Aconitum heterophyllum Wall., popularly known as Atis, is a sion in root transcriptome compared to shoot transcriptome high-value medicinal herb of North-Western Himalayas. No suggesting their key role in biosynthesis of aconite alkaloids. information exists as of today on genetic factors contributing Five genes, GMPase (geranyl diphosphate mannose py- to the biosynthesis of secondary metabolites accumulating in rophosphorylase), SHAGGY, RBX1 (RING-box protein 1), tuberous roots, thereby, limiting genetic interventions to- SRF receptor kinases and b-amylase, implicated in tuberous wards genetic improvement of A. heterophyllum.Illumina root formation in other plant species showed higher levels of paired-end sequencing followed by de novo assembly yielded expression in tuberous roots compared to shoots. A total of 75,548 transcripts for root transcriptome and 39,100 tran- 15,487 transcription factors belonging to bHLH, MYB, bZIP scripts for shoot transcriptome with minimum length of families and 399 ABC transporters which regulate biosyn- 200 bp. Biological role analysis of root versus shoot tran- thesis and accumulation of bioactive compounds were iden- scriptomes assigned 27,596 and 16,604 root transcripts; tified in root and shoot transcriptomes. The expression of 5 12,340 and 9398 shoot transcripts into gene ontology and ABC transporters involved in tuberous root development was clusters of orthologous group, respectively. KEGG pathway validated by quantitative PCR analysis. Network connectivity mapping assigned 37 and 31 transcripts onto starch–sucrose diagrams were drawn for starch–sucrose metabolism and metabolism while 329 and 341 KEGG orthologies associated isoquinoline alkaloid biosynthesis associated with tuberous with transcripts were found to be involved in biosynthesis of root growth and secondary metabolism, respectively, in root various secondary metabolites for root and shoot transcriptome of A. heterophyllum. The current endeavor will be of practical importance in planning a suitable genetic in- Tarun Pal and Nikhil Malhotra contributed equally to this work. tervention strategy for the improvement of A. heterophyllum. Electronic supplementary material The online version of this Keywords Aconitum Á Network connectivity diagrams Á article (doi:10.1007/s00425-015-2304-6) contains supplementary material, which is available to authorized users. Pathway mapping Á RNA-seq Á Transcript abundance Á Transcriptome analysis Á Tuberous roots & Rajinder Singh Chauhan [email protected] Abbreviations AHSR Root transcriptome 1 Department of Biotechnology and Bioinformatics, Jaypee University of Information Technology, AHSS Shoot transcriptome Waknaghat 173234, Himachal Pradesh, India COG Cluster of orthologous group 123 Planta GO Gene ontology on tuberous root formation process of Ipomoea batatas KO KEGG orthology and Manihot esculenta (Indira and Kurian 1977; Wang MEP 2-C-Methyl-D-erythritol 4-phosphate et al. 2005). The genes/proteins like SRF, GIGANTEA, MVA Mevalonate MADS-box and NAM-like have been implicated in the NGS Next-generation sequencing tuberous root development in these plant species (You FPKM Fragments per kilobase of transcript per million et al. 2003; Tanaka et al. 2005; Sheffield et al. 2006). fragments mapped The activity of AGPase and associated enzymes in SSR Simple sequence repeat tuberous roots has been found to regulate biomass yield in M. esculenta (Ihemere et al. 2006). Moreover, the underlying genetic mechanism that controls tuberous root formation in Rehmannia glutinosa has been carried out to unravel the role of tuberous root development genes (Sun Introduction et al. 2010). However, no molecular information exists on the tuberous root development in A. heterophyllum. Herbs are staging a comeback and ‘herbal revolution’ is The process of tuberous root development in this plant happening all over the globe. The North-Western Hi- species is simple, yet interesting. The roots grow im- malayas are a reservoir of important medicinal plant mediately after seed germination from the radicle and species that are used either in the preparation of herbal those primary roots transform into tuberous roots rather drugs or for the isolation of highly valuable phyto- formed from adventitious roots due to secondary growth chemicals/metabolites. Atis (Aconitum heterophyllum of vascular cambium in other plant species. Morpho- Wall.) is an important medicinal plant species belong- logically distinct developmental stages of tuberous root ing to family Ranunculaceae. It is a biennial herb dis- formation in A. heterophyllum are depicted in Fig. 1. The tributed in sub-alpine and alpine regions of the North- proliferation and swelling of primary tuberous root re- Western Himalayas found at altitudes of 2400–3600 m. sults in further branching and bulking of storage organ The tuberous roots of A. heterophyllum contain non- with the passage of time. toxic alkaloids like atisine, aconitine, hetidine and The availability of whole transcriptome data can be used heterophyllinine (Pelletier et al. 1968; Zhaohong et al. not only to discover candidate genes involved in tuberous 2006) which are widely used in the treatment of diar- root development and secondary metabolites production, rhea, vomiting, cough, cold, etc. (Thatte et al. 1993; but also for understanding molecular basis of various bio- Mitra et al. 2001). A. heterophyllum has been listed as a logical processes (Sigurdsson et al. 2010; Xie et al. 2012). ‘critically endangered species’ by the International Further, the whole transcriptomes offer an opportunity to Union for Conservation of Nature and Natural Re- explore microsatellites in expressed genes which may en- sources (Nautiyal et al. 2002;Srivastavaetal.2011). In rich the number of molecular markers to assist DNA fin- order to meet the ever increasing industrial demands gerprinting, gene mapping and marker-assisted breeding in due to its vast medicinal properties and healthcare A. heterophyllum. The next-generation sequencing (NGS) needs, A. heterophyllum needs to be grown commer- technique has been successfully utilized in analyzing the cially. No information exists as of today on genetic non-model plant species including, I. batatas (Wang et al. improvement of A. heterophyllum either towards in- 2010c), Hevea brasiliensis (Xia et al. 2011), Jatropha creased production of secondary metabolites or in the curcas (Costa et al. 2010), Sesamum indicum (Wei et al. biomass (tuberous roots) accumulating those metabo- 2011), Picrorhiza kurroa (Gahlan et al. 2012), Boehmeria lites. Moreover, a genetic intervention strategy would nivea (Liu et al. 2013) and so on. As a first step to gain require information on candidate genes contributing to insight of tuberous root development, we utilized Illumina the formation of tuberous roots. Generating whole paired-end sequencing technology to characterize mole- genome transcriptome of A. heterophyllum would, cular components that are possibly involved in tuberous therefore, be an ideal staring point to capture genetic root formation in A. heterophyllum. Fragments per kilobase components contributing to a trait of economic impor- of transcript per million mapped fragment (FPKM) based tance (Hussain et al. 2012). comparative expression profiling study was done to sys- Tuberous roots are storage organs to store nutrients tematically characterize the RNAs to identify differentially that are required as a source of energy for regeneration. regulated genes involved in tuberous root formation. Net- Their formation and development constitutes complex work connectivity diagrams were drawn for the molecules biological processes involving morphogenesis as well as that interact in various developmental and regulatory pro- dry matter accumulation. Several studies involving ana- cesses for biosynthesis of aconites and tuberous root de- tomical and physiological functions have been carried out velopment in A. heterophyllum. 123 Planta Fig. 1 Schematic representation of root developmental stages in A. 24-month-old age group represents intermediate stage (c, d); heterophyllum showing morphological changes occurring during 36-month-old represents mature stage (e) having fully developed tuberous root development. Tuberous roots of 6 months and 12-mon- tuberous roots th-old age group represents young stage (a, b); 18-month and Materials and methods started with mRNA fragmentation followed by reverse transcription, second-strand synthesis, pair-end
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