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Comparative transcriptomics uncovers differences in photoautotrophic versus photoheterotrophic modes of nutrition in relation to secondary metabolites biosynthesis in Swertia chirayita

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Abstract

Swertia chirayita is a high-value medicinal herb exhibiting antidiabetic, hepatoprotective, anticancer, antiediematogenic and antipyretic properties. Scarcity of its plant material has necessitated in vitro production of therapeutic metabolites; however, their yields were low compared to field grown plants. Possible reasons for this could be differences in physiological and biochemical processes between plants grown in photoautotrophic versus photoheterotrophic modes of nutrition. Comparative transcriptomes of S. chirayita were generated to decipher the crucial molecular components associated with the secondary metabolites biosynthesis. Illumina HiSeq sequencing yielded 57,460 and 43,702 transcripts for green house grown (SCFG) and tissue cultured (SCTC) plants, respectively. Biological role analysis (GO and COG assignments) revealed major differences in SCFG and SCTC transcriptomes. KEGG orthology mapped 351 and 341 transcripts onto secondary metabolites biosynthesis pathways for SCFG and SCTC transcriptomes, respectively. Nineteen out of 30 genes from primary metabolism showed higher in silico expression (FPKM) in SCFG versus SCTC, possibly indicating their involvement in regulating the central carbon pool. In silico data were validated by RT-qPCR using a set of 16 genes, wherein 10 genes showed similar expression pattern across both the methods. Comparative transcriptomes identified differentially expressed transcription factors and ABC-type transporters putatively associated with secondary metabolism in S. chirayita. Additionally, functional classification was performed using NCBI Biosystems database. This study identified the molecular components implicated in differential modes of nutrition (photoautotrophic vs. photoheterotrophic) in relation to secondary metabolites production in S. chirayita.

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Abbreviations

6PGD:

6-Phosphogluconate dehydrogenase

6PGL:

6-Phosphogluconolactonase

7-DLGT:

7-Deoxyloganetic acid glucosyl transferase

8-HGO:

8-Hydroxygeraniol oxidoreductase

AAC:

Acetyl-CoA carboxylase

AACT:

Acetoacetyl-CoA thiolase

ADH:

Arogenate dehydrogenase

ADT:

Prephenate dehydratase

AH:

Aconitate hydratase

C3H:

p-Coumarate 3-hydroxylase

C4H:

Trans-cinnamate 4-hydroxylase

CM:

Chorismate mutase

COG:

Clusters of orthologous groups

CS:

Chorismate synthase

CRS:

Citrate (si)-synthase

DAHPS:

3-Deoxy-D-arabinoheptulosonate-7-phosphate synthase

DHQD:

3-Dehydroquinate dehydratase

DHQS:

3-Dehydroquinate synthase

DL7H:

7-Deoxyloganic acid hydroxylase

DLD:

Dihydrolipoamide dehydrogenase (part of oxoglutarate dehydrogenase complex)

DLST:

Dihydrolipoamide S-succinyl transferase (part of oxoglutarate dehydrogenase complex)

DXR:

1-Deoxy-D-xylulose 5-phosphate reductoisomerase

DXS:

1-Deoxy-D-xylulose 5-phosphate synthase

ENO:

Enolase

EPSPS:

5-Enolpyruvylshikimate-3-phosphate synthase

FBA:

Fructose bisphosphate aldolase

FBP:

Fructose bisphosphatase

FUM:

Fumarate hydratase

G10H:

Geraniol 10-hydroxylase/8-oxidase

G6PD:

Glucose 6-phosphate dehydrogenase

GAPDH:

Glyceraldehyde 3-phosphate dehydrogenase

GDPS:

Geranyl diphosphate synthase

GES:

Geraniol synthase

GO:

Gene ontology

GPI:

Phosphoglucose isomerise

HMGR:

3-Hydroxy-3-methylglutaryl-CoA reductase

HMGS:

3-Hydroxy-3-methylglutaryl-CoA synthase

HXK:

Hexokinase

IDH:

Isocitrate dehydrogenase

IO:

Iridoid oxidase

IPPI:

Isopentenyl diphosphate isomerase

IS:

Iridoid synthase

ISPD:

2-C-Methyl-D-erythritol 4-phosphate cytidylyltransferase

ISPE:

4-(Cytidine-5′-diphospho)-2-C-methyl-D-erythritol kinase

ISPF:

2-C-Methyl-D-erythritol 2,4-cyclodiphosphate synthase

ISPG:

(E)-4-Hydroxy-3-methylbut-2-enyl diphosphate synthase

ISPH:

(E)-4-Hydroxy-3-methylbut-2-enyl diphosphate reductase

KEGG:

Kyoto encyclopedia of genes and genomes

LMT:

Loganic acid O-methyltransferase

MEP:

2-C-Methyl-D-erythritol 4-phosphate

MQO:

Malate:quinone oxidoreductase

MVA:

Mevalonate

MVDD:

Mevalonate diphosphate decarboxylase

MVK:

Mevalonate kinase

OGDH:

Oxoglutarate dehydrogenase E1 subunit (part of oxoglutarate dehydrogenase complex)

PAL:

Phenylalanine ammonia lyase

PAT:

Aspartate–prephenate aminotransferase

PFK1:

Phosphofructokinase

PGAM:

Phosphoglycerate mutase

PGK:

Phosphoglycerate kinase

PHAT:

Phenylalanine (histidine) aminotransferase

PMK:

Phosphomevalonate kinase

PRK:

3-Epimerase phosphoribulokinase

PVK:

Pyruvate kinase

RPE:

Ribulose 5-phosphate 3-epimerase

RPI:

Ribose 5-phosphate isomerase

RuBisCO:

Ribulose-1,5-bisphosphate carboxylase/oxygenase

SAK:

Shikimate kinase

SCFG:

Swertia chirayita green house grown plant

SCTC:

Swertia chirayita tissue cultured plants

SDH:

Shikimate dehydrogenase

SLS:

Secologanin synthase

SUCLG:

Succinate-CoA ligase

TAL:

Tyrosine ammonia-lyase

TALD:

Transaldolase

TKT:

Transketolase

TPI:

Triosephosphate isomerise

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Acknowledgements

The authors are thankful to the Department of Biotechnology, Ministry of Science and Technology, Government of India for providing financial support to RSC in the form of a programme support on high-value medicinal plants.

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Author notes

  1. Tarun Pal and Jibesh Kumar Padhan contributed equally to this work.

Authors and Affiliations

  1. Department of Biotechnology and Bioinformatics, Jaypee University of Information Technology, Waknaghat, Solan, Himachal Pradesh, 173234, India

    Tarun Pal, Jibesh Kumar Padhan, Pawan Kumar & Hemant Sood

  2. Department of Biotechnology, Bennett University, a Times Group Initiative, Plot No 8-11, TechZone II, Greater Noida, Uttar Pradesh, 201310, India

    Rajinder S. Chauhan

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  1. Tarun Pal
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Contributions

RSC conceptualized and hypothesized the biological questions. HS and JKP generated the study materials. TP and JKP did the computational analyses, JKP and PK analyzed literature into experiments, results and interpretations. All authors have contributed to, seen, and approved the manuscript.

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Correspondence to Rajinder S. Chauhan.

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Data accessibility All scripts and sequence data used in this study are accessible via http://14.139.240.55/NGS/download.php.

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Pal, T., Padhan, J.K., Kumar, P. et al. Comparative transcriptomics uncovers differences in photoautotrophic versus photoheterotrophic modes of nutrition in relation to secondary metabolites biosynthesis in Swertia chirayita. Mol Biol Rep 45, 77–98 (2018). https://doi.org/10.1007/s11033-017-4135-y

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