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Transcriptome Analysis for Gaining Insight into Gingerol Biosynthesis and MAPK-Dependent Hormonal Signaling Pathway Involved in Resistance Mechanism in Fusarium Wilt Tolerant Ginger (Zingiber officinale Rosc.) Produced Through In Vitro Mutagenesis and Selection

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Abstract

Ginger (Zingiber officinale Rosc.) is the most widely used medicinal herb of the ancient “Ayurveda” and “Unani” system of medicine due to bioactive compounds present in its rhizomes, i.e., volatile oils (terpenoids), diarylheptanoids (curcuminoids), and gingerols (phenols), which serve as an important panacea for treating arthritis, heart diseases, cancer, diarrhea, and respiratory disorders. It is a vegetatively propagated crop through underground rhizomes and its production is hampered by various soil-borne pathogens which predominantly include Fusarium oxysporum f.sp. zingiberi. During the preceding research, the technique of in vitro mutagenesis and selection was employed in ginger cv. Himgiri for the development of Fusarium tolerant lines, resulting in mutant Himgiri-17.5, which displayed improved accumulation of gingerol and demonstrated enhanced tolerance to Fusarium wilt. The present study reveals the first-ever transcriptome data of in vitro-raised Himgiri-17.5 to unravel the role of gingerol biosynthesis and MAPK-dependent hormonal signaling pathways in imparting tolerance to Fusarium wilt as compared to conventionally propagated Himgiri. Through transcriptome analysis, a total of 13.84 GB data was generated encoding 57,939 genes, out of which 3745 were differentially expressed genes (DEGs) in both the samples with 351 upregulated and 3394 downregulated. The expression patterns of genes in Himgiri-17.5 linked to antioxidant activity and MAPK-dependent hormonal signaling exhibited notable upregulation suggesting their possible participation in mediating plant defense response. Additionally, the investigation provided insights into volatile oil, diarylheptanoids, and gingerol biosynthetic pathway in ginger governed by crucial regulatory genes, namely DCS, CURS2, and ClPKS10. The examination also revealed the presence of 165 upregulated transcription factors primarily belonging to the ERF, bHLH, MYB, NAC, and bZIP families which exhibited a strong correlation with the biosynthesis of gingerol and MAPK-mediated hormonal signaling pathway, contributing to stress tolerance. The discovery of these DEGs related to antioxidant activity, MAPK-mediated hormonal signaling, and the biosynthetic pathway of gingerol holds a promise for the development of improved varieties of ginger through molecular approaches.

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Data Availability

The data presented in the study have been submitted in National Center for Biotechnology Information (NCBI; Submission ID—SUB12515620) under accession number PRJNA921959.

Abbreviations

ABA:

Abscisic acid

bHLH:

Basic helix-loop-helix

bZIP:

Basic leucine zipper

C2H2:

Cysteine 2 Histidine 2 zinc finger motifs

C3H:

Cysteine 3 Histidine zinc finger motifs

CAT:

Catalase

ClPKS10:

Chalcone synthase like protein 10

CURS2:

Curcuminoid synthase 2

cv:

Cultivar

DCS2:

Diketide-CoA synthase 2

DEG:

Differentially expressed genes

Dof:

DNA binding with one finger

EIN:

Ethylene insensitive

ERF:

Ethylene responsive factor

ETR:

Ethylene receptor

FCF:

Fungal culture filtrate

GO:

Gene ontology

HPLC:

High performance liquid chromatography

KAAS:

KEGG automatic annotation server

KEGG:

Kyoto encyclopedia of genes and genomes

MADS:

Minichromosome maintenance factor 1 Agamous Deficiens serum response factor 

MAPK/MPK:

Mitogen activated protein kinases

MYB:

v-Myb myeloblastosis viral oncogene homolog 

NAC:

NAM (no apical meristem), ATAF1 and - 2, and CUC2 (cup-shaped cotyledon)

NBS LRR:

Nucleotide binding site-leucine rich repeats

POX:

Peroxidase

PYL:

PYR-like

PYR:

Pyrabactin resistance

ROS:

Reactive oxidative species

RT-qPCR:

Reverse transcriptase-quantitative polymerase chain reaction

SOD:

Superoxide dismutase

TF:

Transcription factor

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Acknowledgements

Authors are highly thankful to NxGenBio Life Sciences (New Delhi, India) for transcriptome sequencing and partial data analysis. The help rendered by ICAR- Directorate of Mushroom Research (Solan, Himachal Pradesh) for assisting in gene expression studies is highly acknowleged.

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Contributions

PS and MT were involved in designing and execution of molecular research experiments, data analysis, contributed in writing and editing of the manuscript. SK and AC contributed to gene expression analysis. HD provided the planting material (Himgiri rhizomes), technical help required for ginger transplantation and RG performed partial transcriptome analysis.

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Correspondence to Manisha Thakur.

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Sharma, P., Thakur, M., Kamal, S. et al. Transcriptome Analysis for Gaining Insight into Gingerol Biosynthesis and MAPK-Dependent Hormonal Signaling Pathway Involved in Resistance Mechanism in Fusarium Wilt Tolerant Ginger (Zingiber officinale Rosc.) Produced Through In Vitro Mutagenesis and Selection. J Plant Growth Regul (2023). https://doi.org/10.1007/s00344-023-11078-w

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  • DOI: https://doi.org/10.1007/s00344-023-11078-w

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