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Comparative study of codon usage profiles of Zingiber officinale and its associated fungal pathogens

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A Correction to this article was published on 25 August 2021

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Abstract

Codon usage bias influences the genetic features prevalent in genomes of all the organisms. It also plays a crucial role in establishing the host–pathogen relationship. The present study elucidates the role of codon usage pattern regarding the predilection of fungal pathogens Aspergillus flavus, Aspergillus niger, Fusarium oxysporum and Colletotrichum gloeosporioides towards host plant Zingiber officinale. We found a similar trend of codon usage pattern operative in plant and fungal pathogens. This concurrence might be attributed for the colonization of fungal pathogens in Z. officinale. The transcriptome of both plant and pathogens showed bias towards GC-ending codons. Natural selection and mutational pressure seem to be accountable for shaping the codon usage pattern of host and pathogen. We also identified some distinctive preferred codons in A. flavus, F. oxysporum and Z. officinale that could be regarded as signature codons for the identification of these organisms. Knowledge of favored, avoided and unique codons will help to devise strategies for reducing spice losses due to fungal pathogens.

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Change history

  • 26 August 2021

    The original online version of this article was revised: the corresponding author was processed incorrectly. The actual corresponding author of the article is Prof. Ravail Singh.

  • 25 August 2021

    A Correction to this paper has been published: https://doi.org/10.1007/s00438-021-01813-x

References

  • Badet T, Peyraud R, Mbengue M, Navaud O, Derbyshire M, Oliver RP, Raffaele S (2017) Codon optimization underpins generalist parasitism in fungi. Elife 6:e22472

    Article  Google Scholar 

  • Barbhuiya RI, Uddin A, Chakraborty S (2019) Compositional properties and codon usage pattern of mitochondrial ATP gene in different classes of Arthropoda. Genetica 147:231–248

    Article  CAS  Google Scholar 

  • Bhai RS (2020) Infectivity and management of dry rot, eye rot and soft rot of ginger (Zingiber officinale Rosc). J Plant Crops 48:11–20

    Google Scholar 

  • Biswas K, Palchoudhury S, Chakraborty P, Bhattacharyya UK, Ghosh DK, Debnath P, Lee RF (2019) Codon usage bias analysis of Citrus tristeza virus: Higher codon adaptation to citrus reticulata host. Viruses 11(4):331

    Article  CAS  Google Scholar 

  • Chen W, Xie T, Shao Y, Chen F (2012) Genomic characteristics comparisons of 12 food-related filamentous fungi in tRNA gene set, codon usage and amino acid composition. Gene 497(1):116–124

    Article  CAS  Google Scholar 

  • Cheng YT, Zhang L, He SY (2019) Plant-microbe interactions facing environmental challenge. Cell Host Microbe 26(2):183–192

    Article  CAS  Google Scholar 

  • Christgen SL, Becker DF (2019) Role of proline in pathogen and host interactions. Antioxid Redox Signal 30(4):683–709

    Article  CAS  Google Scholar 

  • Darshana CN, Praveena R, Ankegowda SJ, Biju CN (2014) Morphological variability, mycelial compatibility and fungicidal sensitivity of Colletotrichum gloeosporioides causing leaf spot of ginger (Zingiber officinaleRosc). J Spices Aroma Crop. 23(2):211–223

    Google Scholar 

  • Deng Y, de Lima HF, Kalfon J, Chu D, Von Der Haar T (2020) Hidden patterns of codon usage bias across kingdoms. J R Soc Interface 17(163):20190819

    Article  CAS  Google Scholar 

  • Du MZ, Liu S, Zeng Z, Alemayehu LA, Wei W, Guo FB (2018) Amino acid compositions contribute to the proteins’ evolution under the influence of their abundances and genomic GC content. Sci Rep 8(1):1–9

    Google Scholar 

  • Frumkin I, Lajoie MJ, Gregg CJ, Hornung G, Church GM, Pilpel Y (2018) Codon usage of highly expressed genes affects proteome-wide translation efficiency. PNAS 115(21):E4940–E4949

    Article  Google Scholar 

  • Fuller ZL, Haynes GD, Zhu D, Batterton M, Chao H, Dugan S, Ongeri F (2014) Evidence for stabilizing selection on codon usage in chromosomal rearrangements of Drosophila pseudoobscura. G3 Genes Genom Genet 4(12):2433–2449

    Google Scholar 

  • Hassan S, Mahalingam V, Kumar V (2009) Synonymous codon usage analysis of thirty two mycobacteriophage genomes. AdvBioinforma. https://doi.org/10.1155/2009/316936

    Article  Google Scholar 

  • Herbeck JT, Wall DP, Wernegreen JJ (2003) Gene expression level influences amino acid usage, but not codon usage, in the tsetse fly endosymbiontWigglesworthia. Microbiology 149(9):2585–2596

    Article  CAS  Google Scholar 

  • Ikechi-Nwogu CG, Odogwu BA, Pikibo A (2019) Morphological and molecular characterization of post-harvest fungal of ginger (Zingiber officinale) rhizomes fungi. Nigerian J Mycol 11:196

    Google Scholar 

  • Iriarte A, Sanguinetti M, Fernández-Calero T, Naya H, Ramón A, Musto H (2012) Translational selection on codon usage in the genus Aspergillus. Gene 506(1):98–105

    Article  CAS  Google Scholar 

  • Knight RD, Freeland SJ, Landweber LF (2001) A simple model based on mutation and selection explains trends in codon and amino-acid usage and GC composition within and across genomes. GenomBiol Res 2(4):0010–1

    Google Scholar 

  • Labella AL, Opulente DA, Steenwyk JL, Hittinger CT, Rokas A (2019) Variation and selection on codon usage bias across an entire subphylum. PLoS Genet 15(7):e1008304

    Article  Google Scholar 

  • Li X, Song H, Kuang Y, Chen S, Tian P, Li C, Nan Z (2016) Genome-wide analysis of codon usage bias in Epichloe festucae. Int J Molecular Sci 17(7):1138

    Article  CAS  Google Scholar 

  • Li G, Pan Z, Gao S, He Y, Xia Q, Jin Y, Yao H (2019) Analysis of synonymous codon usage of chloroplast genome in Porphyraumbilicalis. Genes Genomic 41(10):1173–1181

    Article  CAS  Google Scholar 

  • Lloyd AT, Sharp PM (1991) Codon usage in Aspergillus nidulans. Mol General Genetics 230(1–2):288–294

    Article  CAS  Google Scholar 

  • Muthabathula P, Suneetha S, Grace R (2018) Genome-wide codon usage bias analysis in Beauveriabassiana. Bioinformation 14(9):580

    Article  Google Scholar 

  • Paul P, Malakar AK, Chakraborty S (2018) Codon usage vis-a-vis start and stop codon context analysis of three dicot species. J Genet 97(1):97–107

    Article  CAS  Google Scholar 

  • Pawar NV, Patil VB, Kamble SS, Dixit GB (2008) First Report of Aspergillus niger as a Plant Pathogen on Zingiber officinale from India. Plant Dis 92(9):1368–1368

    Article  CAS  Google Scholar 

  • Payne BL, Alvarez-Ponce D (2019) Codon usage differences among genes expressed in different tissues of Drosophila melanogaster. Genom Biol Evol 11(4):1054–1065

    CAS  Google Scholar 

  • Qian W, Yang JR, Pearson NM, Maclean C, Zhang J (2012) Balanced codon usage optimizes eukaryotic translational efficiency. PLoS Genet 8(3):e1002603

    Article  CAS  Google Scholar 

  • Roy A, Van Staden J (2019) Comprehensive profiling of codon usage signatures and codon context variations in the genus Ustilago. World J MicrobiolBiotechnol 35(8):118

    Article  Google Scholar 

  • Sadhana M, Kalyan SK, Chandra ST, Jibon K (2012) Antifungal property of NaraveliaZeylanica (L.) DC against storage pathogens of Ginger (Zingiberofficinalis). Int Res J Pharm 3(9):198–200

    Google Scholar 

  • Sahoo S, Das SS, Rakshit R (2019) Codon usage pattern and predicted gene expression in Arabidopsis thaliana. Gene X 2:100012

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sharifi-Rad M, Varoni EM, Salehi B, Sharifi-Rad J, Matthews KR, Ayatollahi SA, Sharifi-Rad M (2017) Plants of the genus Zingiber as a source of bioactive phytochemicals: From tradition to pharmacy. Molecules 22(12):2145

    Article  Google Scholar 

  • Song H, Liu J, Song Q, Zhang Q, Tian P, Nan Z (2017) Comprehensive analysis of codon usage bias in seven Epichloe species and their peramine-coding Genes. Frontiers Microbiol 8:1419

    Article  Google Scholar 

  • Sur S, Sen A, Bothra AK (2007) Mutational drift prevails over translational efficiency in Frankianif operons. IJBT 6(3):321–328

    CAS  Google Scholar 

  • Sushma S, Shanmugam V, Singh BG, Neelam T, Sapna T, Priyanka T, Nath YA (2019) Genetic diversity and phylogenetic profiling of Fusarium sp., the causing storage rot of ginger (Zingiberofficinale) in Himachal Pradesh and their potential environmental eco-friendly management strategies. Res. J Biotechnol 5(14):44–54

    Google Scholar 

  • Thakur MP, Van der Putten WH, Cobben MM, Van Kleunen M, Geisen S (2019) Microbial invasions in terrestrial ecosystems. Nature Rev Microbiol 17(10): 621–631

    Article  CAS  Google Scholar 

  • Uddin A, Chakraborty S (2019) Codon usage pattern of genes involved in central nervous system. Mol Neurobiol 56(3):1737–1748

    Article  CAS  Google Scholar 

  • Wang L, Xing H, Yuan Y, Wang X, Saeed M, Tao J, Sun X (2018) Genome-wide analysis of codon usage bias in four sequenced cotton species. PLoS One 13(3):e0194372

    Article  Google Scholar 

  • Wibowo DP, Mariani R, Hasanah SU, Aulifa DL (2020) Chemical constituents, antibacterial activity and mode of action of elephant ginger (Zingiber officinale var. officinale) and Emprit Ginger Rhizome (Zingiber officinale var. amarum) Essential Oils. Pharmacog J 12(2):404–409

    Article  CAS  Google Scholar 

  • Wu Y, Zhao D, Tao J (2015) Analysis of codon usage patterns in herbaceous peony (PaeonialactifloraPall.) based on transcriptome data. Genes 6(4): 1125–1139

    Article  CAS  Google Scholar 

  • Zhou Z, Dang Y, Zhou M, Li L, Yu CH, Fu J, Liu Y (2016) Codon usage is an important determinant of gene expression levels largely through its effects on transcription. PNAS 113(41): E6117–E6125

    Article  CAS  Google Scholar 

  • Zhu Q, Mai U, Pfeiffer W, Janssen S, Asnicar F, Sanders JG, Kosciolek T (2019) Phylogenomics of 10,575 genomes reveals evolutionary proximity between domains Bacteria and Archaea. Nat Commun 10(1):1–14

    Article  Google Scholar 

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Acknowledgements

The authors would like to acknowledge the Director CSIR-Indian Institute of Integrative Medicine for providing the facilities. We thank Negenome Bioinformatics groups for their help.

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Authors and Affiliations

  1. Plant Biotechnology Division, CSIR-Indian Institute of Integrative Medicine, Jammu, 180001, India

    Suruchi Gupta & Ravail Singh

  2. Academy of Scientific and Innovative Research (AcSIR), Jammu, 180001, India

    Ravail Singh

  3. DZMB Senckenberg am Meer, Wilhelmshaven, Germany

    Ravail Singh

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  1. Suruchi Gupta
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  2. Ravail Singh
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Correspondence to Ravail Singh.

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Gupta, S., Singh, R. Comparative study of codon usage profiles of Zingiber officinale and its associated fungal pathogens. Mol Genet Genomics 296, 1121–1134 (2021). https://doi.org/10.1007/s00438-021-01808-8

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