Abstract
Bamboos are perennial, arborescent, monocarpic, and industrially important non-timber grasses that are used as a pristine source of inorganic nutrients. However, conventional vegetative propagation methods demonstrated inadequate multiplication potential. This study investigates how Bambusa balcooa’s in vitro growth, photosynthetic pigment content, and antioxidant capacity were affected by citrate- and cetyltrimethylammonium bromide-coated gold nanoparticles (AuNPs). Further, to unravel the regulatory mechanism underlying gold nano-elicitation and in vitro plant behavior, we conducted RNA sequencing of non-treated control, 400 µM citrate-AuNPs-treated, and 600 µM CTAB-AuNPs-treated plantlets. Numerous morphological, physiological, and biochemical parameters were observed to be variably impacted along the citrate- and CTAB-coated AuNPs concentration gradient (200–600 µM). B. balcooa in vitro shoots supplemented with Murashige and Skoog medium enriched with 6-benzylaminopurine, naphthaleneacetic acid, and 400 µM citrate-AuNPs displayed statistically significant shoot proliferation, photosynthetic pigment accumulation, and antioxidant activities. Contrarily, a decline in growth parameters was observed in MS media supplemented with BAP, NAA, and 600 µM CTAB-AuNPs. Transcriptome profiling revealed various differentially expressed genes (DEGs) and metabolic pathways associated with nano-elicitation and plant growth. Furthermore, identifying genes (such as Glyoxalase, Expansin, and ZAT) governing in vitro proliferation and oxidative stress responses could enhance our understanding of the mechanisms underlying AuNPs’ ability to modulate various physiological and biochemical activities during micropropagation. Therefore, gene ontology (GO) enrichment, Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis, and the exploration of DEGs involved in the in vitro modulations regulated by AuNPs offer novel insights into the molecular mechanisms governing nano-elicited plant organogenesis more comprehensively.
Graphical abstract
Key message
In vitro elicitation of differentially coated gold nanoparticles improves the biomass, photosynthesis, and antioxidant potential of Bambusa balcooa. RNA sequencing reveals transcriptional reprogramming in response to nano-elicitation.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Not applicable.
References
Ahmed AF, Attia FA, Liu Z, Li C, Wei J, Kang W (2019) Antioxidant activity and total phenolic content of essential oils and extracts of sweet basil (Ocimum basilicum L.) plants. Food Sci Hum Wellness 8:299–305. https://doi.org/10.1016/j.fshw.2019.07.004
Alkhatib R, Alkhatib B, Abdo N (2021) Effect of Fe3O4 nanoparticles on seed germination in tobacco. Environ Sci Pollut Res 28:53568–53577. https://doi.org/10.1007/s11356-021-14541-x
Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15. https://doi.org/10.1104/pp.24.1.1
Asante KOH, Akoto DS, Derkyi NSA, Abugre S (2024) Advancing circular economy for the growth, root development and elemental characteristics of bamboo (Bambusa vulgaris) on galamsey-degraded soil. Adv Bamboo Sci 6:100054. https://doi.org/10.1016/j.bamboo.2023.100054
Baharuddin N, Abdul Karim SR, Kassim AS, Osman Al-Edrus SS, Lee SH (2023) Global bamboo industries: an overview. In: Md Tahir P, Lee SH, Osman Al-Edrus SS, Uyup MKA (eds) Multifaceted bamboo. Springer, Singapore, pp 15–41. https://doi.org/10.1007/978-981-19-9327-5_2
Banerjee J, Kole C (2016) Plant nanotechnology: an overview on concepts, strategies, and tools. In: Kole C, Kumar D, Khodakovskaya M (eds) Plant Nanotechnology. Springer, Cham, pp 1–14. https://doi.org/10.1007/978-3-319-42154-4_1
Bansal AK (2020) Unlocking the potential of bamboo sector in India. NCCF Working Paper No. 2/2020, New Delhi, India
Bharathiraja B, Devaki P, Dheepa S, Mageshwari R, Jayamuthunagai J, Chakravarthy M, Yuvaraj D, Praveenkumar R (2016) Environmental eco-friendly marine resource macro algae (Seaweeds): an omnipotent source for value added products and its applications-A review. Int J Curr Microbiol Appl Sci 5:19–47. https://doi.org/10.20546/ijcmas.2016.507.002
Broad RC, Bonneau JP, Beasley JT, Roden S, Sadowski P, Jewell N, Brien C, Berger B, Tako E, Glahn RP, Hellens RP (2020) Effect of rice GDP-L-galactose phosphorylase constitutive overexpression on ascorbate concentration, stress tolerance, and iron bioavailability in rice. Front Plant Sci 11:595439. https://doi.org/10.3389/fpls.2020.595439
Dhindsa RS, Plumb-Dhindsa PA, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Expt Bot 32:93–101. https://doi.org/10.1093/jxb/32.1.93
Dykman L, Shchyogolev S (2018) The effect of gold and silver nanoparticles on plant growth and development. In: Saylor Y, Irby V (eds) Metal nanoparticles. Nova, New York, pp 263–300
Emamverdian A, Ding Y, Mokhberdoran F, **e Y, Zheng X, Wang Y (2020) Silicon dioxide nanoparticles improve plant growth by enhancing antioxidant enzyme capacity in bamboo (Pleioblastus Pygmaeus) under lead toxicity. Trees 34:469–481. https://doi.org/10.1007/s00468-019-01929-z
Emamverdian A, Ding Y, Mokhberdoran F, Ahmad Z, **e Y (2021) The effect of silicon nanoparticles on the seed germination and seedling growth of moso bamboo (Phyllostachys edulis) under cadmium stress. Pol J Environ Stud 30:3033–3042. https://doi.org/10.15244/pjoes/129683
Farooq MA, Ali S, Hameed A, Ishaque W, Mahmood K, Iqbal Z (2013) Alleviation of cadmium toxicity by silicon is related to elevated photosynthesis, antioxidant enzymes; suppressed cadmium uptake and oxidative stress in cotton. Ecotoxicol Environ Saf 96:242–249. https://doi.org/10.1016/j.ecoenv.2013.07.006
Fazal T, Ismail B, Khan AM, Khan RA, Naqvi AA, Hamid FS, Sabir MA, Faridullah, Khan AR (2016) Comparative studies on the use of binary and ternary combinations of various acidifying agents for the reduction of soil pH. Commun Soil Sci Plant Anal 47:11–18. https://doi.org/10.1080/00103624.2015.1104335
Gantait S, Pramanik BR, Banerjee M (2018) Optimization of planting materials for large scale plantation of Bambusa balcooa Roxb.: influence of propagation methods. J Saudi Soc Agric Sci 17:79–87. https://doi.org/10.1016/j.jssas.2015.11.008
Ghawana S, Paul A, Kumar H, Kumar A, Singh H, Bhardwaj PK, Rani A, Singh RS, Raizada J, Singh K, Kumar S (2011) An RNA isolation system for plant tissues rich in secondary metabolites. BMC Res Notes 4:85. https://doi.org/10.1186/1756-0500-4-85
Ghosh A, Islam T (2016) Genome-wide analysis and expression profiling of glyoxalase gene families in soybean (Glycine max) indicate their development and abiotic stress specific response. BMC Plant Biol 16:87. https://doi.org/10.1186/s12870-016-0773-9
Hada S, Roat P, Chechani B, Kumar S, Yadav DK, Kumari N (2020) An overview on biomass of bamboo as a source of bioenergy. In: Kumar N (ed) Biotechnology for biofuels: a sustainable green energy solution. Springer, Singapore, pp 241–265. https://doi.org/10.1007/978-981-15-3761-5_10
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198. https://doi.org/10.1016/0003-9861(68)90654-1
Honi U, Amin MR, Kabir SM, Bashar KK, Moniruzzaman M, Jahan R, Jahan S, Haque MS, Islam S (2020) Genome-wide identification, characterization and expression profiling of gibberellin metabolism genes in jute. BMC Plant Biol 20:306. https://doi.org/10.1186/s12870-020-02512-2
Joshi S, Joshi R (2024) Comparative transcriptome profiling unveils the role of differentially charged gold nanoparticle in growth, metabolic regulation and defence response of micro-propagated Nardostachys Jatamansi Wall. Ex DC. S Afr J Bot 167:585–596. https://doi.org/10.1016/j.sajb.2024.02.052
Joshi SG, Cooper M, Yost A, Paff M, Ercan UK, Fridman G, Friedman G, Fridman A, Brooks AD (2011) Nonthermal dielectric-barrier discharge plasma-induced inactivation involves oxidative DNA damage and membrane lipid peroxidation in Escherichia coli. Antimicrob Agents Chemother 55(3):1053–1062. https://doi.org/10.1128/aac.01002-10
Joshi S, Dar AI, Acharya A, Joshi R (2022) Charged gold nanoparticles promote in vitro proliferation in Nardostachys jatamansi by differentially regulating chlorophyll content, hormone concentration, and antioxidant activity. Antioxidants 11:1962. https://doi.org/10.3390/antiox11101962
Karimi J, Mohsenzadeh S (2016) Effects of silicon oxide nanoparticles on growth and physiology of wheat seedlings. Russ J Plant Physiol 63:119–123. https://doi.org/10.1134/S1021443716010106
Krishnakumar N, Kanna SU, Parthiban KT, Rajendran P (2017) Physical properties of thorn less bamboos (Bambusa balcooa and Bambusa vulgaris). Agricul Update 12:946–951. https://doi.org/10.15740/HAS/AU/12
Kumari A, Joshi S, Dar AI, Joshi R (2023) Physio-biochemical integrators and transcriptome analysis reveal nano-elicitation associated response during Dendrocalamus asper (Schult. And Schult. F.) Backer ex K. Heyne Micropropagation. Genes 14:1725. https://doi.org/10.3390/genes14091725
Lan Y, Wu L, Wu M, Liu H, Gao Y, Zhang K, **ang Y (2021) Transcriptome analysis reveals key genes regulating signaling and metabolic pathways during the growth of moso bamboo (Phyllostachys edulis) shoots. Physiol Plant 172:91–105. https://doi.org/10.1111/ppl.13296
Lathwal M, Rani M, Singh AN, Chongtham N (2023) Impacts of bamboo biochar amendment on growth, morphological traits, and biomass allocation of Bambusa balcooa under copper-contaminated soil conditions. Int J Plant Sci 35:599–611. https://doi.org/10.9734/ijpss/2023/v35i193590
Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform 12:323. https://doi.org/10.1186/1471-2105-12-323
Liu Y, Khan AR, Gan Y (2022) C2H2 zinc finger proteins response to abiotic stress in plants. Inter J Mol Sci 23:2730. https://doi.org/10.3390/ijms23052730
Mawale KS, Giridhar P (2024) Chitosan nanoparticles modulate plant growth, and yield, as well as thrips infestation in Capsicum spp. Int J Biol Macromol 254:127682. https://doi.org/10.1016/j.ijbiomac.2023.127682
Milewska-Hendel A, Gepfert W, Zubko M, Kurczyńska E (2022) Morphological, histological and ultrastructural changes in Hordeum vulgare (L.) roots that have been exposed to negatively charged gold nanoparticles. Appl Sci 12:3265. https://doi.org/10.3390/app12073265
Mohiuddin M, Muntha ST, Ali A, Faizan M, Samrana S (2023) The Ecology of Reactive oxygen species Signalling. In: Faizan M, Hayat S, Ahmed SM (eds) Reactive oxygen species. Springer, pp 69–93. https://doi.org/10.1007/978-981-19-9794-5_5
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x
Musau Z (2016) Bamboo: Africa’s untapped potential. Afr Renew 30:22–25. https://doi.org/10.18356/d3c16c7c-en
Nagdalian AA, Blinov AV, Siddiqui SA, Gvozdenko AA, Golik AB, Maglakelidze DG, Rzhepakovsky IV, Kukharuk MY, Piskov SI, Rebezov MB, Shah MA (2023) Effect of selenium nanoparticles on biological and morphofunctional parameters of barley seeds (Hordéum vulgáre L). Sci Rep 13:6453. https://doi.org/10.1038/s41598-023-33581-6
Nair R (2016) Effects of nanoparticles on plant growth and development. In: Kole C, Kumar D, Khodakovskaya M (eds) Plant nanotechnology. Springer, Cham, pp 95–118. https://doi.org/10.1007/978-3-319-42154-4_5
Najafi Disfani M, Mikhak A, Kassaee MZ, Maghari A (2017) Effects of nano Fe/SiO2 fertilizers on germination and growth of barley and maize. Arch Agron Soil Sci 63:817–826. https://doi.org/10.1080/03650340.2016.1239016
Patel RK, Jain M (2012) NGS QC Toolkit: a toolkit for quality control of next generation sequencing data. PLoS ONE 7:e30619. https://doi.org/10.1371/journal.pone.0030619
Patial M, Suryavanshi V, Devi K, Pal PK, Joshi R (2024) Morpho-physiological and biochemical response of Monk Fruit plant to charged gold nanoparticles under in vitro conditions. Sugar Tech 26:709–718. https://doi.org/10.1007/s12355-024-01387-z
Phimmachanh S, Ying Z, Beckline M (2015) Bamboo resources utilization: a potential source of income to support rural livelihoods. Appl Ecol Environ Sci 3:176–183. https://doi.org/10.12691/aees-3-6-3
Rajput BS, Jani M, Ramesh K, Manokari M, Jogam P, Allini VR, Kher MM, Shekhawat MS (2020) Large-scale clonal propagation of Bambusa balcooa Roxb.: an industrially important bamboo species. Ind Crops Prod 157:112905. https://doi.org/10.1016/j.indcrop.2020.112905
Ray SS, Ali MN, Mukherjee S, Chatterjee G, Banerjee M (2017) Elimination and molecular identification of endophytic bacterial contaminants during in vitro propagation of Bambusa balcooa. World J Microbiol Biotechnol 33:31. https://doi.org/10.1007/s11274-016-2196-z
Shen Y, Guan Y, Song X, He J, **e Z, Zhang Y, Zhang H, Tang D (2019) Polyphenols extract from lotus Seedpod (Nelumbo nucifera Gaertn.): phenolic compositions, antioxidant, and antiproliferative activities. Food Sci Nutrit 7:3062–3070. https://doi.org/10.1002/fsn3.1165
Singh G, Reeta V (2020) Green gold as super power potential in for green India and mystery behind bamboo blossom. J Med Plants 8:112–117
Singh A, Mehta S, Yadav S, Nagar G, Ghosh R, Roy A, Chakraborty A, Singh IK (2022) How to cope with the challenges of environmental stresses in the era of global climate change: An update on ROS stave off in plants. Intern J Mol Sci 23:1995. https://doi.org/10.3390/ijms23041995
Sun C, Song R, Zhou J, Jia Y, Lu J (2023) Fermented bamboo Fiber improves productive performance by regulating gut microbiota and inhibiting chronic inflammation of sows and piglets during late Gestation and Lactation. Microbiol Spect 12:e04084–e04022. https://doi.org/10.1128/spectrum.04084-22
Suwal MM, Lamichhane J, Gauchan DP (2021) Assessment of genetic stability of micropropagated Bambusa balcooa Roxb. Using RAPD marker. Plant Tiss Cult Biotech 31:81–95. https://doi.org/10.3329/ptcb.v31i1.54114
Thakur RK, Dhirta B, Shirkot P (2018) Studies on effect of gold nanoparticles on Meloidogyne incognita and tomato plants growth and development. BioRxiv 428144. https://doi.org/10.1101/428144
Thapa P, Sareen B, Swarnkar MK, Sood A, Bhattacharya A (2022) De novo transcriptome analysis of bamboo in vitro shoots for identification of genes differentiating juvenile and aged plants. Ind Crops Prod 176:114353. https://doi.org/10.1016/j.indcrop.2021.114353
Acknowledgements
The authors thank the Director, CSIR-Institute of Himalayan Bioresource Technology, Palampur, India, for their support and for providing the infrastructure. Authors also thank Dr Amitabha Acharya, Principal Scientist, CSIR-IHBT, Palampur, India for providing nanoparticles for the study. Authors duly acknowledge Dr. Mohit Kumar Swarnkar, Sr. Technical Officer (1), for assistance in RNA sequencing. A.K. and S.J. thanks to the UGC, GOI (NTA Ref. No.: 191620063807) and DBT, GOI (file No.: DBT/JRF/BET-19/1/2019/AL/212) respectively for providing SRF. The authors acknowledge the financial support provided by CSIR (MLP-201) and DBT (BT/PR45280/NER/95/1918/2022).
Funding
The authors acknowledge the financial support provided by CSIR (MLP-201) and DBT (BT/PR45280/NER/95/1918/2022).
Author information
Authors and Affiliations
Contributions
A.K. performed the experiment, data collection, and manuscript writing; S.J. participated in data analysis and manuscript writing; A.I.D. prepared the gold nanoparticles; R.J. conceived idea, designed the study, reviewed and edited the final manuscript. All authors have read and agreed to the published version of the manuscript. The study was approved by the Institutional Review Board. This manuscript represents CSIR-IHBT communication no. 5368.
Corresponding author
Ethics declarations
Competing interest
The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.
Additional information
Communicated by Klaus Eimert.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Kumari, A., Joshi, S., Dar, A.I. et al. Physiological responses and transcriptomic profiles unveil pivotal genes and pathways implicated in nano-elicited in vitro shoot proliferation of Bambusa balcooa. Plant Cell Tiss Organ Cult 158, 9 (2024). https://doi.org/10.1007/s11240-024-02812-7
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11240-024-02812-7