Skip to main content
SpringerLink
Log in

Organogenesis, direct somatic embryogenesis, and shoot proliferation of Rheum spiciforme Royle: an endemic and vulnerable medicinal herb from Indian Trans Himalayas

  • Medicinal Plants
  • Published:
In Vitro Cellular & Developmental Biology - Plant Aims and scope Submit manuscript

Abstract

Rheum spiciforme Royle is a high value medicinal herb restricted to NW Himalayas. The medicinal properties of Rheum include anti-oxidant, anti-microbial, antitumor, anti-inflammatory, anti-fungal, anti-atherosclerotic, anti-proliferative, hepatoprotective, and immuno-enhancing. The species is threatened and endemic which demands its conservation. In this context, we have developed a premiere efficient in vitro regeneration system for this herb. The seed germination displayed phenomenal increase when transferred from soil (13.6 ± 3.1%) to half-strength Murashige and Skoog (MS) medium (92.6 ± 1.3%) fortified with 0.005 mM gibberellic acid (GA3) and 1 mM potassium nitrate (KNO3) and calcium chloride (CaCl2) each with mean germination time (MGT) of 8.5 ± 1.8 d. Among four types of explants used for callusing, leaf explants responded highest with 87.3 ± 1.4% at 2 μM 2,4-dichlorophenoxyacetic acid (2,4-D) and 6-benzylaminopurine (BA) each. Nodal-segment-derived brown calluses exhibited significantly high regeneration (96.3 ± 1.6 %) at 8.0 μM BA and kinetin (KIN) each with 4.0 μM GA3. Leaf explants observed direct somatic embryogenesis which displayed maximum (91.0 ± 3.4%) germination at 25 μM BA, 1.0 μM NAA (naphthaleneacetic acid), 2.0 μM GA3, 50.0 μM glutamine (GTM), and adenine sulfate (ADS) each. Multiple shoot induction with mean number of 10.1 ± 2.6 shoots and elongation 4.2 ± 0.4 cm was observed at 12.5 μM BA and 0.5 μM NAA along with 25 μM GTM and ADS each. The rooted seedlings developed in half-strength liquid MS with 2.5 μM NAA were hardened and subsequently transferred to the field. The developed protocol could be utilized for various attributes which include development of large-scale micropropagation system as a conservation measure, Agrobacterium-mediated genetic transformation studies, and industrial production of important bioactive chemical constituents.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure. 1
Figure. 2
Figure. 3
Figure. 4

Similar content being viewed by others

References

  • Abbasi NA, Pervaiz T, Hafiz IA, Yaseen M, Hussain A (2013) Assessing the response of indigenous loquat cultivar Mardan to phytohormones for in vitro shoot proliferation and rooting. J Zhejiang Univ Sci B 14:774–784

    CAS  PubMed  PubMed Central  Google Scholar 

  • Acemi A (2020) Chitosan versus plant growth regulators: a comparative analysis of their effects on in vitro development of Serapias vomeracea (Burm. f.) Briq. Plant Cell Tiss Org Cult 141:327–338

    CAS  Google Scholar 

  • Beligni MV, Lamattina L (2000) Nitric oxide stimulates seed germination and de-etiolation, and inhibits hypocotyl elongation, three light-inducible responses in plants. Planta 210:215–221

    CAS  PubMed  Google Scholar 

  • Bethke PC, Gubler F, Jacobsen JV, Jones RL (2004) Dormancy of Arabidopsis seeds and barley grains can be broken by nitric oxide. Planta 219:847–855

    CAS  PubMed  Google Scholar 

  • Bisht S, Bisht NS, Bhandari S (2012a) In vitro micropropagation in Polygonatum verticillatum(L.) in an important threatened medicinal herb of northern India. Physiol Mol Biol Plant 18:89–93

    Google Scholar 

  • Bisht S, Bisht NS, Bhandari S (2012b) In vitro plant regeneration from seedling explants of Hedychium coronarium J. Koenig. J Med Plant Res 6:5546–5551

    CAS  Google Scholar 

  • Bo Song, Ju¨rg, Yong-Qian Gao, Zhi-Qiang Zhang, Yang Yang, Zhi-Ming Li, Hang Sun (2013) Habitat-specific responses of seed germination and seedling establishment to soil water condition in two Rheum species in the high Sino-Himalayas. Ecol Res 28: 643–651. https://doi.org/10.1007/s11284-013-1057-6

  • Burstrom H (1968) Calcium and plant growth. Biol Rev 43:287–316

    CAS  Google Scholar 

  • Chai B, Sticklen MB (1998) Applications of biotechnology in turfgrass genetic improvement. Crop Sci 38:1320–1338

    Google Scholar 

  • Chand S, Sahrawat AK (2002) Somatic embryogenesis and plant regeneration from root segments of Psoralea corylifolia L., an endangered medicinally important plant. In Vitro Cell Dev Biol - Plant 38:33–38

  • Chee PP (1990) High frequency of somatic embryogenesis and recover of fertile cucumber plants. Hortic Sci 25:792–793

    Google Scholar 

  • Cui Y, Deng Y, Zheng K, Hu X, Zhu M, Deng X, Xi R (2019) An efficient micropropagation protocol for an endangered ornamental tree species (Magnolia sirindhorniae Noot. & Chalermglin) and assessment of genetic uniformity through DNA markers. Sci Rep 9:9634. https://doi.org/10.1038/s41598-019-46050-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cui Y, Liu X, Han J, Wang B, Guo D (2008) Biotransformation of podophyllotoxin by cell suspension culture and root culture of Rheum palmatum. Zhongguo Zhong Yao Za Zhi 33:989–991

    CAS  PubMed  Google Scholar 

  • Ćulafić L, Samofalova A, Nešković M (1987) In vitro organogenesis in two dioecious species, Rumex acetosella L. and R. acetosa L.(Polygonaceae). Plant Cell Tiss Org Cult 11:125–131

    Google Scholar 

  • Dabski M, Kozak D (1998) Micropropagation of Polygonum aubertii L. Scientific Journals of the Agricultural University of Krakow. Sci Session 2:687–691

    Google Scholar 

  • Darrudi R, Hassandokht MR, Nazeri V (2014) Effects of KNO3 and CaCl2 on seed germination of Rheum khorasanicum B. Baradaran & A. Jafari. J Appl Sci Res 10:171–175

    CAS  Google Scholar 

  • Das G, Rout G (2002) Direct plant regeneration from leaf explants of Plumbago species. Plant Cell Tiss Org Cult 68:311–314

    CAS  Google Scholar 

  • Derek J (1997) Seed dormancy and germination. Plant Cell 9:1055–1066

    Google Scholar 

  • Dorjey K, Tamchos S, Kumar S (2012) Ethnobotanical observations in trans-himalayan region of ladakh. J Plant Dev Sci 4:459–464

    Google Scholar 

  • Duangporn P, Siripong P (2009) Effect of auxin and cytokinin on phyllanthusol A production by callus cultures of Phyllanthus acidus skeels. American-Eurasian J Agric Environ Sci 5:258–263

    CAS  Google Scholar 

  • Evans DA, WR S, CE F (1981) Growth and behavior of cell cultures: embryogenesis and organogenesis. Plant tissue culture: methods and application in agriculture/edited by Trevor A. Thorpe. Academic press

  • Fang S, Gao K, Hu W, Snider JL, Wang SS, Chen BL, Zhou ZG (2018) Chemical priming of seed alters cotton floral bud differentiation by inducing changes in hormones, metabolites and gene expression. Plant Physiol Biochem 130:633–640.https://doi.org/10.1016/j.plaphy.2018.08.010

  • Farzami SM, Ghorbanli M (2011) Breaking of dormancy in rhubarb (Rheum ribes L.). Iran J Plant Physiol 1:118–124

    Google Scholar 

  • Feher A (2019) Callus, dedifferentiation, totipotency, somatic embryogenesis: what these terms mean in the era of molecular plant biology. Front Plant Sci 10:1–11

    Google Scholar 

  • Finch-Savage WE, Leubner-Metzger G (2006) Seed dormancy and the control of germination. New Phytol 171:501–523

    CAS  PubMed  Google Scholar 

  • Gao N, Cui G, Lai Y, Zheng S, Li J, Wang J, Liu F (2011) Effects of different treatments on the germination of Oriental lily seeds. Acta Agr Univer Jiang 33:660–664

    Google Scholar 

  • George EF, Hall MA, De Klerk G-J (2008) Plant propagation by tissue culture. Springer, Dordrecht p 502

  • Gilissen LJW, van Staveren MJ, Hakkert JC, Smulders MJM (1996) Competence for regeneration during tobacco internodal development. Plant Physiol 111:1243–1250

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gniazdowska A, Dobrzyńska U, Babańczyk T, Bogatek R (2007) Breaking the apple embryo dormancy by nitric oxide involves the stimulation of ethylene production. Planta 225:1051–1057

    CAS  PubMed  Google Scholar 

  • Gokhale M, Bansal Y (2009) Direct in vitro regeneration of a medicinal tree Oroxylum indicum (L.) Vent. through tissue culture. Afr J Biotechnol 8:3777–3781

    CAS  Google Scholar 

  • Green B, Tabone T, Felker P (1990) A comparison of amide and ureide nitrogen sources in tissue culture of tree legume Prosopis alba clone B 2 V 50. Plant Cell Tiss Org Cult 21:83–86

    CAS  Google Scholar 

  • Gupta SM, Pandey P, Grover A, Ahmed Z (2011) Breaking seed dormancy in Hippophae salicifolia, a high value medicinal plant. Physiol Mol Biol Plant 17:403–406

    Google Scholar 

  • Gutiérrez IEM, Nepomuceno CF, Ledo CAS, Santana JRF (2011) In vitro regeneration via direct organogenesis of Bauhinia cheilantha. Rural Sci 41:260–265

    Google Scholar 

  • Harper JF, Breton G, Harmon A (2004) Decoding Ca2+ signals through plant protein kinases. Ann Rev Plant Biol 55:263–288

    CAS  Google Scholar 

  • Ho W-J, Vasil IK (1983) Somatic embryogenesis in sugarcane (Saccharum officinarum L.) I. The morphology and physiology of callus formation and the ontogeny of somatic embryos. Protoplasma 118:169–180

    Google Scholar 

  • Hunault G, Maatar A (1995) Enhancement of somatic embryogenesis frequency by gibberellic acid in fennel. Plant Cell Tiss Org Cult 41:171–176

    CAS  Google Scholar 

  • Ikeda-Iwai M, Satoh S, Kamada H (2002) Establishment of a reproducible tissue culture system for the induction of Arabidopsis somatic embryos. J Exp Bot 53:1575–1580

    CAS  PubMed  Google Scholar 

  • Ipekci Z, Gozukirmizi N (2004) Indirect somatic embryogenesis and plant regeneration from leaf and internode explants of Paulownia elongata. Plant Cell Tiss Org Cult 79:341–345

    CAS  Google Scholar 

  • Ishimaru K, Satake M, Shimomura K (1990) Production of (+)-catechin in root and cell suspension cultures of Rheum palmatum L. Plant Tiss Cult Lett 7:159–163

    Google Scholar 

  • Jayanthi M, Mandal P (2001) Plant regeneration through somatic embryogenesis and RAPD analysis of regenerated plants in Tylophora indica (Burm. f. Merrill.). In Vitro Cell Dev Biol - Plant 37:576–580

  • Jeelani SM, Farooq U, Gupta AP, Lattoo SK (2017) Phytochemical evaluation of major bioactive compounds in different cytotypes of five species of Rumex L. Ind Crop Prod 109:897–904

    CAS  Google Scholar 

  • Ji-yong J (2010) Tissue culture of Rhubarb [J]. Yinshan Academic Journal (Natural Science Edition) 2

  • Kala CP (2005) Indigenous uses, population density, and conservation of threatened medicinal plants in protected areas of the Indian Himalayas. Conserv Biol 19:368–378

    Google Scholar 

  • Kamiya Y, Yamaguchi S, Nambara E (2002) Gibberellins and light-stimulated seed germination. J Plant Growth Regul 20:369–376

    Google Scholar 

  • Kauth PJ, Vendrame WA, Kane ME (2006) In vitro seed culture and seedling development of Calopogon tuberosus. Plant Cell Tiss Org Cult 85:91–102

    Google Scholar 

  • Kumar GP, Kumar R, Chaurasia O, Singh SB (2011) Current status and potential prospects of medicinal plant sector in trans-Himalayan Ladakh. J Med Plant Res 5:2929–2940

    Google Scholar 

  • Kumar HA, Murthy H, Paek K (2002) Somatic embryogenesis and plant regeneration in Gymnema sylvestre. Plant Cell Tiss Org Cult 71:85–88

    Google Scholar 

  • Lal N, Ahuja PS (1989) Propagation of Indian Rhubarh (Rheum emodi Wall.) using shoot-tip and leaf explant culture. Plant Cell Rep 8:493–496

    CAS  PubMed  Google Scholar 

  • Lapasin R, Pricl S (1995) Rheology of industrial polysaccharides: theory and applications. Blackie Academic & Professional/Chapman & Hall, Glasgow

  • Lassus C, Voipio I (1994) Micropropagation of rhubarb with special reference to weaning stage and subsequent growth. Agric Food Sci 3:189–194

    Google Scholar 

  • Lepse L Comparison of in vitro and traditional propagation methods of Rhubarb (Rheum rhabarbarum) according to morphological features and yield. In: III International Symposium on Acclimatization and Establishment of Micropropagated Plants 812, 2007. pp 265-270

  • Liu Z, Sanford J (1988) Plant regeneration by organogenesis from strawberry leaf and runner tissue. Hort Sci 23:1057–1059

    Google Scholar 

  • Maithani U (2015) In-vitro propagation studies of Rheum moorcroftianum Royle: a threatened medicinal plant from Garhwal Himalaya. Int J Curr Microbiol App Sci 4:596–599

    CAS  Google Scholar 

  • Mamun A, Islam R, Reza M, Joadar O (1996) In vitro differentiation of plantlet of tissue culture of Samonea saman. Plant Tissue Cult 6:1–5

    Google Scholar 

  • Martin K (2003) Plant regeneration through somatic embryogenesis on Holostemma ada-kodien, a rare medicinal plant. Plant Cell Tiss Org Cult 72:79–82

    CAS  Google Scholar 

  • Martinez-de la Cruz E, Garcia-Ramirez E, Vazquez-Ramos JM, de la Cruz HR, Lopez-Bucio J (2015) Auxins differentially regulate root system architecture and cell cycle protein levels in maize seedlings. J Plant Physiol 176:147–156. https://doi.org/10.1016/j.jplph.2014.11.012

    Article  CAS  PubMed  Google Scholar 

  • Mok M, Mok D, Armstrong D, Shudo K, Isogai Y, Okamoto T (1982) Cytokinin activity of N-phenyl-N′-1, 2, 3-thiadiazol-5-ylurea (thidiazuron). Phytochemistry 21:1509–1511

    CAS  Google Scholar 

  • Mosca G, Sapala A, Strauss S, Routier-Kierzkowska AL, Smith RS (2017) On the micro-indentation of plant cells in a tissue context. Phys Biol 14:015003. https://doi.org/10.1088/1478-3975/aa5698

    Article  CAS  PubMed  Google Scholar 

  • Mun S-C, Mun G-S (2016) Development of an efficient callus proliferation system for Rheum coreanum Nakai, a rare medicinal plant growing in Democratic People’s Republic of Korea. Saudi J Biol Sci 23:488–494

    CAS  PubMed  Google Scholar 

  • Munazir M et al (2010) Primary callus induction, somatic embryogenesis and regeneration studies in selected elite wheat varieties from Pakistan. Pak J Bot 42:3957–3965

    CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    CAS  Google Scholar 

  • Pandith SA, Dar RA, Lattoo SK, Shah MA, Reshi ZA (2018) Rheum australe, an endangered high-value medicinal herb of North Western Himalayas: a review of its botany, ethnomedical uses, phytochemistry and pharmacology. Phytochem Rev 17:573–609

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pandith SA, Khan MI, Ramazan S. Genus Rheum (Polygonaceae): a global perspective (2020) CRC press, Taylor and Francis; ISBN 9780367355760, Catalogue No. 321468 (In production)

  • Quiroz-Figueroa F, Fuentes-Cerda C, Rojas-Herrera R, Loyola-Vargas V (2002) Histological studies on the developmental stages and differentiation of two different somatic embryogenesis systems of Caffea arabica. Plant Cell Rep 20:1141–1149

    CAS  Google Scholar 

  • Rashid S, Kaloo ZA, Singh S, Bashir I (2014) Callus induction and shoot regeneration from rhizome explants of Rheum webbianum Royle-a threatened medicinal plant growing in Kashmir Himalaya. J Sci Innov Res 3:515–518

    Google Scholar 

  • Rashmi R, Trivedi MP (2014) Effect of various growth hormone concentration and combination on callus induction, nature of callus and callogenic response of Nerium odorum. Appl Biochem Biotechnol 172:2562–2570. https://doi.org/10.1007/s12010-013-0693-1

    Article  CAS  PubMed  Google Scholar 

  • Ray M, Ghosh S, Ghosh B (1996) Plant regeneration from embryogenic calli of heat tolerant and sensitive cultivars under thermal stress. Physiol Mol Biol Plant 2:59–66

    Google Scholar 

  • Rayirath UP, Lada RR, Caldwell CD, Asiedu SK, Sibley KJ (2011) Role of ethylene and jasmonic acid on rhizome induction and growth in rhubarb (Rheum rhabarbarum L.). Plant Cell Tiss Org Cult 105:253–263

    CAS  Google Scholar 

  • Ren JW, Lei Y, Li XL (2017) Tissue culture of callus and establishment of regeneration system of Tussilago farfara petiole. Zhongguo Zhong Yao Za Zhi 42:3895–3900. https://doi.org/10.19540/j.cnki.cjcmm.2017.0156

    Article  PubMed  Google Scholar 

  • Roggemans J, Claes M-C (1979) Rapid clonal propagation of rhubarb by in vitro culture of shoot-tips. Sci Hortic 11:241–246

    CAS  Google Scholar 

  • Rutherford P, Ali N (1977) Sugar and enzyme changes during cold storage of rhubarb. Ann Appl Biol 85:159–160

    CAS  Google Scholar 

  • Samuelson ME, Campbell WH, Larsson CM (1995) The influence of cytokinins in nitrate regulation of nitrate reductase activity and expression in barley. Physiol Plant 93:533–539

    CAS  Google Scholar 

  • Sepehr MF, Ghorbanli Z (2005) Formation of catechin in callus cultures and micropropagation of Rheum ribes L. Pak J Biol Sci 8:1346–1350

    CAS  Google Scholar 

  • Shekhawat N, Kackar A, Rathore M, Singh M, Dagla H, Arya V (2006) Establishment and Economic evaluation of micropropagated Jeewanti (Leptadenia reticulata Wight & Arn.) plants in field. Nat Prod Rad 5:311–314

    Google Scholar 

  • Siwach P, Gill AR (2011) Enhanced shoot multiplication in Ficus religiosa L. in the presence of adenine sulphate, glutamine and phloroglucinol. Physiol Mol Biol Plant 17:271–280

    CAS  Google Scholar 

  • Sugimoto K, Gordon SP, Meyerowitz EM (2011) Regeneration in plants and animals: dedifferentiation, transdifferentiation, or just differentiation. Trend Cell Biol 21:212–218

    CAS  Google Scholar 

  • Taiz L, Zeiger E (1991) Plant physiology. The Benjamin/Cummings publishing company, Inc, California 559 p

  • Tan M, Li G, Qi S, Liu X, Chen X, Ma J, Zhang D, Han M (2018) Identification and expression analysis of the IPT and CKX gene families during axillary bud outgrowth in apple (Malus domestica Borkh.). Gene 651:106–117. https://doi.org/10.1016/j.gene.2018

    Article  CAS  PubMed  Google Scholar 

  • Teardo E, Carraretto L, Moscatiello R, Cortese E, Vicario M, Festa M, Maso L, De Bortoli S, Cali T, Vothknecht UC, Formentin E, Cendron L, Navazio L, Szabo I (2019) A chloroplast-localized mitochondrial calcium uniporter transduces osmotic stress in Arabidopsis. Nat Plant 5:581–588. https://doi.org/10.1038/s41477-019-0434-8

    Article  CAS  Google Scholar 

  • Thomas TD, Shankar S (2009) Multiple shoot induction and callus regeneration in Sarcostemma brevistigma Wight & Arnott, a rare medicinal plant. Plant Biotech Rep 3:67–74

    Google Scholar 

  • Van Stedan J, Zazimalova E, George EF (2008) Cytokinins, their analogoues and antagonists. In: George EF, Hall M and Delkleck GJ eds. Plant propagation by tissue culture: Plant growth regulators II. Springer The Netherlands 1:205–226

    Google Scholar 

  • Vasudevan A, Selvaraj N, Ganapathi A, Kasthurirengan S, Anbazhagan VR, Manickavasagam M (2004) Glutamine: a suitable nitrogen source for enhanced shoot multiplication in Cucumis sativus L. Biol Plant 48:125–128

    CAS  Google Scholar 

  • Verdeil JL, Hocher V, Huet C, Grosdemange F, Escoute J, Ferriere N, Nicole M (2001) Ultrastructural changes in coconut calli associated with the acquisition of embryogenic competence. Ann Bot 88:9–18. https://doi.org/10.1006/anbo.2001.1408

    Article  Google Scholar 

  • Viéitez Martín AM, Barciela J (1990) Somatic embryogenesis and plant regeneration from embryonic tissues of Camellia japonica L. Plant Cell Tiss Org Cult 21:267–274

    Google Scholar 

  • Wakhlu A, Bhau BS (2000) Callus formation and plant regeneration from tubercles of Coryphantha elephantidens (Lem.) Lem In Vitro. Cell Dev Biol - Plant 36:211–214

    Google Scholar 

  • Wojtania A, Gabryszewska E (2000) Effect of growth regulators on the in vitro propagation of Coccoloba unifera L. in vitro Zeszyty Naukowe Instytutu Sadownictwa i Kwiaciarstwa w Skierniewicach (Poland)

  • Xu W, Chen G, Li Y, Wang L (2004) Studies on tissue culture technique of Rheum tanguticum. Acta Bot Boreali-occidentalia Sin 24:1734–1738

    CAS  Google Scholar 

  • Zargar BA, Masoodi MH, Ahmed B, Ganie SA (2011) Phytoconstituents and therapeutic uses of Rheum emodi wall. ex Meissn. Food Chem 128:585–589

    CAS  PubMed Central  Google Scholar 

  • Zhao Y, Grout B, Crisp P (2002) Unexpected susceptibility of novel breeding lines of European rhubarb (Rheum rhaponticum) to leaf and petiole spot disease. In: XXVI International Horticultural Congress: Advances in Vegetable Breeding, vol 637, pp 139–144

  • Zhao Y, Grout BWW, Roberts AV (2005) Abnormal chromosomes and DNA content in micropropagated rhubarb (Rheum rhaponticum L.) PC49. Plant Cell Tiss Organ Cult 83:335–338

    Google Scholar 

  • Zhao Y, Zhou Y, Grout BW (2006) Variation in leaf structures of micropropagated rhubarb (Rheum rhaponticum L.) PC49. Plant Cell Tiss Org Cult 85:115–121

  • Zhao Y, Zhou Y, Grout BWW (2007) Crop failure of micropropagated rhubarb (Rheum rhaponticum L.) PC49 caused by somaclonal variation. Acta Hort. 764:13–19

Download references

Acknowledgements

Work in the SAP laboratory is supported by the Department of Science and Technology (DST), Govt. of India, under the INSPIRE Faculty Scheme [DST/INSPIRE/04/2016/001059]. The supporting staff of Plant Biotechnology lab and USIF at AMU, Aligarh, UP, is acknowledged for their help and kind support. We are also thankful to two anonymous reviewers who very critically analyzed the manuscript which has improved its overall quality.

Author information

Authors and Affiliations

  1. Department of Botany, University of Kashmir, Hazratbal, Srinagar, Jammu, Kashmir, 190006, India

    Mohd Ishfaq Khan & Shahzad A. Pandith

  2. Plant Biotechnology Section, Department of Botany, Aligarh Muslim University, Aligarh, Uttar Pradesh, 202002, India

    Mohd Ishfaq Khan, Anwar Shahzad & Irfan Bashir Ganie

Authors
  1. Mohd Ishfaq Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anwar Shahzad
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Irfan Bashir Ganie
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shahzad A. Pandith
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceived and designed the experiments: AS and SAP. Performed the experiments: MIK and AS. Analyzed the data: AS, MIK, and SAP. Contributed reagents/materials/analysis tools: SAP and AS. Wrote the paper: MIK, AS, and SAP.

Corresponding author

Correspondence to Shahzad A. Pandith.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Editor: Adriana Pinheiro Martinelli

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khan, M.I., Shahzad, A., Ganie, I.B. et al. Organogenesis, direct somatic embryogenesis, and shoot proliferation of Rheum spiciforme Royle: an endemic and vulnerable medicinal herb from Indian Trans Himalayas. In Vitro Cell.Dev.Biol.-Plant 58, 35–50 (2022). https://doi.org/10.1007/s11627-021-10211-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11627-021-10211-2

Keywords

Search

Navigation