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Forever young: stem cell and plant regeneration one century after Haberlandt 1921

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Abstract

Plants are characterized by a post-embryonic mode of organ development, which results in a need for these photoautotrophic organisms to regenerate lost parts in the course of their life cycle. This capacity depends on the presence of “pluripotent stem cells,” which are part of the meristems within the plant body. One hundred years ago, the botanist Gottlieb Haberlandt (1854–1945) published experiments showing wounding-induced callus formation, which led ultimately to plant regeneration in tissue culture and thence to the techniques of “plant biotechnology,” with practical applications for mankind. Here, we recount Haberlandt’s discovery within the context of his long research life and his most influential book Physiologische Pflanzenanatomie. In the second part, we describe and analyze a plant tissue-culture regeneration system using sterile, dark-grown sunflower (Helianthus annuus) seedlings as experimental material. We document that excised hook segments, which contain a “stem cell niche,” can regenerate entire miniature H. annuus–plantlets that, raised in a light/dark regime, develop flowers. Finally, we discuss molecular data relevant to plant regeneration with reference to phytohormones and conclude that, one century after Haberlandt, 1921, the exact biochemical/genetic mechanisms responsible for the capability of stem cells to remain “forever young” are, although already complex, really just beginning to become known.

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taken from an aseptically raised flower were sterile (left sample), while those from an inoculated culture contained pink methylobacteria (right sample). b On the green leaves of aseptic 50-day-old sunflower plantlets, no epiphytic bacteria were observed using scanning electron microscopy (left sample), whereas on the plantlets raised with methylobacteria, numerous microbes were detected (right sample). Methylobacteria (M) formed clusters on the cuticle of the epidermal cells that, in several documented cases, also occurred around the stomatal pore (s)

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References

  • Abanda-Nkpwatt D, Müsch M, Tschiersch J, Boettner M, Schwab W (2006) Molecular interaction between Methylobacterium extorquens and seedlings: growth promotion, methanol consumption, and localization of the methanol emission site. J Exp Bot 57:4025–4032

    Article  CAS  PubMed  Google Scholar 

  • Abbas M, Alabadí D, Blázquez M (2013) Differential growth at the apical hook: all roads lead to auxin. Front Plant Sci 4(441):1–9

    Google Scholar 

  • Aggarwal S, Sardana C, Ozturk M, Sarwat M (2020) Plant stem cells and their applications: special emphasis on their marketed products. 3 Biotech 10:291–299

    Article  PubMed  PubMed Central  Google Scholar 

  • Barnes ME (2014) Ernst Haeckel’s Biogenetic Law (1866). Embryo Project Encyclopedia (2014–05–03). ISSN: 1940–5030 http://embryo.asu.edu/handle/10776/7825

  • Bosch M, Cheung AY, Hepler PK (2005) Pectin methylesterase, a regulator of pollen tube growth. Plant Physiol 138:1334–1346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boysen-Jensen P, Nielsen N (1926) Studien über die hormonalen Beziehungen zwischen Spitze und Basis der Avena coleoptile. Planta 1:321–331

    Article  Google Scholar 

  • Brucke E (1862) Die Elementarorganismen. Sitzungsber. Akad Wiss Wien. Math Nat Cl 44:381–406

  • Darwin F (1903) The statolith theory of geotropism. Nature 67:571–572

    Article  Google Scholar 

  • Dietz A, Kutschera U, Ray PM (1990) Auxin enhancement of mRNAs in epidermis and internal tissues of the pea stem and its significance for control of elongation. Plant Physiol 93:432–438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doerges L, Kutschera U (2014) Assembly and loss of the polar flagellum in plant-associated methylobacteria. Naturwissenschaften 101:339–346

    Article  CAS  PubMed  Google Scholar 

  • Edelmann HG (2018) Graviperception in maize plants: is amyloplast sedimentation a red herring? Protoplasma 255:1877–1881

    Article  PubMed  PubMed Central  Google Scholar 

  • Fall R, Benson AA (1996) Leaf methanol. The simplest natural product from plants. Trends Plant Sci 1:296–301

    Article  Google Scholar 

  • Gautheret RJ (1983) Plant tissue culture: a history. Bot Mag (Tokyo) 96:393–410

    Article  Google Scholar 

  • Greb T, Lohmann JU (2016) Plant stem cells. Curr Biol 26:R816–R821

    Article  CAS  PubMed  Google Scholar 

  • Guttenberg HV (1955) Gottlieb Haberlandt. Phyton 6:1–14

    Google Scholar 

  • Haberlandt G (1884) Physiologische Pflanzenanatomie im Grundriss dargestellt. Wilhelm Engelmann, Leipzig

    Google Scholar 

  • Haberlandt G (1924) Physiologische Pflanzenanatomie, 6th edn. Wilhelm Engelmann, Leipzig

    Google Scholar 

  • Haberlandt G (1893) Ein botanische Tropenreise. Indo-Malayische Vegetationsbilder und Reiseskizzen. Julius Springer, Berlin

    Book  Google Scholar 

  • Haberlandt G (1900) Über die Perception des geotropischen Reizes. Ber Deut Bot Ges 18:261–272

    Google Scholar 

  • Haberlandt G (1902a) Kulturversuche mit isolierten Pflanzenzel-len. Sitzungsber. Akad Wiss Wien, Math-Naturwiss Kl. Abt J 111:69–92

  • Haberlandt G (1902b) Über Erklärung in der Biologie, 2nd edn. Leuschner & Lubensky, Graz

  • Haberlandt G (1921a) Zur Physiologie der Zellteilung. 6. Mitteilung: Über Auslösung von Zellteilungen durch Wundhormone. Sitzungber Akad Wiss Berlin 1(2):221–234

    Google Scholar 

  • Haberlandt G (1921b) Wundhormone als Erreger von Zellteilungen. Beitr Allg Bot 2 H 1:1–53

    Google Scholar 

  • Haberlandt G (1922) Über Zellteilungshormone und ihre Beziehungen zur Wundheilung, Befruchtung, Parthenogenesis und Adventiv-Embryonie. Biol Zentralbl 42:145–172

    CAS  Google Scholar 

  • Haberlandt G (1925) Zelle und Elementarorgan. Biol Zentralbl 45:257–272

    Google Scholar 

  • Haberlandt G (1933) Erinnerungen, Bekenntnisse und Betrachtungen. Julius Springer, Berlin

    Book  Google Scholar 

  • Haeckel E (1866) Generelle Morphologie der Organismen. Bd 1 /2. Verlag Georg Reimer, Berlin

    Book  Google Scholar 

  • Härtel O (1996) Gottlieb Haberlandt – Ein Gedenkblatt anläßlich der 50. Wiederkehr seines Todestages. Mitt Naturwiss Ver Steiermark 126:21–26

    Google Scholar 

  • Härtel O (2003) Gottlieb Haberlandt (1854–1945): a portrait. In: Laimer M, Rücker W (eds) Plant Tissue Culture, 100 years since Gottlieb Haberlandt. Springer, Berlin, pp 55–66

    Google Scholar 

  • Heupel T, Kutschera U (1996) Effect of white light on meristematic activity in developing sunflower hypocotyls. Protoplasma 192:1323–1329

    Article  Google Scholar 

  • Hornschuh M, Grotha R, Kutschera U (2006) Moss-associated methylobacteria as phytosymbionts: an experimental study. Naturwissenschaften 93:480–486

    Article  CAS  PubMed  Google Scholar 

  • Höxtermann E (1996) “Das Wetter wird vermutlich schön...” a memory on Gottlieb Haberlandt (1854–1945) at the 50th anniversary of his death. Biol Zentralbl 115:214–240

    Google Scholar 

  • Höxtermann E (1997) Cellular ‘elementary organisms’ in vitro. The early vision of Gottlieb Haberlandt and its realization. Physiol Plant 100:716–728

    Article  Google Scholar 

  • Ikeuchi M, Iwase A, Rymen B, Lambolez A, Kojima M et al (2017) Wounding triggers callus formation via dynamic hormonal and transcriptional changes. Plant Physiol 175:1158–1174

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ikeuchi M, Shibata M, Rymen B, Iwase A, Bågman A-M et al (2018) A gene regulatory network for cellular reprogramming in plant regeneration. Plant Cell Physiol 59:770–782

    Article  CAS  PubMed Central  Google Scholar 

  • Ikeuchi M, Favero DS, Sakamoto Y, Iwase A, Coleman D, Rymen B, Sugimoto K (2019) Molecular mechanisms of plant regeneration. Annu Rev Plant Biol 70:377–406

    Article  CAS  PubMed  Google Scholar 

  • Kenrick PK, Crane PR (1997) The origin and early diversification of land plants, a cladistic study. Smithsonian Institution Press, Washington

    Google Scholar 

  • Klikno J, Kutschera U (2017) Regulation of root development in Arabidopsis thaliana by phytohormone-secreting epiphytic methylobacteria. Protoplasma 254:1867–1877

    Article  CAS  PubMed  Google Scholar 

  • Koopmann V, Kutschera U (2005) In-vitro regeneration of sunflower plants: Effects of a Methylobacterium strain on organ development. J Appl Bot 79:59–62

    Google Scholar 

  • Krikorian AD, Berquam D (1969) Plant cell and tissue cultures: the role of Haberlandt. Botan Rev 35:59–67

    Article  Google Scholar 

  • Krug L, Morauf C, Donat C, Muller H, Cernava T, Berg G (2020) Plant growth-promoting methylobacteria selectively increase the biomass of biotechnologically relevant microalgae. Front Microbiol 11(427):1–12

    Google Scholar 

  • Kutschera U (2001) Gravitropism of axial organs in multicellular plants. Adv Space Res 27:851–860

    Article  CAS  PubMed  Google Scholar 

  • Kutschera U (2007) Plant-associated methylobacteria as co-evolved phytosymbionts: a hypothesis. Plant Signal Behav 2:74–78

    Article  PubMed  PubMed Central  Google Scholar 

  • Kutschera U (2019) Physiologie der Pflanzen. Sensible Gewächse in Aktion. LIT-Verlag, Berlin

    Google Scholar 

  • Kutschera U, Briggs WR (2016) Phototropic solar tracking in sunflower plants: an integrative perspective. Ann Bot 117:1–8

    Article  CAS  PubMed  Google Scholar 

  • Kutschera U, Briggs WR (2019) Photomorphogenesis of the root system in developing sunflower seedlings: a role for sucrose. Plant Biol 21:627–633

    Article  CAS  PubMed  Google Scholar 

  • Kutschera U, Koopmann V (2005) Growth in liverworts of the Marchantiales is promoted by epiphytic methylobacteria. Naturwissenschaften 92:347–349

    Article  CAS  PubMed  Google Scholar 

  • Kutschera U, Niklas KJ (2011) Ontogenetic changes in the scaling of cellular respiration with respect to size among sunflower seedlings. Plant Signal Behav 6:72–76

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kutschera U, Niklas KJ (2012) Organ-specific rates of cellular respiration in developing sunflower seedlings and their bearing on metabolic scaling theory. Protoplasma 249:1049–1057

    Article  CAS  PubMed  Google Scholar 

  • Laimer M, Rücker W (eds) (2003) Plant tissue culture, 100 years since Gottlieb Haberlandt. Springer, Berlin

    Google Scholar 

  • Lidstrom ME, Christoserdova L (2002) Plants in the pink: cytokinin production by Methylobacterium. J Bact 184:1818

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller CO, Skoog F, Von Saltza MH, Strong EM (1955) Kinetin, a cell division factor from deoxyribonucleic acid. J Am Chem Soc 77:1392

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Němec B (1900) Über die Art der Wahrnehmung des Schwerkraftreizes bei den Pflanzen. Ber Deut Bot Ges 18:241–245

    Google Scholar 

  • Niklas KJ, Cobb ED, Kutschera U (2016) Haeckel’s biogenetic law and the land plant phylotypic stage. Bioscience 66:510–519

    Article  Google Scholar 

  • Noé AC (1934) Gottlieb Haberlandt 1854. Plant Physiol 9:851–855

    Google Scholar 

  • Paterson KE (1984) Shoot tip culture of Helianthus annuus – flowering and development of adventitious and multiple shoots. Am J Bot 71:925–931

    Article  Google Scholar 

  • Paterson KE, Everett NP (1985) Regeneration of Helianthus annuus inbred plants from callus. Plant Sci 42:125–132

    Article  CAS  Google Scholar 

  • Ray PM (1972) The Living Plant, 2nd edn. Holt, Rinehart and Winston Inc., New York

    Google Scholar 

  • Ray PM, Bret-Harte MS (2019) Elastic and irreversible bending of tree and shrub branches under cantilever loads. Front Plant Sci 10(59):1–19

    CAS  Google Scholar 

  • Sablowski R (2004) Plant and animal stem cells: conceptually similar, molecularly distinct? Trends Cell Biol 14:605–611

    Article  CAS  PubMed  Google Scholar 

  • Sablowski R (2010) Stem cells in plants and animals. Nat Educ 3:4–9

    Google Scholar 

  • Schauer S, Kutschera U (2011) A novel growth-promoting microbe, Methylobacterium funariae sp. nov., isolated from the leaf surface of a common moss. Plant Signal Behav 6:510–515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma VK, Fletcher JC (2002) Maintenance of shoot and floral meristem cell proliferation and fate. Plant Physiol 129:31–39

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schwendener S (1874) Das mechanische Princip im anatomischen Bau der Monocotylen. W Engelmann, Leipzig

    Google Scholar 

  • Shin J, Bae S, Seo PJ (2020) De novo shoot organogenesis during plant regeneration. J Exp Bot 71:63–72

    Article  CAS  PubMed  Google Scholar 

  • Thorpe TA (2007) History of plant tissue culture. Mol Biotechnol 37:169–180

    Article  CAS  PubMed  Google Scholar 

  • Torres KC (1989) Tissue culture techniques for horticultural crops. Van Nostrand Reinhold, New York

    Book  Google Scholar 

  • Vasil IK (2008) A history of plant biotechnology: from the cell theory of Schleiden to Schwann to biotech crops. Plant Cell Rep 27:1423–1440

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Zhang K, Xu L, Wang E (2011) Quantifying the Waddington landscape and biological paths for development and differentiation. Proc Natl Acad Sci U S A 108:8257–8262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Went FW (1926) On growth-accelerating substances in the coleoptile of Avena sativa. Proc Kon Ned Akad Wetensch 30:10–19

    Google Scholar 

  • Zádníková P, Petrásek J, Marhavy P, Raz V, Vandenbussche F, Ding Z et al (2010) Role of PIN-mediated auxin efflux in apical hook development of Arabidopsis thaliana. Development 137:607–617

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The cooperation of the authors was initiated by the Alexander von Humboldt-Stiftung (AvH Fellowship Stanford 2013/14 to UK, Scientific Collaborator, R. Khanna-team/Briggs-Lab, Carnegie Institution, & P. M. Ray-Group, Biology Dept., S.U., Stanford, CA 94305, USA). We are greatly indebted to, and thank, the authors of several references for details of Gottlieb Haberlandt’s life and work, including Noé (1934), Höxtermann (1997), Härtel (2003), and Laimer and Rücker (2003). Besides their writings used here, Otto Härtel (1996), Ekkehard Höxtermann (1996), and H. von Guttenberg (1955) published lengthier accounts of Gottlieb Haberlandt’s life, which are cited here but which we could not access; they would doubtless provide important information beyond what is given here.

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Authors and Affiliations

  1. I-Cultiver, Inc., Treasure Island, San Francisco, CA, 94130, USA

    Ulrich Kutschera

  2. Department of Biology, Stanford University, Stanford, CA, 94305, USA

    Ulrich Kutschera & Peter M. Ray

  3. Institute of Arctic Biology, University of Alaska Fairbanks, Anchorage, AL, 99775, USA

    Peter M. Ray

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  1. Ulrich Kutschera
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Correspondence to Ulrich Kutschera or Peter M. Ray.

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Dedicated to the memory of Winslow R. Briggs (1928–2019).

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Kutschera, U., Ray, P.M. Forever young: stem cell and plant regeneration one century after Haberlandt 1921. Protoplasma 259, 3–18 (2022). https://doi.org/10.1007/s00709-021-01683-5

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